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Evolution of the brain and social behavior in chimpanzeesTetsuro Matsuzawa

Available online at www.sciencedirect.com

The comparison of humans and chimpanzees is a unique way

to highlight the evolutionary origins of human nature. This

paper summarizes the most recent advances in the study of

chimpanzee brains, cognition, and behavior. It covers the

topics such as eye-tracking study, helping behavior, prefrontal

WM volume increase during infancy, and fetal brain

development. Based on the facts, the paper proposed the

‘‘social brain hypothesis’’. Chimpanzees are good at capturing

images as a whole, while humans are better at understanding

the meaning of what they see. Chimpanzees apparently focus

on the salient objects, neglecting the social context. In contrast,

humans always recognize things within the social context,

paying preferential attention to people, as agents. This is

consistent with the fact that humans are highly altruistic and

collaborative from a very young age. Thus, humans have

evolved towards increased collaboration and mutual support.

This kind of evolutionary pressure may have provided the basis

for the development of the human brain with its unique

functions.

Address

Primate Research Institute, Kyoto University, Japan

Corresponding author: Matsuzawa, Tetsuro

([email protected])

Current Opinion in Neurobiology 2013, 23:xx–yy

This review comes from a themed issue on Social & emotional

neuroscience

Edited by Ralph Adolphs and David Anderson

0959-4388/$ – see front matter, # 2013 Elsevier Ltd. All rights

reserved.

http://dx.doi.org/10.1016/j.conb.2013.01.012

Cognitive development in chimpanzeesThis paper aims to summarize the most recent advances

in the study of chimpanzee brains, cognition, and beha-

vior. The comparison of humans and chimpanzees pro-

vides a unique opportunity to highlight the evolutionary

origins of human nature.The first section addresses cog-

nitive development. We have conducted a series of

studies on comparative cognitive development in humans

and chimpanzees both in the wild and in the laboratory

[1,2]. The methodology used [1,2] in the laboratory is

called participant observation, whose unique aspect, in

contrast to previous ape-language studies, is that infants

are not separated from their mothers. The approach

instead has infants raised by their biological mothers,

Please cite this article in press as: Matsuzawa T. Evolution of the brain and social behavior in ch

www.sciencedirect.com

and nurtures a long-standing rapport between these chim-

panzee mothers and the researchers. This has allowed us

to test the cognitive development of infants in an intimate

face-to-face situation, in the presence and with the tol-

erance of the chimpanzee mother. Recent advances have

been made in this line of research in elucidating a wide

variety of processes including: visual illusions [3], move-

ment and depth perception [4,5], face recognition [6],

gaze detection [7], social cueing [8–10], contagious yawn-

ing [11], self-awareness [12], object manipulation [13],

tool use [14,15], cooperation [16], and others.

The most striking difference reported to date between the

two species is a remarkable ability to use visual working

memory in young chimpanzees, who can outperform even

adult humans on certain tasks [17–19] (Figure 1).

Specifically, chimpanzees can learn to touch the Arabic

numerals, 1–9, in ascending order. Once trained to criterion

on this task, we introduced a masking task to measure

working memory ability. Upon touching the lowest num-

ber, the remaining eight numbers are masked by white

squares and subjects are then required to touch the masked

stimuli in ascending order of the hidden numerals. This is

not an easy task for humans; however, three out of three

young chimpanzees succeeded. The young chimpanzees

performed better in terms of speed and accuracy than both

their own mothers and human adults. Ayumu, the most

skilled participant, can do the task with nine numerals at

5.5-year old, with a latency of 0.67 seconds to touch the first

number ‘1’ and a level of accuracy above 80% [17]. This

cannot be achieved by human subjects even if they are

trained for an extended period.

Chimpanzees also learned two versions of the matching-

to-sample (MTS) task: either an identity task, or a sym-

bolic task [19]. In an example identity MTS task, the

sample is the color red and the alternative response

choices the color red versus the color green. Touching

the matching color, red, is the correct choice. In the

symbolic MTS task, the sample is a color, for example

red, and the alternative responses are symbols, represent-

ing the matching color, red, and a different symbol

representing a non-matching color (e.g. green). Touching

the symbol corresponding to the sample color, in this case

red, is the correct choice.

Chimpanzees can learn the identity MTS task, but have

difficulty with the symbolic MTS task. Continuous train-

ing allowed the chimpanzees to master the task of choosing

the symbol corresponding to the sample color. A reversed-

order task can then be introduced, that is, presenting a

impanzees, Curr Opin Neurobiol (2013), http://dx.doi.org/10.1016/j.conb.2013.01.012

Current Opinion in Neurobiology 2013, 23:1–7


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2 Social & emotional neuroscience


Figure 1

Current Opinion in Neurobiology

Visual working memory in chimpanzees. Chimpanzee Ayumu is doing

the masking task of memorizing nine numerals at a glance.

Photo taken by T. Matsuzawa.

symbol as the sample, and colors as the alternative

responses. This reversed task is easy for humans, but

appears not to be so for chimpanzees [19]. This finding

was replicated in a recent study of collaborative MTS in

which two chimpanzees were required to collaborate on the

task [20�].

These findings support the interpretation that chimpan-

zee cognition is characterized by quickly grasping the

whole image, somewhat like capturing an image with a

camera (eidetic or photographic memory), while human

cognition is better characterized by seeing things while

understanding the associated meaning.

Eye-tracking studies in chimpanzeesThis human tendency to see things within context and

meaning has also received support from a recent series of

studies by Kano and Tomonaga using eye-tracking with a

range of ape species (chimpanzees, gorillas, orangutans)

[21–23]. The subject sits in front of the monitor screen,

with an eye-tracker located below. Stimuli, either a still

picture or a video clip, are then displayed on-screen.

These studies found that both humans and chimpanzees

preferred to look at the face in comparison to other parts

of the body. However, though the total time allocation

was the same, the fixation pattern was different. Fixation

in Chimpanzees moved quickly from one place to another

with large amplitude saccades, for example, from eye to

foot to eye to shoulder. Human spontaneous gaze shift

instead changes more smoothly, for example, moving

from eye to nose, to mouth, to chin [23].

One qualitative way to describe the difference between

the fixation pattern in humans and chimpanzees comes



from a study in which stimuli were a mixture of face and

non-face pictures presented briefly in alternating succes-

sion. Chimpanzees spontaneously and rapidly followed

the contents of each picture with their gaze, whereas

human gaze tended to stick on the face stimuli. Humans

have a strong spontaneous tendency to fixate longer on

faces compared to other stimuli [21].

A recent eye-tracking study clearly demonstrated the

importance of social context to human infants [24��].The subjects, chimpanzees and one-year-old human

babies sat in front of the monitor in the presence of their

caretaker or mother. The stimulus presented was a video

clip showing a young woman holding a bottle of juice and

pouring it into a glass. Chimpanzees watched the bottle

and the glass and did not attend preferentially to the

woman. In contrast, human infants’ gaze shifted back and

forth between the woman’s face, the bottle and the glass.

Humans appear to see target events within a social con-

text, always paying preferential attention to the person

(Figure 2).

Taken together, the studies reviewed thus far suggest

that humans have a tendency to focus on the meaning of

what they see, and also to see things within a social

context.

Altruistic behaviorChimpanzees in the wild show a highly developed tool

technology [25] and also altruistic behavior [26–29].

Altruistic behavior has also been investigated in the

laboratory [30]. Yamamoto and Tanaka carried out a series

of experiments in which two chimpanzees faced a colla-

borative task [31,32�,33–35]. Most striking was the lack of

reciprocity in chimpanzees, consistent with field obser-

vations of chimpanzee interaction [1]. Chimpanzees in

the wild behave altruistically, for example, a mother

chimpanzee helps or shares food with her offspring.

However, the reverse is not true; the infant chimpanzee

never gives food to his/her mother. In contrast, altruistic

behavior emerges at a very early phase in human de-

velopment.

Mutual help is referred to as reciprocity. Reciprocal

altruism was not found in chimpanzees. For example,

in one study, chimpanzee A is in one room while another,

chimpanzee B, is next door. Chimpanzee A can insert a

token into a vending machine that then delivers food to

chimpanzee B. At the same time, conversely, chimpanzee

B can insert a token resulting in the output of food to

chimpanzee A. The two chimpanzees were given 500

tokens each, simultaneously. Suppose that this was done

with human subjects — we would surely expect them to

collaborate by inserting the tokens for delivering food for

their neighbor reciprocally. The chimpanzees, however,

did not insert any tokens and so both failed to get a food

reward [33].




Evolution of the brain and social behavior in chimpanzees Matsuzawa 3


Figure 2


Eye-tracking in human and chimpanzee. Dotted areas represent the fixation points.

Photo provided by Myowa-Yamakoshi and Satoshi Hirata.

A recent study revealed an interesting aspect of chim-

panzee collaboration: helping behavior on demand.

Chimpanzee A had a set of tools such as sticks, straw,

rope, etc. Chimpanzee B, in a room next-door, was pre-

sented with a foraging task to solve, for example, a bottle

of juice was placed out of reach so that chimpanzee B

needed a stick to retrieve it. In another example, a tiny

hole in the wall allowed chimpanzee B to access a bottle

of juice with a straw, if she has one. Thus, chimpanzee A

had the tool-set required for solving the problems pre-

sented to chimpanzee B. The results showed that chim-

panzee A did not spontaneously help chimpanzee B.

However, when chimpanzee B extended and waved a

hand through a window between the adjacent rooms (in

request) chimpanzee A gave the necessary tool to chim-

panzee B. It must be noted that chimpanzee A handed the

correct tool for the task, for example, a stick for retrieving

the out-of-reach bottle. This strongly suggests that chim-

panzee A understood why chimpanzee B was in need

[30,32�] (Figure 3).

Suppose that this was done with human subjects — they

would be likely to spontaneously give the right tool to

their neighbor, even in the absence of any explicit request

from the person in difficulty. In chimpanzees, altruistic

behavior was not evident until it was clearly requested.



Taken together, humans show spontaneous altruistic

behavior without requests, and also display reciprocal

altruism. These results indicate that mutual support in

a social context may be uniquely human.

There are good amount of empirical studies reporting a

New World monkey species, capuchin monkeys (CebusApella), also show altruistic behavior (for review: [36]).

There are, however, very few systematic studies on the

altruistic behavior in the other apes and monkeys. There

are some anecdotes in captive bonobos about the human-

like spontaneous altruistic behavior. The apes raised by

humans in the human environment can show many

human-specific behavior including altruistic behavior.

However, the reciprocal altruism is not yet reported.

Suppose that there is a human mother with her young

child at the age of two years sitting in front of a plate of

strawberries. Mother may pick up a piece and give it to

her child. Then, the child may put a piece into the mouth

of the mother. This kind of behavior is ubiquitous in

humans but not in the other species.

Brain function and development inchimpanzeesHuman brains increased dramatically in size after the

emergence of the genus Homo. The size of the cerebrum,






Figure 4


EEG recordings in a chimpanzee. The chimpanzee quietly sat on the

chair and allowed the experimenter to put electrode patches on the skin

of her forehead, top of the head.

Photo provided by Satoshi Hirata.

Figure 3


Altruistic behavior in chimpanzees. A chimpanzee is giving a stick to

another chimpanzee on demand.

Photo provided by Shinya Yamamoto.

in particular, is much larger in humans than in other

primate species. While it is possible to estimate total

brain volume from cranial capacity, fossil records do not

provide more detailed information than that, because the

brain itself cannot, of course, be preserved in fossils.

Chimpanzees are the closest living relatives of humans

and give us the only opportunity to examine real brains

closely related to our own. A recent trend in cognitive

studies on chimpanzees has been a focus on uncovering

the neural correlates of behavior using noninvasive tech-

niques, just as with human subjects. Hirata and colleagues

were the first to successfully record an EEG from an

awake chimpanzee using a completely noninvasive tech-

nique, similar to that used for humans [37,38]. The

chimpanzee quietly sat in a chair and allowed the exper-

imenter to put electrode patches on the skin of her

forehead, top of the head, etc. (Figure 4).

The EEG and ERP studies showed clearly that the chim-

panzee was able to recognize her own name: ‘Mizuki’



[39,40]. Previous behavioral studies supported this kind

of auditory comprehension in chimpanzees to some extent.

Moreover, chimpanzees may have visual-auditory integ-

ration, just like humans [41�,42]. While the detailed neural

mechanisms behind these effects will require further

investigation, this is the first case of recording chimpanzee

brain activity in a very humane way (Figure 4).

Another recent study showed longitudinal brain devel-

opment through structural MRI imaging, again using a

relatively noninvasive technique. Chimpanzees can be

anesthetized by injection in a face-to-face situation, as are

human subjects.

Sakai and collaborators collected MRI images of the brain

in three chimpanzees soon after birth [43�] and continued

for the first 6.5 years longitudinally. The chimpanzee data

were compared with data from humans and macaque

monkeys. The focus was a comparison of the develop-

mental pattern of white matter (WM) within the pre-

frontal region, thought to mediate complex cognitive






Figure 5


Developmental neuroscience. Fetal brain development in chimpanzees

was measured by a noninvasive ultrasound technique.

Photo provided by Satoshi Hirata.

processes through its reciprocal connections with

posterior brain regions. Prefrontal WM volume in chim-

panzees was immature and had not yet reached its adult

level during pre-puberty, similar to what was observed in

humans, but not in macaques. However, the rate of

prefrontal WM volume increase during infancy was

slower in chimpanzees than in humans. The results

suggest a more developmentally protracted elaboration

of neuronal connections in the prefrontal portion of the

developing brain in chimpanzees, a pattern that likely

existed in the last common ancestor of chimpanzees and

humans. The rapid development of prefrontal WM in

human infants may assist in the development of complex

social interactions as well as in the acquisition of experi-

ence-dependent knowledge and skills, such as language

acquisition and learning to use modern technology.

There have been a few studies investigating chimpanzee

brain development even in the fetus [44,45]. The most

recently published study used a noninvasive ultrasound

technique [46�,47], and found that while the growth rate

of brain volume accelerated throughout gestation in

human fetuses, as expected, this was not so in chimpan-

zee fetuses through the later stages of pregnancy. This

indicates that humans and chimpanzees differ with

respect to the development of brain volume during the

fetal period [46�]. Uniquely human encephalization

already begins in utero (Figure 5).

Social brain hypothesis: trade-off betweenmemory and language based on social lifeRecent studies of cognition and behavior demonstrate

clearly the difference between humans and chimpanzees.



Chimpanzees are good at capturing images rapidly as a

whole, while humans are better at understanding the

meaning of what they see. Chimpanzees apparently focus

on any salient objects, neglecting the social context. In

contrast, humans always recognize things within a social

context, paying preferential attention to people, as

agents. This is consistent with the fact that humans are

highly altruistic and collaborative from a very young age.

Such differences in humans may be traced to the social

organization of early hominids, especially the way they

reared their offspring. Chimpanzees give birth to one

infant at a time with an average inter-birth-interval of

five years [48]. Chimpanzee mothers rear their young

more or less alone. However, humans are cooperative

breeders, raising the next generation through the collab-

oration of many adults.

The distinctive factor in human communication is, of

course, language. However, it is important to appreciate

the broader implications of the nature of language, such as

its portability. Suppose that you have witnessed an event:

language allows you to bring the experience back to your

home-base. Because of language, you can share it with the

other members of your family or community. Chimpan-

zee-like photographic memory may well aid individuals

in their everyday life. Human adults appear to have lost

this extraordinary ability for eidetic memory. However,

language has helped us to collaborate with each other and,

moreover, to share benefits communally. Thus, this may

be one mechanism for how humans have evolved toward

increased collaboration and mutual support. This kind of

evolutionary pressure may have provided the basis for

the development of the human brain with its unique

functions.

References and recommended readingPapers of particular interest, published within the period of review,have been highlighted as:

� of special interest�� of outstanding interest

1. Matsuzawa T, Humle T, Sugiyama Y: The Chimpanzees in Bossouand Nimba. Springer; 2011.

2. Matsuzawa T, Tomonaga M, Tanaka M: Cognitive Development inChimpanzees. Springer; 2006.

3. Imura T, Tomonaga M: Moving shadows contribute to thecorridor illusion in a chimpanzee (Pan troglodytes). J CompPsychol 2009, 123:280-286.

4. Matsuno T, Tomonaga M: Visual search for moving andstationary items in chimpanzees (Pan troglodytes) andhumans (Homo sapiens). Behav Brain Res 2006, 172:219-232.

5. Matsuno T, Tomonaga M: Stream/bounce perception and theeffect of depth cues in chimpanzees (Pan troglodytes). AttentPercept Psychophys 2011 http://dx.doi.org/10.3758/s13414-011-0126-6. (published online).

6. Hirata S, Fuwa K, Sugama K, Kusunoki K, Fujita S: Facialperception of conspecifics: chimpanzee (Pan troglodytes)attend to proper orientation and open eyes. Anim Cogn 2010,13:679-688.



http://dx.doi.org/10.3758/s13414-011-0126-6

http://dx.doi.org/10.3758/s13414-011-0126-6




7. Tomonaga M, Imura T: Visual search for human gaze directionby a chimpanzee (Pan troglodytes). PLoS ONE 2010, 5:e9131http://dx.doi.org/10.1371/journal.pone.0009131.

8. Hattori Y, Kano F, Tomonaga M: Differential sensitivity toconspecific and allospecific social cues in chimpanzees (Pantroglodytes) and humans (Homo sapiens): a comparative eye-tracking study. Biol Lett 2010, 6:610-613 http://dx.doi.org/10.1098/rsbl.2010.0120.

9. Hattori Y, Tomonaga M, Fujita K: Chimpanzees (Pan troglodytes)show more understanding of human attentional states whenthey request food in the experimenter’s hand than on the table.Interact Stud 2011, 12:418-429.

10. Okamoto-Barth S, Tomonaga M, Tanaka M, Matsuzawa T:Development of using experimenter-given cues in infantchimpanzees: longitudinal changes in behavior and cognitivedevelopment. Dev Sci 2008, 11:98-108.

11. Anderson J, Myowa-Yamakoshi M, Matsuzawa T: Contagiousyawning in chimpanzees. Biol Sci 2004, 271:S468-S470.

12. Kaneko T, Tomonaga M: The perception of self-agency inchimpanzees. Proc R Soc Ser B 2011, 278:3694-3702.

13. Hayashi M: A new notation system of object manipulation inthe nesting-cup task for chimpanzees and humans. Cortex2007, 43:308-318.

14. Bril B, Smaers J, Steele J, Rein R, Nonaka T, Dietrich G,Biryukova E, Hirata S, Roux V: Functional mastery of percussivetechnology in nut-cracking and stone-flaking actions:experimental comparison and implications for the evolution ofthe human brain. Philos Trans R Soc B: Biol Sci 2012, 367:59-74.

15. Schrauf C, Call J, Fuwa K, Hirata S: Do chimpanzees use weightto select hammer tools? PLoS ONE 2012, 7:e41044 http://dx.doi.org/10.1371/journal.pone.0041044.

16. Hirata S, Fuwa K: Chimpanzees (Pan troglodytes) learn to actwith other individuals in a cooperative task. Primates 2007,48:13-21.

17. Inoue S, Matsuzawa T: Working memory of numerals inchimpanzees. Curr Biol 2007, 17:R1004-R1005.

18. Inoue S, Matsuzawa T: Acquisition and memory of sequenceorder in young and adult chimpanzees (Pan troglodytes). AnimCogn 2009, 12:S59-S69.

19. Matsuzawa T: Symbolic representation of number inchimpanzees. Curr Opin Neurobiol 2009, 19:92-98.

20.�

Martin CF, Biro D, Matsuzawa T: Chimpanzees’ use ofconspecific cues in matching-to-sample tasks: publicinformation use in a fully automated testing environment. AnimCogn 2011, 14:893-902.

This is the first study of ‘collaborative MTS’ in which two chimpanzeeswere required to collaborate on the task. The test booth has two sets ofcomputer-controlled touch panels.

21. Kano F, Call J, Tomonaga M: Face and eye scanning in gorillas(Gorilla gorilla), orangutans (Pongo pygmaeus), and humans(Homo sapiens): unique eye-viewing patterns in humansamong hominids. J Comp Psychol 2012 http://dx.doi.org/10.1037/a0029615. (published online).

22. Kano F, Hirata S, Call J, Tomonaga M: The visual strategyspecific to humans among hominids: a study using the gap-overlap paradigm. Vision Res 2011, 51:2348-2355.

23. Kano F, Tomonaga M: How chimpanzees look at pictures: acomparative eye-tracking study. Proc R Soc Ser B 2009 http://dx.doi.org/10.1098/rspb.2008.1811. (published online).

24.��

Myowa-Yamakoshi M, Scola C, Hirata S: Humans andchimpanzees attend differently to goal-directed actions. NatCommun 2012, 3:693 http://dx.doi.org/10.1038/ncomms1695.

This is a most recent eye-tracking study comparing humans and chim-panzees. The subjects sat in front of the monitor in the presence of theircaretaker or mother. The stimulus presented was a video clip showing ayoung woman holding a bottle of juice and pouring it into a glass.Chimpanzees watched the bottle and the glass and did not attendpreferentially to the woman. In contrast, human infants’ gaze shiftedback and forth between the woman’s face, the bottle and the glass.



25. Carvalho S, Biro D, Cunha E, Hockings K, McGrew WC,Richmond BG, Matsuzawa T: Chimpanzee carrying behaviourand the origins of human bipedality. Curr Biol 2012,22:R180-R181.

26. Biro D, Humle T, Koops K, Sousa C, Hayashi M, Matsuzawa T:Chimpanzee mothers at Bossou, Guinea carry the mummifiedremains of their dead infants. Curr Biol 2010, 20:R351-R352.

27. Hayashi M, Ohashi G, Heung Jin R: Responses toward a trappedanimal by wild bonobos at Wamba. Anim Cogn 2012,15:731-735.

28. Hockings KJ, Anderson JR, Matsuzawa T: Road crossing inchimpanzees: a risky business. Curr Biol 2006,16:R668-R670.

29. Hockings K, Humle T, Anderson J, Biro D, Sousa C, Ohashi G,Matsuzawa T: Chimpanzees share forbidden fruit. PLoS ONE2007, 2:1-4.

30. Yamamoto S, Humle T, Tanaka M: Chimpanzees help each otherupon request. PLoS ONE 2009, 4:e7416 http://dx.doi.org/10.1371/journal.pone.0007416.

31. Tanaka M, Yamamoto S: Token transfer between mother andoffspring chimpanzees (Pan troglodytes): mother–offspringinteraction in a competitive situation. Anim Cogn 2009,12:S19-S26.

32.�

Yamamoto S, Humle T, Tanaka M: Chimpanzees’ flexibletargeted helping based on an understanding ofconspecifics’ goals. Proc Natl Acad Sci U S A 2012,109:3588-3592.

This study revealed an interesting aspect of chimpanzee collaboration:helping behavior on demand. Chimpanzee A had a set of tools such assticks, straw, rope, etc. Chimpanzee B, next-door was presented with aforaging task to solve, for example, a bottle of juice was placed out ofreach so that chimpanzee B needed a stick to retrieve it. The resultsshowed that chimpanzee A did not spontaneously help chimpanzee B.However, when chimpanzee B extended and waved a hand through awindow between the adjacent rooms (in request) chimpanzee A gave thenecessary tool to chimpanzee B.

33. Yamamoto S, Tanaka M: Do chimpanzees (Pan troglodytes)spontaneously take turns in a reciprocal cooperation task? JComp Psychol 2009, 123:242-249.

34. Yamamoto S, Tanaka M: Selfish strategies develop in socialproblem situations in chimpanzee (Pan troglodytes) mother–infant pairs. Anim Cogn 2009, 12:S27-S36.

35. Yamamoto S, Tanaka M: The influence of kin relationship andreciprocal context on chimpanzees’ other-regardingpreferences. Anim Behav 2010, 79:595-602.

36. Brosnan SF, de Waal FBM: A proximate perspective onreciprocal altruism. Human Nat 2002, 13:129-152 http://dx.doi.org/10.1007/s12110-002-1017-2.

37. Ueno A, Hirata S, Fuwa K, Sugama K, Kusunoki K, Matsuda G,Fukushima H, Hiraki K, Tomonaga M, Hasegawa T: AuditoryERPs to stimulus deviance in an awake chimpanzee (Pantroglodytes): towards hominid cognitive neurosciences. PLoSONE 2008, 3:e1442 http://dx.doi.org/10.1371/journal.pone.0001442.

38. Fukushima F, Hirata S, Ueno A, Matsuda G, Fuwa K, Sugama K,Kusunoki K, Hirai M, Hiraki K, Tomonaga M, Hasegawa T: Neuralcorrelates of face and object perception in an awakechimpanzee (Pan troglodytes) examined by scalp-surfaceevent-related potentials. PLoS ONE 2010, 5:e13366 http://dx.doi.org/10.1371/journal.pone.0013366.

39. Ueno A, Hirata S, Fuwa K, Sugama K, Kusunoki K, Matsuda G,Fukushima H, Hiraki H, Tomonaga M, Hasegawa T: Brain activityin an awake chimpanzee in response to the sound of her ownname. Biol Lett 2010 http://dx.doi.org/10.1098/rsbl.2009.0864.(published online).

40. Hirata S, Matsuda G, Ueno A, Fuwa K, Sugama S, Kusunoki K,Fukushima H, Hiraki K, Tomonaga M, Hasegawa T: Event-relatedpotentials in response to subjects’ own names: a comparisonbetween humans and a chimpanzee. Commun Integr Biol 2011,4:1-3.



http://dx.doi.org/10.1371/journal.pone.0009131

http://dx.doi.org/10.1098/rsbl.2010.0120




http://dx.doi.org/10.1037/a0029615

http://dx.doi.org/10.1037/a0029615

http://dx.doi.org/10.1098/rspb.2008.1811

http://dx.doi.org/10.1098/rspb.2008.1811

http://dx.doi.org/10.1038/ncomms1695



http://dx.doi.org/10.1007/s12110-002-1017-2

http://dx.doi.org/10.1007/s12110-002-1017-2









41.�

Ludwig VU, Adachi I, Matsuzawa T: Visuoauditory mappingsbetween high luminance and high pitch are shared bychimpanzees (Pan troglodytes) and humans. Proc Natl Acad SciU S A 2011, 108:20661-20665.

This is the first study demonstrating the visuoauditory mapping of chim-panzees. Both humans and chimpanzees showed a strong bias towardchoosing bright color when the high pitch tone was presented, andchoosing dark color when low pitch tone was presented

42. Martinez L, Matsuzawa T: Auditory–visual intermodal matchingbased on individual recognition in a chimpanzee (Pantroglodytes). Anim Cogn 2009, 12:S71-S85.

43.�

Sakai T, Mikami A, Tomonaga M, Matsui M, Suzuki J, YuzuruHamada Y, Tanaka M, Miyabe-Nishiwaki T, Makishima H,Nakatsukasa M, Matsuzawa T: Differential prefrontal whitematter development in chimpanzees and humans. Curr Biol2011, 21:1397-1402.

This study collected MRI imaging of brain development in three chim-panzees soon after birth. Brain development was recorded for the first 6.5years longitudinally. The focus was a comparison of the developmentalpattern of white matter (WM) within the prefrontal region. The prefrontalWM volume in chimpanzees was immature and had not reached the adultlevel during pre-puberty, similar to what was observed in humans, but notin macaques. However, the rate of prefrontal WM volume increase duringinfancy was slower in chimpanzees than in humans.

44. Kawai N, Morokuma S, Tomomaga M, Horimoto N, Tanaka M:Associative learning and memory in a chimpanzee fetus:



learning and long-lasting memory before birth. Dev Psychobiol2004, 44:116-122.

45. Morokuma S, Fukushima K, Kawai N, Tomonaga M, Satoh S,Nakano H: Fetal habituation correlates with functional braindevelopment. Behav Brain Res 2004, 153:459-463.

46.�

Sakai T, Hirata S, Fuwa K, Sugama K, Kusunoki K, Makishima H,Eguchi T, Yamada S, Ogihara N, Takeshita H: Fetal braindevelopment in chimpanzees versus humans. Curr Biol 2012,22:R791-R792.

This paper revealed fetal brain development in chimpanzees using anoninvasive ultrasound technique. The growth rate of brain volumeaccelerated throughout gestation in human fetuses, but not in chimpan-zee fetuses through the later stages of pregnancy. This indicates thathumans and chimpanzees differ with respect to the development of brainvolume during the fetal period.

47. Takeshita H, Myowa-Yamakoshi M, Hirata S: A new comparativeperspective on prenatal motor behaviors: preliminaryresearch with four-dimensional (4D) ultrasonography. InCognitive Development in Chimpanzees. Edited by Matsuzawa T,Toimonaga M, Tanaka M. Tokyo: Springer-Verlag; 2006:37-47.

48. Thompson ME, Jones JH, Pusey AE, Brewer-Marsden S,Goodall J, Marsden D, Matsuzawa T, Nishida T, Reynolds V,Sugiyama Y, Wrangham RW: Aging and fertility patterns in wildchimpanzees provide insights into the evolution ofmenopause. Curr Biol 2007, 17:2150-2156.




evolution of the brain and social behavior in chimpanzees · evolution of the brain and social...

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