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Jacques Paillard

The neurobiological roots of rational thinking

1. INTRODUCTION

Computational theories of mind that approach the performance of high levelcognitive operations through the manipulation of symbolic representation, as promotedby Artificial intelligence, has long dominated the study of higher cognitive functions. Newapproaches of contemporary robotics tend to look at lower level of intelligent behavior.Their explicit ambition is to explain how rational thinking might progressively emergefrom a coordinated combination of basic sensori-motor devices that allows autonomous

systems to survive in a given ecological niche.

This could, in a sense, be considered by psychologists as a pragmatic resurgenceof the developmental approaches in the constructivist framework of Piagetianepistemology. The study of the transitions in children between what Piaget termed"practical" intelligence of the early sensori-motor stages and the later emergence of"operative" intelligence based on constraining logical rules is at the heart of ourunderstanding of how rational behavior could progressively emerge from more primitive"prerational" mechanisms.

In the mature organism there is obviously a coexistence and co-operation of acognitive apparatus with a basic sensori-motor machinery. Higher cognitive levelsmay adaptively control or supersede this basic machinery in various ways taking into

account intrinsic constraints that set definite bounds to their operating range.Considering the impressive development of contemporary biology, the challengeof exploring how behavioural and mental activities are tied, phylogenetically andontogenetically to their biological roots is seriously worth considering.

Biologists believe that evolutionary pressures generally preserve basic neuralmechanisms that have served to solve adaptation or survival problems in antecedentforms, but these mechanisms have to be restructured, often in baffling ways, in newneural assemblages for coping with new problems of adaptation. The warning ofFrancois Jacob (1981) is here apposite: "evolutionary mechanisms are obviously notthe product of the logical brain of an engineer but are more likely to be the result of a bricolage gnialthe work of a tinkering genius.

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H.Cruse et al. (eds.), Prerational Intelligence: Adaptative Behavior and Intelligent Systems Without Symbols

and Logic, Volume 1, 343-355

2000 Kluwer Academic Publishers. Printed in the Netherlands


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344 JACQUES PAILLARD

This feature explains the various and often perplexing solutions that biological systemsreveal to the analytical sagacity of experimentalists and theoreticians.

With this context in mind, this paper aims at illustrating how neurobehavioral studiesmay contribute to our understanding of the way in which prerational intelligence may

progressively emerge in the animal kingdom from a continuous process of evolution.Three points will be considered:

- The first concerns the nature and the extent of the remodeling of cerebralarchitectures which coincides with the development of manual skill in primates andthe emergence of a prerational sensori-motor intelligence. Precentral cortical areas,parietal associative cortex and neocerebellar structures will be here especiallyconsidered.

- The second point addresses the functional significance, in anthropoids, of thecharacteristic enlargement of the prefrontal cortex together with the development ofthe neostriatum in relation to the emergence of new ways in which basic sensori-motor instruments become controllable by the cognitive brain.

- A third point considers the consequences of the development of language skills inman, especially in relation to hemispheric specialization and to lateralization ofmanual "dexterity" on the one side; to enrichment of the individual's cognitiveapparatus and to the availability of cultural sources of "knowledge", on the otherside. We will try to show how both aspects condition the emergence of what couldbe considered as "rational" thinking.

2. PROMOTING THE HAND BY REMODELING THE BRAIN

The evolution of manual skills is a major zoological trend. Reaching with aprehensile hand belongs to the most basic components of the natural behavioralrepertoire of primates. Reaching and grasping developed primarily in accord with thespecific requirements of the arboreal mode of locomotion used by primates. Jumpingfrom one tree branch to another requires a secure grasp of the support by the limbsand, in the new world monkeys, by the tail. For a baby monkey holding on to its mothersfur, grasping is a vital reflex. In bipedal anthropoids, the liberation of the prehensilehand from the requirements of locomotion allowed it to become a privileged interfacebetween the organism and its physical environment. This development reduced thepreeminent role of the mouth. It is associated with a major transformation of cerebralarchitectures. The motor cortex, the parietal associative areas and the neocerebellarloopsare chiefly concerned.


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THE NEUROBIOLOGICAL ROOTS OF RATIONAL THINKING 345

2.1The Primary Motor CortexThe evolutionary corticalization of motor areas in vertebrates is characterized by the

development of control systems able to bypass or disrupt the built-in neural circuitry of

the repertoire of "fixed action patterns" thatcompose basic behavioral responses. Directcortico-spinal connections develop, allowing the independent command of muscles ormuscle groups normally embedded within prewired synergies of locomotion, posture orprimitive grasp reflexes, which are mediated by brain stem networks and the spinalmotor machinery. The topography of cortical motor areas reflects the fine-grainextension of the cortical keyboard on which new kinetic melodies can be played. Thus,in the case of arboreal primates, the cortical representation of the segments of theprehensile limbs takes a major place. Likewise, the mapping of the hand occupiesalmost a third of the total surface of the motor cortex in man, reflecting its prominentrole in the control of manipulative activities.

A similar expansion occurred in somatosensory areas devoted to the processing of

cutaneous and proprioceptive information originating from hand and fingers, providingthe refinement of control required for manual dexterity and exploratory palpation. Wemay mention here the recent identification of two separate representations of the handin the primary motor cortex of the monkey. One is mainly dependent on tactileinformation whereas the second, more rostrally located area receives proprioceptiveinformation (Strick & Preston 1982). Similarly, a functional contrast between neuronsinvolved in precision and power grips has been established (Lemon 1981).

Accordingly, the growing importance of the pyramidal tract in anthropoids (itcontains more than 2 million fibers in man) attests to the increasing ascendancy of themotor cortex over the motor machinery. This cortico-motoneuronal pathway, which

directly links the large pyramidal cells of the cortical motor area with the motoneurons atthe spinal level (a system which is notably developed in man), supplies the cortex withits increasing capacities for direct control over the spinal keyboard. This development isclosely associated with the improvement of manual skills. The pyramidal tract, whichallows the control of independent finger movements, is, thereby, the chief mediator ofthe acquisition of new motor skills.

2.2 The Parietal Association Areas

Reaching and grasping with the hand are predominantly triggered and guided byvision. Prehension space is essentially a visual space. Vision intervenes in various

ways in the programming and adjustment of arm movements in reaching and inpresetting the hand configuration for gripping. (Paillard & Beaubaton 1978, Jeannerod


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Figure 2: Comparative lateral views of monkey and human cerebral hemispheres, showing the topographyof corresponding cyto-architectural zones of the frontal, central, and parietal cortex (modified fromAndersen 1987). The premotor area (PM) is divided into a superior and an inferior sector in the monkey.Together with the supplementary motor area (SMA) the superior sector is involved in the intentionalplanning of action (memory-driven) whereas the inferior sector trigger action reactively (stimulus-driven).Notice the expansion in man of the prefrontal areas with the frontal eye field (F E F ) and the area 46. The

Broca area which is mainly devoted to speech function in man has an equivalent in Monkey devoted to thesequencing of manual skills. The areas numbered 5, 7a and 7b correspond to areas located in the caudalpart of the superior parietal cortex. They are associated to the coordination of the body space with thevisual space. The whole region of the angular gyrus (G A) is considered as newly developed in man inassociation with speech function (from Paillard 1990)

More interesting is also the discovery in primates in the inferior parietal cortex (whereinformation from area 5 and 7a converge) of "projection neurons" whose activity isspecifically associated with the projection of the hand to a definite position in theprehension space (Mountcastle et al. 1975). A visual target presented outside theboundaries of this space does not trigger the activity of these neurons. Additionally,

"manipulation neurons"have been identified in the same inferior parietal cortical field(area 7b) that is associated with manipulation of an object. These data attest to theincreasing role of these associative parietal areas in the control of hand activities. Theyalso show an interesting topographical segregation of neuronal networks controlling thevisually guided positioning of the hand in prehension space from those for the tactually-driven manipulative activity of the hand (figure 2).


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2.3 The Neo-Cerebellar Loops

The efficacy of the manual grip requires accurate positioning in action space.

Transport of the arm requires fine coordinated control of the shoulder articulation. Thelarge extension of the lateral cerebellar zones characteristic of primates is accompaniedby expanded independent control of the forelimb and the shoulder articulation inparticular. The lateral mobility of the shoulder, of course, is derived from the arboreallocomotion of monkeys. The neocerebellum thus becomes the chief tuner of the corticalkeyboard in the programming and execution of the transport of arm movements inprehension space (reviewed in Paillard 1982b). The 20 million fibers composing thecortico-ponto-cerebello-cortical loop in man (compared with the 2 million fibers of man'spyramidal tract) reflect the functional importance of this control system which interveneas a shunting loop over the main cortico-spinal routes for movement control. Thefunctional segregation of two separate cerebellar output nuclei can be described as aproactive function of the dendate nuclei for initiation and feedforward tuning ofpreprogrammed reaching movement and, through the interpositus, a retroactiveguidance (notably visual) of ongoing movement toward the target (Evarts & Thach1969). Moreover, an important contingent of descending fibers from the parietal regionto the ponto-cerebellar input system contributes to feeding the cerebellum with the visualinformation necessary for the preprogramming and ongoing-control of reachingmovement. (Reviewed in Paillard 1990).

3. FROM PREHENSION TO MANUFACTURE

The neocortical region that has undergone the largest phylogenetic expansion isdefinitely the frontal cortex (Fuster, 1985). Although numerous architectonicsubdivisions have been described, we shall consider here two main cortical territories,which are well identified on a histological level, namely the agranular premotor area infront of the primary motor cortex and still more rostrally, the granular prefrontalassociative cortex. The first, which in monkey is about the same size as the primarymotor cortex, has become six times larger in man. The second, which increasesregularly from the lemurian (10%) to the chimpanzee (25%), occupies in man about35% of the total neocortical areas (reviewed in Damasio, 1994).

3.1 The Premotor Areas

The premotor function of the agranular area 6 of the frontal cortex is now well-documented (Humphrey & Freund, 1991). Schematically, the neuronal activities ofthese regions reflect merely the quality of the action that they are going to initiate


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(set-neurons considered as task-related) but not the parametric prescriptions of itsexecution (speed, direction, amplitude and force). Moreover, neurons involved in aspecific act (power or precision grip, pushing, throwing, mouth-oriented handmovement, etc.) seem to be grouped in functional modules located in topographicaldistinct regions. The recent identification in the premotor cortex of the monkey of four

topographically distinct representation of the hand is reminiscent of the old neurologicalconcept of "kinetic formulae" introduced by Liepmann (1900). Impairment by lesionslocalized in these regions in man produces selective "motor apraxia" affecting oneparticular skill without compromising the expression of others (reviewed in Paillard1982b).

An important functional distinction has recently been introduced between superiorand inferior premotor and prefrontal areas on the basis of converging embryological,anatomical and neurobiological evidence (Goldberg 1985a). The inferior ventro-lateralregion is directly linked with the inferior parietal association areas (7a and b) and thetemporal regions and mainly receives information on exteroceptive cues (visual space).In contrast, the superior dorso-medial region including the supplementary motor areas

receives most of its information from area 5 (somatosensory representation of thebody space) and from the limbic structures involved in internal drive and motivation.Moreover, the first is mainly modulated by the neocerebellar loops whereas the secondis the principal return pathway of the striatal loops (basal ganglia).

Therefore two modes of steering motor activities are postulated: a reactive modein which activity is directly triggered by environmental stimulation (stimulus-driven) anda projective modein which activity is driven by internal cues, imagery or representationof desired goals (memory-driven). (Goldberg 1985b). The prefrontal region itself,whose impressive development in man has already been emphasized above, will addits specific and essential contribution to the emergence of these new potentialities,

which will endow the prehensile hand with the skill of a tool-maker.

3.2 The Prefrontal Cortex

The neurological semiology of pathological or traumatic disorders of these areashas long been unclear. Converging evidence from the renewed investigation of thesesstructures in monkey and man using new neuroanatomic, neurophysiologic andneuropsychological techniques indicates that the expansion of this sector is mainlyassociated with the acquisition of greater autonomy of control over the sensori-motormachinery that react to the immediate stimuli presented by the environment (Goldman-Rakic, 1987). In addition, the growth of the prefrontal region is associated with the

development of the neostriatum (caudate nucleus of the basal ganglia) and of theventro-medial nuclei of the thalamus. Together, these components constitute severalprefronto-caudo-thalamo-prefrontal loops now implicated in the so-called "cognitive"control of action.


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Figure 3: The driving of action. Segregation between a cognitive driving, based on semantic

knowledge (savoir) and rational thinking and a sensori-motor prerational driving of know-how (savoir

faire) based on pragmatic knowledge. Main cortical areas involved in man in the cognitive processingof information related to the various functional fields. The know-how competence relies on a more

primitive inbuilt neural circuitry (from Paillard 1994).

Many examples can be given which illustrate the fundamental role that frontalassociation cortex plays in the acquisition of a predictive mode of control of actions onthe basis of action plans, objectives to achieve, and problems to solve. Schematically,we can summarize the role of the prefrontal cortex and its multiple regulatory loop asfollows: it inhibits immediate reactivity and diminishes interference, it facilitatessustained concentration and focus on objectives, and it organizes temporal planning

and sequencing of action.

But we are now facing the intriguing problem of understanding in term of theorganization of nervous structures the decisive step that, in the process of"humanization", crossed the "cerebral Rubicon" (Leroy-Gourhan, 1964) whichseparates man from other primates and which paleontologists associate with the


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appearance of hand-made tools and manufacture. But, at this stage, it was no longerthe limitations of the mechanical performance of the hand that constrained theevolution of brain architectures that control it. It was the skillful hand, which thenbecame the obedient servant of a planning and creative brain whose capacity forsymbolic thinking then was considerably enlarged by the development of spoken

language.

4. FROM MANUFACTURE TO RATIONAL THINKING

Paleontological evidence demonstrates that the evolutionary links which lead theanthropoids from Australopithecus to Homo Sapiens seem to establish a closeassociation between the emergence of language and of manual technology, asmarked by the first manufactured tools (Leroy-Gourhan 1964). The hand is no longer just the organ for grasping food, displacing, grooming, attacking or defending andeventually using an external object as an extension of the body. It now becomes a toolfor making tools and an instrument for symbolic communication. The questiontherefore arises: Why does the frontal cortex, which exercises most of the abovefunctions in higher primates, not allow these species to manufacture tools even in theabsence of language?

The evolution of cerebral structures embodies the tight interaction of manualactivity and the symbolic activity of language. The neuro-anatomical and functionalasymmetry of the cerebral hemispheres, which is particularly marked in the humanspecies and which is closely bound up with language functions, is also displayed in theasymmetry of manual functions. It is the left hemisphere (in right-handed subjects)which speaks and which controls the dominant right hand. It is also the left

hemisphere, which generates the operative sequences of spoken, written and gesturallanguage. In the same way, sequential programs which are the basis of manualdexterity, and of motor skills in general, are developed in the left hemisphere (Kimura1977), whereas the right hemisphere becomes the organizer of spatial referents whichprovide coherence and efficacy to spatially oriented behavior (de Renzi 1982);

The monkey apparently does not display functional specialization of the twohemispheres comparable to that of man, although functional asymmetries have beenshown to be more widely displayed in vertebrates than previously thought (Denenberg,1984; McNeilage et al. 1987). Therefore, it would seem that when these new cerebralpotentialities emerge, technical skills develop at an impressive rate. A technique isthe product of gesture and of the tool, organized in an operative chainby a veritable

syntax which gives its coherence and its inventive adaptivity to the motor programs.Operative syntax is generated by memory and arises in the dialogue between thebrain and the material environment mediated by manual activity.


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as in spoken language. Kimura (1988), looking at the relationship between aphasiaand manual skills, found difficulties in complex hand movements that paralleled thesyntactical difficulties of aphasic subjects.

We are then led to consider that the development of manual skills would haveguided the development of some areas alive with respect to object manipulation but

initially dormant with respect to vocal production. Indeed, Mauser et al. (1991)suggested that the homologue of Broca's area in non-human primates is specificallyused for object manipulation but not for vocal production.

When attempting, however, to establish empirical links between behavioral andneural development of language and tools, we have to take in consideration the factthat language and tools are not merely biological phenomena. Both humanenvironments and human biological endowments contribute to the very foundations ofhuman culture and, thus, to the appearance of language and tools. Each stage ofneural development opens new ways for certain interactions with the socioculturaland physical environment, thus influencing both brain and behavior in epigeneticprocesses. This must be as true for phylogeny as it is for ontogeny where historical,

cultural and functional constraints intertwined each contributing on presentmodularization of human brain functions. Understanding the way in whichenvironmental constraints may adaptively shape neural structures during the earlydevelopment of a living brain remains a challenge, which, so far, seems rather far-reaching for present engineering approaches.

Finally, however, we may consider that the ability to maintain the activation of agoal representation in relation to the increasing versatility of manual skills hascontributed to promote the ability to reason casually about future events and, thus,created brain functions which together with the symbolism of language could supportrational thinking.

Centre national de la Recherche Scientifique

UPR Neurobiologie et Mouvements, Marseille, France.

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