ardila a 2012 on the origins of human cognition 1

OONN TTHHEE OORRIIGGIINNSS OOFF HHUUMMAANN CCOOGGNNIITTIIOONN

Department of Communication Sciences and Disorders

Florida International University

Miami, Florida, USA

Alfredo Ardila

2012

ONTENT

1. IntStatement of the Problem 7

2. OrIntrod

There tal phas a sy

Other

Three

C

roduction 7

References 15

igins of Language 23 uction 23

are only two fundamen a i ndromes 24

The selection disorder 25

The sequencing disorder 29

aphasia syndromes 30

stages in language development 36

Initial communication systems 37

The function of noises (grunts) in human communication 41

Second stage: Lexical/semantic 41

Third stage: Grammar 43

Brain representation of nouns and verbs 45

Memory systems for nouns and verbs 46

Using verbs and using grammar is a single ability 46

Understanding Broca’s area 47

Conclusions 60

3. OrIntrod

How

Origins of the lexical/semantic system 52

Origins of the grammatical system 54

Grammar at the origin of the executive functions 56

References 60

igins of Spatial Abilities 81 uction 81

we get oriented in the space? 83

Perceptual Constancy 83

Reference Systems 84

Cultural Differences in Visuoperceptual Abilities 85

Acquired spatial cognition disorders 86

Neuroimaging studies 89

Conclusions 92

4. Or

References 93

igins of Writing 100

Introduction 100

How did writing appear? 101

How many people can write? 106

Agraphia as a neuropsychological syndrome 107

Dysexecutive agraphia 108

Is any area in the brain specialized for writing? 108

Conclusions 117

5. Or

Nume

Numerical abilities in pre-school children 127

Conclusion 150

161

or

167

Brain activation during writing 109

Writing in different systems 110

From ‘‘agraphia’’ to ‘‘dystypia’’ 113

References 118

igins of Calculation Abilities 124 Introduction 124

rical concepts in animals 125

Development of calculation abilities in children 126

Development of numerical abilities at school 131

Calculation abilities in pre-historic man 132

Further developments of arithmetical abilities 142

The neuroscience of calculation abilities 147

References 151

6. Origins of Executive Functions 161 Introduction

What does “executive functions” mean? 162

Is there any fundamental core ability accounting f

executive functions?

Is

re-h storic l man

Tentative conclusions 184

7. Ho

Conclusions 217

8. Cu

What

Why itiv

Patterns of abilities

Cultural values

Two proposed fundamental executive functions 169

Metacognitive executive functions as an internalization

of action 173

there anything special in the prefrontal cortex? 178

Executive functions in p i a 181

Metacognitive executive functions as a cultural product 183

References 186

w we recognize other people? 202 Introduction 202

Own-species members’ recognition 203

Gender recognition 208

Emotional expression and emotional recognition 210

Individuals' recognition 212

References 218

lture and Cognitive Testing 230 Introduction 230

is culture? 231

culture affects cogn e test performance? 233

235

235

groups

Norms in different national and cultural groups 249

References 254

Familiarity 238

Language 239

Education 240

Culture minorities 246

1. Introdu

”

eption,

tion that can

e approached from different perspectives, including a neuropsychological one.

This book includes a collection of papers around the general question: How - from a

did cognition emerge in human history?

ction

“Nothing in biology makes sense

except in the light of evolution

(Theodosius Dobzhansky, 1973)

Understanding the historical evolution of cognition represents a crucial question for our

interpretations of the human specie. This is a question that has been approached since

long ago by different classical authors, including Wundt (1863/1864), James (1890),

Vygotsky (1931), Luria (1974, 1976), Leontiev (1981), and many others, and still remains

an unsettled question. As a matter of fact, during the last decades, a myriad of books and

journal papers has been published (e.g., Ardila, 1993; Cummins & Allen, 1998; Heyes &

Huber, 2000; Parker & McKinney, 1999; Tomasello, 2001; Travis, 2007; Walsh, 2001;

Woods, 1996; Zimmer, 2005) approaching this question and attempting to shed light on

the origins of complex psychological processes, such as language, complex perc

and executive functions. This is a question that in no way is easy to answer but is most

important for understanding the idiosyncrasies of our own specie. It is a ques

b

neuropsychological perspective -,

Statement of the Problem

http://www.google.com/search?tbs=bks:1&tbo=p&q=+inauthor:%22Denise+D.+Cummins%22

are human groups that are still

nomad

crasies of his brain adaptation. It

would

s guided an important proportion of the anthropological

Anthropology has striven to understand how man's living conditions were 10,000, 100,000

or 1,000,000 years ago. The Stone Age (usually divided in the Old Stone Age or Paleolithic,

and New Stone Age or Neolithic) extended until some 3,000-6,000 years ago (Hours, 1982;

Toth & Schick, 2007). Agriculture appeared some 10,000 years ago; first cities some 6,000

years ago; first civilizations about 5,000 years ago; writing has only five or six thousand

years history; and arithmetical abilities, about 6,000 years (Childe, 1936; No author, 1993;

Sampson, 1985; Toth & Schick, 2007). But most important to bear in mind, when

considering that agriculture appeared some 10,000 years ago and writing has five or six

thousand years history, it does not mean that the whole human species began to live in

cities 10,000 years ago and to use written language five or six thousand years ago. It only

means that some few people began to live a sedentary life and to use written language.

The diffusion of the changes that occurred during the last 10,000 years has been a

particularly slow process. Nowadays, for instance, there

s (regardless that the first cities were created some 10,000 years ago), and about

20% of the world population is illiterate (UNESCO, portal.unesco.org) (regardless that

writing was invented some five-six thousand years ago).

Contemporary man (Homo sapiens sapiens) has lived on the earth probably since

about 200,000 years ago (Wells, 2003; Wood, 1996; Zimmer, 2005). We can state, with

certain level of confidence, that during this time, his brain structural changes have been

minimal (Barkow, Cosmides & Tooby, 1992; Harris, 1983; Streidter, 2005). It is easy to

conclude that human brain adaptation was accomplished to survive more exactly in

Stone-Age life conditions (during about 99% of human technological history) than in those

existing nowadays. Only when departing from the analysis of these original living conditions

can we understand the specific characteristics and idiosyn

seem reasonable for any neuroscientist to raise the question: What type of

information processing abilities did the human brain become adapted for? Consequently,

which are man's basic or universal cognitive abilities?

The search for universals ha

d linguistic activity during the last decades. Anthropology and linguistics have departed

th

poken by the prehistorical man:

ik, 1957; Harris, 1983), and contemporary man speaks close to 7,000

ifferent languages (www.ethnologue.com). By comparing all these cultures and all these

ting cultures and/or living languages into consideration, similar in a

specific parameter to prehistorical cultures and/or languages, it is possible to propose how

prehist

hen comparing different human groups, and to use an existing human

p, imilar in a certain parameters to the prehistorical groups) are potentially useful,

and, a a

ct how some neuropsychological characteristics

ay have been several thousand years ago, departing from some archeological

an

from ree different approaches, attempting to reconstruct the way of life and the languages

s

1. Archeological findings are used as elements to reconstruct prehistoric ways of life.

2. By comparing existing human groups, it is possible to find some common social,

behavioral, and linguistic characteristics. Those common characteristics that eventually are

disclosed most likely already existed in prehistorical times, and probably are the result of

man's specific biological adaptation. Several thousands of different cultures have been

described (Bernatz

d

languages, some universals can be discovered (Greenberg, 1978; Haviland, 2007;

Swadesh, 1971).

3. By taking exis

orical living forms and language characteristics could have been with regard to that

particular parameter.

These three approaches (to use archeological findings, to find common

characteristics w

grou s

s a matter of fact, have been used in neuropsychological research, although in

restricted way.

1. We can attempt to reconstru

m

findings. For instance, we can study handedness in Neolithic man departing from

On the Origins of Human Cognition 10

pictorial rests (Spennemann, 1984).

2. We can search for commonality among existing groups. For example, we can

tudy aphasic language disturbances throughout different world languages, looking for

o figure out how linguistic or praxic abilities were in pre-writing societies

(e.g., A

al performance

(e.g., H

s

common characteristics and consequently, basic brain language organization (Menn &

Obler, 1990; Paradis, 2001). And finally,

3. We can study some neuropsychological variables in living human groups, similar

in a specific parameters to the prehistorical man. For instance, we can analyze illiteracy in

order to attempt t

rdila et al., 1989; Rosselli et al., 1990; Ardila et al., 2010; Lecours et al., 1987,

1988); or we can analyze constructional abilities among Stone Age-like Amazonian Indians

(Pontius, 1989).

Undoubtedly, neuropsychology has tremendously advanced in some specific areas;

for instance, in the assessment of the sequelae of brain pathology; or in the establishment

of clinical/anatomical correlations. Our fundamental and basic knowledge about the brain

organization of cognitive activity under normal and pathological conditions has significantly

advanced during the last decades thanks very specially to the use of contemporary

neuroimaging techniques (e.g., Cabeza & Nyberg, 2000; Brodmann’s interactive atlas,

www.fmriconsulting.com/ brodmann/). Nevertheless, we do not have enough understanding

about what can be understood and what can be considered as "basic cognitive abilities".

Thus, for instance, classification of spatial cognition disturbances is still very confusing and

partially contradictory (e.g., De Renzi, 1982; Rizzolatti, Berti & Gallese, 2000; Robertson,

2003). We barely have dealt with individual differences in neuropsychologic

artlage & Telzrow, 1985). And our understanding of cultural differences is, to be

optimistic, very insufficient (Ardila, 1995; Fletcher-Janzen, Strickland & Reynolds, 2000;

Helm, 1992; Uzzell, Pontón & Ardila, 2007; Pedraza & Mungas, 2008).

Some significant interest toward cultural and historical issues, however, has recently

been observed in neuropsychology. However, this interest in obtaining a better


s-linguistic analysis of aphasias; the comparison of alexias in different

writing

f socioeducational factors in neuropsychological performance (e.g.,

Ardila

This collection of papers attempts to direct the attention of behavioral neurosciences,

ook is, in consequence, multiple:

understanding of cultural and historical issues in the neuropsychology sphere is not new.

Some precursor attempts are found in literature. For instance, A.R. Luria is well-known in

neuropsychology for his contributions to the analysis of the brain organization of language;

or, his research on the prefrontal syndrome. However, his cultural approach to

neuropsychology is less recognized. Nonetheless, Luria departed from the analysis of

cultural issues (Luria, 1934, 1976; see Footnote 1) and only moved further toward

neuropsychology. Unfortunately, most of his cross-cultural research proposals in

neuropsychology (for example, the analysis of hemi-neglect syndrome in different cultural

groups; the cros

systems, etc.) never turned into concrete research programs. But his great interest

and emphasis on cultural and historical variables in neuropsychology was always reflected

in his writings.

During the last decades a significant number of papers devoted directly or indirectly

to the analysis of cultural variables on neuropsychological performance have been

recorded in literature. It could be mentioned: the bilingualism research (e.g., Albert & Obler,

1978; Dupont et al., 1992; Paradis, 1987, 2004; Vaid, 1986); the studies on illiteracy (e.g.,

Ardila et al., 1989, 2010; Lecours et al., 1987, 1988; Matute, 2000; Ostrosky et al., 1998;

Reis & Castro-Caldas,1998; Rosselli et al., 1990 ); the cross-linguistic analysis of aphasia

(e.g., Bates et al., 1987a, 1987b, 1988; Menn & Obler, 1990; Paradis, 2001); the research

about the influence o

et al., 2000; Ostrosky et al., 1985; Rosselli & Ardila, 1990); and the studies on

cultural variables on handedness (e.g., Ardila et al., 1989a; Bryden, 1987; Bryden et al.,

1993; Harris, 1990).

toward some potentially relevant historical and cultural variables in neuropsychological

performance. The purpose of this b

1 The book "Cognitive Development" was initially written in the 1930', but it was published in Russian only in 1974 with the name "About the Historical Development of Cognitive Processes". In 1976 it was translated to English with the name "Cognitive Development: Its Cultural and Social Foundations"


s in

europsychological performance.

3. To analyze how the inclusion of a historical and cultural perspective in behavioral

os ganization

f cognition. And, finally,

t it is also related to the

ability

rallel way with cultural evolution

and ec

1. To integrate some information regarding cross-cultural difference

n

2. To review some evidence about the historical origins of cognitive activity.

neur ciences can contribute to obtain a better understanding about the brain or

o

4. To propose some general guidelines for future research in the area.

Different problems are analyzed.

In the chapter “Origins of Language” it is emphasized that there are two

fundamental forms of aphasia which are linked to defects in the lexical/semantic and

grammatical systems of language (Wernicke-type aphasia and Broca-type aphasia,

respectively). Grammar correlates with the ability to represent actions (verbs) and depends

on what is known as Broca’s area and its related brain circuits, bu

to quickly carry out the sequencing of the articulatory movements required for

speaking (speech praxis). Language as a grammatical system seemingly appeared

relatively recently and seems to be exclusive to Homo sapiens.

The paper “Origins of Spatial Abilities” analyzes the development and

cross-cultural differences of spatial cognition. It is proposed that: (1) Spatial abilities are

found to be significantly associated with the complexity of geographical conditions and

survival demands; (2) spatial cognition has evolved in a pa

ological demands; and (3) contemporary city-man may be using those spatial

abilities in some new, non-existing in pre-historical times, conceptual tasks (such as

mathematics, reading, writing, mechanics, music, etc.).


ptual knowledge of written language

can be

ropsychological syndrome associated with left angular

gyrus d

In the chapter “Origins of Writing” it is argued that there is no brain area

specialized for writing, but rather that writing relies on some basic abilities that existed long

before writing was invented. Pre-writing was initially a visuoconstructive and ideomotor

ability, and only later did it become the language-related ability of writing. It is also

emphasized that most of the neuropsychological syndromes, including agraphia, were

described during the late 19th and early 20th century, but living conditions have changed

dramatically during the last 100 years. Writing no longer means only using pencil and

paper, but also includes using computer word processing programs. Writing using paper

and pencil does not require the same cognitive, motor, and spatial tasks as those required

when using a computer keyboard. Although the conce

the same, the motor activity and the spatial abilities that are used are rather

different. It can be anticipated that new neuropsychological syndromes resulting from these

new living conditions will be described in the future.

In the chapter “Origins of Calculation Abilities “ it is pointed out that counting,

departing from finger sequencing, is observed in different ancient and contemporary

cultures, whereas number representation and arithmetic abilities are found only during the

last five-six thousand years. The paper analyzes the rationale of selecting a base of ten in

most numerical systems, and the clinical association between acalculia and finger agnosia.

Finger agnosia, right-left discrimination disturbances, semantic aphasia, and acalculia is

proposed to conform a single neu

amage. It is hypothesized that acalculia, finger agnosia, and disorders in right-left

discrimination (as in general, in the use of spatial concepts) result from the disruption of

common cognitive mechanisms.

In the paper “Origins of Executive Functions ” it is proposed that the prefrontal

lobe participates in two closely related but different executive function abilities: (1)

“metacognitive executive functions”: problem solving, planning, concept formation, strategy

development and implementation, controlling attention, working memory, and the like; that

is, executive functions as they are usually understood in contemporary neuroscience; and


written

ifferent

"subsy

(2) “emotional/motivational executive functions”: coordinating cognition and

emotion/motivation (that is, fulfilling biological needs according to some existing conditions).

The first one depends on the dorsolateral prefrontal areas, whereas the second one is

associated with orbitofrontal and medial frontal areas. Current tests of executive functions

basically tap the first ability (metacognitive). Solving everyday problems (functional

application of executive functions), however, mostly requires the second ability

(emotional/motivational); therefore, these tests have limited ecological validity. Contrary to

the traditional points of view, recent evidence suggests that the human prefrontal lobe is

similar to other primates and hominids. Other primates and hominids may possess the

second (emotional executive functions) prefrontal ability, but not the first (metacognitive

executive functions) one. It is argued that metacognitive executive functions are

significantly dependent on culture and cultural instruments. They probably are the result of

the development and evolution of some “conceptualization instruments”; language (and

language as an extension of oral language) may represent the most important one.

The second executive function ability (emotional/motivational) probably is the result of a

biological evolution shared by other primates.

The question of recognizing other individuals is further analyzed ("How we

recognize other people? "). It is emphasized that not only visual, but also auditory and

even olfactory information may be involved in people recognition. Visual information is

proposed to include not only the perception of faces, but also the perception of whole-body

and gait, clothes, emotional expressions, and individual marks. Departing from clinical

observation, a model for people recognition is presented. It is hypothesized that d

stems" or "modules" may be involved in individuals' recognition: "living" versus

"nonliving", "own-species" versus "other-species", "familiar" versus "nonfamiliar", "males"

versus "females", and "individual identification" versus "emotional identification".

The chapter “Culture and Cognitive Testing” attempts to summarize the major

cultural variables affecting neuropsychological test performance. Initially, culture is defined

as the specific way of living of a human group, and further, the question “why culture affects


ting of so-called “minority groups” is analyzed in

a spec

riables in cognition, and will

ntribute to the development and strengthening of cross-cultural neuropsychology. No

oubt, cross-cultural neuropsychology represents a critical new direction of research, and

ill challenge neuropsychologists during the coming years.

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cognitive test performance seems to be as important as obtaining a large number of norms

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Finally, my sincere gratitude goes out to all the colleagues and friends who

encouraged me to write this book. I want to thank Florida International University for the

opportunity to write this book during my sabbatical year. My gratitude to Natasha

Aiguesvives for her editorial support. I sincerely hope that this collection of papers will

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ells, S. (2002). The Journey of Man: A Genetic Odyssey. Princeton: Spencer Wells,

Bioessays, 18, 945-54.

). Vorlesungen über die Menschen -und Tierseele [Lectures about

uman and Animal Psychology].

immer, C. (2005). Smithsonian Intimate Guide to Human Origins. Smithsonian Institute:

mithsonian Books

Associates.

Vygotsky, L.S. (1931). История развития высших психических функций [History of the

develop

Walsh, D. M. (2001). Naturalis

Press.

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Princeton University Press.

Wood, B (1996). Human evolution.

Wundt, W. (1863/1864

H

www.ethnologue.com

Z

S


2. Origins of Language

t

explan

ed in understanding the origins of human language (e.g.,

Bicker

view and discuss the historical origins

of lang

Introduction

For many years, the origin of human language has been a controversial topic and differen

atory proposals have been presented (e.g., Atkinson, 2011; Bickerton, 2009;

Christiansen & Kirby, 2003; Nowak & Komarova, 2001). At a certain point in history, the

debate became so complex and hot, that in 1866 the Linguistic Society of Paris banned

discussion of the origin of language, arguing that it is to be an unanswerable problem.

Contemporary research on linguistics, archeology, comparative psychology and

genetics has significantly advanc

ton, 1990; Corballis, 2002; Enard et al., 2002; Mallory, 1989; Nowak & Krakauer,

1999; Ruhlen, 1994; Scott-Phillips, 2010; Swadesh, 1967; Tallerman, 2005). Different

disciplines have contributed from their own perspective to make the human communication

system more comprehensible.

The purpose of this chapter is not to further re

uage, but to relate what is known (or supposed) on the origins of language, with

contemporary neurology and neuropsychology data, particularly in the area of aphasia.

Aphasia knowledge can potentially make a significant contribution to the understanding

about the origin and evolution of human language.

Initially, some basic neuropsychological data about language impairments in the

case of brain pathology will be presented. It will be emphasized that there are two basic


) (for a review, see Ardila, 2010).

ence, in considering language evolution these two different dimensions of language have

be recognized. Each one may have emerged at a different historical moment. Analyzing

nguage evolution can

otentially further language evolution understanding.

sia tends to

involve

linguistic operations (selecting and sequencing; i.e., language as a paradigm and language

as a syntagm) (Jacobson & Halle, 1956; Jacobson, 1971). There are also two basic types

of aphasia syndromes named in different ways (e.g., motor/sensory; anterior/ posterior;

nonfluent/ fluent; Broca-type/ Wernicke-type; encoding /decoding disorder; expressive/

receptive disorder, etc.), each one related with the disturbance of one of these two basic

language elements (lexical/semantic and grammatical

H

to

this basic distinction and including it in an interpretation about la

p

There are only two fundamental aphasia syndromes

Since the XIX it is well known that there are two major aphasic syndromes (see Table 2.1),

named in different ways, but roughly corresponding to Wernicke-type aphasia and Broca-

type aphasia (e.g., Albert et al., 1981; Bastian, 1898; Benson & Ardila, 1996; Freud,

1891/1973; Goldstein, 1948; Head, 1926; Hécaen, 1972; Kertesz, 1979; Lichtheim, 1885;

Luria, 1976; Pick, 1931; Schuell et al., 1964; Taylor-Sarno, 1998; Wilson, 1926). These two

major aphasic syndromes have been related to the two basic linguistic operations: selecting

(language as paradigm) and sequencing (language as syntagm) (Jacobson & Halle, 1956;

Jacobson, 1971; Luria, 1972/1983). Jacobson (1964) proposed that apha

one of two types of linguistic deficiency. A patient may lose the ability to use

language in two rather different ways: the language impairment can be situated on the

paradigmatic axis (selection or similarity disorder; Wernicke-type aphasia) or the

syntagmatic axis (contiguity or sequencing disorder; Broca-type aphasia).

It is important to emphasize that when Dejerine (1914) first proposed the concept of

“language zone” or “language area” in the brain, he referred indeed to three areas: Broca’s


e 2.1.).

hence, he recognized two brain areas related with spoken language and one cortical area

e it was clear that there are

o different spoken language areas in the brain: Broca’s area and Wernicke’s area, and

es of acquired language disorders.

___ _____ _____________

aradigmatic impairment syntagmatic impairment

ernicke-type Broca-type

_______________________________________________

able 2.1. Different names used to refer to the two basic aphasic syndromes.

, etc). These patients may instead fill out their discourse with

area, Wernicke’s areas, and the angular gyrus (involved in written language) (Figur

T

participating in written language. But the point is that for Dejerin

tw

consequently, there are two fundamental typ

__________________ _ ________

expressive receptive

motor sensorial

anterior posterior

no fluent fluent

p

coding impairment decoding impairment

W

_

T

The selection disorder

The selection (similarity) disorder restricts the patient’s ability to select words from the

paradigmatic axis. These patients (Wernicke-type aphasia) cannot find words that exist as

parts of the system (vocabulary). These aphasics have severely limited access to this

language repertoire system. Specific nouns tend to be inaccessible and more general ones

(cat becomes animal) take their place. These patients cannot select among alternative

names (dog, cat, fox


ircumlocutions (the clock is referred as “to know the time"). Words no longer have a

” can be referred as “animal”,

c

generic (paradigmatic) meaning for these patients, so verbal expressions tend to be

strongly contextualized, and speech becomes empty. A “dog

“it barks”, “fox”, etc.

Figure 2.1. The language zone in the brain (Dejerine, 1914.)

Luria (1972/1983) emphasized that the selection disorder can be observed at

different levels of the language, corresponding to different aphasia subtypes: phoneme

selection (aphasia acoustic agnosic), word selection (aphasia acoustic amnesic), and


sia) or

sequen

vident

that a

n defects observed in cases of Wernicke-type of aphasia.

er specific semantic category (e.g., people’s names, living things, tools,

eographical names, etc) (e.g., Harris & Kay, 1995; Goodglass et al., 1986; Lyons et al.,

2002; Warrington & Shallice, 1984) and even as specific as “medical terms” (Crosson et al.,

1997). A brain “mapping” of the memory organization of different semantic categories could

meaning selection (amnesic aphasia). By the same token, the contiguity disorder can be

observed at different levels: sequencing words (kinetic motor aphasia –Broca apha

cing sentences (dynamic aphasia –transcortical motor aphasia). Noteworthy,

different subtypes of Wernicke aphasia are frequently distinguished (e.g., Ardila, 2006).

Luria’s acoustic agnosic, acoustic amnesic, and amnesic aphasia are indeed subtypes of

the language impairment syndrome referred to as a whole as Wernicke aphasia.

In Wernicke aphasia, the lexical repertoire tends to decrease and language

understanding difficulties are evident. Wernicke aphasia patients do not fully discriminate

the acoustic information contained in speech. Lexical (words) and semantic (meanings)

association become deficient. Patients have problems in recalling the words (memory of the

words) and also in associating the words with specific meanings. Consequently, it is e

t least three different deficits underlie Wernicke-type aphasia: (1) phoneme

discrimination defects, (2) verbal memory defects, and finally (3) lexical/semantic

association deficits. Figure 2.2 presents the model proposed by Ardila (1993) to account for

the language recognitio

In Wernicke-type aphasia obviously the language defect is situated at the level of the

meaningful words (nouns). Phoneme and word selection are deficient, but language syntax

(contiguity: sequencing elements) is well preserved and even overused (paragrammatism

in Wernicke aphasia).

Nouns seem to depend on an organized pattern of brain activity. Contemporary

clinical and neuroimaging studies have corroborated that different semantic categories are

differentially impaired in cases of brain pathology. For instance, in anomia it has been

traditionally recognized that naming body-parts, external objects and colors depend (and

are altered) upon the activity of different brain areas (Hécaen & Albert, 1978). It has also

been found that finer distinctions can be made with regard to naming defects, which can be

limited to a rath

g


be supposed.

ear

Verbal acoustic short -term memory

Verbal -acoustic recognition (lexical)

Long -term memory for features

Short - term memoryfor features

Long -term memory for phonemes

Primary auditoryanalysis

Frequency Šintensity recognition Features recognition Phoneme recognition

Short - term memoryfor phonemes

Verbal -acoustic long Šterm memory

Associations(visual, tactile, etc)

Semantic Recognition

A B C

D

E

F G

H

I

J

K

L

M

N

Categorical perceptionn

Categorical perception

language recognitionlevel II

Categorical perception

language recognitionlevel I

l-acoustic memory defects (acoustic-amnesic or

ernicke aphasia type II), and semantic association defects (amnesic, nominal or

xtrasylvian sensory aphasia).

language recognitiolevel III

Figure 2.2. Diagram model for language recognition proposed by Ardila (1993).Three

levels of language recognition potentially impaired in Wernicke-type aphasia can be

distinguished: phonemic (categorical perception level I), lexical (categorical

perception level II), and semantic (categorical perception level III). Three different

sub-syndromes can be found: phonemic discrimination defects (acoustic-agnosic or

Wernicke aphasia type I), verba

W

E


nderstand which one could

The sequencing disorder

Broca-type of aphasia represents the clinical syndrome characterized by impairments in the

sequencing process (syntagmatic axis defect). It is usually recognized that Broca aphasia

has two different distinguishing characteristics: (a) a motor component (lack of fluency,

disintegration of the speech kinetic melodies, verbal-articulatory defects, etc., that is usually

referred as apraxia of speech); and (b) agrammatism (e.g., Benson & Ardila, 1996; Luria,

1976; Goodglass, 1993; Kertesz, 1985). If both defects are simultaneously observed (i.e.,

they are very highly correlated), it simply means they both are just two different

manifestations of a single underlying defect. It is not easy to u

be the single factor responsible for these two clinical manifestations; but it may be kind of

an "inability to sequence expressive elements" (Figure 2.3).

Broca aphasia

Factor

ability to sequence expressive elements ?

Apraxia of speech Agrammatism


Figure 2.3. A single factor (probably the ability to sequence expressive elements)

can un

ge grammar (Poizner et., 1987). Probably, the lack of verbal articulatory

ormal development is necessarily associated with a lack of normal grammatical

evelopment.

t types of aphasia (e.g., Luria, 1966, 1970) and suggested a

eventh one. Only in his later writings (e.g., Luria, 1976) he overtly referred to seven

ifferent types of aphasia.

derlie the two disturbances observed in Broca aphasia (Ardila & Bernal, 2007).

A single common factor underlying both defects should be assumed. Broca's area,

most likely, is not specialized in producing language, but in certain neural activity that can

support not only skilled movements required for speech, but also morphosyntax. It is

interesting to note that deaf-mute subjects (who, in consequence have never produced

verbal articulatory movements) present a virtually total impossibility to learn, understand,

and use langua

n

d

Other aphasia syndromes

Some aphasic syndromes can eventually be considered as variants of the Broca and

Wernicke aphasia. For instance, amnesic or anomic or nominal aphasia (usually due to

damage in the vicinity of Brodmann’s area 37) (Hécaen & Albert, 1978; Head, 1926; Luria,

1976) can be interpreted as a subtype of Wernicke aphasia in which the semantic

associations of the words are significantly impaired (see Figure 2.4). Luria himself during a

long time was unsure if amnesic aphasia should be regarded an independent aphasia

syndrome; or rather, it should be considered simply as a subtype of the “sensory aphasia”

(in addition to the acoustic-agnostic and acoustic-amnesic subtypes). During a long time,

Luria referred to six differen

s

d


reted

s a paradigmatic disturbance situated at the level of semantic recognition.

Figure 2.4. Amnesic or nominal or extrasylvian sensory aphasia can be interp

a

Some other aphasic syndromes can be interpreted as language disturbances due to

a more general underlying disorder. For instance, extrasylvian (transcortical) motor aphasia

associated with left convexital prefrontal damage could be interpreted as an executive

function defect specifically affecting the language use. The ability to actively and

appropriately using the language (pragmatics) appears impaired while the phonology,

lexicon, semantics, and grammar are preserved. Simply speaking, the question is: should

the ability to correctly use language be regarded as a linguistic ability (i.e., cognitive ability)

as executive function ability?(i.e., metacognitive ability). It does not seem difficult to argue

that the ability to correctly use the language can be interpreted as an executive function

and as a metacognitive ability rather than a purely linguistic ability. Some rationales to

support this interpretation are: (1) It could be argued that in extrasylvian (transcortical)


cus of the damage from posterior frontal to polar

and/or

deomotor

apraxia

iting difficulties (apraxic agraphia);

motor aphasia there is a defect in verbal initiative rather than in language knowledge

(Kleist, 1934). (2) Some authors (Luria, 1976, 1980) have emphasized that this type of

aphasia shares the general characteristics of the prefrontal (i.e., dysexecutive) syndrome

but specifically with regard to the verbal processes. That means it is the prefrontal

(dysexecutive) syndrome affecting the verbal processes. (3) Further, the language defect in

extrasylvian (transcortical) motor aphasia does not affect the language understanding, and

the fundamental linguistic processes are preserved (Berthier, 1999). And finally, (4) it could

be argued that the prefrontal cortex does not participate in basic cognition but in

metacognition (e.g., Ardila & Surloff, 2010). Extrasylvian (transcortical) motor aphasia could

indeed be referred as “dysexecutive aphasia”. Some authors have interpreted extrasylvian

motor aphasia in a similar way (e.g., Luria, 1976, 1980). Alexander (2006) suggested that

transcortical motor aphasia could be more accurately defined as an executive function

disorder than as an aphasia. He proposed that the progression of clinical disorders from

aphasia to discourse impairments can be interpreted as a sequence of procedural

impairments from basic morpho-syntax to elaborated grammar to narrative language,

correlated with a progression of the fo

lateral frontal to medial frontal.

Conduction aphasia, on the other hand, usually has been interpreted as a

disconnection syndrome (e.g., Damasio & Damasio, 1980; Geschwind, 1965; Wernicke,

1874) usually due to an impairment in the arcuate fasciculus and sporadically in an indirect

pathway passing through inferior parietal cortex (Catani et al., 2005) (Figure 2.5).

Alternatively, conduction aphasia has also been interpreted as a segmentary i

(e.g., Ardila & Rosselli, 1990; Brown, 1972, 1975; Luria, 1976, 1980).

Usually it is recognized that conduction aphasia has three fundamental and five

secondary characteristics; so-called secondary characteristics are frequently but not

necessarily found in conduction aphasia (Benson et al., 1973; Benson & Ardila, 1996). The

three basic characteristics are: (1) fluent conversational language; (2) almost normal

comprehension; (3) significant impairments in repetition. Secondary characteristics include,

(1) defects in naming; (2) reading defects; (3) variable wr


) ideomotor apraxia; (5) neurological abnormalities.

(4

e Wernicke’s and Broca’s areas, due to an interruption of the arcuate fasciculus.

at, that means that language repetition cannot be considered as a primary

Figure 2.5. Conduction aphasia frequently is interpreted as a disconnection between

th

This description of conduction aphasia clearly recognizes that spontaneous language

production and language understanding are significantly preserved. In consequence, some

mechanism required for the correct language repetition is abnormal, but the knowledge of

the language itself (phonology, lexicon, semantics, and grammar) is not impaired. Should

conduction aphasia be interpreted as a primary aphasic syndrome? Obviously, if some

animals can repe


nguistic ability.

a direct connection between Wernicke’s and

roca’s area, as illustrated in Figure 2.6.

li

Bernal and Ardila (2009) pointed out that as a matter of fact the arcuate fasciculus

does not connect Wernicke’s area with Broca’s area (BA44), but more exactly with the

premotor area (BA6); hence, there is not

B

labeled BA6, an area with premotor functions

aken from Bernal & Ardila, 2009).

Figure 2.6. Recent findings suggest that there is not a direct connection between

Wernicke’s and Broca’s areas, but there is a relay station located in the precentral

gyrus, represented here by the circle

(T

Conduction aphasia is not really a primary form of aphasia but rather a secondary

(or “peripheral”) defect in language affecting a specific language ability (i.e., the ability to


repeat). The language itself is not impaired, but rather the ability to reproduce the auditory

information that is heard aloud is impaired. Of course, this is a most important ability used

not only to develop but also to correctly use language (moreover, the correct visual-

perceptual recognition of the written information is a most important ability required not only

for lea

aphasi

e it appropriately because of executive control impairments (dysexecutive

phasia).

___________________________________________________________________________

___________________________________________________________________________

rimary (central) aphasias Language system impaired

Wernicke-type aphasia (fluent aphasia) level

Semantic level

Broca-type aphasia (non-fluent aphasia) pressive elements at syntactic and

__________________________________________________________________________

rning to read but also for correctly accessing the written information).

Jakobson (1964) suggested a similar distinction when proposed that in aphasia,

language could be either “disintegrated” or just “limited” (disintegration vs. limitation in

a). Obviously, in conduction aphasia language is limited, not really disintegrated.

Tabla 2.2. presents the aphasia classification proposed by Ardila (2010). A major

distinction in aphasia can be established between primary language disturbances (central

aphasias), and secondary language disturbances resulting from ‘‘peripheral’’ impairments

(secondary or ‘‘peripheral’’ aphasias). Sometimes language is not impaired, but the patient

cannot us

a

_

Type Impairment _

P

Phonological

Lexical level

Sequencing ex

phonetic level

_


econdary (peripheral) aphasias Mechanisms of production impaired

Conduction aphasia ction (or segmentary ideomotora verbal

apraxia)

SMA aphasia nd maintain voluntary speech

__________________________________________________________________________

ysexecutive aphasia Language executive control impaired

__________________________________________________________________________

tive (extrasylvian or transcortical

otor) aphasia is also included (Ardila, 2010).

hree stages in language development

language

egan?” Different steps in language development can be proposed, at least:

S

Disconne

To initiate a

production

_

D

Extra-Sylvian (transcortical) motor aphasia Executive control of language

_

Tabla 2.2. Only two primary aphasic syndromes are recognized: Wernicke-type

aphasia (fluent aphasia) and Broca-type aphasia (non-fluent aphasia). Two

secondary aphasia syndromes are included (conduction aphasia and aphasia of the

supplementary motor area); finally, a dysexecu

m

T

The question “When language began?” could be rephrased as the question “How

b

(1) Initial communication systems using sounds and other types of information –such


r to the communication systems observed in other animals, including

nonhuman primates.

ge development, observed in children around the age 1 to

1.5 years of age (Hoff, 2003).

a system of relations among the

words (language as a syntagm: grammatical system).

itial communication systems

nhuman primates in natural environments can use some

commu

as gestures, etc, simila

(2) Primitive language systems using combined sounds (words) but without a

grammar (language as lexical/semantic system). This type of language could be similar to

the holophrasic period in langua

(3) Communication systems using grammar (language as grammatical system).

During child’s language development, it is observed that the use of grammar is found after

the holophrasic period. It simply means that it is a more advanced and complex stage. By

the end of the second year, children begin to combine words into simple sentences. Initially,

sentences represent a telegraphic speech (around 24-30 months of age), including two-

word utterances in which connecting elements are omitted (e.g., “other dog", “child eat”)

(Hoff, 2003). It means, language initially emerges as a system of words (language as a

paradigm: lexical/semantic system), and only later as

In

It is easy to assume that at the beginning of the human language, communication systems

were similar to the communication systems found in nonhuman primates. It is known that

chimpanzees and other no

nication strategies.

Chimpanzees employ a variety of gestures and facial expressions to communicate

and keep in touch with each other. They possess a simple repertoire of noises and

postures (body language) that can be used in different contexts with specific


chimpa

ns to communicate (Gardner & Garner, 1979; Limber

1982;

y often abandon the order of phrases they have learned and the order

is rathe

re is not a grammatical relationship and hence no grammar is

involve

(language as syntagm) even after intensive

and co

communication purposes. Observations have been collected in different environments,

including natural environments and captive groups in human-controlled environments

(McCrone, 1991). Chimpanzees make use of simple gestures, make facial expressions and

produce a limited amount of vocalizations. Compared to humans, chimps only produce

about twelve different vocalizations. In captive conditions and under human training,

nzees can learn some artificial languages and close to about 200 “words” (symbols).

Different attempts have been made to teach non human primates to use a more

complex communication system. Initially, Hayes and Hayes (1952) trained the chimp Vicki.

She became able to produce only four different sounds in six years! (“mom," "pa," "cup,"

and "up"). Other chimps and gorillas have also participated in communication training

programs: Nim and Koko used signs; Sara used plastic chips; Lana, Sherman, and Austion

manipulated combinations of butto

Patterson & Linden, 1981).

Regardless of the relatively large amount of meaningful elements that chimpanzees

can learn, they fail in developing sequencing of elements (grammar). Kanzi learned to use

around 200 symbols on a portable electronic symbol board. While chimpanzees can learn

to order their symbols to get what they want, it is not clear that they have mastered syntax

(Mitani, 1995; Savage-Rumbaugh & Lewin, 1994). The reason is that when they initiate

communication, the

r random.

There have been occasional reports of chimpanzees signing new combinations of

words in response to new situations. Washoe, for example, once was in a boat on a pond

when she encountered her first duck. She signed 'water bird' (Terrace, 1979). This could be

a new compound noun or it could be two separate responses to the water and a bird. But

between two nouns, the

d in 'water bird'.

In conclusion, there is not convincing evidence that chimpanzees and other

nonhuman primates can learn language syntax

ntrolled training.


ies certainly requires a brain notoriously more

advanc

y have been used even in

ontemporary literature. Some hypotheses are (Yule, 1996):

. It means that words are created

departing from onomatopoeias (bow-wow hypothesis).

with interjections, emotive cries, and emotional expressions

(Pooh-pooh hypothesis).

that gestures represent the most important element in creating human

language.

The question becomes how can this type of simple communication system found in

subhuman primates in natural conditions (i.e., to use some few vocalizations, gestures and

facial expressions) be further developed into contemporary human language? Certain

mechanisms potentially could be used; e.g., words can be created departing from

onomatomepias, emotional expressions, etc. Indeed, a diversity of mechanisms has been

proposed throughout history to account how human words emerged. It means that different

strategies could potentially be useful to create words. This is an ability that is not found in

nonhuman primates. Using these strateg

ed than the chimpanzee’s brain.

During the 19th century different hypotheses were presented in an attempt to explain

the origin of language from the lexical point of view. Jespersen (1922) referred to such

hypotheses using some unusual names as a way of deriding the hypotheses as simplistic

speculation. However, these names became popular and the

c

1. Language began as imitations of natural sounds

2. Language began

3. Gestures are at the origin of language, and body movement preceded language.

Oral language represents the use of oral gestures that began in imitation of hand gestures

that were already in use for communication (ta-ta hypothesis). Recently, Corballis (2002)

has argued

4. Language arose in rhythmic chants and vocalisms uttered by people engaged in


sistance or cooperation accompanied by appropriate

gestures (Yo-he-ho hypothesis).

gan with the easiest syllables attached to the most significant objects

(mama ypothesis).

back vowels. This is often

ferred to as phonetic symbolism (ding-dong hypothesis).

ughter, cooing,

courtship, emotional mutterings and the like (The sing-song hypothesis)

identity (here I am!) and belonging (I’m with you!) (contact

theory) (hey you hypothesis).

tic symbolism is particularly

useful in the creation of adjectives (qualities of the objects).

communal labor. Language began as rhythmic chants, perhaps ultimately from the grunts

of heavy work or related with as

5. Language be

h

6. It has been pointed out that there is a certain correspondence between sounds

and meanings. Small, sharp, high things tend to have words with high front vowels in many

languages, while big, round, low things tend to have round

re

7. It has been also suggested that language comes out of play, la

8. Considering that there is a need for interpersonal contact, language may have

began as sounds to signal both

All these hypotheses may be partially true, and all these factors may have

contributed to the creation of new words. As a matter of fact, these hypotheses attempt to

explain how the initial communication systems (observed in nonhuman primates) evolved to

the second stage in language evolution: the development of a lexical system, which

potentially can be transmitted to offspring. But they do not account for the development of

grammar. These mechanisms for creating new words continue being useful in the

contemporary world. For instance, onomatopeias continue representing a mechanism in the

creation of new words (e.g., the ping-pong game). The phone


he function of noises (grunts) in human communication

peakers

f other languages, but others seem idiosyncratic of Spanish-speaking people.

econd stage: Lexical/semantic

ssure

of the

T

No mention about the function of noises (grunts) in human everyday communication is

readily available. As noted above, noises represent a basic communication strategy in

chimpanzees, and noises have continued playing a communication function throughout

human history. It is evident that people in everyday life use a diversity of noises to say

“yes”, “no”, to express different emotions, to communicate with animals (e.g., “come here”,

“go away”), etc. These noises are close to interjections, and sometimes become real

interjections (e.g., “ooph!”). Even though there is not a “dictionary” of noises, the author of

this paper has been able to identify over 30 different noises commonly used in

contemporary Spanish language. Some of these noises seem understandable by s

o

S

Bickerton (1990) developed the idea that a protolanguage must have preceded the full-

fledged syntax of today’s discourse. Echoes of this protolanguage can be seen, he argued,

(1) in pidgin languages, (2) in the first words of infants, (3) in the symbols used by trained

chimpanzees, and (4) in the syntax free utterances of children who do not learn to speak at

the normal age. Bickerton (2009) considers that such a protolanguage existed already in

the earliest Homo (about 2.3 to 2.4 million years), and was developed due to the pre

behavioral adaptations faced by Homo habilis (2.3 to 1.4 million years ago).

What made up these original words? Again, the analogy with the child’s initial

vocabulary can be taken. (1) They were articulatory easiest to produce, most likely using

those phonemes regarded as “universal” (e.g., /p/, /a/). (2) They contained a simple syllable


“nouns” (real objects) even

though

ions. But the production of these

opposi

ed in part during hominoid evolution and not in a single shift during human

evoluti

e initial meaning sounds and approximately, how the initial

structure (consonant-vowel) that may have been repeated (e.g., papapa). In this regard,

they were similar to the infantile words. (3) They were mostly

they obviously did not have a grammatical category.

To move from grunts, onomatopoeias, and emotional expression to words requires

the progressive development of a series of oppositions. According to Jacobson (1968) the

most basic one is the opposition between vowels and consonants. The second most

important one is between oral and nasal articulat

tions requires some anatomical adaptations.

Human articulatory ability has been related to the specific position and configuration

of the larynx. The human larynx descends during infancy and the early juvenile periods,

and this greatly contributes to the morphological foundations of speech development. This

developmental phenomenon is frequently believed to be unique to humans. However,

Nishimura (2003; Nishimura et al., 2005) demonstrated that chimpanzees’ larynges also

descend during infancy, as in human infants. This descent was completed primarily through

the rapid descent of the laryngeal skeleton relative to the hyoid, but it was not accompanied

by the descent of the hyoid itself. The descent is possibly associated with developmental

changes of the swallowing mechanism. Moreover, it contributes physically to an increased

independence between the processes of phonation and articulation for vocalization. Thus,

the descent of the larynx and the morphological foundations for speech production must

have evolv

on.

Several authors have attempted to find universal language characteristics, and even

to reconstruct extinct languages (e.g., Greenberg, 1978; Hagége, 1982 ; Van den Berghe

1979) such as the Indo-European (Anderson, 1973; Lehmann, 1974; Martinet, 1975;

Shevoroshkin, 1990), whose last speaker passed away over 10,000 years ago.

Furthermore, examples of which ones could have been the initial words in human language

have been proposed. Swadesh (1971) refers to the communality existing in some words

across the world. Although we cannot be sure which were the initial words used by

humans, there are clues about th


ords may have been formed.

hird stage: Grammar

may be similar to the mechanism observed in children during

nguage development.

Suppose that we have two lexical units:

-animal - fruit

elements: animal eats

fruit; a

(8) Actions (e.g., drink), (9) Natural phenomena (e.g., sun), and (10) Colors

(e.g., r

w

T

What was the crucial leap for the development of grammar? (i.e., syntagmatic dimension of

the language). Obviously grammar was initially simple, and “sentences” contained only two

words. How to link two words to create new higher level unit (syntagm)? Further, how to

mark the relationship between the two words? The mechanism has to be the simplest one,

and it is not unlikely that it

la

Different relations between these two words can exist; but the relationship requires

an action (verb); it means that there is an interaction between both

nimal has fruit, animal receives fruit; animal likes fruit, etc.

In consequence, before creating a syntagmatic relationship between the words,

different word categories have to be separated (e.g., objects and actions). According to the

Swadesh word list (1952, 1967), the following categories are found across different

languages, and may represent the initial word categories: (1) Grammatical words (e.g.,

I/me), (2) Quantifiers (e.g., All), (3) Adjectives (e.g., Big), (4) Human distinctions (e.g.,

person), (5) Animals (e.g., fish), (6) High frequency elements (e.g., tree), (7) Body parts

(e.g., hair),

ed).

For creating a phrase, only two types of elements are really required: nouns

(nominal phrase) and verbs (verbal phrase). When putting together two words

corresponding to two different classes (e.g., animal sleep), there is already a syntagm and

grammar that has appeared. In childhood language it is observed that words corresponding


ages, such as Russian). “Mom dad” is not a phrase, but “mom big” is a

primitiv

s

rammar could be described by a small set of functional relationships between words:

mmy sock

8. 'demonstrative + object' there car

er level unit (syntagm). One of the words has to be a noun; the

other u

to two different classes are combined such as, “big dog”, “food good”, “dad gone”. They

contain a grammar because the words belong to two different classes. In the first two

examples, there is an existence verb (to be) that is omitted (as currently observed in some

contemporary langu

e sentence.

Brown (1973) found that the majority of the utterances at the beginning of the child’

g

1. 'agent + action' baby kiss

2. 'action + object' pull car

3. 'agent + object' daddy ball

4. 'action + location' sit chair

5. 'object + location' cup table

6. 'possessor + possession' mo

7. 'object + attribute' car red

So, the crucial point in emerging grammar is not the extension of the vocabulary.

What really is crucial is to have words corresponding to different classes that can be

combined to form a high

sually is a verb.

Hence, the problem becomes how do verbs appear? Creating nouns does not seem

so complicated using the hypothesis mentioned above (e.g., nouns can be created

departing from onomatopoeias, etc). Verbs, on the other hand, can be created departing


y the frontal areas have to

e involved in this second type of association (kiss as a verb).

rain representation of nouns and verbs

eft frontal damage and

Broca

eanings and sensory-motor

from the nouns, but with the meaning of an action (e.g., baby kiss). Action usually means

moving, doing, executing, not simply perceiving and associating with some visual (or

auditory or tactile) information. “Kiss” can be associated with some sensory information,

and obviously the temporal, parietal and occipital brain areas have to participate (kiss as a

noun). “Kiss” can also be associated with an action, and obviousl

b

B

It has been observed that choosing verbs and nouns clearly depends on different brain

area activity, and naming objects and actions are disrupted in cases of different type of

brain pathology. While speaking or thinking in nouns increased activity is observed in the

temporal lobe, while speaking or thinking verbs activates the Broca frontal area (Raichle,

1994). By the same token, impairments in finding nouns are associated with temporal lobe

pathology, whereas impairments in finding verbs is associated with l

aphasia (Ardila & Rosselli, 1994; Damasio & Tranel, 1993)

Naming actions activates the left frontal operculum roughly corresponding to the

Broca’s area (Damasio et al., 2001). The neural correlates of naming concrete entities such

as tools (with nouns) and naming actions (with verbs) are partially distinct: the former are

linked to the left inferotemporal region, whereas the latter are linked to the left frontal

opercular and left posterior middle temporal regions (Tranel et al., 2005). Furthermore, the

pattern of brain activation when processing verbs seems similar across languages, at least

in Spanish/English bilinguals (Willms et al., 2011). However, understanding action verbs

does not rely on early modality-specific visual or motor circuits. Instead, word

comprehension relies on a network of amodal brain regions in the left frontal, temporal, and

parietal cortices that represent conceptual and grammatical properties of words (Bedny &

Caramazza, 2011). Supposedly, interactions between word m


xperiences occur in higher-order polymodal brain regions.

emory systems for nouns and verbs

of the words),

gramm

x.

rocedural memory is related with frontal/subcortical circuitries (Tulving et al., 2004).

sing verbs and using grammar is a single ability

e

M

Two major memory systems are frequently distinguished in contemporary memory

literature: declarative memory (divided into semantic and episodic or experiential) and

procedural memory (Tulving et al., 2004). It has been suggested that the lexical/semantic

and grammar aspects of the language are subserved by different neuroanatomic brain

circuitries and depend upon these two different memory systems (Fabbro, 1999, 2001;

Paradis, 2004; Ullman, 2001; 2004). Whereas lexical/semantic aspects of the language

depend on a declarative semantic memory (knowledge about the meaning

ar depends on a procedural memory.

The lexical/semantic aspect of the language is explicitly learned and represents a

type of knowledge we are aware of (declarative memory). It depends on retro-rolandic

cortical structures and the hippocampus. Grammar (language sequences, contiguity) is

acquired incidentally. Procedural memory for grammar supposes implicit language

knowledge. Procedural grammatical learning is related to the execution of sequences of

elements (skilled articulatory acts and grammar) used for speaking but also for synta

P

U

Broca’s area damage results in a defect in grammar and also in an inability to find verbs. In

consequence, brain representation of actions and brain representation of grammar is

coincidental. Using verbs and using grammar depends upon the very same type of brain

activity and both are simultaneously disrupted in cases of Broca aphasia. It can be

conjectured that verbs and grammar appeared almost simultaneously in human language;


g verbs, using grammar, and rapidly sequencing movements with the

articula

sentation of actions and understanding/using verbs seems

be closely related abilities.

nderstanding Broca’s area

or rather, they are the two sides of the same medal. Furthermore, grammar is associated

with oral praxis skills (i.e., agrammatism and apraxia of speech appear simultaneously in

Broca aphasia), and hence, all three have to appear simultaneously in the evolution of

human language: usin

tory organs.

However, there is a departing condition for using verbs, namely, the ability to

internally represent actions. That is, to interiorize the actions. The obvious question is: can

Broca aphasia patients internally represent actions? Although specific research on this

question is not readily available, the answer seems to be no. Some observations point to a

deficit in internally representing actions in Broca aphasia. For example, Ardila and

Rosselli’s (1994) patient had to make the concrete action to retrieve the corresponding

verb. Thence, the internal repre

to

U

In the last decade there has been a significant interest in re-analyzing the function of

Broca’s area (e.g., Grodzinsky & Amunts, 2006; Hagoort, 2005; Thompson-Schill, 2005).

So-called Broca’s area includes the pars opercularis (Brodmann’s area- BA- 44) and

probably the pars triangularis (BA45) of the inferior frontal gyrus (Foundas, 1998) (see

Figure 2.7). BA45 probably is more ‘‘cognitive’’ than BA44, which seems to be more motor,

more phonetic. From the traditional point of view, Broca’s area corresponds to BA44, but

several contemporary authors also include BA45. In the traditional aphasia literature it was

assumed that damage in the Broca’s area was responsible for the clinical manifestations

observed in Broca’s aphasia. Only with the introduction of the CT scan did it become

evident that the damage restricted to the Broca’s area was not enough to produce the

‘‘classical’’ Broca’s aphasia; extension to the insula, lower motor cortex, and subjacent


ls (Fecteau et al., 2011) and is active during speech perception

aden et al., 2011).

subcortical and periventricular white matter is also required (Alexander et al., 1990).

‘‘Broca’s area aphasia’’ (‘‘minor Broca’s aphasia’’) is characterized by mildly non-fluent

speech, relatively short sentences and mild agrammatism; phonetic deviations and a few

phonological paraphasias can be observed (Mohr, et al., 1978); some foreign accent can

also be noticed (Ardila et., 1988). Interestingly, electrical stimulation of Broca's area

enhances implicit learning of an artificial grammar (de Vries et al., 2010) and can also

modulate naming skil

(V

igure 2.7. Map illustrating the Brodmann’s areas (BA).

F

Simultaneously including both BA44 and BA45 in Broca’s area is problematic. BA 44

is a premotor dysgranular area, whereas BA45 has a granular layer IV and belongs to the

heteromodal prefrontal lobe (granular cortex) (Mesulam, 2002). So, from a

cytoarchitectonic point of view, BA 44 and BA 45 are quite different. BA 44 is a premotor


ing memory, suggesting that there may be more than a single

function of Broca’s area.

area whereas BA 45 corresponds to the prefrontal cortex. From the aphasia perspective,

some authors have referred to different clinical manifestations associated with damage in

BA 44 (Broca-type aphasia) and BA 45 (transcortical motor/dynamic aphasia) (e.g., Luria,

1976). Broca’s area is, more than likely, involved in different language and language related

functions (Fink et al., 2006). Some authors have pointed out that indeed Broca’s area is a

collective term that can be fractionated in different sub-areas (Lindenberg et al., 2007).

Hagoort (2005, 2006) refers to the ‘‘Broca’s complex’’, including BA44 (premotor), and also

BA45 and BA47 (prefrontal cortex). He argues that Broca’s complex is not a language-

specific area, and it becomes active during some nonlanguage activities, such as mental

imagery of grasping movements (Decety et al., 2004). Functional defined sub-regions could

be distinguished in the Broca’s complex: BA47 and BA45 are involved in semantic

processing, BA44, BA45, and BA46 participate in syntactic processing, and BA44 is

involved in phonological processing (Heim et al., 2008; Sahin et al., 2009). Hagoort (2005)

proposes that ‘‘the common denominator of the Broca’s complex is its role in selection and

unification operations by which individual pieces of lexical information are bound together

into representational structures spanning multiword utterances’’ (p. 166). Its core function

is, consequently, binding the elements of the language. Thompson-Schill (2005) analyzed

the different deficits observed in cases of damage in the Broca’s area: articulation, syntax,

selection, and verbal work

Thompson-Schill (2005) analyzed the different deficits observed in cases of damage

in the Broca’s area: articulation, syntax, selection, and verbal working memory, suggesting

that there may be more than a single function of Broca’s area. The author proposes a

framework for describing the deficits observed in different patients. The proposed

framework suggests that Broca’s area may be involved in selecting information among

competing sources. Fadiga et al. (2006) speculates that the original role played by Broca’s

area relates to generating/extracting action meanings; that is, organizing/ interpreting the

sequence of individual meaningless movements. Ardila and Bernal (2007) conjectured that


d with a general cognitive

control mechanism for the syntactic processing of sentences.

also include portions of the right

cerebral hemisphere (Grodz

ne major factor in Broca’s aphasia relates to impairment in verbal

working memory.

the central role of Broca’s area was related to sequencing motor/expressive elements.

Novick et al. (2005) consider that the role of Broca’s area is relate

Grodzinsky (2000, 2006) has presented an extensive analysis of the role of Broca’s

area. He proposed that most syntax is not located in Broca’s area and its vicinity

(operculum, insula, and subjacent white matter). This brain area does have a role in

syntactic processing, but a highly specific one: it is the neural home to receptive

mechanisms involved in the computation of the relation between transformationally moved

phrasal constituents and their extraction sites (syntactic movement). He further assumes

that Broca’s area is also involved in the construction of higher parts of the syntactic tree in

speech production. Interestingly, blood flow in Broca’s area increases when participants

process complex syntax (Caplan et al., 2000). Santi and Grodzinsky (2007) also recognize

its role in working memory related with a specific syntactic role in processing filler–gaps

dependency relations. Syntax is indeed neurologically segregated, and its components are

housed in several distinct cerebral locations, far beyond the traditional ones (Broca’s and

Wernicke’s regions). A new brain map for syntax would

insky & Friederici, 2006).

Haverkort (2005) emphasizes that a clear distinction should be established between

linguistic knowledge and linguistic use. Patients with Broca’s aphasia have a limitation in

the use of grammar, but their grammatical knowledge is available. Broca’s aphasia patients

present a simplified syntax and phrases are usually short. They select simpler syntactic

structures that are less complex because they impose a lesser burden on working memory.

In consequence, o

In summary, regardless that expressive language disturbances have been

associated for over a century with damage in the left inferior frontal gyrus (later known as

‘‘Broca’s area’’), currently there is incomplete agreement about its limits and its specific


plain language

isturbances in so-called Broca’s aphasia, as summarized in Table 2.3.

______________________________________________________________________________

______________________________________________________________________________

05

7

s

______________________________________________________________________________

able 2.3. Different proposals about the role of Broca’s area.

n; lexical/semantic system) and

syntag

ge as a lexical/semantic

system

w

ords. Noises and gestures are actively used nowadays in everyday communication.

functions in language. Different proposals have been presented to ex

d

_

Function Reference

_

Binding the elements of the language Haverkort, 2005

Selecting information among competing sources Thompson-Schill, 20

Generating/extracting action meanings Fadiga et al., 2006

Sequencing motor/expressive elements Ardila & Bernal, 200

Cognitive control mechanism for syntactic processing sentence Novick et al., 2005

Construction higher parts syntactic tree in speech production Grodzinsky, 2000, 2006

Verbal working memory Haverkort, 2005

_

T

As emphasized above, language activity depends on two discrete brain areas (so-

called Wernicke’s and Broca’s areas). Damage in these two brain regions results in

disturbances in language as a paradigm (similarity: selectio

m (contiguity: combination; grammatical system).

At what moment in human history did the first and the second aspect of language

emerge? There is not a simple answer, but obviously langua

appeared before language as a grammatical system.

Pre-human communication systems continue playing a role in contemporary human

communication. Onomatopoeias continue representing a source for the creation of ne

w


rigins of the lexical/semantic system

the temporal lobe was a crucial area in developing a complex lexical/semantic

system

ecause this asymmetry was

observ

O

Paleoneurology (study and analysis of fossil endocasts) can also significantly contribute to

the understanding of the origins of the language. How did the brain areas participating in

human lexical/semantic knowledge (i.e., temporal lobes) evolve? In monkeys, the temporal

lobes are involved in recognizing the sounds and calls of their own species (Rauschecker

et al., 1995; Taglialatela et al., 2009; Wang et al., 1995; Wollberg & Newman, 1972), and

obviously

.

Gannon et al (1998) observed that the anatomic pattern and left hemisphere size

predominance of the planum temporale, a language area of the human brain, are also

present in chimpanzees. They found that the left planum temporale was significantly larger

in 94 percent of chimpanzee brains examined. Hence, the crucial lexical/semantic

difference between humans and chimpanzees cannot be related to the planum temporale.

By the same token, it has been observed that anatomical temporal lobe asymmetries

favoring the left hemisphere are found in several Old and New world monkey species

(Heilbroner & Halloway, 1988). Development of a human lexical/semantic communication

system cannot be related with the temporal lobe asymmetry, b

ed long before the beginning of the human language.

Hopkins and Nir (2010) examined whether chimpanzees show asymmetries in the

planum temporale for grey matter volume and surface area in a sample of 103

chimpanzees from magnetic resonance images. The results indicated that, overall, the

chimpanzees showed population-level leftward asymmetries for both surface area and grey

matter volumes. Furthermore, chimpanzees that prefer to gesture with their right-hand had

significantly greater leftward grey matter asymmetries compared to ambiguously- and left-

handed apes. Development of a human lexical/semantic communication system in


modern human language and before our divergence from the last

commo

consequence cannot be related to the temporal lobe asymmetry, because this asymmetry

is observed long before the beginning of the human language. This asymmetry seems to be

related with a left temporal lobe specialization for intra-specific communication system.

Spocter et al. (2010) affirm that leftward asymmetry of Wernicke's area originated prior to

the appearance of

n ancestor.

Nonetheless, differences can be related with the temporal lobe volume. Rilling et al.

(2002) analyzed the volume of the temporal lobe in different primates. Whole brain, T1-

weighted MRI scans were collected from 44 living anthropoid primates spanning 11

species. The surface areas of both the entire temporal lobe and the superior temporal

gyrus were also measured, as was temporal cortical gyrification. Allometric regressions of

temporal lobe structures on brain volume consistently showed apes and monkeys to scale

along different trajectories, with the monkeys typically lying at a higher elevation than the

apes. Within the temporal lobe, overall volume, surface area, and white matter volume

were significantly larger in humans than predicted by the ape regression lines. The largest

departure from allometry in humans was for the temporal lobe white matter volume which,

in addition to being significantly larger than predicted for brain size, was also significantly

larger than predicted for temporal lobe volume. Among the nonhuman primate sample,

Cebus have small temporal lobes for their brain size, and Macaca and Papio have large

superior temporal gyri for their brain size. The observed departures from allometry might

reflect neurobiological adaptations supporting species-specific communication in both

humans and old world monkeys. The authors concluded that the entire human temporal

lobe and some of its component structures are significantly larger than predicted for a

primate brain of human size. The most dramatic allometric departure is in the volume of the

human temporal lobe white matter, which, in addition to being large relative to brain size, is

also large relative to temporal lobe size. These allometric departures in humans could

reflect a reorganization of the temporal lobes driven by expansion of the language cortex

and its associated connections. In primates it is interesting to note that the superior

temporal gyrus contains neurons tuned to species specific calls, and the magnitude of


unicative signals as

reflecti

ental man could have had a language relatively complex as a

lexical

the word has just a visual association, an occipital extension is found

oux et al., 2006)

rigins of the grammatical system

other

words,

different species’ residuals might relate to the repertoire of vocal comm

ons of the complexity of their respective social environments.

It has been calculated that this enlargement of the temporal lobe occurred some

200-300 thousand years ago (Kochetkova, 1973). Consequently, it can be conjectured that

hominids existing before the contemporary Cro-Magnon Homo sapiens could have

developed a certain complex lexical/semantic communication system. For instance, it could

be speculated that Nearth

/semantic system.

Brain organization of the lexicon seems to be related with the type of association

between words and perceptions. When the word is associated with own-body information,

brain representation of the lexicon seems associated with a parietal extension (e.g., body-

parts names); when

(R

O

Departing from the above observations, it can be speculated that grammar, speech praxis

movements, and using verbs appeared roughly simultaneously in human history. In

they are strongly interrelated and depend upon a common neural activity.

Recently, a milestone observation was made that significantly enlightened our

understanding about the origin of language in general and grammar in particular. In

England a family, usually referred as the KE family, was found. In over three generations of

this family, about half the family members had presented a significant disturbance in

language development. Speech was largely unintelligible, and they were taught sign

language as a supplement to speech as children. Affected members presented severe

disturbances in articulation and other linguistic skills along with broader intellectual and

physical problems. From the genetic point of view the disorder was associated with a


he affected compared with the

unaffe

d disruption of speech and expressive language, including grammar (Fisher

et al., 1

at the mutations have been critical for the

develo

mutation in a single autosomal-dominant gene, FOXP2, located in the chromosome 7

(Vargha-Khadem et al., 1995). The disorder was not restricted to speech and also included

the following characteristics: defects in processing words according to grammatical rules;

understanding of more complex sentence structure such as sentences with embedded

relative clauses; inability to form intelligible speech; defects in the ability to move the mouth

and face not associated with speaking (relative immobility of the lower face and mouth,

particularly the upper lip); and significantly reduced IQ in t

cted in both the verbal and the non-verbal domain.

Further, affected family members presented a pronounced developmental verbal

dyspraxia. The authors refer to the core deficit as one involving sequential articulation and

orofacial praxis (Takahashi & Liu, 2009; Vernes et al., 2006; Vargha-Khadem et al., 1998).

PET studies revealed functional abnormalities in both cortical and subcortical motor-related

areas of the frontal lobe, while quantitative analyses of MRIs revealed structural

abnormalities in several of these same areas, particularly the caudate nucleus, which was

found to be abnormally small bilaterally. An abnormal gene (SPCH1) in the chromosomal

band 7q31 was localized. The genetic mutation or deletion in this region was proposed to

result in marke

998).

Enard et al. (2002) analyzed the evolution of the chromosome FOXP2. They noted

the extremely conservative nature of FOXP2. The mouse FOXP2 differs in just one amino

acid from chimpanzee, gorilla and rhesus monkey. However, human FOXP2 differs from

gorilla, chimp and rhesus macaque in two further amino acids (and thus differs from mouse

in three amino acids out of 715). So, in 75 million years since the divergence of mouse and

chimpanzee lineages only one change occurred in FOXP2, whilst in the six million years

since the divergence of man and chimpanzee lineages two changes have occurred in the

human lineage. The authors estimated that the last two mutations occurred between

10,000 and 100,000 years ago and speculated th

pment of contemporary human speech.

This genetic approach to the origins of language seems particularly important in


s that are connected via cortico-basal ganglia

ircuits (Reimers-Kipping et al., 2011).

rammar at the origin of the executive functions

d from action representation) may depend upon one single

core a

ns are important to support the involvement of prefrontal

ortex in motor representation:

frontal lobe should participate in complex and elaborated motor

(‘‘executive”) activities.

understanding the appearance and evolution of language in humans (Scharff & Petri, 2011;

Tanabe et al., 2011). It has been pointed out that FOXP2 could have contributed to the

evolution of human speech and language by adapting cortico-basal ganglia circuits (Enard,

2011). Although Foxp2 is expressed in many brain regions and has multiple roles during

mammalian development, the evolutionary changes that occurred in the protein in human

ancestors specifically affect brain region

c

G

So-called executive functions represent one of the most intensively studied neuroscience

questions during the last decade (e.g., Garcia-Molina et al., 2010; Koechlin et al., 2003;

Miller & Cohen, 2001; Stuss & Knight, 2002; Stuss & Levine, 2002). Disagreement persists,

however, around the potential unitary factor in executive functions (Mikaye et al., 2000;

Stuss & Alexander, 2007). Ardila (2008) emphasized that ‘‘action representation” (i.e.,

internally representing movements or actions) may constitute at least one basic executive

function factor. It could be speculated that ‘‘action representation” and also ‘‘time

perception” (potentially derive

bility (‘‘sequencing?”).

Two departing observatio

c

(a) Anatomical observation. Prefrontal cortex represents an extension and further

evolution of the frontal motor areas (Miller &. Cummings, 2007; Risberg, 2006). It may be

conjectured that the pre


paratonia, primitive

reflexes, etc. (e.g., Ardila & Rosselli, 2007; Victor & Ropper, 2001).

in particular and cognition in

genera

pment of an instrument (language or any other) that represents a cultural

produc

(b) Clinical observation. A diversity of motor control disturbances are observed in

prefrontal pathology, such as perseveration, utilization behavior,

Throughout recent history several authors have argued that thought, reasoning, and

other forms of complex cognition (“metacognition”) depend on an internalization of actions.

Vygotsky (1929, 1934/1962, 1934/1978) for instance, proposed that thought (and in

general, complex cognitive processes) is associated with some “inner speech”. Vygotsky

represents the most classical author suggesting this interpretation for complex cognition.

More recently, Lieberman (2002a,b) suggested that language

l arise from complex sequences of motor activities.

The central point in Vygotsky’s (1934/1962) idea is that higher forms of cognition

(‘‘cognitive executive functions”) depend on certain mediation (language, writing or any

other); the instruments used for mediating these complex cognitive processes are culturally

developed. According to Vygotsky (1934/1962) the invention (or discovery) of these

instruments will result in a new type of evolution (cultural evolution), not requiring any

further biological changes. Thinking is interpreted as a covert motor activity (‘‘inner

speech”). Vocalization becomes unnecessary because the child ‘‘thinks” the words instead

of pronouncing them. Inner speech is for oneself, while external social speech is for others.

In brief, Vygotsky (1934/1978) argued that complex psychological processes

(metacognitive executive functions) derives from language internalization. Thinking relies in

the develo

t.

Lieberman (2002a,b) refers specifically to the origins of language. He postulates that

neural circuits linking activity in anatomically segregated populations of neurons in

subcortical structures and the neocortex throughout the human brain regulate complex

behaviors such as walking, talking, and comprehending the meaning of sentences. The

neural substrate that regulates motor control (basal ganglia, cerebellum, and frontal cortex)

in the common ancestor of apes and humans most likely was modified to enhance cognitive


ectus most likely talked, had large vocabularies, and commanded

fairly c

vements, a process which may be crucial for understanding

and/or

and linguistic ability. The cerebellum and prefrontal cortex are also involved in learning

motor acts (e.g., Matsumura et al., 2004; Hernandez-Mueller et al., 2005). Lieberman

(2002a,b) proposes that the frontal regions of the cortex are implicated in virtually all

cognitive acts and the acquisition of cognitive criteria; posterior cortical regions are clearly

active elements of the brain’s dictionary. Real-word knowledge appears to reflect stored

conceptual knowledge in regions of the brain traditionally associated with visual perception

and motor control. Some aspects of human linguistic ability, such as the basic conceptual

structure of words and simple syntax, are phylogenetically primitive and most likely were

present in the earliest hominids. Lieberman (2002a,b) further suggests that speech

production, complex syntax, and a large vocabulary developed in the course of hominid

evolution, and Homo er

omplex syntax.

These two authors (Vygotsky and Lieberman), although using rather different

approaches, have both postulated that the development of language and complex cognition

are related with some motor programs, sequencing, internalizing actions, and the like.

Many other authors have presented a similar point of view (e.g., (Hommel et al., 2001;

Jeannerod, 1997; Luria, 1969; Morsella et al., 2009; Prinz, 1999). Some contemporary

research seems to support this interpretation; for instance, Clerget et al. (2009) using

transcranial magnetic stimulation to interfere transiently with the function of left BA44 in

healthy individuals found that a virtual lesion of left BA44 impairs individual performance

only for biological actions, and more specifically for object-oriented syntactic actions. The

authors concluded that these finding provide evidence that Broca's area plays a crucial role

in encoding complex human mo

programming actions.

The recent discovery of mirror neurons (Di Pellegrino et al., 1992; Rizzolatti & Arbib,

1998; Rizzolatti et al., 1996) could significantly contribute to the understanding of the brain

organization for verbs. A mirror neuron is a neuron which fires both when an animal

performs an action and also when the animal observes the same action performed by

another animal. Mirror neurons were initially observed in monkeys (Di Pellegrino et al.,


resent a system that

matche

Conversely, left BA 44 plays a role in motor sequence learning (Clerget et al.,

2011).

tion” may constitute the departing point for both grammar and executive

nctions.

1992), but in humans, brain activity consistent with mirror neurons has been found in the

premotor cortex and the inferior parietal cortex (Rizzolatti et al., 1996; Rizzolatti &

Craighero, 2004). These neurons (mirror neurons) appear to rep

s observed events to similar, internally generated actions.

Transcranial magnetic stimulation and positron emission tomography (PET)

experiments suggest that a mirror system for gesture recognition indeed exists in humans

and includes Broca’s area (Rizzolatti & Arbib, 1998). The discovery of mirror neurons in

Broca’s area might have important consequences for understanding brain language

organization and language evolution (Arbib, 2006; Craighero et al., 2007). An obvious

implication of mirror neurons is that they can participate in the internal representation of

actions, and the internal representation of actions may represent the origin of grammar.

Neuroimaging data have shown that interactions involving Broca’s area and other cortical

areas are weakest when listening to spoken language accompanied by meaningful speech-

associated gestures (hence, reducing semantic ambiguity), and strongest when spoken

language is accompanied by self-grooming hand movements or by no hand movements at

all, suggesting that Broca’s area may be involved in action recognition (Skipper et al.,

2007). PET studies have associated the neural correlates of inner speech with activity of

Broca’s area (McGuire et al., 1996). De Zubicaray et al. (2010) emphasize the importance

of Broca’s area to covert verbalization. Clerget et al. (2009) using transcranial magnetic

stimulation to interfere transiently with the function of left BA44 in healthy individuals found

that a virtual lesion of left BA44 impairs individual performance only for biological actions,

and more specifically for object-oriented syntactic actions. The authors concluded that

these finding provide evidence that Broca's area plays a crucial role in encoding complex

human movements, a process which may be crucial for understanding and/or programming

actions.

In brief, there is some converging evidence that something like “action

representa

fu


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3. Origins of Spatial Abilities

millions) of

years,

n his way of life (the Neolithic Revolution). Paleolithic

repres

Introduction

Contemporary city life, in which direct orientation in space has been replaced by the logical

application of mathematical coordinates, represents not just a recent cultural acquisition,

but also, it is found only in some contemporary human groups. For a very long time,

education consisted of learning how to get oriented in the space, how to recognize the

relevant signals to follow prey, and how to move in the surrounding environment. This, of

course, is still valid for contemporary people living in the Amazonian jungle, for Eskimos, for

desert inhabitants, and many other world inhabitants. For thousands (and even

man’s survival depended on the correct interpretation of spatial signals, memory of

places, calculation of distances, and so forth, and his brain must have become adapted

precisely to handle this type of spatial information (Ardila & Ostrosky, 1984).

Paleolithic (prehistorical era characterized by the development of the first stone

tools) extended since about 2,500,000 years (first hominids using stone tools) until some

10,000 years ago (Childe, 1936; Hours, 1982; Toth & Schick, 2007). About this time,

agriculture appeared, and man began to domesticate and raise some animals. This

produced a tremendous change i

ents in consequence about 99% of human technology history. That means, for about

99% of history, humans were nomads, and the correct spatial orientation represented the

most crucial ability for surviving.

It could be conjectured that biological adaptation was accomplished to survive under

those conditions existing during the Paleolithic time. Recent man’s evolution corresponds in


Agriculture replaced fruit collection; domestication of animals replaced

hunting

branches. He was a nomad and he

had to

bal, logical, and mathematical abilities, not

patial orientation abilities. Of course, those are currently the most useful abilities to live in

a significant extent to a cultural type of evolution, not necessarily requiring further overt

biological changes.

; written language extended oral language; arithmetic extended finger counting; and

the use of maps and logical spatial coordinates replaced the direct orientation in space

(Vygotsky, 1962).

There is evidence that Australopitecus africanus (probably the direct ancestor of

Homo) lived on open savannas. Although his ancestors lived in forests, he moved to live in

open fields (Lee & DeVore, 1968; Wilson, 1975). He strongly depended on animal food,

especially small preys (tortoises, lizards, snakes, rabbits) and fruit collecting. Homo sapiens

appeared in Europe about 50,000 years ago (middle Paleolithic), and it is supposed that he

hunted, usually small but also big prey, used rudimentary stone tools (knives, axes), and

lived in caverns or rudimentary shelters built with tree

be moving from one place to another all the time while looking for prey, fruits, and

shelter. He created some hunting weapons like the arrow and the spear, and used fire

(Washburn, 1978; Hours, 1982; Boyd & Silk, 2003).

It could be supposed that spatial abilities were even more crucial for survival in

prehistorical than in contemporary man. Survival in current urban living conditions

somehow requires different cognitive abilities. We go around in our cities using

logical-mathematical coordinates, reading a printed-on-a-paper map, without taking into

consideration the sun position in the sky, or avoiding potential predators. Adaptation to

contemporary world conditions requires more verbally-based abilities. If the question "What

moon-phase is today?" (instead of "What date is today?") was included in a mental state

examination, it is very likely the majority of city people would probably fail. By the same

token, city people usually ignore the exact sunrise and sunset points (they usually respond

"East and West"), but sunrise and sunset points change a little every day, and it could have

been an important piece of information for prehistorical man's survival, as it is for

contemporary man to know that "Today is May 6th, 2011." Furthermore, our current

educational system strongly emphasizes ver

s


g, city people have limited opportunities to

evelop and use spatial orientation abilities.

porary schooled Western (particularly

Europe

be illustrative. Perceptual

onstancy (stability of perception despite changes in the actual characteristics of the

ost fundamental ability in the interpretation of the surrounding

patial environment (Ardila, 1980; Walsh & Kulikowski, 1998).

uropeans did not perform

o accurately. Perceptual constancy may be expected to have been high (and crucial for

urvival) not only in pre-historical man, but also to be high in people currently requiring a

our contemporary world. Generally speakin

d

How we get oriented in the space?

Cross-cultural differences in spatial orientation strategies under normal and pathological

conditions could be illustrative to understand how pre-historical man could have used

spatial information. Furthermore, it could shed some light about the potential spatial abilities

that contemporary man possesses. Brain organization of spatial abilities under pathological

conditions has been extensively studied in contem

an and North American) people. To my best knowledge, however, no clinical

observations about disturbances in spatial abilities associated with brain pathology in other

(non-Western) culture have ever been reported.

Characteristics of spatial abilities in different cultures can

c

stimuli) represents the m

s

Perceptual Constancy

In general, cross-cultural comparisons have demonstrated that perceptual constancy (size

and shape constancy) is more accurate in low-schooled and non-Western society’s people

than in literate and westernized subjects (Pick & Pick, 1978). Beveridge (1940)

demonstrated a greater constancy of shape and size among West African adults than

among British adults. Myambo (1972) observed almost perfect shape constancy in

uneducated Malawi adults, whereas the educated Africans and E

s

s


of the surrounding spatial environment.

etc). Geographic features affect the

terms

etween specific islands are described in terms of the star patterns and

islands

ungle, they permanently break small bush branches, to recognize later

they ha

complex interpretation

Reference Systems

People living in different environments develop different systems of spatial reference

(rivers, mountains, sun position, streets, buildings,

of local reference systems, and differences in reference systems may, in turn, be

related to differences in perception of spatial orientation (Pick & Pick, 1978). The analysis

of different reference systems can be illustrative.

Gladwin (1970) analyzed the system used by Puluwat sailors to navigate among

clusters of islands in the Western Pacific. He disclosed that many different features of the

sea and sky comprise the information of which the system is based. Knowledge of the

habits of local sea birds provides cues for one's location. The sailors learn to defect the

coral reefs’ formation changes, which of course, differ depending on the conditions of the

weather, sea and sky. Ability to detect change in the "feel" of the boat moving through the

waves on a particular course is a skill used to maintain a course. There is a complex

reference system based on the position and patterns of stars in the night sky, and the rules

for navigating b

. Parallax information is also explicitly included in the system as descriptions of the

way in which the islands "move" as the boat passes on one or the other side of them (Pick

& Pick, 1978).

Amazonian Indians simultaneously use a variety of different types of information to

move around in the jungle. They use small rivers, orientation and color of trees, soil

characteristics, sun position, animal routes, olfactory cues, and many other signals to move

in the jungle. Vegetation is mildly different when closer to rivers, moss grows different in

trees according to the sun direction, and directions of river-flows are different. Additionally,

when moving in the j

ve already crossed (and approximately how long time ago) that particular point. All


han they currently are for contemporary city-man. Evidently,

patial orientation and reference systems used by pre-historical man were closer to

ystems than to our contemporary

rientation system in cities.

n general for illiterate people (Ardila et al.,

1989).

these environmental signals are simultaneously interpreted for getting oriented and moving

around the jungle.

Evidently, members of different cultures dwelling in different spatial environments

operate in terms of complex spatial reference systems, depending on their particular

demands and geographic environments. Demands and geographic environment were quite

different in Paleolithic times t

s

Puluwat sailors' or Amazonian Indians' reference s

o

Cultural Differences in Visuoperceptual Abilities

Cross-cultural differences in perceptual abilities have been extensively studied and can be

particularly illustrative to understand perceptual skills in pre-historical man (Brislin, 1983;

Laboratory of Comparative Human Cognition, 1983; Segall, 1986). Hudson (1960, 1962)

studied depth perception using pictures that contained figures of an elephant, an antelope,

and a man with a spear; the basic question referred to what the man was doing with the

spear. There were four pictures differing with respect to the cues available for the

interpretation of the picture. This set of pictures was used with different groups of people

from Africa and Europe. It was observed that European children around 7-8 years have a

great difficulty perceiving the picture as three-dimensional. However, around 12 years,

virtually all children perceived the picture as three-dimensional. Not so with Bantu or

Guinean children. Nonliterated Bantu and European laborers responded to the picture as

flat, not three-dimensional. They cannot interpret represented-on-a-paper

three-dimensional figures; this also holds true i

However, as mentioned above, illiterate African people do better than Western

literate subjects in perceptual constancy tasks with real objects. But they do worse when

the external space is represented on a paper.


eight of a cow; or any dactylographist can easily and quickly

disting

logy, are necessarily not only partial but, doubtless, biased. Norms for

erceptual performance in a sufficiently broad array of neuropsychological tests and an

xtended analysis of perceptual disturbances in different cultural and ecological contexts

2, 1985; Hécaen, 1962; Morrow & Ratcliff, 1988;

Berry (1971, 1979) proposes that hunting people with specific ecological demands

usually present good visual discrimination and excellent spatial skills. For instance, the

embedded figures tests are better performed by cultural groups for whom hunting is

important for survival. Berry emphasizes that ecological demands and cultural practices are

significantly related to the development of perceptual and cognitive skills. A good example

of a specific culture-dependent cognitive skill was that reported by Gay and Cole (1967);

when Kpelle farmers are contrasted with American working class, the former were

considerably more accurate in estimating the amount of rice on several bowls of different

sizes containing different amounts of rice. By the same token, any cattle farmer is able to

accurately calculate the w

uish two different fingerprints; or any neurologist can distinguish a Parkinsonian

patient at one glance. Demands and training history are strongly associated with

visuoperceptual abilities.

Spatial abilities differ among cultures and depend on the specific ecological

demands. In neuropsychology, the perceptual ability disturbances of a very limited

subsample of the human species -contemporary Western, and most often, urban and

literate brain-damaged individuals have been relatively well analyzed. Nevertheless, our

understanding of the brain organization of spatial abilities, and their disturbances in cases

of brain patho

p

e

are required.

Acquired spatial cognition disorders

Visuospatial impairments resulting from brain damage have been extensively analyzed in

neuropsychology (e.g., De Renzi, 198


Newco

capable to explain it (Ardila & Rosselli, 1992). Spatial agnosia includes

impairm

me is included within visual

explora

in case

mbe & Ratcliff, 1989; Rosselli, 1986; Stiles, Stiles-Davis, Kritchevsky & Bellugi,

1988; Beis et al., 2003; Hodgson & Kennard, 2003; Vallar, 2007). Different brain

syndromes have been distinguished.

Spatial agnosia represents an impairment in the perception and use of

spatial-dependent information resulting from brain pathology. It refers to an acquired

inability to recognize and integrate spatial information, regardless that there is not a primary

sensory defect

ents in the recognition of line orientation, defects in depth perception, impairments

in handling spatial information, and deficits in spatial memory (De Renzi, 1983; Hécaen &

Albert, 1978).

Different types of spatial agnosia have been distinguished. Holmes (1918) separates

different categories of spatial agnosia: defects in objects localization, topographic amnesia,

inability to count objects, inability to perceive movement, loss of stereoscopic vision, and

deficits in eye movements. Critchley (1968) includes the following groups: (1) disorders in

spatial perception with regard to the three-dimensional perception, (2) disorders in spatial

concepts, and (3) disorders in spatial manipulation, which includes disorders in

topographical memory, defects in orientation, and unilateral spatial agnosia. Hécaen (1962)

proposed to separate: (1) disorders in spatial perception, (2) defects in spatial manipulation,

including, the loss of topographical concepts, and unilateral spatial agnosia, (3) loss of

topographical memory, and (4) Balint's syndrome. De Renzi (1982, 1985) presents some

modifications to Hécaen's classification. Balint's syndro

tion disorders, and instead of disorders in manipulation of spatial information,

introduces the group of disorders in spatial thought. Table 3.1 presents the classification of

spatial agnosias proposed by Ardila and Rosselli (2007).

It is interesting to emphasize that all these disorders appear (mainly or exclusively)

s of right hemisphere pathology. That means the right hemisphere seems to be

specialized in spatial cognition. Language and ideomotor praxic abilities developed in left

brain areas that in the right brain are involved in spatial cognition (LeDoux, 1984).

Supposedly, similar spatial cognition disturbances are to be found in a similar way in


ve been reported to be more frequently observed associated with

ft-hemisphere pathology in individuals with a history of low verbal trainings (i.e., low

____________________________

____________________________

ATI N

Bilateral parietal-occipital

ISORDERS IN SPATIAL MANIPULATION

ital-parietal and frontal

specially right

Topographic amnesia Right (or bilateral) parietal-occipital ________________________________________________________________

every individual, regardless of the cultural background and the ecological demands.

However, not only commonality but also differences would be expected to be found. If the

degree (not the direction) of brain lateralization of language depends on literacy, and in

general, on the verbal training history (Lecours et al., 1987, 1988; Matute, 1988), it would

seem reasonable to suppose that the degree of lateralization of spatial cognition would also

depend on the spatial abilities training history. At least some spatial disturbances (e.g.,

hemi-spatial neglect) ha

le

educational level), but normal, and eventually even superior trainings in spatial abilities

(Rosselli et al., 1985).

____________________________________ TYPE OF DISORDER LOCATION OF DAMAGE ___________________________________ DISORDERS IN SPATIAL EXPLOR O Balint's syndrome Bilateral parietal-occipital DISORDERS IN SPATIAL PERCEPTION Inability to locate stimuli Right parietal Impairments in depth perception Distortion in line orientations Right parietal-occipital and frontal Inability to estimate the number of stimuli Right hemisphere especially parietal D Unilateral spatial agnosia Right occip Loss of topographical concepts Parietal-temporal-occipital D

ISORDERS IN ORIENTATION AND SPATIAL MEMORY

Topographic agnosia Biteral temporal-occipital


ition disturbances may also depend on spatial ability training histories.

This, o

atics, painting, playing chess, reading and writing,

nd music abilities can be impaired in cases of right hemisphere damage of

ose same areas that in a Eskimo or Amazonian Indian could imply an impossibility to

move around the snow or the jungle.

Table 3.1. Classification of spatial agnosias (according to Ardila & Rosselli, 2007).

If, despite the existence of some basic characteristics in its brain organization,

language disturbances (oral and written) are associated with language idiosyncrasies (i.e.,

aphasia is not completely equivalent in Chinese and Spanish; alexia can be different in

English and Japanese, etc; Sasanuma & Fujimura, 1971; Yamadori, 1975; Yu-Huan et al,

1990), spatial cogn

f course, has to be demonstrated. And, it can be demonstrated only if spatial

disturbances are analyzed in individuals with different cultural backgrounds and different

spatial demands.

Nevertheless, contemporary city man's spatial abilities are not necessarily inferior to

pre-historical man's or Amazonian Indians' spatial abilities. Spatial abilities may have

evolved with the new living and cultural conditions (in a similar way as spoken language

evolved and extended with the development of new cultural conditions, e.g., through written

language). Spatial abilities can be required in many contemporary, conceptual, and

historically recent skills. The author of this paper had the opportunity to study a university

chemistry professor who suffered a small right-parietal infarction. Although she had no

evidence of spatial difficulty in her everyday activities, and no significant spatial

disturbances were disclosed in formal testing, she could not continue teaching chemistry,

because she was "unable to have a spatial representation of molecules and all the time got

confused". Mathematics (Ardila &Rosselli, 1990; Luria, 1977), painting, playing chess

(Chabris & Hamilton, 1992), reading and writing (Ardila & Rosselli, 1993; Benson & Ardila,

1996), mechanics (Benton, 1989), and even music (Henson, 1985), represent (at least

partially) spatially-based skills. Mathem

mechanics, a

th


Neuroimaging studies

Some few studies have analyzed brain activity in different spatial recognition and

orientation tasks. Thus, by using functional Magnetic Resonance Imaging (fMRI)

techniques, it has been demonstrated that the right posterior part of the parahippocampal

gyrus is critical for the acquisition of novel information about the environment (buildings and

landscapes), and that the same region plus the anterior half of the lingual gyrus and the

adjacent fusiform gyrus play an important role in the identification of familiar buildings and

landscapes (Takahashi & Kawamura, 2002). Ino et al (2008) described two patients who

presented with transient directional disorientation as a manifestation of cerebral ischemia.

The patients suddenly lost sense of direction in a familiar environment despite preserved

ability to recognize landmarks. Brain MRI revealed an ischemic lesion in the right medial

occipital lobe and the corpus callosum in case 1 and in the right parieto-occipital sulcus in

case 2. Using a larger sample, Gil-Néciga et al. (2002) studied 10 patients with transient

topographical disorientation; they found that the episodes of transient topographical

disorientation could be separated into two types: the patients either reported difficulties in

spatial orientation with preserved abilities to recognize landmarks and objects (spatial

agnosia), or the difficulties appeared with the recognition of landmarks (topographical

agnosia). Tests exploring spatial orientation, as well as higher visuoperceptive capacities,

were altered in most of the patients, and brain SPECT showed hypoperfusion of the right

hemisphere in all patients, which could also be demonstrated two years later in some

cases.

The crucial role of the right parieto-occipital area in spatial orientation and

topographical recognition has been confirmed by diverse authors. Thus, van der Ham et al

(2010) reported two cases with navigation problems resulting from parieto-occipital right

hemisphere damage. Rusconi et al (2008) described the case of a young woman with long-

lasting topographical disorientation following a hemorrhagic lesion of the right temporo-


occipital region involving the hippocampus. She was unable to orient herself in novel

environments and to perform learning spatial tasks both in real-world settings and

laboratory conditions. Her ability to recall and navigate through known routes as well as to

recognize familiar landmarks was preserved. A similar neuropsychological pattern was

observed 8 years later when she showed a persistent topographical disorientation and a

slight worsening of verbal and visuo-spatial long-term memory disorders. Turriziani et al

(2003) described a patient who, following cerebral hypoxia, developed severe difficulty in

orienting himself in new environments in the context of a mild global amnesic syndrome.

Some episodes he related suggested that his main difficulty was remembering the

spatial/directional value of landmarks he recognized. A neuroradiological examination

documented severe bilateral atrophy of the hippocampi associated with atrophic changes in

the cerebral hemispheres, mostly marked in the dorsal regions.

Several notable features emerge from consideration of the case reports of relatively

pure topographical disorientation in the presence of a retrosplenial lesion (Maguire, 2001).

The majority of cases follow damage to the right retrosplenial cortex, with Brodmann's area

30 (association cortical area in the transitional region between the posterior cingulate gyrus

and the medial temporal lobe) apparently compromised in most cases. All patients

displayed impaired learning of new routes, and defective navigation in familiar

environments complaining they could not use preserved landmark recognition to aid

orientation. The deficit generally improved during the following weeks. The majority of

functional neuroimaging studies involving navigation or orientation in large-scale space also

activate the retrosplenial cortex, usually bilaterally, with good concordance in the locations

of the voxel of peak activation across studies, again with Brodmann's area 30 featuring

prominently. Currently, there is strong evidence for right medial temporal lobe involvement

in spatial orientation; it also seems that the inputs the hippocampus and related structures

receive from and convey to right retrosplenial cortex have a similar spatial preference, while

the left medial temporal and left retrosplenial cortices seem primarily concerned with more

general aspects of episodic memory.


Conclusions

Some tentative conclusions regarding the evolution of spatial abilities can be proposed:

1. Homo sapiens presented a nomad way of life during the majority of his history.

Sedentary way of life appears only with domestication of animals and development of

insufficiently

nderstood array of impairments. Spatial knowledge has been strongly associated with

is found to be correlated with literacy, that is, with language

omplexization. Spoken language evolved with appearance of new cultural conditions, and

elopment

and complexization, but also the development of new spatially-based abilities may have

agriculture, that if, some ten thousand years ago. Nomad way of life is strongly associated

with high spatial ability demands.

2. Disorders in spatial cognition represent a particularly complex and

u

right hemisphere activity. Virtually all the defects in spatial perception and orientation are

found exclusively or predominantly in cases of right hemisphere damage.

3. It can be supposed that right hemisphere specialization for spatial abilities is

correlated with language acquisition and evolution. Furthermore, it has been suggested that

right hemisphere specialization on spatial skills, as well as left hemisphere specialization in

verbal and praxic abilities,

c

it may be supposed that spatial abilities also evolved with the appearance of new cultural

and ecological conditions.

4. It has been conjectured that earlyhominids and pre-historical man presented a

more bilateral representation of spatial abilities. Visuospatial disorders might have been

expected in cases of right and left hemisphere pathology. Not only language dev


creased the right hemisphere specialization for handling information with a spatial

ontent, as well as the left specialization for linguistic abilities (LeDoux, 1984).

rdila, A. (1980). Psicología de la Percepción [Psychology of Perception]. México: Editorial

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enson, D.F. & Ardila, A. (1996). Aphasia: A Clinical Perspective. New York: Oxford

in

c

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4. Origins of Writing

, but still nowadays, significant changes in writing strategies are observed very

specia

reading

can be

Introduction

Writing represents a relatively recent acquisition in human history. Its development was

particularly slow, advancing through different steps of complexity. Writing began several

millennia ago

lly associated with the progressively more extended use of computer word

processors. The need for a clear understanding of the origins of current cognitive abilities is

evident. The example of reading and writing may be illustrative of the need for a

historical/anthropological analysis of neuropsychological syndromes. Varney (2002) points

out that reading is a cultural, not an evolutionary, development. He emphasizes that ‘‘our

capacity of reading did not evolve biologically; it evolved through cultural developments that

were only acquired as ‘typical’ human abilities within the last 200 years in Europe and

America, and only after World War II in the rest of the World’’ (p. 3). The origins of

found in certain abilities that existed long before reading was developed. Reading

and writing were far from ‘‘universal’’ even at the beginning of the 21st century. According to the United Nations, ‘‘a person who is literate can, with understanding,

both read and write a short simple statement on his or her everyday life…. A person is

functionally literate who can engage in all of those activities in which literacy is required for

effective function of his or her group and community and also for enabling him or her to

continue to use reading, writing, and calculation for his or her own and the community’s

development’’ (UNESCO, 2003). Surveys throughout the world have been conducted to


rld’s population was found to be

illiterat

illion illiterate adults in the world, of whom about two thirds are women

(UNES

uisites that led the way to the cultural

development of reading. Gesture recognition may have existed for several millions of years,

but reading developed just a few millennia ago.

observe populations speaking various languages and their inability to read or write a simple

message. In the first survey (1950), at least 44% of the wo

e. A 1978 study showed the rate to have dropped to 32.5%. In 1990 illiteracy

worldwide dropped to about 27%, and by 1998 to 16%. However, a study by the United Nations Children’s Fund (UNICEF) published in

1998 predicted that the world illiteracy rate would increase in the 21st century because only

a quarter of the world’s children were in school by the end of the 20th century. The highest

illiteracy rates were found in the less developed nations of Africa, Asia, and South America.

The lowest illiteracy rates were found in Australia, Japan, North Korea, and the more

technologically advanced nations of Europe and North America. Currently, there are an

estimated 862 m

CO, 2011). The mean educational level of contemporary man is only about 3–4

years of school! Varney (2002) analyzed the origins of reading ability. He suggested that the ancient

skills of gesture comprehension and animal tracking were the underpinnings of brain

organization that permitted reading to occur. He demonstrated that alexia is significantly

associated with impaired pantomime and animal footprint recognition. Thus, these abilities,

existing since early human history, were prereq

How did writing appear?

Wall paintings appeared during the Paleolithic era, some 30–35,000 years ago (Childe,

1936). Across Europe, particularly in France and Spain, cave paintings dating from the

Paleolithic age have been found. Mainly animals, but also people, instruments, and

environmental conditions, are represented in these paintings. Further evolution in pre-


ly regarded

as the

0 years ago in

hoenicia (Sampson, 1985), and graphemes representing phonemes appeared even later

Greece. The sequence of the evolution of writing in consequence was:

rawings -> pictograms -> logograms -> syllabic graphemes -> phonemic

raphemes

r of

symbols: anything from several hundred to tens of thousands. In fact there is no theoretical

upper limit to the number of symbols in some logographic scripts, such as Chinese.

writing is represented by paintings becoming standardized for representing specific

elements (i.e., a standard bird means ‘‘bird’’). Lecours, Peña-Casanova, and Ardila (1998)

pointed out that writing began with concrete pictograms that reflect realities accessible to

the senses, particularly to vision. These pictograms further evolved and became abstract,

progressively separating from the concrete representation (Figure 4.1). This situation was

observed in Sumer (contemporary Iraq) about 53 centuries ago, and it is usual

beginning of writing in human history. Symbols (graphemes) referred to the meaning

of the words, so these original writing systems are regarded as logographic.

Graphemes representing sounds (syllables) appeared later, about 400

P

in

D

g

Writing systems can be divided in different ways; a major distinction between

logographic (representing meanings) and sonographic (representing sounds) systems can

be established (OMNIGLOT; Sampson, 1985). The fundamental difference between

logographic writing systems and other scripts is that each logographic symbol means

something. As a result, logographic writing systems generally contain a large numbe


Figure 4.1. Evolution from pictograms to cuneiform logograms

Logographic scripts may include the following types of symbols:

1. Logograms—symbols that represent parts of words or whole words. Some

logograms resemble the things they represent and are sometimes known as pictograms or

pictographs (Figure 4.2).


2. Ideograms—symbols that graphically represent abstract ideas.

3. Semantic-phonetic compounds—symbols that include a semantic element, which

represents or hints at the meaning of the symbol, and a phonetic element, which denotes or

hints at the pronunciation.

4. Sometimes symbols are used for their phonetic value alone, without regard for

their meaning.

In sonographic writing systems, syllables (syllabic alphabets) or phonemes

(phonemic alphabets) can be used. Alphabetic writing systems come in two varieties.

1. Abjads (consonant alphabets) represent consonants only, or consonants plus

some vowels. Even though not common, full vowel indication (vocalization) can be

added, usually by means of diacritics.

2. Alphabets (phonemic alphabets) represent consonants and vowels.

Thus, initial writing (or rather, pre-writing) was a visuoconstructive ability (i.e.,

representing external elements visually), and only later did it become an ideomotor praxis

ability (i.e., making certain learned and fixed sequences of movements with the hand to

create a pictogram—a standardized representation of external elements). Still later, after

writing became an ideomotor praxis ability, it became a linguistic ability (i.e., associating the

pictogram with a word, and further analyzing the word in its constituting sounds). It is not

surprising that three major disorders in writing can be observed as a result of brain

pathology: visuoconstructive (spatial or visuospatial agraphia), ideomotor (apraxic

agraphia), and linguistic (aphasic agraphia). In addition, of course, writing requires visual

and motor integrity.


Figure 4.2. Example of a logographic writing system. Japanese Kanji uses Chinese

characters that were imported from China which is use for to write nouns, adjectives,

adverbs and verbs.

It can be proposed that writing is based in three different abilities: visuoconstructive,

praxic and linguistic. Consistent with this notion, three major disorders in writing can be

observed as a result of brain injury or pathology: visuoconstructive (spatial or visuospatial

agraphia), ideomotor (apraxic agraphia), and linguistic (aphasic agraphia) (Table 4.1).

Perhaps not coincidentally, anthropological origins of writing appear to mirror these three

different abilities. In prehistory, writing developed first using a visuospatial modality to

create three-dimensional clay tokens to represent objects, which later progressed into


drawings. It is not surprising that three major disorders in writing can be observed as a

result of brain pathology: visuoconstructive (spatial or visuospatial agraphia), ideomotor

(apraxic agraphia), and linguistic (aphasic agraphia). In addition, of course, writing requires

visual and motor integrity.

---------------------------------------------------------------------------

Spatial or visuospatial agraphia

Apraxic agraphia

Aphasic or linguistic or central agraphia

---------------------------------------------------------------------------

Table 4.1. There are three fundamental forms of agraphia (Ardila, 2004).

How many people can write?

Even though writing began several millennia ago up to as recently as the 1950s, about half

of the world’s population was illiterate. The percentage of illiteracy dramatically increases

as we go back in time, and up to only a couple of centuries ago, the overwhelming majority

were illiterate. Until the 15th century, when the printing press was invented, writing may well

have been limited to a few intellectual people and monks. Even though there are no

statistics available, it may be conjectured that 99% or more of the population was illiterate.

Furthermore, it has to be kept in mind that the mean level of education of contemporary

man is about 3 years of school, which may not be enough to develop automatic reading

and writing. It is evident that writing represents an unusual ability in humans. The overwhelming

majority of members of our species who have lived could not read or write. Reading and

writing is obviously far from being a ‘‘primary’’ or ‘‘biologically based’’ cognitive ability.

Clearly, writing represents a cognitive ability that depends on the human cultural evolution


(Vygotsky, 1962).

Agraphia as a neuropsychological syndrome

Agraphia can be defined as the partial or total loss of the ability to produce written language

and is associated with brain pathology. The ability to write can be impaired as a result of

linguistic defects (aphasia), but other elements not related to language (e.g., motor and

spatial) also participate in the writing ability. It supposes knowledge of the language codes

(phonemes, words), an ability to convert language sounds in graphemes, knowledge of the

graphemic system (alphabet), an ability to perform fine movements, and an appropriate use

of the space for distributing, joining, and separating letters. It is evident that diverse types of

writing disturbances can be found in clinical practice. Different attempts to classify writing disturbances are found in the history of

neuropsychology. Goldstein (1948) distinguished two major types of agraphia:

apractoamnesic and aphasic-amnesic. Luria (1976, 1980) referred to five different types of

agraphia, three of them associated with aphasia (sensory agraphia, afferent motor

agraphia, and kinetic agraphia) and two associated with visuospatial defects. Hecaen and

Albert (1978) distinguished four types of agraphia: pure, apraxic, spatial, and aphasic. Regardless of the diversity of classifications of agraphia, a basic distinction can be

established between (1) agraphias due to a language impairment (linguistic or aphasic

agraphias), (2) agraphias due to other types of impairments (most often, motor or spatial)

disturbing the normal ability to write (Benson & Ardila, 1996), or simply (3) central and

peripheral agraphias (Ellis, 1988). In the first case, agraphia is just a secondary

manifestation of the aphasic syndrome. In the second, it can be interpreted as a result of a

broader visuoconstructive/visuospatial impairment (Ardila & Rosselli, 1993), or motor-

apraxic disturbance (Hecaen & Albert, 1978). Consequently, writing can be interpreted as a

particular type of cross-modal learning. Certain visuoconstructive and ideomotor abilities

become associated with language.


It can be proposed that writing is based in three different abilities: visuoconstructive,

praxic and linguistic. Consistent with this notion, three major disorders in writing can be

observed as a result of brain injury or pathology: visuoconstructive (spatial or visuospatial

agraphia), ideomotor (apraxic agraphia), and linguistic (aphasic agraphia). Perhaps not

coincidentally, anthropological origins of writing appear to mirror these three different

abilities. In prehistory, writing developed first using a visuospatial modality to create three-

dimensional clay tokens to represent objects, which later progressed into drawings.

Dysexecutive agraphia

Regardless that many types of writing disorders associated with brain pathology have been

described throughout the history, limited mention to the writing disturbances associated

with prefrontal pathology, however, is found. Clinical observations of patients not only with

focal prefrontal pathology but also with other conditions affecting the frontal lobe system

(e.g., traumatic head injury, dementia) confirm the assumption that these patients present

an overt decrease in the ability to express ideas in writing. It can be argued that complex

aspects of writing, such as planning, narrative coherence, and maintained attention, are

significantly disturbed in cases of impairments of executive functions (dysexecutive

syndrome). Frontal lobe patients not only have difficulties in keeping the effort required for

writing, but also to organize the ideas in the written texts. The term dysexecutive agraphia

(Ardila & Surloff, 2006) has been proposed to refer to this writing disorder.

Is any area in the brain specialized for writing?

Writing is a ‘‘functional system’’ (Luria, 1976) that requires, and is based on, some more

fundamental abilities: praxis abilities (i.e., learning sequences of movements required to

write the letters), spatial abilities (distributing letters and words in the space, and


understanding the value of space in writing), constructional abilities (reproducing a model

using certain movements), and obviously, the knowledge of the language and the

association between verbal auditory elements and visual symbols. Varney (2002) refers to

the anthropological concept of pre-adaptation, which states that the evolution of a structure

for one purpose can enable that structure to perform another purpose.

This must be true for writing (as for any other abilities depending on cultural

evolution). Visuoconstructive and ideomotor abilities represent prerequisites for writing;

they are probably related to the ability to make tools and weapons and generally to use the

hands in a skilled way.

Brain activation during writing

The use of contemporary neuroimagening techniques has significantly advanced the

understanding of the brain organization of writing (see www.fmriconsulting.com/

brodmann/). It has been observed that writing is associated with an extended pattern of

brain activity, usually including a diversity of anterior and posterior, right and left areas.

Indeed, writing is a complex act, requiring not only linguistic but also motor and spatial

abilities.

Functional studies have demonstrated that writing single letters is associated with a

significant activity of Brodmann’s areas 37 (temporal-occipital area, related with auditory-

visual associations) and 7 (superior parietal lobe) (Rektor et al., 2006). Other parietal areas

are also active during writing including the border between the parietal superior and inferior

lobuli Brodmann’s area (Brodmann’s areas 2 and 40), deep in the intraparietal sulcus, with

a surprising right-sided dominance. The right parietal activation may reflect the spatial

dimension of writing.

Comparing the brain activity observed during writing and drawing a relatively similar

pattern of activation for both has been reported (Harrington et al., 2007) including bilaterally


the premotor, inferior frontal, posterior inferior temporal and parietal areas. Significant

differences between the two conditions (writing and drawing) are found in areas of the brain

known for language processing (perisylvian area); greater activation for writing is observed

in the left hemispheres, whereas greater right hemisphere activation for drawing is found in

homologous areas, particularly Brodmann’s area 46 (part of the prefrontal cortex - anterior

middle frontal gyrus) and 37 (temporal-occipital).

Sugihara et al. (2006) recorded the brain activation while writing with the right and

the left hand using Japanese Kana (phonograms representing syllables). Three areas

were found to be activated: (1) the posterior end of the left superior frontal gyrus, which is

superior and posterior to the so-called Exner's area (an area just above Broca's area and

anterior to the primary motor control area, initially described as the “writing center”); (2) the

anterior part of the left superior parietal lobule; and (3) the lower part of the anterior limb of

the left supramarginal gyrus. In the single-subject analysis, whereas the first two of the

above three areas were found to be crucial for writing in all individuals, an interindividual

inconsistency of involvement with writing was observed in last area: the lower part of the

anterior limb of the left supramarginal gyrus (60% involved); the right frontal region (47%);

and the right intraparietal sulcus (47%).

Writing in different systems

Few papers have approached the question of the potential similarities and differences in

agraphia clinical manifestations across different writing systems. Some studies have

approached the comparison of writing disturbances and brain activation patterns in

Japanese Kana and Kanji. More recently, studies of agraphia in other languages have

become available.

Indeed, Japanese represents a unique language using two different writing systems;

Kana is a phonographic system and symbols represents syllables; whereas Kanji is a


logographic system and symbols represent meanings (morphograms). Various types of

alexia with or without agraphia in the Japanese language cause specific type of Kanji/Kana

dissociation; it has been further proposed that there is a semantic reading pathway via

Brodmann’s area 37 on the inferior border of the left temporal lobe and a phonological

reading pathway via middle portion of the left lateral occipital lobe (Iwata, 2004)

Yaguchi et al. (2006) reported a case of pure (apraxic) agraphia observed both in

Kana and Kanji writing to dictation and copying. Most errors in Kana and Kanji writing to

dictation and copying were no response. The patient, however, was able to write numerals

from 1 to 12 precisely. Magnetic resonance imaging showed a cerebral infarction in the left

parietal lobe which included a part of superior parietal lobule and supramarginal gyrus. That

means the apraxic agraphia was similarly affecting both writing systems –Kana and Kanji.

Sakurai et al. (2008) analyzed two patients with lesions of the left posterior middle

temporal gyrus. Patient 1 first presented with pure alexia more impaired for Kana after an

infarction in the left middle and inferior occipital gyri and right basal occipital cortex, and

after a second infarction in the left posterior middle temporal gyrus adjoining the first lesion

he showed alexia with agraphia for Kanji and worsened alexia for Kana; Kanji alexia

recovered over the following six to 10 months. Patient 2 presented with alexia with agraphia

for Kanji following a hemorrhage in the left posterior middle and inferior temporal gyri, which

resolved to agraphia for Kanji at two months after onset. In both patients, Kanji agraphia

was mostly due to impaired character recall. The authors concluded that damage to the left

posterior middle temporal gyrus alone can cause agraphia for Kanji. If the adjacent mid

fusiform/inferior temporal gyri (Brodmann’s area 37) are spared, the Kanji alexia is

transient. This report also demonstrates that agraphia for Kana and for Kanji can be at least

partially dissociated.

Ihori et al. (2006) reported the case of a right-handed patient who exhibited right

unilateral jargonagraphia after a traumatic callosal hemorrhage. The lesions involved the

entire corpus callosum, except for the lower part of the genu and the splenium. The

patient's right unilateral jargonagraphia was characterized by neologisms and perseveration

in Kanji and Kana, and was more prominent in Kana than Kanji. The authors propose that


at least two factors seem to explain that Kana was more defective than Kanji. First, writing

in Kana, which is assumed to be processed mainly via a sub-word phoneme to grapheme

conversion route, might depend more strongly on lateralized linguistic processing than

writing in kanji. Second, kanji, which represent meaning as well as phonology, with much

more complicated graphic patterns than kana, are assumed to be processed in both

hemispheres.

Fukui and Lee (2008) reported three patients with progressive agraphia; initially,

these patients complained primarily of difficulties writing Kanji while other language and

cognitive impairments were relatively milder. It was proposed that agraphia was generally

more prominent, although not exclusive, for Kanji, probably because of later acquisition and

larger total number of Kanji symbols leading to lower frequency of use and familiarity per

symbol. For comparing purpose, it is worthy to mention the case of progressive agraphia in

a Spanish speaking woman reported by Ardila et al., (2003). This patient presented a

progressive deterioration of writing abilities, associated with acalculia and anomia. An MRI

disclosed a left parietal-temporal atrophy. Using Spanish orthography was the initial writing

difficulty noted in this woman. The correct use of orthography (i.e., selecting between two

or more homophone alternatives) represents for normal people the most difficult aspect in

Spanish writing, and it is not surprising to find it was the most fragile writing ability in this

patient. In a further evaluation two years after the initial symptomatology, the patient

demonstrated not only orthographic (homophone) errors, but also letter omissions and

additions, and even non homophone errors. It is noteworthy that, regardless of her inability

to write spontaneously or by dictation, her writing by copy was virtually perfect. It was

conjectured that writing by copy does not really represent a linguistic ability but rather

visuoperceptual and visuoconstructive ability.

Lin et al. (2007) using fMRI examined the neural correlates for Chinese writing, by

comparing the writing of logographic characters and that of pinyin, a phonetic notation

system for Chinese characters. The temporal profile of the activations indicated that the

middle frontal gyrus, superior parietal lobule, and posterior inferior temporal gyrus reflected

more central processes for writing. Although pinyin writing elicited greater activity overall


than character writing, the critical finding was that the two types of symbols recruited

essentially the same brain regions. Liu et al. (2007) trained native English speakers with no

knowledge of Chinese on 60 Chinese characters. Following the training, fMRI scans taken

during passive viewing of Chinese characters showed activation in brain regions that

partially overlap the regions found in studies of skilled Chinese readers, but typically not

found in alphabetic readers. Areas include bilateral middle frontal (Brodmann’s area 9),

right occipital (Brodmann’s area 18/19), and fusiform (Brodmann’s area 37) regions. The

results suggest that learners acquired skill in reading Chinese characters using a brain

network similar to that used by Chinese native speakers.

Meschyan and Hernandez (2006) compared the pattern of brain activation during

single word reading in a group of English/Spanish bilinguals. Participants were slower in

reading words in their less proficient language (Spanish) than in their more proficient

language (English). fMRI revealed that reading words in the less proficient language

yielded greater activity in the articulatory motor system, consisting of supplementary motor

area/cingulate, insula, and putamen. Orthographic transparency also played a

neuromodulatory role. More transparent Spanish words yielded greater activity in superior

temporal gyrus (Brodmann’s area 22), a region implicated in phonological processing, and

orthographically opaque English words yielded greater activity in visual processing and

word recoding regions, such as the occipital-parietal border and inferior parietal lobe

(Brodmann’s area 40).

From ‘‘agraphia’’ to ‘‘dystypia’’

Contemporary literate man is using handwriting less and less, and relying on computers

more and more. In an informal survey of 40 people with a college-level education

background, they reported using a computer about 90% of the time when writing and

handwrote only 10% of the time. Obviously, this sample does not represent all of

humankind, and computers are not accessible to a large percentage of the human


population. But this sample seems to illustrate the way in which writing is evolving: from

handwriting to typing on a computer.

Handwriting and using computers represent significantly different cognitive and

motor abilities. During handwriting, fingers are maintained in a relatively steady position

while the hand moves. In typing, the opposite pattern is observed. When typing, the right

hand does not move from one side to the other and back as in handwriting, but the hands

remain relatively stationary and only the fingers are moved. Letters are not written but

selected. Both hands have to be used in a similar way when typing. Because of using both

hands, we have to assume that a major interhemispheric integration is required. It is

obvious to assume that right-hemisphere lesions located in the frontal and parietal areas

should significantly impair the typewriting ability of the left hand. Similarly, the use of the

space is different.

The normal spatial distribution of the words on the page is automatic on the

computer and, hence, writing in this way cannot be spatially disorganized, which may be

the case in handwriting. By the same token, letters are neatly written and easily

recognizable. When typing, we are not using a space that is directly manipulated with the

hands (‘‘constructional space’’), but only a ‘‘visual space.’’ Furthermore, typing is not a

constructional task (we do not have to construct the letters) but rather a motor-spatial task.

Many people type using a spatial memory for the position of the letters in the keyboard.

This is a type of memory not required in handwriting, and it probably depends on right

hippocampal and parietal activity (Moser, Hollup, & Moser, 2002). Other people have to

look at the keys to select the letters when typing. In this case, literal reading is a

prerequisite for writing. Letters have to be recognized visually before they are written. In

handwriting, we use a mental representation of the visual form of the letters. Interestingly,

few people—if any, regardless of how well they can type—are able to reproduce (i.e.,

describe verbally or by drawing) how the different letters are arranged on the keyboard.

Memory for their location seems to be a purely spatial and motor memory of which we are

poorly aware.

For typing some special symbols (e.g., interrogation marks) and letters (the Spanish


N˜ ), some relatively sophisticated motor maneuvers are required, sometimes requiring the

use of special keys or sequences of movements. In handwriting, however, special symbols

are written using the mental forms that we have learned. When typing, if a letter needs to

be lower or upper case, a key has to be pushed. No other change to the movement is

made. We can also select different writing styles and letter sizes using some special

commands and menus, all without changing the sequences of the hand movements. In

cases of brain damage, how is typewriting altered? To the best of my knowledge, only one

case of agraphia for typewriting has been published (Otsuki, Soma, Arihiro, Watanabe,

Moriwaki, & Naritomi, 2002). Nonetheless, it can be assumed that different types of brain

pathology may affect the ability for typing on a computer word processor. The following can

be conjectured.

1. An anterior callosal lesion would impair the ability to coordinate the movements

between the hands. Furthermore, the left hand would be isolated from the linguistic left

hemisphere and would be unable to write. Left-hand hemiagraphia in callosal lesions has

been observed (Benson & Ardila, 1996).

2. By the same token, it has been observed that damage in the supplementary motor

area results in disturbances in the coordinated movements between both hands (Middleton

& Strick, 2001). We can anticipate supplementary motor area typing agraphia.

3. Spatial memory disturbances should result in difficulties in recalling the positions

of the letters on the keyboard. Typing would be slow and would require a continual search

for the letters.

Otsuki et al. (2002) reported on a 60-year-old right-handed Japanese man who

showed an isolated persistent typing impairment without aphasia, agraphia, apraxia, or any

other neuropsychological deficit. They proposed the term ‘‘dystypia’’ for this peculiar

neuropsychological manifestation. The symptom was caused by an infarction in the left


frontal lobe involving the foot of the second frontal convolution and the frontal operculum.

The patient’s typing impairment was not attributable to a disturbance of the linguistic

process, since he had no aphasia or agraphia. Nor was it attributable to an impairment of

the motor execution process, since he had no apraxia. Thus, it was deduced that his typing

impairment was based on a disturbance of the intermediate process where the linguistic

phonological information is converted into the corresponding performance. The authors

hypothesized that the foot of the left second frontal convolution and the operculum may

play an important role in the manifestation of ‘‘dystypia.’’

Using a computer is somehow ‘‘equivalent’’ to a new writing system. Obviously,

there is no brain area related to typing on a computer, as there is no brain area related to

reading and writing. These are cultural and technological elements recently developed

through human evolution. However, there are basic cognitive abilities (pre-adaptative

abilities) that are required for the use of these new cultural elements: e.g., certain

visuoperceptual abilities and cross-modal associations for reading, phonological awareness

and some fine movements for writing, etc. Using computers is notoriously more complex,

yet we can assume a ‘‘functional system’’ participating in their use.

It can be conjectured that using computers requires at least the following abilities:

1. A conceptual ability (executive functioning) to understand the principles governing

the functioning of a computer.

2. Some visuoperceptual abilities to recognize icons, windows, etc.

3. Some skilled movements to type on the keyboard and manoeuvre the mouse

correctly.

4. Some spatial abilities to handle the working space (monitor screen).

5. Some memory abilities to learn programs, to use the spatial position of the keys,


etc.

Obviously, the ability to use computers can potentially be disrupted as a

consequence of a failure in any one of these abilities (‘‘acumputuria syndrome’’). In the

future, apart from ‘‘dystypia,’’ more complex disturbances in the ability to use computers will

probably be established.

Conclusions

The origins of writing can be traced back to cave paintings. Writing (or pre-writing) was

initially a visuoconstructive ability, later involving some stereotyped movements to

represent pictograms, and finally involving spoken language. It makes sense, therefore,

that the ability to write can be disturbed in three major forms: as a

visuospatial/visuoconstructive dexterity, as an ideomotor skill, and as a linguistic ability.

Writing has followed a long evolution since cave painting during the Palaeolithic times.

Different strategies have been used to represent spoken language visually

(ideograms, alphabets, etc). Writing, however, has continued to evolve since its initial

invention. The use of punctuation marks and the distinction between upper and lower case

in writing—to mention just two examples—are relatively recent in history (Sampson, 1985).

Evolution has continued with the development of different technical instruments for writing:

the feather, the pencil, the typewriter, and the computer. Brain representation of written

language has necessarily changed in some way, too. Neuropsychological syndromes

associated with brain pathology have evolved over time.

We can assume that the consequences of brain pathology in a Palaeolithic man

were not the same as for a 19th-century individual (when agraphia was first described), or

for contemporary man or woman (some of whom frequently spending most of their working

day in front of a computer screen). It can be anticipated that in the future new


neuropsychological syndromes resulting from new living conditions will be described.

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5. Origins of Calculation Abilities2 Introduction

Calculation ability represents an extremely complex cognitive process. It has been

understood to represent a multifactor skill, including verbal, spatial, memory, and executive

function abilities (Ardila et al., 1998). Calculation ability is quite frequently impaired in cases

of focal brain pathology (Ardila & Rosselli, 2002; Dansilio, 2008; Domahs et al., 2011;

Grafman, 1988; Hecaen et al., 1961) and dementia (Deloche et al., 1995; Grafman et al.,

1989; Parlatto et al., 1992; Rosselli & Ardila, 1998). The loss of the ability to perform

calculation tasks resulting from a cerebral pathology is known as acalculia or acquired

dyscalculia. Acalculia has been defined as an acquired disturbance in computational ability

(Loring, 1999). The developmental defect in the acquisition of numerical abilities, on the

other hand, is usually referred to as developmental dyscalculia or dyscalculia.

Calculation abilities have followed a long process from the initial quantification

systems up to modern algebra, geometryy, and physics. Some rudimentary numerical

concepts are observed in animals, and there is no question that pre-historic man used

some quantification. However, the ability to represent quantities, the development of a

numerical system, and the use of arithmetical operations are found only in old civilizations.

This chapter reviews the evolution of calculation abilities, including numerosity and

counting in non-human animals, calculation abilities in primitive and modern humans, and

links between language and number concepts throughout human history. In addition, the

paper reviews contemporary studies of the neurological substrates of numerical abilities

and discusses the implications of technological advances with regard to continued evolution

of these abilities.

1. A previous version of this paper was published in: Ardila, A. On the evolution of calculation abilities. Frontier in Evolutionary Neurosciences, 2, 1-8.


Numerical concepts in animals

The origin of mathematical concepts can be traced to sub-human species. Throughout

recent history different reports have argued that animals (horses, rats, dogs, chimpanzees,

dolphins, and even birds) can use numerical concepts and perform arithmetical operations.

Some of these reports represent evident charlatanry directed to the general public. Some

others, however, are rigorous and highly controlled scientific studies (e.g., Rugani et al.,

2009).

There is, in general, agreement that some rudimentary numerical concepts are

observed in animals. These basic numerical skills can be considered as the real origin of

the calculation abilities found in contemporary man. For instance, pigeons can be trained to

peck a specific number of times on a board, and rats can be trained to press a lever a

certain amount of times to obtain food (Koehler, 1951; Mechner, 1958; Capaldi & Miller,

1988). It could be conjectured that pigeons and rats can count, at least up to a certain

quantity; that is, they can recognize how many times a motor act – to peck on a board or to

press a lever – has been repeated. Whether or not this behavior can really be interpreted

as counting is nonetheless questionable. However, this behavior can be observed after

long and painstaking training. Nonetheless, these animal responses (to peck or to press the

lever) are not precise but just approximate. In other words, when the rat is required to press

the lever seven times, the rat presses it about seven times (i.e., 5, 6, 7, 8 times). As

Dehaene (1997) emphasizes, for an animal, 5 plus 5 does not make 10, but only about 10.

According to him, such fuzziness in the internal representation of numbers prevents the

emergence of exact numerical arithmetical knowledge in animals. Using highly controlled

and sophisticated designs, it has been pointed out that chimpanzees can even use and add

simple numerical fractions (e.g., 1/2 + 1/4 = 3/4) (Woodruff & Premack, 1981). These

observations support the assumption that some quantity concepts can be found in different

animals.


Counting (or rather, approximately counting) motor responses is a motor act as is

walking or running. “Counting” lever pressings is not very different from estimating the effort

(e.g., number of steps or general motor activity) required in going from one point to another.

Counting in such a case could be linked to some proprioceptive and kinesthetic information.

In the human brain Kansaku et al. (2006) identified a network of areas involved in

enumerating small numbers of auditory, visual, and somatosensory stimuli, and in

enumerating sequential movements of hands and feet, in the bilateral premotor cortex, pre-

supplementary motor area, posterior temporal cortex, and thalamus. The most significant

consistent activation across sensory and motor counting conditions was observed in the

lateral premotor cortex. Lateral premotor activation was not dependent on movement

preparation, stimulus presentation timing, or number word verbalization. Furthermore,

movement counting, but not sensory counting, activated the anterior parietal cortex.

Chimpanzees, but also rats and many other animals, can distinguish numerosity

(i.e., global quantification); for instance, they prefer a bowl containing a larger number of

nutritive elements (such as chocolates or pellets) when selecting between two bowls

containing different amounts (Davis & Perusse, 1988). It may be conjectured that global

quantification (numerosity perception) and counting (at least the approximate counting of

motor responses) represent kinds of basic calculation abilities found at the animal level.

Rats prefer a bowl containing 20 pellets to a bowl containing only 10 pellets; however, they

do not prefer a bowl containing 20 pellets to a bowl containing 21 pellets. Obviously,

numerosity perception is related to the size and shape of the visual image projected to the

retina. It can be assumed that 20 pellets in a bowl result in a larger and more complex

retinal image than 10 pellets. But the visual image corresponding to 20 pellets is difficult to

distinguish from the visual image corresponding to 21 pellets.

Development of calculation abilities in children


During child development, different stages in the acquisition of numerical knowledge are

observed (Klein & Starkey, 1987). They include global quantification, recognition of small

quantities, numeration, correspondence construction, counting, and arithmetic (Table 5.1).

As mentioned, some fundamental numerical concepts can be observed at the animal level,

and it is not surprising to find them in small children. The initial levels of numerical

knowledge are found in pre-school children. The development of complex numerical

concepts requires long school training. Complex arithmetical concepts depend upon a

painstaking learning process, and they are not usually found in illiterate people. The

different stages in the acquisition of numerical concepts are associated with the language,

perceptual, and general cognitive development. Variability is normally observed, and some

children can be faster in the acquisition of numerical abilities. The different stages appear in

a sequential way, and the understanding of more complex concepts requires the acquisition

of more basic levels. A percentage of otherwise normal children can fail in using numerical

concepts normally expected at their age. The term developmental dyscalculia has been

used to refer to this group of underperforming children.

Numerical abilities in pre-school children

Global quantification or numerosity perception represents the most elementary

quantification process. Global quantification supposes the discrimination between

collections containing different number of objects (Davis et al., 1985). Global quantification

simply means which set of elements is bigger and which one is smaller. Global

quantification is observed at the animal level: Many animals can select the larger collection

of elements when they have to choose. However, the ability to distinguish which collection

is larger depends upon the number of elements in the collections. To distinguish 3 and 4

elements may be easy (4 is 25% larger than 3). To distinguish 10 and 11 elements is

obviously harder (11 is only 10% larger than 10). By the same token, to distinguish 10 from

20 elements is easy (the double), but to distinguish 100 from 110 is hard (one tenth). What


is important is the ratio existing between the two collections of elements (so called

psychophysics Weber's fraction).

__________________________________________________________________________________

Global quantification What collection is bigger and smaller

Recognition small quantities Differentiate one, two and three elements

Enumeration Sequencing the elements in a collection

Correspondence construction To compare collections.

Counting A unique number name is paired with each object

one-one principle Each object in a collection is to be paired with one and only one

number name

stable order principle Each name is assigned to a permanent ordinal position in the list

cardinal principle The final number name used in a counting sequence refers to the

cardinal value of the sequence

Arithmetic Number permutability (e.g., adding, subtracting).

__________________________________________________________________________________

Table 5.1. Different levels of numerical knowledge (adapted from Klein and Starkey,

1987)

Global quantification is expressed in the language with words such a "many", "a lot"

and similar terms. For small quantities, the words "several", "a few" and similar quantity


adverbs are included in the language. Quantity adverbs used in everyday speech represent

global quantifiers. Quantity adverbs appear early in language history and also in child

language development earlier than the numerical system. As mentioned before, all known

world languages use global quantification and possess words to refer to “many”, “a lot”. All

languages oppose small quantities (one, two, a few) to “many”, “a lot”. As a matter of fact,

“many”, “much” and similar global quantifiers represent early words in language

development.

Global quantification, however, does not represent a truly numerical process

because it does not suppose a one-to-one correspondence. Enumeration (sequencing the

elements in a collection of elements; this process supposes the individualization of each

element) represents the most elementary type of true numerical knowledge (Klein &

Starkey, 1987). Enumeration is required to distinguish the individual elements in the

collection (‘this, this, and this”, etc). In child language development, the most elementary

distinction is between “this” and “other”. “This” and “other” are also early words in child

language development.

Correspondence construction constitutes a type of enumeration used to represent

the number of objects in a collection and to compare collections. The amount of elements

in a collection is matched with the amount of elements in an external aid (fingers, pebbles,

knots, strokes, marks, dots, etc.). It implies, in consequence, a one-to-one correspondence:

Each one of the elements in the collection corresponds to one finger, or pebble, knot,

stroke, mark, or dot, or whatever. An external devise can be used for making the

correspondence construction. The most immediate devise are the fingers. During

enumeration usually the fingers are used to point the objects.

Counting represents a sophisticated form of enumeration: a unique number name is

paired with each object in a collection, and the final number name that is used stands for

the cardinal value of that collection. The initial object that is pointed to corresponds to

“one”, the following to “two” and so on. Some times, the very same finger name is used as


number name (i.e., the very same word is used for one and thumb, two and index finger,

etc.). The collection has the amount of objects that corresponds to the last pointed object

(cardinal principle). Arithmetic represents an advanced numerical system, which comprises

number permutability (e.g., adding, subtracting).

Human infants are able to recognize numerosity for small quantities (usually up to

three-six items) (Antell & Keating, 1983), but the ability to construct correspondences

emerges only during the child's second year (Langer, 1986). During the second year the

child also begins to use some number name, and usually develops the ability to correctly

count up to three. The child thus acquires the knowledge of two basic principles in counting.

(1) One-to-one principle (i.e., each object in a collection is to be paired with one and only

one number name). (2) The stable order principle (each name is assigned to a permanent

ordinal position in the list; the sequence of numbers is always the very same: one, two,

three, etc.). At this point, however, the child does not yet exhibit a cardinal principle; i.e.,

the final number name used in a counting sequence refers to the cardinal value of the

sequence. If a collection is counted “one, two, three”, it means that in that collection there

are three objects) (Klein & Starkey, 1987). Cardinal principle will be observed in

three-year-old children (Gelman & Meck, 1983).

At this point, the child can count small quantities, usually below 10. During this

period the child is also learning how the numerical system works and memorizing the

number words. Most often, the numerical system contains three different segments: (1)

from one to ten different words are used. (2) From 10 to 20 counting becomes idiosyncratic

and quite frequently irregular. In English “eleven” has not any apparent relationship with

“one”; “twelve” has an evident relation with “two” but it is a unique word number; from 13 to

19 the ending “teen” is used. In Spanish, from 11 (“once”) to 15 (“quince”) the ending “ce” is

used. From 15 to 19 the words numbers are formed as “ten and six”, “ten and seven” etc.

20 (”veinte”) has not any apparent relation with 2 (“dos”). And (3) from 20 on the numerical

system becomes regular. Word numbers are formed as “twenty and one”, “twenty and two”,

etc. Learning of the whole numerical system usually is completed at school.


Computational strategies (e.g., adding; if a new item is included in a collection, the

collection will become larger and the next cardinal number-name will be given to that

collection) are found in three-to five-year-old children, initially only for small quantities.

Development of numerical abilities at school

Adding and subtracting numerical quantities and the use of computational principles are

observed during in first-and-second grade children, but they only become able to

manipulate the principles of multiplying and dividing after a long and painstaking training

period, usually during third to fifth grade.

Understanding that subtracting is the inverse operation of adding is usually acquired

at about five to six years of age. At this age the child begins to use three different

procedures for performing additions and subtractions: (1) Counting using the fingers. (2)

Counting aloud not using the fingers. And, (3) memorizing additions and subtractions for

small quantities (one plus one is two; two plus two is four; two minus one is one, etc.). The

last strategy becomes progressively stronger when advancing age and schooling.

Nonetheless, children continue using the finger for adding and subtracting larger quantities.

From the age of 10 until about 13 years, counting using the fingers progressively

disappears, but counting aloud, and performing arithmetical operations aloud, remains.

Automatic memory not only for additions and subtractions, but also multiplications

(multiplication tables) and divisions, becomes progressively more important. (Siegler, 1987;

Grafman, 1988). As a matter of fact, adding and subtracting one digit quantities (e.g., 7 + 5

= 12; 4 + 5 = 9; 8 – 5 = 3; etc.) represents a type of numerical rote learning, similar to the

multiplication tables. Interesting to note, the performance of arithmetical operations aloud

may remain during adulthood, even in highly educated people.

It should be emphasized that there is a significant variability in the specific strategies

used by different children at the same age. Furthermore, the very same child can recur to

different strategies when solving different arithmetical problems. In some situations, for


instance, the child can recur to the fingers, whereas in a different operation, it may not

require using the fingers. Or, the child can be able to use some multiplication tables

whereas failing with others.

At about the age of eight to nine the children usually learn to multiply. This requires

the memorization of the multiplication tables. The errors most frequently found when

learning the multiplication tables are those answers that could be correct for other number

within the same series (e.g., 4 X 5 = 16). These errors may be the result of some

interference. They can be observed in children at any age, and even they are some times

found in normal adults (Graham, 1987).

Development of abstract reasoning and increase in working memory span contribute

to the use of mathematical algorithms, i.e., the set of rules used for solving arithmetical

problems following a minimal number of steps. The development of algorithms begins when

learning the basic arithmetical operations. Progressively, they become more automatic,

representing basic strategies for solving arithmetical problems. Development of abstract

thinking allows for the use of magnitudes to be applied to different systems (use of the

numerical system in measuring time, temperature, etc.) and to the understanding of

quantities expressed in a symbolic way

Calculation abilities in pre-historic man

Chimpanzees are capable of various forms of numerical competence, including some

correspondence constructions (that is, comparing two collections of elements) for low

quantities (Premack, 1976; Davis & Perusse, 1988). Most likely, these numerical abilities

also existed in pre-historic man. Homo sapiens antecessors may have been capable of

using correspondence constructions in some social activities, such as food sharing. It has

been proposed that Homo habilis (ancestor of Homo erectus, living about 2.3 million to 1.4

million years ago) needed to use correspondence constructions when butchering large

animal carcasses (Parker & Gibson, 1979). Distributing pieces of a divided whole (e.g.,


prey) into equal parts required the ability to construct one-to-one correspondences.

Paleolithic man was probably able to match the number of objects in different groups and,

eventually, the number of objects in a collection with the number of items in some external

cue system, e.g., fingers or pebbles (incidentally, calculus means pebbles).

The immediate recognition of certain small quantities is found not only in animals,

but also in small children. Animals and children can readily distinguish one, two, or three

objects (Fuson, 1988; Wynn, 1990, 1992; Cook & Cook, 2009). Antell and Keating (1983)

observed that newborn infants were able to discriminate among visual stimulus arrays

consisting of a few dots. It was found that infants were able to discriminate between small

numbers (2 versus 3) but not for larger sets. This ability for discriminating and also

representing and remembering small numbers of items has also been reported by other

authors (e.g., Starkey & Cooper, 1980). Interestingly, evoked potentials at three months are

already capable of marking changes in the nature and number of a set of objects, and

these activation changes relate to the parietal lobe (Dehaene & Dehaene-Lambertz, 2009).

Noteworthy, in normally developing children and adults, the increase in arithmetic

competence is associated with shift of activation from frontal brain areas to parietal areas.

A shift of activation is also observed within the parietal lobe from the intraparietal sulci to

the left angular gyrus; experts’ arithmetic proficiency depends on a more extended

activation than the network found in beginners. In expert individuals with solid, extensive

mathematical training, specific brain activation changes are also observed (Zamarian et al.,

2009).

Oneness, twoness, and threeness seemingly are basic perceptual qualities that our

brain can distinguish and process without counting. It can be conjectured that when pre-

historic humans began to speak, they may have been able to name only the numbers one,

two, and three, corresponding to specific perceptions. To name them was probably no

more difficult than naming any other sensory attribute (Dehaene, 1997). Of note, all world

languages can count up to three, even though three may represent “many”, “several”, or “a

lot” (Hurford, 1987). “One” is obviously the unit, the individual (the speaker may also be

“one”). “Two” conveys the meaning of “another” (for example, in English and also in


Spanish, “second” is related with the verb “to second” and the adjective “secondary”).

“Three” may be a residual form of “a lot”, “beyond the others”, or “many” (for example,

“troppo”, which in Italian means “too much”, is seemingly related with the word three -tre).

In the original Indo-European language, spoken perhaps some 15000–20000 years ago,

apparently the only numbers were “one”, “one and another” (two), and “a lot”, “several”, or

“many” (three) (Dehaene, 1997). Interestingly, in some contemporary languages, two

different plurals are found: a plural for small quantities (usually two, sometimes three and

four) and a second plural for larger quantities; for instance, in Russian, “one house” is “odin

dom”, “two, three, or four houses” is “dva, tri, cheterye doma” but “five houses” is “pyat

domov”.

Of note, in different world languages, the word “one” does not have any apparent

relationship with the word “first”; and the word “two” is also not related with the word

“second”. “Three” may sometimes, but not always, hold some relationship with “third”.

Beyond three, ordinals are clearly associated with cardinal numbers (Table 5.2). The con-

clusion is obvious: for small quantities (one, two, three), cardinals and ordinals must have a

different origin. For larger quantities, ordinal numbers are derived from cardinals. As a

matter of fact, one/first and two/second correspond to different conceptual categories.

It may be speculated that for pre-historic man the first person and the second person

in a line (or the first animal and the second animal during hunting, or other similar concepts)

do not seem to be related with the number one and the number two. For small children

“first” has the meaning of “initial” (e.g., “I go first”) whereas “second” is related to “later” or

“after” (e.g., “you go second”). These words have a temporal and also spatial meaning, but

not an evident numerical meaning. The association between “one” and “first”, and “two” and

“second” seems a relatively advanced process in the development of numerical concepts.

That is, the numerical meaning of “first” and “second” seems to appear after its temporal

and spatial meaning. The association between ordinals and cardinals becomes evident only

for larger quantities (more than three) and seems to represent a later acquisition in human

evolution and the complexization of numerical concepts. Moreover, in many contemporary

languages (e.g., the Huitoto language, spoken by the Huitoto Indians in the Amazonian


jungle; indian-cultures.com/ Cultures/huitoto.html) there are no ordinal numbers. For “first”,

the Huitoto language uses “the beginning”; to express “second” the word “another” is used.

____________________________________________________________________________________

English Spanish Russian Greek Persian Arab Hindi Aymara(1) Ibo (2) ____________________________________________________________________________________

One Uno Odin Ena Yek Wahid Ek Maya Nbu

First Primero Pervie Proto Aval Awal Pahla Nairankiri Onye-nbu

Two Dos Dva Dio Dou Ethnaim Do Phaya Ibua

Second Segundo Vtoroi Deftero Douvoum Thani Dusra Payairi Onye-ibua

Three Tres Tri Tria Seh Thalatha Tin Kimsa Ito

Third Tercero Treti Trito Sevoum Thalith Tisra Kimsairi Nke-ito

Four Cuatro Cheterie Tesera Chahaar Arrbaa Char Pusi Ano

Fourth Cuarto Chetviorti Tetarto Chaharoum Rabiek Chautha Pusiiri Nke-ano

Five Cinco Piat Pente Pang Khamsa Panch Pheschka Ise

Fifth Quinto Piati Pemto Panjoum Khamis Panchvan Pheskairi Nke-ise

Six Seis Shest Exi Shash Sitta Chha Sojjta Isi

Sixth Sexto Shestoi Ekto Shashoom Sadis Chhatha Sojjtairi Nke-isi


Seven Siete Siem Epta Haft Sabaa Sat Pakallko Isaa

Seventh Septimo Sidmoi Evthomo Haftoom Sabieh Satvan Pakallkoiri Nke-isaa

Eight Ocho Vosiem Octo Hasht Thamania Ath Kimsakallko Asato

Eighth Octavo Vosmoi Ogdoo Hashtoom Thamin Athvan Kimsakallkiri Nke-asato

Nine Nueve Dievit Enea Nouh Tisaa Nau Llatunca Itonu

Ninth Noveno Diviati Enato Houhum Tasih Nauvan Llatuncairi Mke-Itonu

Ten Diez Diesit Deka Dah Ashra Das Tunca Iri

Tenth Decimo Disiati Dekato Dahoom Asher Dasvan Tuncairi Mke-iri

____________________________________________________________________________________ (1) Ameridian language spoken in Bolivia; (2) Ibo: Eastern Nigeria

Table 5.2. Cardinal and ordinal numbers in different languages

Arithmetical abilities are clearly related with counting. Counting – not simply

recording the approximate amount of motor responses required for obtaining reinforcement,

but actually saying aloud a series of number words that correspond to a collection of

objects – is relatively recent in human history. Counting also occurs relatively late in child

development. In human history, as well as in child development, counting using number

words begins with sequencing the fingers (i.e., using a correspondence construction) (Hitch

et al., 1987). The name of the finger and the corresponding number can be represented

using the very same word (that means the very same word is used for naming the thumb

and the number one; the very same word is used to name the index finger and the number

two, etc.). The fingers (and toes; as a matter of fact, many languages such as Spanish use


a single word (dedo) to name both the fingers and toes) are usually sequenced in a

particular order. This strategy represents a basic procedure found in different ancient and

contemporary cultures around the world (LevyBruhl, 1910/1947; Cauty, 1984; Klein &

Starkey, 1987; Dansilio, 2008). Interestingly, it has been demonstrated that children with

low arithmetical skills also present a finger misrepresentation on the Draw-a-Person test

(Pontius, 1989). This observation has been confirmed in different cultural groups. By the

same token, difficulty in recognizing and naming the fingers represents a reliable predictor

of developmental dyscalculia (Kaufmann, 2008).

Taking a typical example as an illustration, the Colombian Sikuani or Guahibo

Amazonian jungle Indians (indian-cultures.com/Cultures/guahibo.html) count in the following

way: the person (an adult when counting or a child when learning to count) places his/her

left hand in supination; to point to number one, the right index points to the left little finger,

which is then bent (Queixalos, 1989). The order followed in counting is always from the little

finger to the index. To point to number five, the hand is turned and the fingers opened; for

six, both thumbs are joined, the left fingers are closed, and the right opened; they are

opened one after the other for seven, eight, nine and ten. Between 11 and 20, the head

points to the feet and the sequence is re-initiated. The lexicon used is:

1: kae (the unit, one)

2: aniha-behe (a pair, both)

3: akueyabi

4: penayanatsi (accompanied; that is, the fingers together)

5: kae-kabe (one hand)

Numbers from six to nine, are formed with “one hand and (a certain number) of

fingers”. Ten becomes “two hands”:

6: kae-kabe kae-kabesito-nua (one hand and one finger)

7: kae-kabe anih-akabesito-behe (one hand and a pair of fingers)


10: anih-akabe-behe (two hands)

“Two hands” is maintained between 10 and 20. Toes (taxawusito) are added

between 11 and 14; and “one foot” (kaetaxu) is used in 15. Twenty is “two hands together

with two feet”:

11: aniha-kabe-behe kae-taxuwusito (two hands and one toe)

12: aniha-kabe-behe aniha-tuxuwusito-behe (two hands and two toes)

15: aniha-kabe-behe kae-taxu-behe (two hands and one foot)

16: aniha-kae-behe kae-taxu-behe kaetaxuwusito (two hands, one foot, and one toe)

20: aniha-kabe-behe aniha-taxu-behe (two hands and two feet)

Fingers are named according to their order in counting (as mentioned above,

counting begins always with the little finger of the left hand). The Sikuani language

possesses number words only up to three (kae, aniha-behe, akueyabi). Four (penayanatsi

= accompanied, together) represents a correspondence construction. Strictly speaking, the

Sikuani language counts only up to three. From four to twenty, they use a correspondence

construction, not really counting; and for higher quantities, they resort to a global

quantification.

Sometimes not only the fingers (and toes) but also other body segments may be

used in counting: the wrist, the shoulders, the knees, etc. (Levy-Bruhl, 1910/1947; Cauty,

1984; Dansilio, 2008). However, sequencing the fingers (and toes) represents the most

universal procedure in counting. Some languages (e.g., some Mayan dialects and

Greenland Eskimo) use the same word to denote the number 20 (that is, “all the fingers

and all the toes”) and “a person”.

In different Amerindian languages, for higher than 10 or 20 figures, most often

“many” is used (global quantification principle) (Cauty, 1984; Ifrah, 2000). Or, they can refer

to other people’s hands (correspondence construction) (e.g., thirty-five might be something

like “my two hands, my two feet, my father’s two hands, my father’s one foot”). As


mentioned, “twenty” sometimes becomes something like “one person”, a sort of higher

order numeral. It is interesting to note that in some contemporary languages (like English

and Spanish) “one” means the unit, but it is also used as a sort of indefinite personal

pronoun. In English and Spanish we can also use “one” as synonymous with “myself”.

Twenty is found to be the base number in the Mayan numerical system (Swadesh, 1967;

Cauty, 1984). In many contemporary languages, a 10 and/or 20 base is evident.

“Digit” (from Latin digitus) means both number and finger. The correspondence

construction between numbers and fingers is evident. Latin number notation was originally

Etruscan (Turner, 1984) and referred (as in other languages) to the fingers. One, two, and

three were written simply by making vertical strokes. In four, the Latin system resorts to a

simplification. Originally, four was written IIII, but later on it became IV. Five (V) represented

the whole hand with the arm bent (that is, all the fingers of the hand), and ten (X) the two

arms crossed.

From a neuropsychological perspective, a strong relationship between numerical

knowledge, finger gnosis, and even lateral (right–left) knowledge is evident (Ardila and

Rosselli, 2002; Kaufmann, 2008). Finger agnosia (and probably right–left discrimination

disturbances) could be interpreted as a restricted form of autotopagnosia (inability to

recognize or localize the various body parts) (Ardila et al., 1989, 2000).

It is not surprising to find that a decimal (or vigesimal, i.e., with a base of 20) system

has been most often developed. Simultaneously or very close in time, decimal systems

appeared in different countries (Sumer, Egypt, India, and Crete). Different symbols were

used to represent 1, 10, 100, and 1000 (Childe, 1936; Dansilio, 2008) (Figure 5.1.).


Tabla 5.3. Different numerical systems

There is, however, an interesting and intriguing exception: Sumerian and later

Babylonians (about 2,000 BC) developed not only a decimal but also a sexagesimal

system: a symbol represented 60 or any 60-multiple and another different symbol

represented the number 10 and any 10-multiple. Thus, for example, the number 173 was

then represented: 2 × 60 (the symbol for 60 repeated twice) + 5 × 10 (the symbol for 10

repeated five times) + 3 (a symbol for units repeated three times). A base of 60 has

remained for some contemporary time measures (e.g., minutes and seconds). Twelve is

also frequently maintained as a “second-order” unit (e.g., a dozen). Evidently, 60 results

from “five times twelve”. Five obviously is “one hand”, and the question becomes, where


does 12 come from? What are the two additional units? It might be speculated that 12

means the 10 fingers plus the two feet – or even the two elbows or the two shoulders or the

two knees (individuality of components is easier to appreciate in the hands than in the feet).

But this is only speculation, although it is feasible according to our knowledge about

counting procedures used in different cultural groups (Levy-Bruhl, 1910/1947; Ifrah, 2000;

Dansilio, 2008).

Maya Indians developed a similar system, but had 20 as a base (Leon-Portilla,

1986). They used different symbols to represent 20, 400 (20 × 20), and 8000 (20 × 20 × 20)

(Cauty, 1984) (Figure 5.1.)

Figure 5.1. Maya vigesimal numerical system.


Thus, reviewing the history of numerical concepts, it is found that world languages

developed a base 10 (10 fingers) or 20 (10 fingers plus 10 toes) or even five (five fingers)

to group quantities. In some contemporary languages a residual 20-base can be found

(e.g., in French 80 can be “four twenties”). In many contemporary languages, different

words are used between 1 and 10. Between 10 and 20, the numerical systems usually

become irregular, unpredictable, and idiosyncratic. From 20 onward, numbers are formed

simply with the words “twenty plus one”, “twenty plus two”, etc. Some contemporary

languages still use a five-base in counting. For instance, in the Amerindian language

Tanimuca in South America (www.ethnologue.com), speakers count up to five. Between

five and 10, numbers are “five one”, “five two”, and so on.

Further developments of arithmetical abilities

Writing numbers appeared earlier in history than writing language. Some cultures (e.g.,

Incas) developed a number representing system, but not a language representing system

(Swadesh, 1967). As mentioned before, “calculus” means pebble. Pebbles, marks, knots,

or any other element were used as a correspondence construction to record the number of

elements (people, cows, fishes, houses, etc). In Sumer, the first number writing system has

been found (about 3,000 BC) (Childe, 1936; Ifrah, 2000): Instead of using pebbles, fingers,

or knots, it was simpler just to make a mark (a stroke or a point) on the floor, on a tree

branch, or on a board if one wanted to keep the record. In Egypt, India and later in Crete, a

similar system was developed: units were represented by a conventional symbol (usually a

stroke) repeated several times to mean a digit between one and nine; a different symbol

was used for 10 and 10-multiples. Incas Indians developed a special system to represent

numbers with knots in a rope (quipus) (Ascher & Ascher, 1980) (Figure 5.2).


Positional digit value is clearly evident in Babylonians, and around 1,000 BC, the zero was

introduced. Positional value and zero are also evident in Maya Indians (Leon-Portilla,

1986). Egyptians and Babylonians commonly used fractions. Small fractions (1/2, 1/3, and

1/4) are relatively simple numerical concepts, and even chimpanzees can be trained to use

small fractions (Woodruff & Premack, 1981).

As pointed out, recognition of individual marks or elements up to three is easy: It

represents an immediate perception readily recognizable. Beyond three, the number of

marks (strokes or dots) usually has to be counted and errors are more likely. Furthermore,

it is rather time-consuming and cumbersome to be constantly counting marks. Interestingly,

the different digit notational systems always represent one, two and three with strokes (or

points, or any specific mark). In other words, the numbers one, two and three are written

making one, two or three strokes. But beyond these figures, digit writing may give way to

other strategies. In our Arabic digit notation system, “one” is a vertical line whereas two and

three were originally horizontal lines that became tied together by being handwritten (Ifrah,

2000). This observation may be related with the inborn ability to perceptually recognize up

to three elements. Beyond three, errors become progressively more likely. Perceptually dis-

tinguishing eight and nine strokes is not as easy as distinguishing between two and three

strokes. The introduction of a different representation for quantities over three was a useful

and practical simplification.


Figure 5.2. Example of an Inca Indian quipu.

The numerical system, along with measurement units, were developed departing

from the body dimensions (fingers, hands, arm, steps, etc.). This tendency to use the

human body not only to count but also as measure units is still observed in some contem-

porary measurement units (e.g., foot).

Adding, subtracting, multiplying and dividing were possible in the Egyptian system,

but of course, following procedures was quite different from those procedures we currently

use. Egyptians based multiplication and division on the “duplication” and “halving” method

(Childe, 1936). Interestingly, this very same procedure (duplicating and halving quantities)

is also observed in illiterate people when performing arithmetical operations. Thus, to

multiply 12 × 18 in the Egyptian system the following procedure was followed:


1 18

2 36

*4 72

*8 144

_____

Total 216

(The number 18 is duplicated one or several times, and the amounts corresponding to 12

(4 + 8 in this example) are selected and summed up: 72 + 144 = 216. To divide, the inverse

procedure was used. Therefore, the procedure used to divide 19 by 8 would be:

1 8

*2 16

2 4

*4 2

*8 1

That is, 2 + 4 + 8 (2 + 1/4 + 1/8), which is 2.375

In brief, different steps were followed in the development of arithmetical abilities:

representing quantities, initially as correspondence constructions (i.e., one mark represents

one element), later new marks were added to represent larger quantities (usually 10);

providing a positional value to the marks; using fractions; and computing quantities (adding

and subtracting; and later multiplying and dividing). As pointed out, recognition of individual

marks or elements up to three is easy: It represents an immediate perception readily

recognizable. Beyond three, the number of marks (strokes or dots) usually has to be

counted and errors are more likely. Furthermore, it is rather time-consuming and

cumbersome to be constantly counting marks. Interestingly, the different digit notational


systems always represent one, two and three with strokes (or points, or any specific mark).

In other words, the numbers one, two and three are written making one, two or three

strokes. But beyond these figures, digit writing may give way to other strategies. In our

Arabic digit notation system, “one” is a vertical line whereas two and three were originally

horizontal lines that became tied together by being handwritten (Ifrah, 2000) (Figure 5.3.)

This observation may be related with the inborn ability to perceptually recognize up to three

elements. Beyond three, errors become progressively more likely. Perceptually dis-

tinguishing eight and nine strokes is not as easy as distinguishing between two and three

strokes. The introduction of a different representation for quantities over three was a useful

and practical simplification.

Figure 5.3. Origins of the Arabic numbers 1, 2 and 3.

The numerical system, along with measurement units, was developed departing

from the body dimensions (fingers, hands, arm, steps, etc.). This tendency to use the

human body not only to count but also as measure units is still observed in some contem-

porary measurement units (e.g., foot).


The neuroscience of calculation abilities

Since primary acalculia (a basic defect in computational ability) was initially described by

Henschen (1925) it has been associated with left posterior parietal damage (e.g., Mazzoni

et al., 1990; Ardila et al., 2000; Mayer et al., 2003). Furthermore, it was suggested that

different cerebral pathways are responsible for processing rote numerical knowledge (e.g.,

multiplication tables) and semantic knowledge of numerical quantities. Dehaene and Cohen

(1997) have proposed that a left subcortical network contributes to the storage and retrieval

of rote verbal arithmetical facts, whereas an inferior parietal network is dedicated to the

mental manipulation of numerical quantities.

Neuroimaging techniques (e.g., fMRI) have been used to analyze the pattern of

brain activity during diverse calculation tasks. It has been demonstrated that different brain

areas are active during arithmetical tasks, but the specific pattern of brain activity depends

on the particular type of task that is used. At minimum, the following brain areas become

activated during calculation: the upper cortical surface and anterior aspect of the left middle

frontal gyrus (Burbaud et al., 1995); the supramarginal and angular gyrus (bilaterally)

(Rueckert et al., 1996); the left dorsolateral prefrontal and premotor cortices, Broca’s area,

and the inferior parietal cortex (Burbaud et al., 1999); and the left parietal and inferior

occipitotemporal regions (lingual and fusiform gyri) (Rickard et al., 2000). The diversity of

brain areas involved in arithmetical processes supports the assumption that calculation

ability represents a multifactor skill, including verbal, spatial, memory, body knowledge, and

executive function abilities (Ardila & Rosselli, 2002). Dehaene et al. (2004), however,

proposed that regardless of the diversity of areas that become active during arithmetical

tasks, the human ability for arithmetic is associated with activation of very specific brain

areas, in particular, the intraparietal sulcus (Figure 5.4). Neuroimaging studies with humans

have demonstrated that the intraparietal sulcus is systematically activated during a diversity


of number tasks and could be regarded as the most crucial brain region in the

understanding and use of quantities (Ashkenazi et al., 2008). These observations have

been supported using brain electrostimulation (Roux et al., 2009). Other brain areas, such

as the precentral area, the inferior prefrontal cortex, and the inferior parietal cortex are also

activated when subjects engage in mental calculations (Kas et al., 2011). RoŞca (2009)

has proposed that there exists a fronto–parieto–subcortical circuit responsible for complex

arithmetic calculations and that procedural knowledge relies on a visuo-spatial sketchpad

that contains a representation of each sub-step of the procedure.

Figure 5.4. Left hemisphere intraparietal sulcus.


Traditionally, calculation defects have been associated with posterior left parietal

damage (Henschen, 1925; Boller & Grafman, 1983), and are frequently included in the so-

called Gerstmann’s (or angular gyrus) syndrome. Symptoms of Gerstmann’s syndrome

(acalculia with agraphia, disorders in right-left orientation, and finger agnosia) (Gerstmann,

1940) can be found during direct cortical stimulation in the angular gyrus region (Roux et

al., 2003). Using fMRI, it has been observed that the left angular gyrus is not only involved

in arithmetic tasks requiring simple fact retrieval, but may show significant activations as a

result of relatively short training of complex calculation (Delazer et al., 2003).

Colvin et al. (2005) investigated numerical abilities in a split-brain patient using

experiments that examined the hemispheres’ abilities to make magnitude comparisons.

One experiment examined the ability to enumerate sets of stimuli, and another two

experiments required judgments about two concurrently presented stimuli that were either

identically coded (i.e., two Arabic numerals, two number words, or two arrays of dots) or

differently coded (e.g., an Arabic numeral and a number word). Both hemispheres were

equally able to enumerate stimuli and make comparisons between numerical

representations regardless of stimuli coding. However, the left hemisphere was more

accurate than the right when the task involved number words.

Cohen et al. (2000) reported a patient with a lesion in the left perisylvian area who

showed a severe impairment in all tasks involving numbers in a verbal format, such as

reading aloud, writing to dictation, or responding verbally to questions of numerical

knowledge. In contrast, her ability to manipulate non-verbal representation of numbers, i.e.,

Arabic numerals, was comparatively well preserved. This observation supports the proposal

that language and calculation disorders can be dissociated (Basso et al., 2000). Some

authors have assumed that language and numerical concepts are organized differently in

the brain and follow distinct developmental patterns in children (Gelman & Butterworth,

2005). Other authors have suggested that calculation and language are mediated by

partially different and also partially overlapped brain systems (Baldo & Dronkers, 2007).


Semenza et al. (2006) have emphasized that calculation and language usually share the

same hemisphere.

In summary, diverse brain areas are activated during the performance of different

arithmetical tasks, although contemporary evidence suggests that the intraparietal sulcus

seems to play the most crucial role. During the learning of new calculation abilities,

additional brain areas become involved and the specific pattern of brain activity depends on

the particular type of test that is used. It can be assumed that during human history, the

development of new numerical abilities was correlated with the involvement of new brain

areas during the performance of progressively more complex numerical tasks.

Conclusion

Arithmetical abilities and number representation have existed for only some 5000–6000

years. Most likely, during the Stone-Age, only simple counting up to three and, of course,

“bigger” and “smaller” (magnitude judgment) concepts were present. Global quantification is

observed at the pre-human level. Correspondence constructions allowed for increasing the

amount of numbers to be used. The most immediate correspondence construction is

performed with the fingers. Finger knowledge and counting represent, to a certain extent,

the same cognitive ability, as is still evident in some contemporary languages, such as

Sikuani.

Counting, finger gnosis, and even lateral spatial knowledge may present a common

historical origin. Seemingly, calculation abilities were derived from finger sequencing.

Number representation and arithmetical operations are observed only since some 5000–

6000 years ago. Currently, calculation abilities are rapidly evolving due to the introduction

of modern technology and resulting cognitive demands. Right-left discrimination (as well as

the use of other spatial concepts) most likely was present in pre-historic man, because

requirements of spatial abilities may have been very high, even higher than in


contemporary man (Hours, 1982; Ardila and Ostrosky, 1984; Ardila, 1993). Right-left

discrimination and finger gnosis are strongly interdependent, and they can even be inter-

preted as components of the autotopagnosia syndrome. It seems, in consequence, that

there is a rationale for finding a common brain activity for finger gnosis, calculation, and

right-left discrimination (and in general, spatial knowledge mediated by language) (Ardila

and Rosselli, 2002).

Contemporary neuroimaging techniques, specifically fMRI, have demonstrated that

the left parietal lobe, particularly the intraparietal sulcus, is systematically activated during a

diversity of number tasks; other areas, particularly the frontal lobe, are also involved in

processing numerical information and solving arithmetical problems. Also, it has been

suggested there exists a fronto–parieto–subcortical circuit responsible for complex

arithmetic calculations and procedural knowledge.

It can be conjectured that numerical abilities continue evolving due to advances in

mathematical knowledge and the introduction of new technologies; for instance, instead of

writing numbers down on paper and applying certain computational rules, we more often

require the ability to use a pocket calculator or a computer program. Doubtless,

computation ability is evolving in a new direction. Brain representation of calculation may be

taking a new direction, and even the acalculia syndrome may present different clinical

manifestations.

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6. Origins of Executive Functions3

Introduction

"Executive functions" is a relatively new term in the neurosciences. Luria (1966, 1973,

1980) is the direct antecessor of the concept of executive functions. He distinguished three

functional units in the brain: (1) arousal-motivation (limbic and reticular systems); (2)

receiving, processing, and storing information (post-rolandic cortical areas); and (3)

programming, controlling, and verifying activity, depending on the activity of the prefrontal

cortex (Figure 6.1). Luria mentions that this third unit has an executive role. Lezak (1983)

referred to "executive functioning" to discriminate cognitive functions from the "how" or

"whether" of human behaviors. Baddeley (1986) grouped these behaviors into cognitive

domains that included problems in planning, organizing behaviors, disinhibition,

perseveration, reduced fluency, and initiation. Baddeley also coined the term "dysexecutive

syndrome."

3 A previous version of this paper was published in: Ardila, A. (2008). On the evolutionary origins of executive functions. Brain and Cognition, 68, 92-99


Figure 6.1. Three functional units in the brain (Luria, 1966, 1973, 1980)

What does “executive functions” mean?

The definition of executive function includes the concept of mental flexibility and also

ability to filter, interference, engage in goal-directed behaviors, and anticipate the

consequences of one's actions (Ardila & Surloff, 2007; Denckla, 1994, 1996; Goldberg,

2001; Luria 1969, 1980; Stuss & Benson 1986; Stuss & Knight, 2002). The concept of

morality, ethical behaviors, self-awareness, and the idea of the frontal lobes as manager

and programmer of the human psyche are also included (Anderson et al., 1999; Damasio,

1994; Moll et al., 2005; Luria, 1980). During the late 19th and early 20th centuries, clinical investigations documented

diverse behavioral disorders in cases of frontal pathology. "Frontal lobe syndrome" was


conceptualized by Feuchtwanger (1923). He correlated frontal pathology to behaviors that

were not related to overt speech, memory, or sensorimotor deficits. He emphasized the

personality changes in motivation, affective dysregulation, and the capacity to regulate

and integrate other behaviors. Goldstein (1944) expanded the capacity of frontal lobe

behaviors to include "the abstract attitude," initiation, and mental flexibility. Luria (1966,

1969) related prefrontal lobe activity with programming motor behavior, inhibiting

immediate responses, abstracting, problem solving, verbal regulation of behavior, and

reorienting behavior according to behavioral consequences, temporal integration of

behavior, personality integrity, and consciousness. During the 1970s, 1980s, and 1990s

several books exclusively devoted to the analysis of the prefrontal cortex were published

(e.g., Fuster, 1989; Miller & Cummings, 1998; Levin et al., 1991; Perecman, 1987;

Pribram & Luria, 1973; Roberts, 1998; Stuss & Benson, 1986). These works usually

assumed that "frontal" ("prefrontal") syndrome was synonymous with executive

dysfunction (Figure 6.2).

Progressively, it became apparent that “prefrontal syndrome” and “executive

dysfunction” are not synonymous. The prefrontal cortex plays a key monitoring role in

executive functions, but other brain areas are also involved (Elliott, 2003). Intact frontal

processes, although not synonymous with intact executive functioning, are an integral part

of it. Attempts to localize executive functioning to discrete frontal areas have been

inconclusive. The emerging view is that executive function is mediated by dynamic and

flexible networks. Neuroimaging results have also implicated posterior, cortical, and

subcortical regions in executive functioning (Park et al., 2011; Roberts et al., 2002).


Figure 6.2. Frontal lobe and its major areas.

Historically, Phineas Gage has become the most classical example for prefrontal

lobe pathology and disturbances in executive functions (Harlow 1868) (Figure 6.3).

Phineas Gage was a reliable foreman for a railroad company who suffered a tragic

accident in which a tampering rod was projected through his frontal lobes. Miraculously he

survived, but after this accident, he was described as "profane," "irascible," and

"irresponsible." Profound personality changes were reported, and according to Harlow, he

began to behave as an animal. The Phineas Gage case is usually cited as a typical

example of executive function disturbances. It is obvious however, that Phineas Gage’s

impairments were mostly situated at an emotional/motivational level, not at a purely

cognitive (or “metacognitive”) level. Overt behavioral changes were observed as

frequently found in frontal lobe pathology, but purely cognitive impairments were ill-

documented, partially due to the lack of appropriate cognitive assessment instruments.

Most frequently, executive functions are analyzed in experimental conditions using


diverse research strategies, such as solving diverse problems, finding similarities between

two words, providing an answer that requires inhibiting another, etc. A paradigm is

created, and the subject is required to solve it. The brain activity can be simultaneously

recorded, using brain electrical activity or recording the regional level of activation (e.g.,

Osaka, 2004). Alternatively, executive functions are analyzed in brain-damaged

populations in order to find the contribution of different brain systems (e.g., Jacobs et al.,

2007). This last approach represents the classical neuropsychological method. Executive

functions, however, rarely are analyzed in natural ecological conditions. How is it that

people solve everyday problems? This is obviously a crucial question in understanding

human behavior.

Figure 6.3. Reconstruction of the wound suffered by Phineas Gage (according to

Damasio et al., 1994)


Tests for executive function typically represent external tasks, requiring the correct

application of some intellectual abilities to be solved; for example, the Wisconsin Card

Sorting Test (Berg, 1948; Heaton, 1981), the Tower of Hanoi (Simon, 1975) (Figure 6.4),

and the Stroop test (Stroop, 1935) represent unusual and unfamiliar tasks, requiring the

development of new strategies, planning, thought, flexibility, etc. Nonetheless, they are

emotionally neutral tasks.

Figure 6.4. Tower of Honoi as an example of an executive functions test.

Although executive functions depend on extended networks including different

brain areas, it is assumed that the prefrontal cortex plays a major controlling and

monitoring role. Most important, prefrontal cortex does not only participate in those

classically recognized executive operations (sequencing, alternating, inhibiting, etc), but

also plays a crucial role in coordinating cognition and emotion (Mitchell & Phillips, 2007).


Most of the disturbances reported in Phineas Gage (and in many other cases of prefrontal

syndromes) refer to behavioral/emotional disturbances; or more exactly, disturbances in

coordinating cognition and emotion/motivation. The prefrontal lobe has extensive

connections to the subcortical and limbic system areas (Barbas, 2006; Damasio &

Andersen, 1993) and even its orbital portion could be regarded as an extension of the

limbic system. It seems that no laboratory test for executive function taps into the ability to

coordinate cognition and emotion, and in that regard, no executive function test has

significant ecological validity.

By coordinating cognition and emotion, the prefrontal lobe plays a major function:

controlling the limbic system impulses; that is, making limbic impulses “socially

acceptable” (e.g., Beer, John, Scabini & Knight, 2006; Blair, 2004; Lezak et al., 2004).

The inability to make basic biological needs socially acceptable, as clearly described in

Phineas Gage’s case, frequently represents a major disturbance in prefrontal patients. Of

course, we all would like to hit somebody when frustrated, to take possession of anything

we want, to stay at home instead of performing fatiguing work, and to approach any

potential sexual partner. That is exactly what many patients with prefrontal lobe pathology

frequently do.

Is there any fundamental core ability accounting for executive

functions?

Some disagreement exists around the question of unity or diversity (non-unitary) of

executive functions (e.g., Duncan et al., 1996; de Frias, Dixon & Strauss, 2006; Grafman,

2006; Kimberg, d’Esposito & Farah, 1997; Parkin & Java, 1999; Stuss, 2011). It is not clear

what the particular unitary factor saturating the different executive function tests is.

Behavior inhibition has been considered as a potential candidate for the single factor

responsible for successful performance in different executive tests (Barkley, 1997) or in

combination with working memory (Pennington & Ozonoff, 1996). Salthouse (1996, 2005)


suggested that reasoning and perceptual speed represent the underlying factors related to

all executive functions. Salthouse (2005) observed that performance on two common tests

of executive functioning, the Wisconsin Card Sorting Test (Berg, 1948; Heaton, 1981) and

the Controlled Oral Word Association Test (Benton, Hamsher & Sivan, 1994), were strongly

correlated with reasoning ability and perceptual speed.

Other authors challenge the existence of such a unitary factor. Godefroy et al.

(1999) emphasized that certain frontal lobe patients perform well on some tests purported

to assess executive abilities but not on others. Correlations among different executive tests

are frequently moderate or low, and many times lacking statistical significance (Lehto,

1996; Friedman et al., 2006; Salthouse, Atkinson & Berish, 2003).

Miyake et al. (2000) adopted an intermediate position. They studied three often-

postulated aspects of executive functions (shifting, updating, and inhibition) and concluded

that, although they are clearly distinguishable, they do share some underlying commonality.

Based on the results of their study, the authors stated that executive functions are

“separable but moderately correlated constructs” thus suggesting both unitary and non-

unitary components of the executive system. By the same token, several authors have

suggested different subcomponents of executive functions (e.g., Anderson, 2001; Delis,

Kaplan & Kramer, 2001; Denckla 1994; Elliot, 2003; Hobson & Leeds, 2001; Lafleche &

Albert, 1995; Lezak, 1983; Piguet et al., 2002).

Stuss (2011) states that specific frontal regions control discrete functions and those

very basic cognitive processes can be systematically manipulated to reveal those functions.

According to him, recent studies have demonstrated consistent anatomical/functional

relationships: dorsomedial for energization, left dorsolateral for task setting, and right

dorsolateral for monitoring, and consequently, there is no central executive. There are,

instead, numerous domain general processes discretely distributed across several frontal

regions that act in concert to accomplish control. Stuss further supports the point of view

that there are two additional "frontal" anatomical/functional relationships: ventral-


medial/orbital for emotional and behavioral regulation, and frontopolar for integrative-even

meta-cognitive-functions.

Two proposed fundamental executive functions

It may be conjectured that there are two different, but closely related types, of prefrontal

lobe abilities (e.g., Fuster, 2002; Happaney, Zelazo, & Stuss, 2004; Stuss, 2011):

(1) “Metacognitive executive functions” which include problem solving,

abstracting, planning, strategy development and implementation, and working memory

(the usual understanding of executive functions, generally measured in neuropsychology

executive functions tests); these are abilities mostly related with the dorsolateral area of

the prefrontal cortex (e.g., Stuss & Knight, 2002).The dorsolateral prefrontal cortex has

been observed to participate in diverse planning, abstracting, problem solving, and

working memory tasks. Using fMRI dorsolateral prefrontal activation has been found in

tasks such as solving the Tower of Hanoi (Fincham, Carter, van Veen, Stenger &

Anderson, 2002), Controlled Word Association Test (letter fluency) (Baldo, Schwartz,

Wilkins & Dronkers, 2006), working memory (Yoon, Hoffman & D'Esposito, 2007), and

solving the Wisconsin Card Sorting Test (Lie, Specht, Marshall & Fink, 2006).

(2) “Emotional/motivational executive functions”, which is responsible for

coordinating cognition and emotion. That means, the ability to fulfill basic impulses

following socially acceptable strategies. In the last case, what is most important does not

necessarily include what the best conceptual and intellectual result is, but what is in

accordance with personal impulses (e.g., Bechara, Damasio & Damasio, 2000). In that

regard, the core function of the prefrontal lobe is to find acceptable justifications for limbic

impulses. Following socially acceptable strategies actually involves inhibition of selfish or

unsociable basic impulses in the first place, but not necessarily arriving at the best


conceptual solution. The ventromedial areas of the prefrontal cortex are involved in the

expression and control of emotional and instinctual behaviors (Fuster, 1997, 2002). This

function is related with so-called “inhibitory control” of behavior (Miller & Wang, 2006).

Clinical evidence (e.g., Luria, 1969; Stuss & Knight, 2002) as well as experimental

research (e.g., Leung & Cai, 2007; Medalla, Lera, Feinberg & Barbas, 2007) suggest that

the neural substrate for this inhibitory function resides mainly in the medial and orbital

portions of the prefrontal cortex. Fuster ( 2002) points out that “The apparent

physiological objective of inhibitory influences from orbitomedial cortex is the suppression

of internal and external inputs that can interfere with whatever structure of behavior,

speech, or cognition is about to be undertaken or currently underway” (page 382).

There is no question that if metacognitive executive functions were indeed used in

solving external problems without the involvement of limbic impulses, most world-wide

problems would have been solved by man, because contemporary man has sufficient

resources to solve all the major social problems (such as poverty and war). Human

conflicts in general would also be significantly reduced.

Direct observation suggests that everyday problems usually have an emotional

content: talking with a friend, a boss or a spouse; driving in the street; deciding how to

approach somebody; spending money, etc., are not emotionally neutral activities, as are

the Wisconsin Card Sorting Test (Berg, 1948; Heaton, 1981) and the Tower of Hanoi

(Simon, 1975). When other people are involved, it is not easy to remain emotionally

neutral. Social issues, simply speaking, are not emotionally neutral, because

power/submission, personal benefits, and diverse biological drives are potentially involved

(Smith, Bond & Kagitcibas, 2006). Most likely, throughout evolution of mankind (i.e.,

during the last 150,000 years) fulfilling these drives has been the major application of the

prefrontal functions: to get power, to have a dominant role, to take food and goods for

ourselves, to get a sexual partner, etc. That means that emotional/motivational executive

functions have played a crucial role in survival and reproduction (e.g., facilitating

behaviors such as acquiring dominant roles, obtaining sexual partners, etc).

Mitchell and Phillips (2007) have argued that emotion can affect executive function


ability. They propose that mild manipulations of negative mood appear to have little effect

on cognitive control processes, whereas positive mood impairs aspects of updating,

planning and switching. This effect of emotion on cognition has been supported for

different executive function tasks, such as working memory (Spies, Hesse & Hummitzsch,

1996) and planning (Oaksford, Morris, Grainger & Williams, 1996) and using the Tower of

London (Shallice, 1982) as a paradigm. In other words, when emotion is involved,

metacognitive executive function ability decreases. Mitchell and Phillips (2007) emphasize

that current evidence on the effects of mood on regional brain activity during executive

functions demonstrates that the prefrontal cortex represents an area of integration

between mood and cognition.

These two types of executive functions (“metacognitive” and “emotional/

motivational”) depend on relatively different prefrontal areas, and as a matter of fact, two

major variants in the prefrontal syndrome are frequently distinguished: one mostly

impairing cognition (or rather, cognitive control, that is, “metacognition”); the other one

mostly impairing behavior:

(1) Dorsolateral syndrome. Cummings (1993) indicated that the dorsolateral

circuit is the most important to executive functioning (Figure 6.5). The most noted deficit is

an inability to organize a behavioral response to novel or complex stimuli. Symptoms are

on a continuum and reflect capacity to shift cognitive sets, engage existing strategies, and

organize information to meet changing environmental demands. Various researchers,

including Luria (1969), have noted perseveration, stimulus-bound behavior, echopraxia,

and echolalia. Lateralization has been noted in executive dysfunction (Goldberg, 2001).

Ventral and dorsal portions of prefrontal cortex are bilieved to interact in the maintenance

of rational and “nonrisky” decision making (Manes et al., 2002). According to Fuster

(1997, 2002), the most general executive function of the lateral prefrontal cortex is the

temporal organization of goal-directed actions in the domains of behavior, cognition, and

language.


Figure 6.5. Location of the dorsolateral prefrontal cortex.

(2) Orbitofrontal and medial frontal syndrome. Orbitofrontal damage has been

associated with desinhibition, inappropriate behaviors, personality changes, irritability,

mood liability, tactlessness, distractibility, and disregard of important events (Stuss &

Knight, 2002). These patients are unable to respond to social cues. Noteworthy, it was

observed by Laiacona and colleagues (1989) that these patients have no difficulty with

card-sorting tasks. Eslinger and Damasio (1985) coined the term "acquired sociopathy" to

describe dysregulation that couples both a lack of insight and remorse regarding these

behaviors. The orbitofrontal cortex appears to be linked predominantly with limbic and

basal forebrain sites. Medial frontal lobe damage causes apathy or abulia (a severe form

of apathy). Acute bilateral lesions in the medial frontal area can cause akinetic mutism, in

which the individual is awake and has self awareness, but does not initiate behaviors

(Ross & Stewart, 1981). According to Fuster (1997, 2002) the ventromedial areas of the

prefrontal cortex are involved in expression and control of emotional and instinctual

behaviors (Figure 6.6).

It is evident that the two prefrontal syndromes can have rather different clinical


expressions (metacognitive and emotional/motivational) depending upon the specific

location of the damage.

Figure 6.6. Location of the orbitofrontal cortex.

Metacognitive executive functions as an internalization of actions

As pointed above, disagreement persists around the potential unitary factor in executive

functions. I will suggest that “action representation” (i.e., internally representing

movements) may constitute at least one basic metacognitive executive function factor. I

will refer to “action representation” and “time perception”, derived from it; both ultimately

potentially depending upon one single core ability (“sequencing?”).

Two departing observations are important to support the involvement of the

prefrontal cortex in motor representation:


1. Anatomical observation: Prefrontal cortex represents an extension and further

evolution of the frontal motor areas. It may be conjectured that the prefrontal lobe should

participate in complex and elaborated motor (“executive”) activities.

2. Clinical observation: A diversity of motor control disturbances are observed in

prefrontal pathology, such as perseveration, utilization behavior, paratonia, primitive

reflexes, etc. (e.g., Ardila & Rosselli, 2007a; Victor & Ropper, 2001).

Several authors have argued that thought, reasoning, and other forms of complex

cognition (metacognition) depend on an interiorization of actions. Vygotsky (1929,

1934/1962, 1934/1978), for instance, proposed that thought (and in general, complex

cognitive processes) is associated with some inner speech. Vygotsky represents the most

classical author suggesting this interpretation for complex cognition. More recently,

Lieberman (2002a, 2002b) suggested that language in particular and cognition in general

arise from complex sequences of motor activities.

Vygotsky (1934/1978) developed the concept of “extracortical organization of

higher mental functions” to account for the interaction of biological and cultural factors in

the development of human cognition. Vygotsky’s (1934/1962, 1934/1978) understanding of

“higher mental functions” is roughly equivalent to “metacognitive executive functions”.

According to Vygotsky, a major factor in systemic organization of higher cognitive

processes is the engagement of external instruments (objects, symbols, signs), which have

an independent history of development within culture. Vygotsky called this principle of

construction of brain functional systems the principle of “extracortical organization of

complex mental functions”, implying that all types of mankind’s conscious activities are

formed with the support of external auxiliary tools or aids. However, different mediators and

means, or significantly different details within them, (e.g., the direction of writing and degree

of letter-sound correspondence, orientation by maps or by the behavior of sea-birds, etc.,)

may develop, and in fact are developed in different cultures. Therefore, the analysis of


cognitive processes must necessarily take into account these cross-cultural differences

(Kotik-Friedgut & Ardila, 2004).

The central point in Vygotsky’s (1934/1962) idea is that higher forms of cognition

(“cognitive executive functions”) depend on certain mediation (language, writing or any

other); the instruments used for mediating these complex cognitive processes are culturally

developed. According to Vygotsky (1934/1962), the invention (or discovery) of these

instruments will result in a new type of evolution (cultural evolution), not requiring any

further biological changes. Thinking is interpreted as a covert motor activity (“inner

speech”).

Vygotsky (1929) assumes that thought and speech develop differently and

independently having different genetic roots. Before two years of age, the development of

thought and speech are separate. They converge and join at about the age of two years,

and thought from this point on becomes language mediated (verbal thought). Language in

consequence becomes the primary instrument for conceptualization and thinking.

According to Vygotsky (1934/1962), speech develops first with external

communicative/social speech, then egocentric speech, and finally inner speech.

Vocalization becomes unnecessary because the child "thinks" the words instead of

pronouncing them. Inner speech is for oneself, while external, social speech is for others.

Vygotsky considered that thought development is determined by language.

Vygotsky (1987) separated two different types of concepts: spontaneous and

scientific. Spontaneous concepts are developed in a parallel way with language, whereas

scientific concepts are concepts learned at school. Children progressively develop reflective

consciousness through the development of scientific concepts. School is intimately related

with learning a new conceptual instrument: reading. Written language is an extension of

oral language, and represents the most elaborated form of language.

Luria further extended Vygotsky’s ideas and attempted to find the neurological

correlates for different components of complex cognitive processes. He clearly stated that

mental functions are “…social in origin and complex and hierarchical in their structure and

they all are based on a complex system of methods and means...” (Luria, 1973; p. 30).


In brief, Vygotsky (1934/1962) argued that complex psychological processes

(metacognitive executive functions) derives from language internalization. Thinking relies

on the development of an instrument (language or any other) that represents a cultural

product.

Lieberman (2002a, 2002b) refers specifically to the origins of language. He

postulates that neural circuits linking activity in anatomically segregated populations of

neurons in subcortical structures and the neocortex throughout the human brain regulate

complex behaviors such as walking, talking, and comprehending the meaning of sentences.

The neural substrate that regulates motor control (basal ganglia, cerebellum, frontal cortex)

in the common ancestor of apes and humans most likely was modified to enhance cognitive

and linguistic ability. Lieberman (2002a, 2002b) suggests that motor activity is the departing

point for cognition. Speech communication played a central role in this process. The neural

bases of mankind’s linguistic abilities are complex, involving structures other than Broca’s

and Wernicke’s areas. Many other cortical areas and subcortical structures form part of the

neural circuits implicated in the lexicon, speech production and perception, and syntax. The

subcortical basal ganglia support the cortical-striatal-cortical circuits that regulate speech

production, complex syntax, and the acquisition of the motor and cognitive pattern

generators that underlie speech production and syntax. They most likely are involved in

learning the semantic referents and sound patterns that are instantiated as words in the

brain’s dictionary.

The cerebellum and prefrontal cortex are also involved in learning motor acts (e.g.,

Hernandez-Mueller et al., 2005; Matsumura et al., 2004). Lieberman (2002a, 2002b)

proposes that the frontal regions of the cortex are implicated in virtually all cognitive acts

and the acquisition of cognitive criteria; posterior cortical regions are clearly active elements

of the brain’s dictionary. The anterior cingulate cortex plays a part in virtually all aspects of

language and speech. Real-word knowledge appears to reflect stored conceptual

knowledge in regions of the brain traditionally associated with visual perception and motor

control. Some aspects of human linguistic ability, such as the basic conceptual structure of

words and simple syntax, are phylogenetically primitive and most likely were present in the


earliest hominids. Lieberman (2002a, 2002b) further suggests that speech production,

complex syntax, and a large vocabulary developed in the course of hominid evolution, and

Homo erectus most likely talked, had large vocabularies, and commanded fairly complex

syntax. Full human speech capability, enhancing the robustness of vocal communication,

most likely is a characteristic of anatomically modern humans.

These two authors (Vygotsky and Lieberman), although using rather different

approaches, have both postulated that the development of language and complex cognition

are related with some motor programs, sequencing, internalizing actions, and the like.

The recent discovery of so-called “mirror neurons” represents a new element in

understanding inner speech and action representation. A mirror neuron is a neuron which

fires both when an animal performs an action and also when the animal observes the same

action performed by another animal. In humans, brain activity consistent with mirror

neurons has been found in the premotor cortex and the inferior parietal cortex (Rizzolatti et

al., 1996; Rizzolatti & Craighero, 2004). In monkeys, the rostral part of ventral premotor

cortex (area F5) contains neurons that discharge, both when the monkey grasps or

manipulates objects and when it observes the experimenter performing similar actions.

These neurons (mirror neurons) appear to represent a system that matches observed

events to similar, internally generated actions.

Transcranial magnetic stimulation and positron emission tomography (PET)

experiments suggest that a mirror system for gesture recognition also exists in humans and

includes Broca's area (Rizzolati & Arbib, 1998). The discovery of mirror neurons in the

Broca’s area might have immense consequences for understanding the organization and

evolution of mankind cognition (Arbib, 2006; Craighero, Metta, Sandini & Fadiga, 2007). An

obvious implication of mirror neurons is that they can participate in the internal

representation of actions. Neuroimaging data have showed that interactions involving

Broca's area and other cortical areas are weakest when listening to spoken language

accompanied by meaningful speech-associated gestures (hence, reducing semantic

ambiguity), and strongest when spoken language is accompanied by self-grooming hand

movements or by no hand movements at all suggesting that Broca’s area may be involved


in action recognition (Skipper, Goldin-Meadow, Nusbaum & Small, 2007). PET studies have

associated the neural correlates of inner speech with activity of the Broca’s area (McGuire,

Silbersweig, Murray, David, Frackowiak & Frith, 1996).

Is there anything special in the prefrontal cortex?

For some time it has been assumed that the prefrontal cortex is significantly larger in

humans than in other primates (e.g., Blinkov & Glezer, 1968). This difference in volume

was assumed to represent a major reason to account for differences in complex forms of

cognition (executive functions) observed in humans.

Nonetheless, such an assumption turned out to be incorrect. Measures of prefrontal

lobe volumes have not found differences between mankind and non-human primates.

Semendeferi et al (1997, 2002) measured the volume of the frontal lobe as a whole and of

its main sectors (including cortex and immediately underlying white matter) in humans,

chimpanzees, gorillas, orangutans, gibbons, and macaques using three-dimensional

reconstructions of magnetic resonance (MR) scans of the brain. Although the absolute

volume of the brain and the frontal lobe was found to be largest in humans, the relative size

of the frontal lobe was similar across hominoids: macaque (28.1%), gibbon (31.1%),

orangutan (35.3%), gorilla (32.4%), chimpanzee (35.9%) and human (36.7%). Most

significantly, it was found that humans do not have a larger frontal lobe than expected from

a primate brain of mankind size (Figure 6.7 and 6.8). Furthermore, the relative size of the

sectors of the frontal lobe (dorsal, mesial, and orbital) was similar across the primate

species studied. Semendeferi and colleagues suggested that the special cognitive abilities

attributed to a frontal advantage may be due to differences in individual cortical areas and

to a richer interconnectivity, none of which required an increase in the overall relative size

of the frontal lobe during hominid evolution.


Figure 6.7. Relative size of the prefrontal cortex in different primates (according to

Semendeferi et al., 1997, 2002).

Schoenemann, Sheehan, and Glotzer (2005) found that a major difference

between humans and other primates was the white matter volume. Using MRI from 11

primate species, the authors measured gray, white, and total volumes for both prefrontal

and the entire cerebrum on each specimen. In relative terms, prefrontal white matter was

found to have the largest difference between human and nonhuman, whereas gray matter

showed no significant difference. Increased brain interconnectivity may represent a major

characteristic of the human brain. As a note of caution, it is important to keep in mind that

subjects used in this study were contemporary people, living in city environments, with a

high level of education, etc., not humans living in those conditions existing 150,000 years


ago. Stimulation can be rather different not only qualitatively but even probably

quantitatively, potentially impacting on brain interconnectivity.

It can be tentatively concluded that it is questionable that the size of the prefrontal

cortex can account for the human executive functions. Some other factors have to be

considered, such as connectivity (increased stimulation?).

Figure 6.8. Volume of the frontal lobe across species. Values include both

hemispheres (according to Semendeferi et al., 1997, 2002).

Executive functions in pre-historical man


Some recent studies have approached the question of the evolution of the prefrontal cortex

and executive functions (Roth & Dicke, 2005; Risberg, 2006; Winterer & Goldman, 2003). It

is usually accepted that Homo sapiens sapiens appeared about 150,000 years ago, and

during this time, his brain evolution has been minimal (Wood, 1992). It means that humans

existing since about 150,000 years ago had basically the very same neurological

organization of contemporary individuals, including the biological foundations for the so-

called executive functions.

How were executive functions used by pre-historical man? Of course, we cannot

be sure, but some few papers have approached this question (e.g., Bednarik, 1994, 2003;

Coolidge & Wynn, 2001, 2005; Sugarman, 2002; Wayne, 2006).

Coolidge and Wynn (2001) raised the question of how executive functions

(supposedly, one of the key evolutionary acquisitions that led to the development of modern

thinking) were demonstrated by prehistoric people. Coolidge and Wynn assumed that it is

possible to match many of the features of executive function with activities reconstructed

from archaeological evidence. The potential application of several components of executive

function (such as sequential memory, task inhibition, and organization and planning) is

analyzed by the authors: (1) Sequential memory: it can be speculated in the Palaeolithic

Lithic reduction sequences, but even sophisticated procedures like Levallois can be

explained without resort to closely-linked sequences of action. The production and use of

barbed bone projectile points is another potential marker. The final product depends much

more closely on a set sequence of actions. It is a true multi-step technology. (2) ‘Tasks of

inhibition’, in which immediate gratification and action are delayed, are harder to identify

archaeologically. Agriculture requires such inhibition. Facilities such as traps that capture

remotely are technologies of inhibition and were probably present in the European

Mesolithic. Palaeolithic examples are less convincing. Coolidge and Wynn (2001, 2005)

consider that nothing of Middle Palaeolithic foraging, however, would require tasks of

inhibition (indeed, they conclude that nothing in the archaeological record of Palaeolithic

appears to require executive function). (3) ‘Organization and planning’ is another basic


executive function ability that likely was required for activities such as migration and

colonization.

Coolidge and Wynn’s (2001) review of the archaeological evidence finds no

convincing demonstration for executive functions among the traces left by Neanderthals.

The authors conclude that the archaeological records support the hypothesis that executive

function was a late and critical acquisition in human cognitive evolution. In a very ingenious

study, Stout and Chaminade (2007) using Positron Emission Tomography (PET) recorded

the brain activity from six inexperienced subjects learning to make stone tools of the kind

found in the earliest archaeological records. The authors found that tool making is

associated with the activation of diverse parieto-frontal perceptual-motor systems, but no

activation was observed in dorsolateral prefrontal cortex. They concluded that human

capacities for sensorimotor adaptation, rather than abstract conceptualization and planning,

were central factors in the initial stages of human technological evolution, such as making

stone tools. Nonetheless, complex cognitive processes (i.e., metacognitive executive

functions) seem to be crucial for further development and survival of Homo sapiens. The

key factor for Homo sapiens late evolution seems to be the mental ability to plan and

strategize, which allowed them to find innovative solutions to the many changing

environmental problems to which they were exposed (Coolidge & Wynn, 2008). This may

be one reason to account why Homo sapiens survived while Homo neanderthalensis

disappeared. Changing environmental conditions (e.g., global climates changes) may

require flexible survival strategies. It has been conjectured that during the past history

changing physical environment conditions resulted in a selection that gave human

ancestors adaptive versatility to endure increasing environmental instability (Bonnefille,

Potts, Chalié, Jolly, Peyron, 2004; Potts, 1996, 2004).

Mithen (1994, 1996) has proposed the accessibility of mental modules as the

impetus for mankind culture at the time of the Middle/Upper Palaeolithic transition, about

60,000 to about 30,000 years ago. He identified these mental modules as general

intelligence, social intelligence, natural history intelligence, technical intelligence, and

language. Probably, language was the most important one, increasing communication, and


facilitating the transmission of knowledge, potentially resulting in an increased probability of

survival and reproduction.

It could be speculated that at the beginning of human history, transmitting

knowledge from generation to generation was limited. Although some forms of learning can

be transmitted by modeling or imitation (vicarious learning or social learning or modeling)

(e.g., Bandura, 1977), language development represented a powerful instrument to

accumulate and transmit knowledge about the world. The crucial point in the origins of

executive functions becomes the possibility to conceptualize the environment (concepts are

represented in words) and to transmit and progressively accumulate this knowledge about

the world.

Metacognitive executive functions as a cultural product

There is no convincing evidence that Paleolithic individuals used executive functions

(Coolidge & Wynn, 2001), which can be understood as “the ability for planning…etc.” (first

interpretation of prefrontal abilities: metacognitive executive functions). For thousands of

years, prefrontal abilities were in consequence exclusively used to fulfill basic impulses

following socially acceptable strategies (e.g., hierarchy in the group) (second interpretation

of prefrontal abilities: emotional/motivational executive functions).

Which were the milestones for cultural development and how did metacognitive

executive functions appear? It could be speculated that some crucial inventions fueled the

development of cultural evolution (Vygotsky, 1934/1962). For instance, a kind of cognitive

fluidity has been postulated as a basic requisite for executing complex human activities

(Gardner, 1983). The most important candidate for this crucial invention that fueled the

development of cultural evolution is language. Language allows for the transmission of

knowledge and facilitates survival and reproduction. Without language, children can learn

from parents by imitation, but imitation is limited to some elementary activities, such as


making a simple stone ax. Language represents a major instrument of internal

representation of the world and thinking (Vygotsky,1934/1978). Language development

obviously was a slow process taking thousands of years, but the most critical element of

human language is the use of grammar, likely appearing some 10,000-100,000 years ago

(Ardila, 2006). Probably, Homo neanderthalensis did not have a grammatical language and

according to archeological evidence, did not use executive functions (Coolidge & Wynn,

2008). Language grammar likely developed from action internalization (Ardila, 2006).

Written language represents an extension of oral language. Written language

appeared only some 6,000-8,000 years ago and its diffusion has been so slow that even

nowadays about 20% of the world population is illiterate (UNESCO, 2000). Performance in

psychometric executive function tests has been observed to be very significantly correlated

with subjects’ educational level (e.g., Ardila, Rosselli & Rosas,1989; Ardila et al., 2000;

Ardila & Rosselli, 2007b; Ostrosky et al., 1998; Reis & Castro-Caldas, 1997; Rosselli et al.,

1990). For instance, Gomez -Perez and Ostrosky-Solis (2006) observed that whereas tests

related to memory are sensitive to aging, those related to executive functioning are mostly

sensitive to education. It can be argued that illiterates possess basic executive functions

(e.g., ability to internally represent actions) but they lack an important instrument to

organize executive functions: written language.

Tentative conclusions

The analysis of executive functions represents one of the most intensively studied

neuroscience questions during the last decade. The emphasis in reasoning, abstracting

skills, behavioral control, anticipating the consequences of behavior, and similar abilities

has contributed to the frequently found false idea that human behavior is guided by

rationality. Human history blatantly contradicts this idea.


This misinterpretation of mankind behavior is linked to the assumptions that the

human brain is unique and “superior” to the brain of other species. We refer to our species

as the “wise man” (Homo sapiens). By analyzing executive functions, it may be concluded

that two different types of executive functions could be separated: metacognitive and

emotional/motivational, depending on different brain systems. It could be argued that only

the first one should be referred to as executive functions; usually, however, they are

considered together in most definitions of executive functions, assuming a certain unity.

Contemporary testing of executive functions has focused on abstracting, problem-

solving, and similar metacognitive abilities. These metacognitive abilities seem to be useful

in solving external and emotionally neutral problems. When social situations and biological

drives are involved, the ability to rationally solve problems seems to decrease in a

significant way. In this regard, contemporary testing of executive functions has limited

ecological validity.

Archeological analysis has discovered only some –if any– evidence of

metacognitive executive functions in prehistorical man. We have to conclude that

metacognitive abilities represent a recent acquisition, not obviously dependent on recent

biological changes. The development of some cultural instruments, potentially resulting in a

new type of evolution has been suggested. Language as an instrument not only to

conceptualize the immediate experience, but for its transmission of knowledge, has been

proposed as the major cultural instrument for metacognition. Language complexity has

historically increased with the development of written language. There is no question that

some other cultural instruments have also contributed to the development of metacognitive

abilities; for instance, mathematics, drawing, and technology (from the wheel to

computers). From the point of view of the brain, metacognitive executive functions are not

necessarily correlated with a further brain development; increased neural interconnectivity

may potentially support the increased complexization of executive functions found in

contemporary Homo sapiens.


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7. How we recognize other people?

Introduction

Recognition of own-species members represents a basic survival ability not only for

prehistorical man, but also for every living creature. Lacking this ability, any species would

quickly disappear. Recognition of the own species members is based on a wide range of

multiple sensory information. For instance, insects rely especially on olfactory information to

identify other members of their own species, whereas primates use mainly –but not

exclusively – visual information (de Waal , 2003; Hinde, 1974; Jolly, 1972; Rössler & Zube,

2010). In mankind, the critical and distinguishing signal features used in the recognition of

other species members have somehow evolved in a parallel way with cultural evolution, as

a result of the use of different clothes, costumes, paintings, hair-styles, make-ups, etc.

People also use a diversity of non-verbal behavior strategies to communicate a given

intention without pre-established conventions (Noordzij et al., 2009). Paleolithic man most likely lived in small social groups, similar in size to a primate

troop, that is, about 10-100 individuals, composed by one or several couples and their

offsprings (Ridley, 1986); noteworthy, in modern society, we keep affectively living in a

primate-like troop composed by some 10-100 individuals –relatives and friends–with whom

we maintain a close affective relationship. Some primitive societies that depend on hunting

and gathering of patchy distributed resources form casual societies not unlike the primate

model (Lee & DeVore, 1968; Wilson, 1975), and the primate model was most likely the first

type of social organization (Van den Berghe, 1979). However, the number of individual

faces that we are potentially able to recognize -"familiar faces", is notoriously over 100, and

probably it can be situated in the order of several thousands.

For the prehistorical man, recognition of other species members was most critical.

According to the living conditions of the prehistorical man, people recognition was suppose

to answer at least two of the following questions: (1) Does the other individual belong to the


same species (i.e., is he/she another Homo sapiens individual)?; (2) what is his/her

gender?; (3) what is his/her emotional state; i.e., is he/she a friend or an enemy? Is he/she

a known (endogroup member; "familiar individual") or unknown (exogroup person;

"nonfamiliar individual") person? And (4) what particular individual is he/she?

Own-species members’ recognition

Recognition of the own species members does not seem so critical for the contemporary

man, as it was for prehistorical people. However, for people currently living in the

Amazonian jungle –and other natural environments, it continues being equally critical as it

was during prehistorical times. It is evident that in Bogotá, New York or Paris, the

possibilities to meet a member of another species (for instance, a bear, a lion, etc.) are

quite low. For the prehistorical man, (and it is for a contemporary Tucano Indians living in

the Amazonian jungle) a moving animal supposed the question about what species in

particular it is.

Brain organization of other people recognition has been studied under normal, but

pathological, conditions. Its disturbance is usually known as prosopagnosia (e.g., Bodamer,

1947; Busigny & Rossion, 2009; Damasio et al, 1982). Prosopagnosia can be defined as an

acquired disturbance in the ability to identify familiar faces.

Specialized brain areas involved in face recognition have been studied. Usually, the

damage in the occipito-temporal area, either bilateral (e.g., Bruyer et a, 1983; Damasio et

al, 1982; Ettlin et al, 1992; Meadows, 1974) or right (e.g. Benton, 1990; De Renzi, 1986a;

Landis et al, 1986, 1988; Whiteley & Warrington, 1977) have been associated with

disturbances in face recognition. It is usually assumed that a bilateral occipitotemporal

network mediates face perception (Minnebusch et al., 2009); when this network is

disrupted, face recognition defects are observed.

fMRI procedures have significantly contributed to further our understanding on brain


organization of face perception. It has been found that the brain areas involved in face

recognition include the right middle fusiform gyrus, the left inferior occipital gyrus, and in the

right posterior superior temporal sulcus. The dorsal part of the lateral occipital complex and

the human middle temporal cortex are localized bilaterally (Freeman et al., 2009; Sorger et

al., 2007). Marotta et al., (2001) investigated whether patients with prosopagnosia would

show functional activation in the fusiform gyrus, -the most important brain area usually

regarded as the neural substrate for face processing (Furi et al., 2010)-, when viewing

faces. While the patients did show activation in the fusiform gyrus, with significantly more

voxels in posterior areas than their control subjects, this activation was not sufficient for

face processing. In one of the patients, the posterior activation was particularly evident in

the left hemisphere, which is thought to be involved in feature-based strategies of face

perception, but not in the global recognition of faces. The authors concluded that an

increased reliance on feature-based processing in prosopagnosia leads to a recruitment of

neurons in posterior regions of the fusiform gyrus, regions that are not ideally suited for

processing faces.

Although testing for prosopagnosia is usually carried out using photographs of faces

(Benton et al., 1994; Warrington, 1984), this method obviously represents an extremely

artificial situation. It is interesting to note that untrained people are unable to recognize

individual faces and even everyday objects in photographs. Moldiano et al. (1982) observed

in Mexican Indian children an average error rate of 20% in identifying color paintings of

everyday objects. There is no question that recognition of individuals in photographs

represents a learned and highly trained ability that we usually take for granted. Little

children have a great difficulty to recognize even their own parents and siblings in

photographs. This ability is usually achieved around the age of two years, if adequate

training opportunities are provided (Ellis, 1992).

Face recognition disturbances usually present some specific characteristics: (1)

prosopagnosic patients most often recognize different human races (caucasian, mongoloid,

black), and they can sort human and animal faces (Benton, 1980, 1990; De Renzi, 1986b);

(2) they can also distinguish fruits from flowers, and cars from furniture, although they are


unable to know what specific category member it is (i.e., what particular fruit, flower, car, or

furniture is); (3) prosopagnosic patients usually recognize the general category "human

face" (or "fruit" or "flower), and they can even separate human faces from their

corresponding cartoons (Lopera & Ardila, 1992), but they fail in recognizing the individual

members of the category. These clinical characteristics would suppose the existence of a

highly specialized brain system adapted to recognize own-species members.

Nonetheless, although prosopagnosic patients usually can separate pictures

corresponding to people (own species) from picture corresponding to animals (other

species), they eventually can fail in performing this task (Benson et al., 1974; Bornstein et

al., 1969). This failure supposes an impairment in those specialized own-species brain

detector systems.

Farah et al. (1991) have pointed that the visual recognition of living and nonliving

things can be selectively impaired in cases of brain damage. Patients with prosopagnosia

can present an evident difficulty in recognizing animals and plants; nonetheless, they

usually present a better preserved ability to recognize inanimate objects. A neural system

relatively more important for recognizing living than nonliving things was proposed by the

authors; this system can be selectively impaired by brain damage. Higher visual centers

would be specialized not just to recognize faces, but for the perception of biological forms.

One subsystem of this higher system specialized in the perception of biological forms would

correspond to "human face recognition". Farah et al (1991) point of view in general

supports the perceptual model proposed by Konorski (1967). This perceptual model

postulates the existence of different gnosic brain areas specialized in the recognition of

manipulable and nonmanipulable objects, human faces, emotional facial expressions, and

animated objects. By the same token, in cases of anomia associated with brain damage, it

has been observed that some specific semantic categories can be selectively impaired,

while others are better preserved (Ardila & Rosselli, 2007; Warrington & Shallice, 1984).

This specificity has been also shown in memory (Farah et al., 1989).

Human species members recognize one another basically (although, not exclusively)

based in some visual information. Ethology has carefully studied different species' "sign


stimuli" (Eibl-Eibesfeldt, 1970; Mazur, 2005; Tinbergen, 1951). A sign stimulus refers to

some features of the objects that have been shown to be of major importance in eliciting

responses (Hinde, 1970). The human face evidently could be considered as a "sign

stimulus".

The visual recognition of own species members, as well as the auditory recognition

of own species calls, in several animal species (including mankind) have been shown to be

somehow biologically programmed (Martinez & Matsuzawa, 2009). Some neurons in

different animals' auditory cortex only fire when using the same species calls (Brugge &

Reale, 1985), and probably, this also holds true when visually perceiving members of the

own species (Gross et al, 1972; Rolls, 1984). Perret et al. (1982) found that about 10% of

the neurons they sampled in the superior temporal sulcus of the macaque monkey

selectively respond to faces and not to other stimuli. Desimone et al (1984) found in the

inferior temporal cortex a population of cells that responded selectively to faces. The

responses of these cells were dependent on the configuration of specific face features, and

their selectivity was maintained over changes in stimulus size and position. A particularly

high incidence of such cells was found deep in the superior temporal sulcus. Baylis et al.

(1985) observed that 77% of 44 face-neurons in this temporal area reliably responded more

to some specific faces than to others. Perret et al. (1984) claimed to have found cells that

are peculiarly responsive to a particular human face often seen by the monkey. And

Heywood and Cowey (1992) described cortical neurons that are selectively sensitive to

faces, part of faces and particular facial expressions concentrated in the banks and floor of

the superior temporal sulcus in macaque monkeys. The neurons of the superior temporal

sulcus of monkeys would be, in consequence, part of a system specialized in faces.

Ojemann et al (1992) recorded neuronal activity in adult human subjects and observed that

62% of the studied neuronal populations in the nondominant temporal lobe presented

significant changes in activity during matching of faces and 52% during labeling of facial

emotional expressions. These results would support the specificity of a highly specialized

neuronal face-recognition brain system.


Although the overwhelming majority of cases of prosopagnosia reported in the

literature presented in addition to the face recognition impairments, some associated

deficits in the recognition of individual members belonging to other visual categories (most

often, living things -fruits, flowers, etc., but also nonliving things -buildings, cars, furnitures,

etc.) prosopagnosia can be occasionally restricted only to the recognition of faces (De

Renzi, 1986; De Renzi et al, 1992; Farah, 1990). Conversely, there are patients with severe

visual agnosia for real objects without any evident defect in face recognition (Feiberg et al.,

1986; Hecaen & Ajuriaguerra, 1956). Furthermore, prosopagnosic patients can be able to

perform very complex perceptual tasks and can perceive and recognize many stimuli that

are visually more complex than human faces (Benton & Van Allen, 1972; Busigny et al.,

2010; Damasio, 1985). This supposes specificity in face recognition defects.

Busigny et al. (2010) tested a prosopagnosic patient in three delayed forced-choice

recognition experiments in which visual similarity between a target and its distractor was

manipulated parametrically: novel 3D geometric shapes, morphed pictures of common

objects, and morphed photographs of a highly homogenous familiar category (cars). In all

experiments, the patient showed normal performance and speed, and there was no

evidence of a steeper increase of error rates and RTs with increasing levels of visual

similarity when compared to controls. According to the authors, these data rule out an

account of acquired prosopagnosia in terms of a more general impairment in recognizing

objects from visually homogenous categories. They assume that overall, these

observations allow for the conclusion that brain damage in adulthood may lead to selective

recognition impairment for faces, perhaps the only category of visual stimuli for which

holistic/configural perception is not only potentially at play, but is strictly necessary to

individualize members of the category efficiently.

In conclusion, it seems reasonable to suppose the existence of some brain neuronal

subsystems specialized in the recognition of own-species members. These subsystems

would participate in a higher neuronal system specialized in the recognition of biological

forms. Individual members (individual faces) would be encoded into the "face recognition

subsystem". The record of neuronal activity would affirm the existence of highly specialized


neuronal subsystems involved in the perception of faces (Desimone et al, 1984; Gross et

al, 1972; Heywood & Cowey (1992); Ojemann et al, 1992; Perret et al, 1982; Righart et al.,

2010; Rolls, 1984).

Gender recognition

Gender recognition (filognosis; from the Greek, filo = gender) represents a crucial

perception that will define further social behavior (100,000 years ago, and even nowadays).

Taking into account that in mankind a moderate sexual dimorphism exists (females usually

have an average smaller height and possess sexual signals that can be easily recognized

either by the front or by the back; additionally, gait is different), it is easy to suppose that

visual signals were for the pre-historical man, and continue being for contemporary man,

relevant and effective (Morris, 1977). Furthermore, not only body configuration but also

male's and female's clothes are quite different and identifiable in their construction, shape,

and even colors. Some female primates have areas of "sexual skin" which swell and/or

change in color with changes in the reproductive state of the animal (Hinde, 1974)

representing an evident visual identification mark.

Prosopagnosic patients may be unable to identify male and female faces (Bruyer,

1986; Damasio et al., 1990; Lopera & Ardila, 1992), and it can be proposed that they will

also present general defects in recognizing males and females according to other (not

facial) sexual signals. They can also present kind of whole-body recognition defect. Indeed,

in prosopagnosia a defect not only in face but also in body perception can be found

(Righart & de Gelder, 2007). The prosopagnosic patient described by Bauer (1982) decided

to cancel his subscription to the journal Playboy after becoming prosopagnosic; Bauer

suggested the possibility that his patient could present an agnosia for individual nudes,

analogous to the defect in the recognition of individual faces. Conversely, the author of this

paper studied a prosopagnosic patient with a virtually complete inability to recognize any

face, and even to sort males and females faces. However, he easily and accurately


distinguished male and female bodies. This implies that facial and whole-body

males-females distinction can become dissociated. Or at least, that body recognition can be

preserved, while face recognition is impaired. If this last assumption were true, it would

imply a "sensitivity hierarchy": it is easier (and better preserved in brain-damaged patients)

to recognize males-females using whole-body than facial signals.

The idea that gender differences aid in the ability to recognize human faces has

been suggested. Ino et al. (2010) performed a fMRI experiment in which participants

encoded and recognized male and female faces. Behaviorally, the facial recognition ability

of men and women was similar and was superior for female faces compared to male faces.

At the neural level, widespread areas showed greater responses for men vs. women during

the encoding and recognition phase, and several areas, including the hippocampal region,

showed greater responses to female vs. male faces during recognition. The authors

proposed that the reduced activation of women's brains during encoding and recognition

suggests that the relevant neural systems were more efficiently recruited in women than in

men.

Noteworthy, visual signals are not the only ones used in gender recognition: there

are also auditory signals resulting from a different voice timbre, and additionally, distinctive

olfactory signals. Auditory and olfactory signals are probably more readily used in low

illumination conditions, while visual signals are easily available in daytime conditions.

These visual, auditory, and olfactory gender signals remain in our contemporary

mankind members, despite the differences in cultural backgrounds. Visual marks have not

changed, although usually they can be covered. Height differences remain, although

women may use higher shoes for increasing their heights. The differences in gait are

evident. Voice-timbre differences supposedly have not changed during the last 150,000

years. And olfactory signals can be artificially covered and replaced by other new olfactory

signals, but anyhow they remain as gender marks.

Olfactory recognition deserves some special consideration. Olfactory communication

plays a crucial communication role in most animals, including primates (Hinde, 1970; Jolly,

1972; Mundy, 2006). Very often, sexual behavior is partially under olfactory control: a


pheromone is produced that acts as a powerful attractant to the male (Hoover, 2010). The

tendency of women living together to menstruate simultaneously may be mediated by

olfactory stimuli (Carlson, 2009). A male pheromone is detected most easily by women of

reproductive age, but men can smell it if given oestrogen; and olfactory threshold have

been observed to vary during the menstrual cycle (Conform, 1970; Hinde, 1974;

Eibl-Eibesfeldt, 1970). So, olfactory signals continue being effective in gender identification.

Perfumery industry has become a solid and well-established enterprise.

In summary, gender identification can be mediated by different types of signals:

facial, whole-body, and even auditory and olfactory signals.

Emotional expression and emotional recognition

Some basic emotional expressions are universals and can be easily recognized by any

member of any culture (Ekman, 1972; Kohler et al., 2004). Aggressive gestures, protective

gestures, threatening signals, submissive postures, and sexual approach signals are

roughly identical in any cultural group, and they are quite similar to those observed in

non-human primates (Eibl-Eibesfeldt, 1970; Morris, 1977). It can be supposed that they

existed in a similar form in the pre-historical man. Some other emotional expressions

present major or minor variations across different cultural groups. Surprise, joy, mourning,

etc., can present important cross-cultural differences. Special ornaments are often used to

make a special emotional state even more easily identifiable: aggression, sexual interest,

mourning, etc. (Ekman, 1972; Eibl-Eibesfeldt, 1973).

During child development, the face represents the earliest visual stimulus capable to

release an emotional response (Fantz, 1961). Facial identification and emotional

recognition can be dissociated in brain-damaged individuals. In some cases of

prosopagnosia the recognition of facial expression can be preserved while face

identification is impaired (Bates et al., 2009; Bruyer et al., 1983; Shuttleworth et al., 1982).


Conversely, some brain-damaged patients can preserve the ability to identify faces, but fail

in recognizing facial emotional expressions. Most often, right hemisphere-damaged patients

present serious difficulties to identify, match and comprehend emotional expressions

(Feyereisen, 1986). Kurucz and Feldmar (1979) found that some patients could recognize

photographs of famous faces, but they were unable to identify their facial expressions. By

the same token, the patient reported by Lopera and Ardila (1992) did not recognize facial

emotional expressions, but usually was able to deduce them (e.g., "This must be a smiling

and joy face, because the teeth are seen through the mouth").

It becomes plausible that facial identification and the recognition of emotional

expressions depend on, at least partially, different brain subsystems (Peelen et al., 2009;

Stephan & Breen, Caine, 2006). Thus, two different visual agnosic syndromes could be

found in brain-damaged patients: agnosia for faces (prosopagnosia) and agnosia for

emotional expressions (prosopo-affective agnosia). Konorski (1967) proposed the

existence of different brain systems (different "gnostic areas") to recognize human faces

and to recognize emotional facial expressions. Recently it has been shown that whereas

face recognition defects are associated with cortical damage (very specially, the right

fusiform gyrus) the recognition of the facial expression of emotion depends on white matter

association tracts, very specially the inferior fronto-occipital fasciculus (Philippi et al., 2009).

Etcoff (1984) postulated the existence of different "modules" for the visual

identification of faces and facial expressions. She observed that the speed and accuracy

with which normal subjects perform a sorting task (to put photographs of faces in different

piles according to either their identity or their expression) is not affected by whether facial

identity is correlated with facial expression, implying that these two proprieties of faces are

processes independently. Etcoff postulated that two separate brain modules underlie the

recognition of facial identity and facial expression but that they are neuroanatomical

neighbors.

It has also been shown that prosopagnosic patients can retain some covert

recognition of faces. These patients present a physiological response for familiar, but not

for unfamiliar faces (Barton et al., 2001; Bates et al., 2009; Bauer, 1984; De Haan & Young,


1987; De Haan et al, 1992; Tranel & Damasio, 1985; Young & De Haan, 1988). By the

same token, in associative learning tasks, performance is better if familiar faces are used

(Bruyer et al., 1983). These findings suggest that despite unawareness in face recognition,

some covert face recognition can remain in prosopagnosia syndrome. However, this not

surprising at all. Everyday experience discloses that very often, when seeing a particular

face, we can be totally unable to identify who he/she is, despite having the "feeling" that we

really know that particular individual; we simply have a "feeling of familiarity". The

recognition of the individual member can be impossible in this everyday experience (and

can be impaired in cases of brain-damage), but the distinction "familiar" and "not familiar"

remains.

Valdés-Sosa et al. (2011) observed in a prosopagnosic patient face-selective

activations bilaterally in his occipital gyri and in his extended face system (posterior

cingulate and orbitofrontal areas), the latter with larger responses for previously-known

faces than for faces of strangers. In the right hemisphere, these surviving face selective-

areas were connected via a partially persevered inferior fronto-occipital fasciculus.

According to the authors, this suggests an alternative occipito-frontal pathway, absent from

current models of face processing, that could explain the patient's covert recognition while

also playing a role in unconscious processing during normal cognition.

Individuals' recognition

Endogroup members are usually very alike (resulting from endogamy) in their height, body

contexture, skin color, and additionally, in the clothes and make-up they wear. Usually, they

can be visually identifiable even at long-distances.

Erroneously, we have learned that individuals are recognized just by their faces. This

can be partially true in our urban societies, where we have very limited possibilities to

perceive other individual characteristics (e.g., his/her body configuration, his/her gait, etc).

In a survey of 1,000 people’s photographs (excluding commercial announcements)


randomly taken from the two most influential newspapers and the two most influential

magazines in Colombia, it was found that face photographs were about four times more

frequently published than whole-body photographs. Evidently, we are over trained in

individuals' recognition relying only on facial cues. However, facial information is quite

insufficient to recognize individuals for anybody living in rural areas, in open fields or in

savannas. People living in Argentinean Pampa or Paraguayan Chaco easily recognize

approaching or passing-by people when they are still 500 meters or farther away. They do

not depend, of course, solely upon face recognition to identify individuals (face can be

recognized only within very short distances) but upon a broader diversity of signals, such as

body configuration, gait, and even clothes. The human brain should possess not simply a

system for encoding and memorizing faces (prosopognosis) but also for encoding and

memorizing body configurations and general personal features (by the way, "prosopos" in

Greek means not only face, but also person, and prosopagnosia should be understood as

the inability to identify not simply faces, but persons).

Thus, recognition of individuals and recognition of faces is not equivalent. The face

is only one of the visual characteristics used to recognize individuals, but it is not the only

one, and eventually, it was not the most important one for the prehistorical man (or for the

current jungle inhabitants, for the inhabitants of the Argentinean Pampa or for army

members), although evidently it is the most important one in our current city-living

conditions. It could be conjectured that that in addition (or superimposed) to the ability to

recognize faces, the human brain should possess an ability to recognize individual body

configurations and body marks. Furthermore, faces yield information not only about the

individual, but also (and eventually even more importantly) about his/her specific emotional

state. By the same token, in everyday conditions, faces are not static but continuously

moving. Interestingly, prosopagnosic patients may recognize faces on the basis of their

idiosyncratic facial movements (Steede et al., 2007). To identify individual members one should be able to recognize body marks and

general configuration (somagnosis, that is, body recognition), and face signals

(prosopognosis). Patients with prosopagnosia cannot discriminate individuals members in a


group, but they can use sufficiently evident visual marks (e.g., a face with wrinkles means

that it should correspond to an elderly person; a face with a beard should correspond to a

male, etc).

Somagnosis has not been systematically analyzed in neuropsychology yet.

Furthermore, it does not seem easy, considering that currently the most important body

marks are the clothes (changing from one day to another), although it seems evident that

some people possess a tremendous ability to identify individuals by their clothes. Our

knowledge about other people's body configuration is in most cases just approximate.

However, it is evident that in addition to memory for people's faces, we also have some

memory for people's height, contexture, gait, etc. It is reasonable to suppose that patients

presenting face recognition deficits may also present body recognition defects.

Interestingly, patients with prosopagnosia usually also present difficulties recognizing

animals, either animal faces or whole body recognition (Farah, 1989). Damasio et al (1982)

reported a prosopagnosic patient with difficulties to identify people's gaits, but usually

patients with prosopagnosia are not tested in recognizing people when using diverse visual

characteristics, such as body configuration and gait.

Different anatomical substrates have been suggested for the recognition of familiar

and nonfamiliar faces (Warrington & James, 1967). Nonaphasic patients with right posterior

lesions present the most remarkable difficulty in discriminating familiar faces. Lopera and

Ardila (1992) proposed further to distinguish two different neuropsychological syndromes:

prosopagnosia (as a more or less isolated perceptual defect in face recognition), and

prosopamnesia (as a memory defect for faces). In the first case (prosopagnosia) right

occipital-temporal damage would be sufficient; prosopamnesia would be associated with

bilateral lesions. Individuals' face recognition would correspond to the specific elements (or

items) of this "familiar faces" subsystem. De Renzi et al (1991) introduced a similar

distinction and separated two forms of prosopagnosia: apperceptive (as a disorder in face

identification), and associative (as amnesia for faces) forms of prosopagnosia. Wilkinson et

al. (2009) observed that unilateral damage to the right cerebral hemisphere disrupts the

apprehension of whole faces and their component parts.


Barton (2008) proposed that, (1) prosopagnosia is more severe with bilateral than

unilateral lesions, indicating a minor contribution of the left hemisphere to face recognition,

(2) perception of facial configuration critically involves the right fusiform gyrus and (3)

access to facial memories is most disrupted by bilateral lesions that also include the right

anterior temporal lobe. According to the author, this supports assertions that more

apperceptive variants of prosopagnosia are linked to fusiform damage, whereas more

associative variants are linked to anterior temporal damage. It has been also further

suggested that (a) the most specific forms of prosopagnosia are due to lesions of a right

posterior network including the occipital face area and the fusiform face area, whereas (b)

the face identification defects observed in patients with left temporo-occipital lesions seem

due to a semantic defect impeding access to person-specific semantic information from the

visual modality. Furthermore, face recognition defects resulting from right anterior temporal

lesions can usually be considered as part of a multimodal people recognition disorder

(Gainotti, G. & Marra, 2011).

Probably, we have learned to identify faces in the same way that an ornithologist has

learned to identify birds or a farmer to identify individual animals. Some reports point to the

possibility of a prosopagnosic deficit restricted to a very specific visual subcategory. Assal

et al. (1984) reported a case of a peasant devoted to caring for cows with a restricted

agnosia for cows, associated with a transient prosopagnosia for human faces, anterograde

and retrograde amnesia, and topographic amnesia. The patient had difficulty in visual

imagery for cows but not for other visual categories, and visual hipoemotionality for cows

faces ("the cows have lost their personality and colorfulness"). This case of restricted

zooagnosia supports the specificity in learned visual recognition of individuals within a

particular visual subcategory. Difficulties in recognizing faces belonging to a different racial

group are well known to everyone, whereas twins are easily and errorless recognized by

their own parents and siblings.

It has been suggested that prosopagnosia arises due to an impairment of a process

that reduces uncertainty about the nature/location of the diagnostic cues for face

individualization: the ability to perceive multiple elements of a face as a single global


representation (holistic processing) (Ramon & Rossion, 2010). Being impaired at

processing individual faces holistically, prosopagnosic patients would tend to perform

relatively worse for processing facial areas containing multiple elements (i.e., the eyes),

and for elements that are widely spaced apart.

Prosopagnosic patients usually recognize people when hearing their voices (e.g.,

Bodamer, 1947; Damasio et al., 1982). Voice recognition disorders impair the ability to

recognize individuals. Phonagnosia has been defined as the acquired inability to recognize

and discriminate voices (Van Lancker & Carter, 1982). A further distinction has been

introduced between the discrimination of familiar and unfamiliar voices (Van Lancker et al.,

1988; Van Lancker et al., 1989). Deficits in recognizing familiar voices are significantly

correlated with damage to the inferior and lateral parietal regions of the right hemisphere,

whereas impairment of voice discrimination abilities is associated with temporal damage to

either hemisphere. This distinction clearly parallels the distinction between prosopagnosia

and prosopamnesia (Lopera & Ardila, 1992) (or between apperceptive and associative

prosopagnosia). It is important to point out that voices (like faces) also convey emotional

information. Occasionally, only auditory (but not visual) information is used to recognize a

particular individual (e.g., by phone).

A whole array of neuropsychological syndromes could have been associated with

defects in the recognition of individuals: some types of visual agnosia (prosopagnosia,

afilognosia, asomagnosia), deficits in voices recognition (phonagnosia), and even

eventually, disturbances in smell perception (hiposmia, anosmia, and potentially

“osmagnosia”).

In summary, it can be proposed that people recognition is based, predominantly but

not exclusively, in some visual information. Different subsystems or modules can be

distinguished. A first level analysis implies separating living (people, animals, plants) from

nonliving things (furnitures, cars, etc). Individual identification supposes the distinction of

familiar and nonfamiliar individuals. Additionally, gender and emotional states are to be

recognized in order to achieve a unitary individual perception.


Conclusions

A great effort has been devoted in neurology and neuropsychology to the analysis of face

recognition under normal, and specially, under pathological conditions. However, cultural

differences in people recognition show that, not only facial perception can be relevant in

individuals' identification, but also other visual signals, such as body and gait

characteristics. Furthermore, not only visual information may be relevant for people

recognition; auditory and even olfactory information can be also important in people

identification. Visual information can be more important in daylight conditions, while

auditory and olfactory signals can become relevant in dim conditions.

In cases of brain damage, sometimes one category or type of information can be

preserved, whereas others are impaired. At least the following perceptual dissociations

have been observed in brain-damaged patients:

1. Perception of living and non living things (Farah et al., 1991);

2. Perception of own-species and other species members; that is, people and

animals (e.g., Benton, 1980, 1990; De Renzi, 1986; Farah, 1990);

3. Perception of familiar and nonfamiliar faces (e.g., Bauer, 1984; De Haan &

Young, 1987; De Haan et al., 1992; Lopera & Ardila, 1992; Warrington and James, 1967);

4. Face identification and recognition of emotional expressions (e.g., Bruyer et al.,

1983; Feyereisen, 1986; Shuttleworth et al., 1982);

5. Facial gender-identification and whole-body gender-identification (Ardila &

Rosselli, unpublished); and


6. Visual and auditory people recognition (e.g., Bodamer, 1947; Van Lancker et al.,

1988; Van Lancker et al., 1989);

Different subsystems (or "modules") could be involved in people recognition.

"People" could represent a subsytem included within the higher level "living things"

system. One subgroup of this "people" subsystem includes "familiar individuals" (versus

"nonfamiliar individuals"). "Familiar individuals" includes all the stock of known people,

perhaps, several thousands. Face can be enough to recognize an individual (although

voice, gait, body configuration signals, etc., can be also enough to recognize the very same

individual). Additionally, gender and emotional expression are conferred to familiar, but also

to nonfamiliar persons. Gender and emotional expression can be recognized not only

departing from visual, but also auditory information. Individual's recognition represents the

final step in this people processing system. Individual's recognition (as it is the meaning of

a particular word) represents a complex perception, including multiple association systems

(especially visual, but also auditory and even olfactory), and maintaining some specific

emotional, memory, and even verbal (individual's name) relationships.

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8. Culture and Cognitive Testing4

Introduction

In neuropsychology, cognitive disturbances associated with brain pathology of a limited

subsample of the human species --contemporary Western, and most often, urban

middle-class and literate brain-damaged individuals-- have been relatively well analyzed.

Our understanding about the brain's organization of cognitive abilities, and the disturbances

in cases of brain pathology, is therefore not only partial but, undoubtedly, culturally biased

(Ardila, 1995; Fletcher-Janzen, Strickland & Reynolds, 2000; Uzzell, Pontón & Ardila,

2007).

Cultural and linguistic diversity is an enormous, but frequently overlooked,

moderating variable. Several thousands of different cultures have been described by

anthropology (e.g., Bernatzik, 1957; Rosaldo, 1993), and contemporary humans speak

over 6,800 different languages (Grimes, 2000; www.ethnologue.com). Norms for

performance in a sufficiently broad array of neuropsychological tests and an extended

analysis of cognitive disturbances in different cultural and ecological contexts are

necessary for us to understand the brain organization and evolution of cognition.

A significant interest in understanding cultural variables in neuropsychology has

been observed since the 1980’s and particularly since the 1990’s (e.g., Ardila, 1993, 1995;

Boivin & Giordani, 2009; Chen et al., 2009; Choudhury et al., 2010; Ferraro, 2002; Fletcher-

Janzen et al., 2000; Nell, 2000; Rendell et al., 2011; Uzzell et al., 2007).

Different questions have been approached including but not limited to: Bilingualism

research; historical origins of cognition; studies on illiteracy; cross-linguistic analysis of

4 A previous version of this chapter was published in: Uzzell, B., Pontón, M. & Ardila A. (eds). (2007). International Handbook of Cross-Cultural Neuropsychology. Mahwah, NJ: Lawrence Erlbaum Associates, pp. 23-45


aphasia, alexia and agraphia; research about the influence of socioeducational factors in

neuropsychological performance; norms in different national and cultural groups; studies on

cultural variables on handedness; neuropsychological assessment and treatment in diverse

human groups; analysis of neuropsychological test bias; cultural application of different

neuropsychological test batteries; legal and forensic significance of cultural factors; and

cognitive abilities in different cultural contexts.

In this chapter, an attempt will be made to summarize the major cultural variables

affecting cognitive test performance. I will attempt to integrate some ideas previously

presented in different publications (Ardila, 1993, 1995, 1996, 1999, 2003, 2007; Ardila et

al., 2000a, 2000b, 2010; Ardila, Rodriguez & Rosselli, 2003; Harris et al., 2001; Ostrosky

et al., 1998; Puente & Ardila, 2000).

What is culture?

Culture refers to the set of learned traditions and living styles, shared by the members of a

society. It includes the ways of thinking, feeling and behaving (Harris, 1983). The minimal

definition of culture could simply be, culture is the specific way of living of a human group.

Three different dimensions of culture can be distinguished: (1) The internal,

subjective or psychological representation of culture, including thinking, feeling, knowledge,

values, attitudes, and beliefs. (2) The behavioral dimension, including the ways to relate

with others, ways of behaving in different contexts and circumstances, festivities and

meeting, patterns of associations, etc. (3) Cultural elements: the physical elements

characteristic of that human group such as symbolic elements, clothes, ornaments, houses,

instruments, weapons, etc.

Culture represents a particular way to adapt to and survive in a specific context.

Cultural differences are strongly related with environmental differences. Eskimo and

Amazonian jungle culture differences are in a significant extent due to the geographical and


environmental differences between the Arctic region and the Amazonian jungle. Cultures,

however, are usually in some contact and a significant cultural diffusion is generally

observed. Cultural evolution and cultural changes are found throughout human history,

depending upon, (a) new environmental conditions, (b) contact with other cultures, and (c)

internal cultural evolution. For example, Gypsies in Russia and Gypsies in Spain have

many cultural commonalties, but also many differences.

Cultures can be grouped into branches using different criteria, but mainly, their

origins (e.g., Latin cultures, Anglo-Saxon cultures, Islamic cultures, Amerindian cultures,

etc.). When comparing two cultures, certain relative distance could be assumed. For

instance, the cultural distance between Mediterranean cultures and Anglo-Saxon cultures is

lower than the cultural distance between the Mediterranean cultures and the Amerindian

cultures. This means that Mediterranean people have more attitudes, beliefs, behaviors,

and physical elements in common with Anglo-Saxons than with Amerindians.

Certain cultural elements have been particularly successful and have tended to

strongly diffuse across cultures. For instance, science and technology have been extremely

successful in solving different human problems and have, in consequence, tended to

spread throughout virtually all-existing worldwide cultures. In this regard, contemporary

man has tended to become more homogeneous and to share the culture of science and

technology. To live in Peking and New York is not so different today as it was living in

Tashkent and Rome several centuries ago. Furthermore, communication is faster today

than it was anytime in history and cultural diffusion has become particularly fast.

Formal education and school have played a crucial role in the diffusion of science

and technology and in the contemporary trend toward the relative cultural homogenization.

In this regard, school can be considered as a subculture, the subculture of school (Ardila,

Ostrosky & Mendoza, 2000). School not only provides some common knowledge but also

trains some abilities and develops certain attitudes. Cognitive testing is obviously based on

those assumptions as well as values of scientific and technologically-oriented societies.

Schooled children usually share more scientific and technological values and attitudes than

their lower educated parents, and schooled subjects significantly outperform illiterate


individuals in cognitive testing (e.g., Ardila et al., 2010; Ostrosky, Ardila, Rosselli,

López-Arango & Uriel-Mendoza, 1999; Reis, Guerreiro & Petersson, 2003; Rosselli, 1993).

Why culture affects cognitive test performance?

Cross-cultural cognitive testing has been a polemic matter because cognitive assessment

uses certain strategies and elements that are not necessarily shared by every culture

(Laboratory of Comparative Human Cognition, 1983). Greenfield (1997) has pointed out

that there are three different reasons to account why cognitive ability assessments do not

cross cultures: (1) Values and meanings, (2) modes of knowing, (3) and conventions of

communication.

“Values and meanings” means that there is not a general agreement on the value or

merit of particular responses to particular questions. For example, some people may

consider that in the Raven’s Progressive Matrices test, it is a better answer that one

following an aesthetic principle (i.e., the figure that looks better in that position) than the

one according to a conceptual principle (i.e., the figure that continues the sequence).

Furthermore, the same items do not necessarily have the same meaning in different

cultures, regardless of how appropriate and accurate the translation is. An item referring to

the protection of animals may have a rather different meaning in Europe than in a hunting

society. The question “Why should people pay taxes?” may trigger quite different

associations in a society where people consider that taxes are fairly expended than in a

society where people think that taxes are misused.

“Knowing” may be a collective endeavor and not an individual task. Many collective

societies find it surprising that the testing situation requires individual’s responses without

the participation of the social group. If most activities are carried out in a collective way,

why should answering a test be the exception? Many cultures, on the other hand, do not

make a distinction between the process of knowing and the object of knowing. In


consequence, questions such as “why do you think?”, or “why do you consider?” may be

incomprehensible. The point is not what I think or I consider; the point is how it is.

“Conventions of communication” are highly culture-dependent. The test questions

assume that a questioner who already has a given piece of information can sensibly ask a

listener for the same information. To ask or to answer questions can be highly variable

among cultures. American children, for example, learn that they should not talk to

strangers, but they also learn that they should answer questions to “the doctor”, regardless

that the doctor is a stranger. In many societies adults rarely talk with children (“What could

you talk about with a child?”), and it is not considered appropriate for children to participate

in adults’ conversations. Furthermore, relevant information is not always the same in every

culture. Many types of questions can be difficult to understand. To copy nonsense figures

(e.g., Rey-Osterrieth Complex Figure) can be suspicious for many people. It may be a

relevant item for an American school child, but it is absurd for somebody living in a non-

psychometrically oriented society. Certain question formats used in testing can be

unfamiliar or less familiar in many cultures. For instance, after his first multiple-choice test,

a college Haitian student in the US returned it to the instructor pointing out “I simply do not

have the minimal idea of what I am supposed to do”. Conversely, I have found that

American university students score notoriously lower in open-question exams than in

multiple-choice formats.

Effect of culture is not limited to verbal abilities, but is also clearly found on

nonverbal abilities too (Rosselli & Ardila, 2003). When nonverbal test performance in

different cultural groups is compared, significant differences are evident. Performance on

non-verbal tests such as copying figures, drawing maps or listening to tones can be

significantly influenced by the individual’s culture.

Five different cultural aspects potentially affecting neuropsychological test

performance will be emphasized: (1) patterns of abilities, (2) cultural values, (3) familiarity,

(4) language, and (5) education.


Patterns of abilities

While basic cognitive processes are universal, cultural differences in cognition reside more

in the situations to which particular cognitive processes are applied than in the existence of

the process in one cultural group and its absence in the other (Cole, 1975). Culture

prescribes what should be learned, at what age and by which gender. Consequently,

different cultural environments lead to the development of different patterns of abilities

(Ferguson, 1956). Cultural and ecological factors play a role in developing different

cognitive styles (Berry, 1979).

Cognitive abilities usually measured in neuropsychological tests represent, at least in

their contents, learned abilities whose scores correlate with the subject's learning

opportunities and contextual experiences. Cultural variations are evident in test scores, as

culture provides us with specific models for ways of thinking, acting and feeling (Ardila,

1995; Berry, 1979).

Cultural values

Culture dictates what is and what is not situationally relevant and significant. What is

relevant and worth to learn or to do for an Eskimo does not necessarily coincide with what

is relevant and worth learning or doing for an inhabitant of the Amazonian jungle. A culture

provides specific models for ways of thinking, acting and feeling, and cultural variations in

cognitive test scores are evident (Anastasi, 1988).

Current neuropsychological testing uses specific conditions and strategies that may not

be only unfamiliar to many people, but also may violate some cultural norms. At least the

following cultural values underlay psychometrically oriented cognitive testing (Ardila, 2005):


1. One-to-one relationship. There is a tester and there is a testee. Hence, it is a one-

to-one relationship between two people that very likely have never met before, are

aliens, and will not meet again in the future.

2. Background authority. The testee will follow (obey) the instruction given by the

tester, and hence, the tester has a background or situational authority. It is not so

easy, however, to understand who and why this authority was conferred.

3. Best performance. The testee will perform at best. Performance “at best” is only

done in those endeavors that are perceived and regarded as extremely important

and significant. It is supposed in consequence that the testee has to perceive testing

as a most important and significant endeavor. It may not be clear enough in many

cultural groups why it is so important and relevant to repeat a series of nonsense

digits or to draw an absurd figure.

4. Isolated environment. Testing is done in an isolated room. The door is closed and

even locked. Usually, nobody else is allowed to be present, and in this regard it is a

private and intimate situation. Private appointments with aliens may be quite

inappropriate in many cultures. The testee has to accept this type of unusual social

relationship.

5. Special type of communication. Tester and testee do not maintain a normal

conversation. Tester uses a stereotyped language, repeating over and over again

the same phrases in a rather formal language. Testee is not allowed to talk about

him/herself. Nothing points to a normal social relationship and usual conversation.

This is a type of relationship that can be different from any type of relationship

existing in the subject’s past experience. For Hispanics, as an example, the personal


relationship with the examiner may be more important than the test results

(Geisinger, 1992). Dingfelder (2005) points out that “The detached professional

relationship that many therapists cultivate with their clients may seem alien to those

Latinos that adhere to the value of close interpersonal relationship. Therapist might

consider sharing some minor details of their lives with these clients, to make the

clients feel more comfortable and welcome” (p. 59).

6. Speed. In many tasks the tester warns that the testee must perform “as fast as

possible” and even time is measured. In the middle of the task, however, the tester

frequently interrupts saying, “stop!” For many cultural groups speed tests are frankly

inappropriate. Speed and quality are contradictory, and good products are the

results of a slow and careful process. Speed, competitiveness and high productivity

are most important cultural values in literate Anglo-American society, but that is not

true in other cultural groups.

7. Internal or subjective issues. The tester may ask questions that can be perceived

as a violation of privacy. Questions about cognitive issues (e.g., “How is your

memory?”) are also questions about internal subjective representations, the most

personal private sphere. Frequently, intellectual or cognitive testing may be

perceived as aversive in some cultures. In Latin America, usually highly educated

people dislike and try to avoid cognitive testing. Intellectual testing may even be

perceived as kind of humiliating situation and disrespect to the privacy.

8. Use of specific testing elements and testing strategies. The tester uses figures,

blocks, pictures, etc., and the reason for presenting them may not be easy to

understand. That is, the reason may be evident for the tester (e.g., to assess

memory) but not for the testee. Sometimes the tester explains that it is like a game,

but there is no evident reason to come to play with this alien tester. Sometimes the


tester refers to “exercises”, but exercises are by definition useless activities without

any evident goal. “Exercises” are indeed “preparation for something”. Preparation for

what? Furthermore, it they are just “exercises” why to perform “at best”? In brief, it is

not easy to understand (and to explain) the reason to memorize meaningless digits

or saying aloud “as many animal names as possible in one minute”, etc.

In summary, the rationale and the procedures used in cognitive testing rely on a whole

array of cultural values that in no way can be regarded as universal values. “When testers

use tests developed in their own culture to test members of a different culture, testees often

do not share the presumptions implicitly assumed by the test” (Greenfield, 1997; p. 1115). It

is not surprising that the members of the culture where the test was developed usually

obtain the highest scores.

Familiarity

Familiarity with the testing situation includes not only the elements used in testing (bikes,

houses, figures, stories, etc.) but also the testing environment (see above), and the cultural

relevance (meaningfulness) of the elements of the test (Ardila & Moreno, 2001). Familiarity

also refers to the strategies needed to solve the task and the attitudes required to succeed.

Competitiveness, for example, in many societies is viewed with suspicion. Cooperation and

social ability may be far more important.

The Boston Naming Test (even the version adapted in Spain) includes naming a

beaver and an acorn, an animal unfamiliar for people living in South America and a virtually

unknown plant. North American people very likely would consider it unfair to be tested by

naming South American animals and plants. The Boston Naming Test also includes a

pretzel, a most typical American element but totally unknown in most countries. Obviously,

it would also be frankly unfair to test naming ability in American subjects using tortillas or


tacos as stimuli. Figures representing snow may be unfamiliar for people living in tropical

and sub-tropical areas.

Cultural relevance (meaningfulness) may be another significant confounding factor in

cross-cultural neuropsychological testing. Items developed in a particular cultural context

do not have the same relevance when translated to another culture. Spelling out words

(frequently included in the Mini-Mental State Exam) is not used in languages with

phonological writing systems (such as Russian, Italian or Spanish), and hence it is

perceived as an artificial task. In many world cities, people get oriented using cardinal

points (North, South, West, and East) but in no way is this strategy found in every culture. I

personally do not know where is North, South, West, and East in my Colombian hometown

simply because I never used it. People in Barcelona (Spain) use to spatial directions:

“toward the sea” and “toward the mountain”. People in Colombia frequently use “up” and

“down”, referring to the numbering system, but “up” and “down” in Guadalajara (México)

mean “from downtown” and “toward downtown”. The Picture Arrangement subtest from the

Wechsler Intelligence Scale may have different levels of difficulty in different cultural

contexts, depending on the familiarity with the story’s elements. Something may be obvious

in a culture, but unusual and weird in another.

Language

Language plays an instrumental role in cognition (Vygotsky, 1962, 1989). As a matter of

fact, it represents the major cognitive instrument. Different languages differ in phonology,

lexicon (semantic field of the words), grammar, pragmatic, and reading systems. These

differences may affect language test performance. Different languages conceptualize the

world in a different way (Whorf, 1956). For instance, the notion of time is quite different in

Latin languages than in Germanic ones. Latin languages have a significantly high number

of tenses pointing to some temporal nuances. Slavic languages use perfective and non

perfective tenses in verbs. Space and casualty are also coded different in different

languages.


Language usage differs according to the cultural (and subcultural) background and

strongly correlates with the subject's educational level. Sometimes, test instructions (and in

general, the language used in testing) are given in a formal language, which may be very

difficult to understand for individuals with limited education. Formal language represents a

sort of academic language, most often found in a written form that many people neither use

nor completely understand. A permanent effort is required to make test instructions and, in

general, test language understandable for less educated people and appropriate for

different cultural and subcultural groups.

Education

Education plays a double role in test performance: school, on one hand, provides some

contents frequently included in cognitive tests; and school, on the other hand, trains some

learning strategies and develops positive attitudes towards intellectual matters and

intellectual testing. In consequence, school could be considered as a subculture into itself.

Greenfield (1997) has emphasized that “A major (probably the major) factor that makes a

culture more or less different from the cultural conventions surrounding ability testing is the

degree of formal education possessed by the participants” (p. 1119).

Learning to read reinforces certain fundamental abilities, such as verbal memory,

phonological awareness, and visuospatial discrimination (Ardila, Ostrosky & Mendoza,

2000; Ardila et al., 2010). It is not surprising that illiterate people underscore in cognitive

tests tapping these abilities. Furthermore, attending school also reinforces certain attitudes

and values that may speed the learning process, such as the attitude that memorizing

information is important, knowledge is highly valuable, learning is a stepwise process

moving from the simpler to more complex, etc. It has been emphasized that schooling

improves an individual’s ability to explain the basis of performance on cognitive tasks

(Laboratory of Comparative Human Cognition, 1983). The fundamental aims of schools are

equivalent for all schools and school reinforces certain specific values regardless of where

they are located. Hence, school could be seen as a culture unto itself, a transnational


culture, the culture of school. School not only teaches, but also helps in developing certain

strategies and attitudes that will be useful for future new learnings. Ciborowski (1979)

observed that schooled and non schooled children can learn a new rule equally well, but

once acquired, schooled children tend to apply it more frequently in subsequent similar

cases.

Interestingly, education is not related with the ability to solve everyday problems.

Cornelious and Caspi (1987) found that educational level has a substantial relationship with

performance on verbal meaning tests but was not systematically related to everyday

problem solving (i.e., functional criterion of intelligence). Craik, Byrd, and Swason (1987)

observed that differences in memory loss during aging are related to socioeconomic status.

Ardila and Rosselli (1989) reported that during normal aging the educational variable was

even more influential on neuropsychological performance than the age variable. Albert and

Heaton (1988) argue that, when education is controlled, there is no longer evidence of an

age-related decline in verbal intelligence.

A significantly decreased neuropsychological test performance has been

documented in illiterate individuals (Ardila, 2000; Ardila et al., 1989, 2010; Goldblum &

Matute, 1986; Lecours et al. 1987a, 1987b, 1988; Manly et al., 1999; Matute et al., 2000;

Ostrosky et al., 1998; Reis & Castro-Caldas, 1997; Reis, Guerreiro & Petersson, 2003).

Rosselli, et al., 1990). Lower scores are observed in most cognitive domains, including,

naming, verbal fluency, verbal memory, visuoperceptual abilities, conceptual functions, and

numerical abilities. Language repetition can be normal for meaningful words, but abnormal

for pseudowords (Reis & Castro-Caldas, 1997; Rosselli et al., 1990). Similarly, copying

meaningful figures can be easier than copying nonsense figures (Ostrosky et al., 1998).

Furthermore, for illiterate people to use concrete situations can be notoriously easier than

using non-real and abstract elements. When the information is related to real life, it can be

significantly easier to understand. Thus, for the illiterate person, it is easier to solve the

arithmetical operation “If you go to the market and initially buy 12 tomatoes and place them

in a bag and later on, you decide to buy 15 additional tomatoes, how many tomatoes will


you have in your bag?” than the operation: “How much is 12 plus 15?” Semantic verbal

fluency is easier than phonological verbal fluency (Reis & Castro-Caldas, 1997; Rosselli et

al., 1990), seemingly because phonological abstraction is extremely difficult for the illiterate

person. Semantic verbal fluency requires the use of concrete elements (animals, fruits)

whereas phonological fluency is tapping a metalinguistic ability. The very low scores

observed in neuropsychological tests in illiterates can be partially due to differences in

learning opportunities of those abilities that the examiner considers most relevant, although,

they are not the really relevant abilities for illiterates' survival. They can be also due to the

fact that illiterates are not used to being tested. Furthermore, testing itself represents a

nonsense situation that illiterate people may find surprising and absurd. This lack of

familiarity with a testing situation represents a confounding variable when testing individuals

with limited education.

Several studies have demonstrated a strong association between educational level

and performance on various neuropsychological measures (e.g., Ardila, Rosselli &

Ostrosky, 1992; Bornstein & Suga, 1988; Finlayson, Johnson & Reitan, 1977; Heaton,

Grant & Mathews, 1986; Leckliter & Matarazzo, 1989; Ostrosky et al., 1985, 1986).

However, some tests are notoriously more sensitive to educational variables (e.g.,

language understanding tests) than others (e.g., orientation tests). Extremely low scores in

current neuropsychological tests are observed in illiterate people (e.g., Ardila, Rosselli &

Rosas, 1989; Rosselli, Ardila & Rosas, 1990). Low scores in neuropsychological tests

observed in illiterates can be partially due not only to differences in learning opportunities of

those abilities that the examiner considers relevant (although, evidently, they are not the

really relevant abilities for illiterates' survival) and to the fact that illiterates are not used to

being tested (i.e., they have not learned how to behave in a testing situation), but also, that

testing itself represents a nonsense (non-relevant) situation (Ardila, 1995).

This educational effect, nonetheless, is not a linear effect, but rather it is a negatively

accelerated curve, ending in a plateau. Differences between zero and three years of

education are highly significant; differences between three and six years of education are


lower; between six and nine are even lower; and so forth. And virtually no differences are

expected to be found between, for example, 12 and 15 years of education. The reason is

simple: the ceiling in neuropsychological tests is usually low (Ardila, 1998). Table 8.1

presents the differences in some cognitive tests between illiterates and subjects with one-

two and three-four years of education and Figure 8.1 illustrates a specific example.

_______________________________________________________________________________

Years of education

Test 0 1-2 3-4

_________________________________________________________________

Digits backwards 2.4 2.6 2.7

Verbal memory 4.2 4.2 4.3

Copy of a figure 7.5 8.8 9.4

Naming 7.3 7.3 7.5

Comprehension 3.7 4.4 4.6

Semantic fluency 13.5 14.6 15.4

Phonologic fluency 3.3 6.5 7.0 ________________________________________________________________________________

Note: mean scores are presented

Table 8.1. Effect of education on test performance in some selected subtests of the

NEUROPSI neuropsychological test battery (n=807) (adapted from Ostrosky et al.,

1999).


Figure 8.1. The educational effect is not a linear effect, but rather it is a negatively

accelerated curve, ending in a plateau. Example of the Copy of a Semi-Complex

Figure test (adapted from Ostrosky et al., 1999).

Although it is well established that there a significant correlation between cognitive

test scores (e.g., IQ) and school attendance (e.g., Matarazzo, 1972) interpreting this

correlation has been polemic (Brody, 1992; Finch et al., 2011; Neisser et al., 1996). The

really crucial question is: Do cognitive (intelligence) tests indeed predict school

performance? Or rather, does school train those abilities appraised in intelligence tests? To

answer these questions is not easy, even though frequently the interpretation has been that

IQ predicts school performance (e.g., Hunter, 1986). Other researchers, however, consider

that IQ scores are to a significant extent a measure of direct and indirect school learning

(e.g., Ardila, 1999; Ceci, 1990, 1991).

Ceci and Williams (1997) presented an impressive and detailed review of the

available data in this area. Seven types of historical evidence for the effect of schooling on

IQ were examined:


(1) The effect of intermittent school attendance: several studies have provided

converging evidence that the longer youngsters stay out of school, the lower their IQs.

(2) The effect of delayed school start-up. Different studies have demonstrated

that children whose schooling was delayed experienced a decrement in several IQ points

for every year that their schooling was delayed.

(3) The effect of remaining in school longer. As a result of extra schooling (to

avoid military service), men born on a particular date (July 9 instead of July 7) earned

approximately a 7% rate of return on their extra years of schooling. The authors point out

that this figure of 7% is very close to the estimate of the return on an extra year of

schooling derived from studies of being born early or late in a given year.

(4) The effect of discontinued schooling. There is a well-established detrimental

effect of dropping out of school before graduating. For each year of high school not

completed, a loss of 1.8 IQ points has been observed.

(5) The summer school vacations. A systematic decline in IQ scores occurs during

summer months. With each passing month away from school, children lose ground from

their end-of-year scores on both intellectual and academic scores.

(6) The effect of early-year birth dates. Given the age limits to enter school in the

US, within a given year, the number of years of schooling completed is the same for those

born during the first nine months of the year. But the amount of school attendance drops off

for those born during the final three months of the year. After coming of age, some

individuals leave school, and students with late-year births are more likely to stay in school

one year less than students with early-year births. It has been observed that for each year

of schooling that is completed there is an IQ gain of approximately 3.5 points.


(7) Cross-sequential trends. A correlation between the length of schooling

completed and intellectual performance among same-age, same-SES children has been

observed.

The general conclusion is that school attendance accounts not only for a substantial

portion of variance in children's IQ but also apparently some, though not all, of the cognitive

processes that underpin successful performance in IQ tests. The magnitude of this

influence ranges between 0.25 to 6 IQ points per year of school (Ceci, 1991). In

consequence, the association between IQ and education cannot be interpreted assuming

that IQ predicts school success. Intelligence and schooling have complex bi-directional

relationships, each one influencing variations in the other (Ceci & Williams, 1997).

According to our results (e.g., Ardila et al., 2000b) even though bi-directional

relationships between intellectual test performance and schooling may exist, the really

significant relationship is between schooling and cognitive test performance. That is,

attending school significantly impacts cognitive test performance.

Culture minorities groups

Cognitive testing of so-called “minority groups” represents a special situation in

neuropsychology assessment. Minority groups constitute a culture or subculture within a

mainstream culture. Quite often, the tester belongs to the majority culture and may have a

limited understanding of the minority culture or subculture. Testing is likely interpreted from

the majority culture perspective. To be a member of a minority group, however, has

significant implications that can affect the testing situation and the testing results.


There are over 120 million people living in a country different from that one where they

were born. They are "minorities” in the new host country: Turkishes in Germany,

Moroccans in Spain, Hindus in England, Colombians in Venezuela, Greeks in Switzerland,

Rwandans in Zaire, Mexicans in US, Greeks in France, etc. There are also some ethnic

groups that are “minorities” in their own countries: African-Americans in US, Kurds in

Turkey, Ameridians in Colombia (and virtually in every country), etc. Finally, there are some

groups that are “minorities” everywhere because they do no have a country. Currently

Gypsies are the best example, but until recently, Jews were also a peoplehood without a

country.

To be different from the mainstream people has a significant psychological impact.

Patterns of behavior, beliefs, and attitudes may be different. Language can impair normal

communication with the majority group. Even physical appearance and dressing can

separate and distinguish the minority people. In the US there are hundreds of groups that

can be regarded as “minorities”.

At least six different variables can potentially distinguish the minorities groups. They

may also affect intellectual test performance and the “psychology of minority”:

1. Nationality: is that person regarded or not as an alien? Intermediate

possibilities can exist. For instance, Hispanics in the US have five different

possibilities: US born (2 possibilities: from the mainland or from Puerto Rico),

acquired citizenship, legal immigrant, and illegal immigrant. It makes a significant

difference if the country where you are living in is legally your country or you are

a non invited alien.

2. Culture (relative distance). Irish immigrants in US have a closer culture to

mainstream American way of life than Ethiopians. The larger the cultural

distance, the more separated you are to understand the new culture and

appropriately behave in it.


3. Language (relative distance). Minorities may speak a different language, may

speak a dialect of the majority language, or may simply speak the same

language. The ability to communicate, and hence, participate (e.g., to have a

job) in the host culture highly depends on the ability to speak. Language distance

between English and German is lower than language distance between English

and Spanish. Language distance between English and Chinese is huge. Age

also plays a crucial role in the ability to learn the new language. Young Moroccan

people in Spain can easily learn Spanish and improve in social status, whereas

adults have to accept low qualified and paid jobs.

4. Normality (how frequent -- normal-- is your group in your living environment). To

be different depends on the community you live in. Hispanics are the “normal

people” in Miami, but very unusual people in Fargo. To be unusual may be

associated with suspiciousness in the majority group and paranoia in the minority

people.

5. Reference group (How many people are like you are). It depends upon with

what specific group is the identification. Hispanics for instance, can consider that

their reference group is Latin America or other US Hispanics. In the fist case the

reference group is even larger than the majority US group. In the second one it

is a notoriously smaller and weak social reference group. Finally,

6. Social image: Positive or negative attitudes in the majority group toward the

minority people. Even though minorities have in general a low social image (e.g.,

they are poor, with low education, inappropriate behaviors, etc.) some times

positive attitudes are also associated with the minority group. For instance,


Oriental people are frequently regarded in the US as “intelligent and hard-

working people”.

Neuropsychological testing of minority groups have progressively become a more

and more important question in neuropsychology, particularly in some countries with a

significant immigration flow (e.g., some European countries). It is not easy for a Spanish

neuropsychologist to test a Moroccan patient, or for a Danish neuropsychologist to test a

Somalian client. There are not obvious answers to questions such as, how to carry the

testing, what specific tests to use, and what conclusions can potentially be drawn from the

testing results.

Norms in different national and cultural groups

A tremendous effort has been devoted in neuropsychology to obtaining test performance

norms (e.g., Ardila et al.., 1994; Lezak, 2004; Spreen & Straus, 1998). Currently, many

neuropsychological tests possess relatively solid and reliable norms. Nonetheless, norms

have been obtained in most cases in white English-speaking, middle-class subjects with a

high-school or college level of education.

In cognitive testing it is usually assumed that norms are always required. Otherwise, no

comparison is reliable. This idea, however, is more a desideratum than a reality. Furthermore,

it does not seem to be a completely realistic idea. As a matter of fact, in the future, the search

for norms may be coordinated with the search for understanding the sources of variation. Two

evident problems with norms are readily observed:

1. Language. To obtain norms in English or Spanish (each one with about 400 million

speakers) seems realistic. But English and Spanish are just two out of the three

largest existing languages accounting together for no more than 15% of the world’s


population. Worldwide, there are about 6,800 different languages

(http://www.ethnologue.com/), most of them, with a limited number of speakers. As

an example, in Mexico 288 Amerindian languages are currently spoken

(http://www.ethnologue.com/). In the USA, over 300 languages are found, when

counting both Amerindian and immigrant languages (http://www.ethnologue.com/).

To obtain norms for all these 6,800 different languages is simply unrealistic.

Furthermore, most of the world languages are small languages, and obtaining a

reliable database would mean testing a high percentage of the speakers. If we

assume that the average language has one million speakers (the real number is

lower), and we want to normalize the neuropsychological instruments using just 200

stratified subjects in each language, it would mean that about one and half million

participants would be required. This is a nonrealistic endeavor for contemporary

neuropsychology. It seems more realistic to determine the linguistic factors

potentially affecting cognitive test performance. A diversity of languages could be

selected, comparison established, and significant variables distinguished. Language

idiosyncrasies seem most important in understanding potential sources of variations.

Obtaining norms is a realistic endeavor in English, Spanish, Quechua or Bengali, but

does not seem realistic for the 288 Amerindian languages spoken in Mexico.

2. Culture. There are solid bases to assume significant cultural variations in

psychological and neuropsychological test performance (e.g., Ardila, 1995;

Fletcher-Janzen et al., 2000; Nell, 2000; Uzzell et al., 2007). Thus, the question

becomes, how many cultural groups should be separated? Although several

thousand different cultures have been described by anthropology (e.g., Bernatzik,

1957), obviously, there is not a definitive answer to this question. Cultures frequently

represent a continuum, and cultures can partially overlap. For example, if asked

whether separate norms should be used when testing Caucasians and Hispanics in

the US, most neuropsychologists might answer “YES”. Nonetheless, a diversity of

conditions may separate Caucasians and Hispanics: primary language (for many


Hispanics, their primary language is English; most Hispanics are bilinguals, some

are monolingual; the degree of mastery of Spanish and English is tremendously

variable), “acculturation” (degree of assimilation of the modal American culture

values is highly variable), etc. So, there does not seem to be an obvious and direct

answer. To be “Hispanic” or “Caucasian” is not a dichotomy. Another question: In

the US, can the norms obtained in San Francisco be used to test people in Boston,

San Antonio, Honolulu, or Anchorage? San Francisco is a quite heterogeneous city

and the question becomes what specific San Francisco norms are going to be used

with what specific population in Boston, San Antonio, Honolulu or Anchorage? The

same type of question can be raised everywhere. For instance, can we use the

norms obtained in Barcelona, Spain to test people in the Canary Islands, Santiago

de Compostela or Bilbao? The answer in all these cases may be, partially yes,

partially no. This is indeed an endless question. If we move to the worldwide

situation (with thousands of cultural variations!), we may conclude that this is also a

nonrealistic endeavor for psychology and neuropsychology. I am proposing that this

question has to be re-stated, and instead of looking for norms in every existing

human group, we should try to understand why culture may impact and how culture

impacts cognitive testing, i.e., which are the specific cultural variables that may

affect the performance in a psychological or neuropsychological tests (Ardila, in

press). For this purpose, it seems more reasonable to select a series of rather

different cultural groups, representing enough cultural dispersion, in an attempt to

pinpoint those cultural variables potentially affecting cognitive test performance.

In brief, understanding the variables that can affect cognitive test performance seems to

be as important as obtaining a large number of norms in different linguistic and cultural

groups. (Ardila, Ostrosky & Bernal, 2006).

For example, there does not seem to exist any reason to find differences in verbal

fluency in pre-school and school children when using an equivalent semantic category in

Spanish and English. If the familiarity with the testing condition is equivalent (both are small


children with little or no familiarity with testing), the level of education is the same (none or

whatever), the age is the same, and the semantic category has the very same semantic

field in both languages, no differences in performance are expected. Table 8.2 presents

the norms obtained by Halperin et al. (1989) in the US and Ardila and Rosselli (1994) in

Colombia. Even though the age groups were divided differently (Halperin et al. used one

year range; Ardila & Rosselli used two-year range) it is evident that performance was

virtually identical.

__________________________________________________________________

Halperin et al., 1989 Ardila and Rosselli, 1994

(USA) (Colombia)

__________________________________________________________________

Age Age

(years) n M SD (years) n M SD

__________________________________________________________________

6 34 10.74 2.40 5-6 49 9.33 3.65

7 40 12.43 2.90

8 32 12.31 2.70 7-8 63 11.49 2.87

9 38 13.76 3.70

10 22 14.27 3.70 9-10 56 14.09 3.99

11 28 15.50 3.80

12 10 18.90 6.20 11-12 65 16.75 4.64

__________________________________________________________________

Table 8.2. Semantic verbal fluency (ANIMALS) in US and Colombia.


Table 8.3. compares performance in two verbal fluency tests (phonological and

semantic verbal fluency) in Spanish and English monolingual speakers. As anticipated,

performance is virtually identical, if confounding variables are controlled. English speakers

do a little better when using some letters; Spanish speakers do a little better when using

other letters, very likely depending upon the frequency of words beginning with that

particular letter in each language, the potential ambiguity existing between homophone

letters, and some other uncontrolled confounding variables. Performance in semantic

verbal fluency using the category ANIMALS was virtually identical.

____________________________________________________________________

English Spanish

____________________________________________________________________

F 12.9 (5.4) 11.7 (4.1)

A 10.7 (5.1) 11.8 (4.6)

S 13.8 (5.4) 11.4 (3.8)

Animals 16.8 (5.2) 16.7 (3.8)

Note. Mean scores and standard deviations are presented.

Table 8.3. Semantic verbal fluency (ANIMALS) in Spanish and English monolinguals

(60-65 years; 13-16 years of education (according to Rosselli et al., 2000).


Nonetheless, unexpected confounding variables can exit. Digit span looks like a

relatively culture-fair test, and similar performance might be anticipated in people from

different human groups. Nonetheless, that is not the case. A significant variability has been

observed. Digit span varies from 5.4 (Poland) to 9.0 (China) (Dehaene, 1997; Nell,

2000).The reason for this variability is not totally clear, but both linguistic and training

factors seem to exist (Dehaene, 1997). The phonological length of digits (number of

phonemes included in digit words) as well as previous exposure to similar tasks (e.g., to

say phone numbers using digit-by-digit strategy) may play a significant role in digit span. In

the Sikuani language spoken in the Amazon jungle digits are: kae (one) , aniha-behe (two),

akueyabi (three), penayanatsi (four), kae-kabe (five), kae-kabe kae-kabesito-nua (six),

kae-kabe aniha-kabesito-behe (seven), kae-kabe aniha-kabesito-akueyabi (eight),

kae-kabe aniha-kabesito-penayatsi (nine). With such long words, it can be conjectured that

digit span will be very low.

What is proposed is that understanding the variables potentially affecting (and

confounding) test performance may be as important as obtaining norms for different human

groups.

No doubt, understanding cultural variables in cognition represents a major research

area during the twenty-first century.

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