Jacques Paillard

The neurobiological roots of rational thinking

1. INTRODUCTION

Computational theories of mind that approach the performance of high level

cognitive operations through the manipulation of symbolic representation, as promoted
by Artificial intelligence, has long dominated the study of higher cognitive functions. New
approaches of contemporary robotics tend to look at lower level of intelligent behavior.
Their explicit ambition is to explain how rational thinking might progressively emerge
from 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 resurgence
of the developmental approaches in the constructivist framework of Piagetian
epistemology. 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 our
understanding 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 a
cognitive apparatus with a basic sensori-motor machinery. Higher cognitive levels
may 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 challenge
of exploring how behavioural and mental activities are tied, phylogenetically and
ontogenetically to their biological roots is seriously worth considering.
Biologists believe that evolutionary pressures generally preserve basic neural
mechanisms that have served to solve adaptation or survival problems in antecedent
forms, but these mechanisms have to be restructured, often in baffling ways, in new
neural assemblages for coping with new problems of adaptation. The warning of
Francois Jacob (1981) is here apposite: "evolutionary mechanisms are obviously not
the product of the logical brain of an engineer but are more likely to be the result of a
bricolage génial ― the work of a tinkering genius.”

343

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
344 JACQUES PAILLARD

This feature explains the various and often perplexing solutions that biological systems
reveal to the analytical sagacity of experimentalists and theoreticians.
With this context in mind, this paper aims at illustrating how neurobehavioral studies
may 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 cerebral
architectures which coincides with the development of manual skill in primates and
the emergence of a prerational sensori-motor intelligence. Precentral cortical areas,
parietal associative cortex and neocerebellar structures will be here especially
considered.
- The second point addresses the functional significance, in anthropoids, of the
characteristic enlargement of the prefrontal cortex together with the development of
the 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 in
man, especially in relation to hemispheric specialization and to lateralization of
manual "dexterity" on the one side; to enrichment of the individual's cognitive
apparatus and to the availability of cultural sources of "knowledge", on the other
side. We will try to show how both aspects condition the emergence of what could
be considered as "rational" thinking.

2. PROMOTING THE HAND BY REMODELING THE BRAIN

The evolution of manual skills is a major zoological trend. Reaching with a

prehensile hand belongs to the most basic components of the natural behavioral
repertoire of primates. Reaching and grasping developed primarily in accord with the
specific requirements of the arboreal mode of locomotion used by primates. Jumping
from one tree branch to another requires a secure grasp of the support by the limbs
and, in the new world monkeys, by the tail. For a baby monkey holding on to its mothers
fur, grasping is a vital reflex. In bipedal anthropoids, the liberation of the prehensile
hand from the requirements of locomotion allowed it to become a privileged interface
between the organism and its physical environment. This development reduced the
preeminent role of the mouth. It is associated with a major transformation of cerebral
architectures. The motor cortex, the parietal associative areas and the neocerebellar
loops are chiefly concerned.
 THE NEUROBIOLOGICAL ROOTS OF RATIONAL THINKING 345

2.1 The Primary Motor Cortex

The 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" that compose basic behavioral responses. Direct
cortico-spinal connections develop, allowing the independent command of muscles or
muscle groups normally embedded within prewired synergies of locomotion, posture or
primitive grasp reflexes, which are mediated by brain stem networks and the spinal
motor machinery. The topography of cortical motor areas reflects the fine-grain
extension 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 the
prehensile limbs takes a major place. Likewise, the mapping of the hand occupies
almost a third of the total surface of the motor cortex in man, reflecting its prominent
role 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, providing
the refinement of control required for manual dexterity and exploratory palpation. We
may mention here the recent identification of two separate representations of the hand
in the primary motor cortex of the monkey. One is mainly dependent on tactile
information whereas the second, more rostrally located area receives proprioceptive
information (Strick & Preston 1982). Similarly, a functional contrast between neurons
involved in precision and power grips has been established (Lemon 1981).
Accordingly, the growing importance of the pyramidal tract in anthropoids (it
contains more than 2 million fibers in man) attests to the increasing ascendancy of the
motor cortex over the motor machinery. This cortico-motoneuronal pathway, which
directly links the large pyramidal cells of the cortical motor area with the motoneurons at
the spinal level (a system which is notably developed in man), supplies the cortex with
its increasing capacities for direct control over the spinal keyboard. This development is
closely associated with the improvement of manual skills. The pyramidal tract, which
allows the control of independent finger movements, is, thereby, the chief mediator of
the acquisition of new motor skills.

2.2 The Parietal Association Areas

Reaching and grasping with the hand are predominantly triggered and guided by
vision. Prehension space is essentially a visual space. Vision intervenes in various
ways in the programming and adjustment of arm movements in reaching and in
presetting the hand configuration for gripping. (Paillard & Beaubaton 1978, Jeannerod
346 JACQUES PAILLARD

Figure 1: Basic visuo-motor operations involved in reaching and grasping (from Paillard & Beaubaton 1976).

1986). The fine tuning of binocular vision together with the progressive autonomy of
conjugate eye movement in relation to the head, is a major phylogenetic achievement
that is assumed to develop in primates in close conjunction with the perfection of
manual skills. Trevarthen (1970) suggested that the functional segregation between a
focal and an ambient vision involving the foveal-parafoveal and the peripheral part of
the retina resulted respectively from the need for selective guidance of individual finger
movement directed to the object and the need for steering arm movement in visual
space.
The characteristic evolution of the parietal association cortex in primates (Andersen
1987) is closely linked with the promotion of the hand to a major interface between the
organism and its environment. Its more posterior region (area 7a) is concerned with the
attentional anchoring of gaze by coding the direction of the optic axis relative to the
head. In contrast, its superior region (area 5) instantiates a representation of the body
encoding the relative positions of its mobile segments. Lesions involving these regions
produce respectively the classical attentional neglect for the contralateral hemispace
when area 7a is concerned and trouble in awareness of the body image when localized
in area 5. aaaaaaaaaaaaaaaaaaaaaaaaaaaaaaaaaaaaaa
 THE NEUROBIOLOGICAL ROOTS OF RATIONAL THINKING 347

Figure 2: Comparative lateral views of monkey and human cerebral hemispheres, showing the topography
of corresponding cyto-architectural zones of the frontal, central, and parietal cortex (modified from
Andersen 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 intentional
planning 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 the
sequencing of manual skills. The areas numbered 5, 7a and 7b correspond to areas located in the caudal
part of the superior parietal cortex. They are associated to the coordination of the body space with the
visual space. The whole region of the angular gyrus (G A) is considered as newly developed in man in
association with speech function (from Paillard 1990)

More interesting is also the discovery in primates in the inferior parietal cortex (where
information from area 5 and 7a converge) of "projection neurons" whose activity is
specifically associated with the projection of the hand to a definite position in the
prehension space (Mountcastle et al. 1975). A visual target presented outside the
boundaries 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 the
increasing role of these associative parietal areas in the control of hand activities. They
also show an interesting topographical segregation of neuronal networks controlling the
visually guided positioning of the hand in prehension space from those for the tactually-
driven manipulative activity of the hand (figure 2).
348 JACQUES PAILLARD

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. The
large extension of the lateral cerebellar zones characteristic of primates is accompanied
by expanded independent control of the forelimb and the shoulder articulation in
particular. The lateral mobility of the shoulder, of course, is derived from the arboreal
locomotion of monkeys. The neocerebellum thus becomes the chief tuner of the cortical
keyboard in the programming and execution of the transport of arm movements in
prehension space (reviewed in Paillard 1982b). The 20 million fibers composing the
cortico-ponto-cerebello-cortical loop in man (compared with the 2 million fibers of man's
pyramidal tract) reflect the functional importance of this control system which intervene
as a shunting loop over the main cortico-spinal routes for movement control. The
functional segregation of two separate cerebellar output nuclei can be described as a
proactive function of the dendate nuclei for initiation and feedforward tuning of
preprogrammed reaching movement and, through the interpositus, a retroactive
guidance (notably visual) of ongoing movement toward the target (Evarts & Thach
1969). Moreover, an important contingent of descending fibers from the parietal region
to the ponto-cerebellar input system contributes to feeding the cerebellum with the visual
information necessary for the preprogramming and ongoing-control of reaching
movement. (Reviewed in Paillard 1990).

3. FROM PREHENSION TO MANUFACTURE

The neocortical region that has undergone the largest phylogenetic expansion is
definitely the frontal cortex (Fuster, 1985). Although numerous architectonic
subdivisions have been described, we shall consider here two main cortical territories,
which are well identified on a histological level, namely the agranular premotor area in
front of the primary motor cortex and still more rostrally, the granular prefrontal
associative cortex. The first, which in monkey is about the same size as the primary
motor cortex, has become six times larger in man. The second, which increases
regularly from the lemurian (10%) to the chimpanzee (25%), occupies in man about
35% 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 of
these regions reflect merely the quality of the action that they are going to initiate
 THE NEUROBIOLOGICAL ROOTS OF RATIONAL THINKING 349

(set-neurons considered as task-related) but not the parametric prescriptions of its

execution (speed, direction, amplitude and force). Moreover, neurons involved in a
specific act (power or precision grip, pushing, throwing, mouth-oriented hand
movement, etc.) seem to be grouped in functional modules located in topographical
distinct regions. The recent identification in the premotor cortex of the monkey of four
topographically distinct representation of the hand is reminiscent of the old neurological
concept of "kinetic formulae" introduced by Liepmann (1900). Impairment by lesions
localized in these regions in man produces selective "motor apraxia" affecting one
particular skill without compromising the expression of others (reviewed in Paillard
1982b).
An important functional distinction has recently been introduced between superior
and inferior premotor and prefrontal areas on the basis of converging embryological,
anatomical and neurobiological evidence (Goldberg 1985a). The inferior ventro-lateral
region is directly linked with the inferior parietal association areas (7a and b) and the
temporal 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 the
body space) and from the limbic structures involved in internal drive and motivation.
Moreover, the first is mainly modulated by the neocerebellar loops whereas the second
is the principal return pathway of the striatal loops (basal ganglia).
Therefore two modes of steering motor activities are postulated: a reactive mode
in which activity is directly triggered by environmental stimulation (stimulus-driven) and
a projective mode in which activity is driven by internal cues, imagery or representation
of desired goals (memory-driven). (Goldberg 1985b). The prefrontal region itself,
whose impressive development in man has already been emphasized above, will add
its 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 areas

has long been unclear. Converging evidence from the renewed investigation of theses
structures in monkey and man using new neuroanatomic, neurophysiologic and
neuropsychological techniques indicates that the expansion of this sector is mainly
associated with the acquisition of greater autonomy of control over the sensori-motor
machinery 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 the
ventro-medial nuclei of the thalamus. Together, these components constitute several
prefronto-caudo-thalamo-prefrontal loops now implicated in the so-called "cognitive"
control of action.
350 JACQUES PAILLARD

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 processing
of 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 frontal
association cortex plays in the acquisition of a predictive mode of control of actions on
the 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 as
follows: it inhibits immediate reactivity and diminishes interference, it facilitates
sustained 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 the
organization of nervous structures the decisive step that, in the process of
"humanization", crossed the "cerebral Rubicon" (Leroy-Gourhan, 1964) which
separates man from other primates and which paleontologists associate with the
 THE NEUROBIOLOGICAL ROOTS OF RATIONAL THINKING 351

appearance of hand-made tools and manufacture. But, at this stage, it was no longer
the limitations of the mechanical performance of the hand that constrained the
evolution of brain architectures that control it. It was the skillful hand, which then
became the obedient servant of a planning and creative brain whose capacity for
symbolic 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 the
anthropoids from Australopithecus to Homo Sapiens seem to establish a close
association between the emergence of language and of manual technology, as
marked by the first manufactured tools (Leroy-Gourhan 1964). The hand is no longer
just the organ for grasping food, displacing, grooming, attacking or defending and
eventually using an external object as an extension of the body. It now becomes a tool
for making tools and an instrument for symbolic communication. The question
therefore arises: Why does the frontal cortex, which exercises most of the above
functions in higher primates, not allow these species to manufacture tools even in the
absence of language?
The evolution of cerebral structures embodies the tight interaction of manual
activity and the symbolic activity of language. The neuro-anatomical and functional
asymmetry of the cerebral hemispheres, which is particularly marked in the human
species and which is closely bound up with language functions, is also displayed in the
asymmetry 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 gestural
language. In the same way, sequential programs which are the basis of manual
dexterity, and of motor skills in general, are developed in the left hemisphere (Kimura
1977), whereas the right hemisphere becomes the organizer of spatial referents which
provide coherence and efficacy to spatially oriented behavior (de Renzi 1982);
The monkey apparently does not display functional specialization of the two
hemispheres comparable to that of man, although functional asymmetries have been
shown to be more widely displayed in vertebrates than previously thought (Denenberg,
1984; McNeilage et al. 1987). Therefore, it would seem that when these new cerebral
potentialities emerge, technical skills develop at an impressive rate. A technique is
the product of gesture and of the tool, organized in an operative chain by 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 the
brain and the material environment mediated by manual activity.
352 JACQUES PAILLARD

Accordingly, the activities of the hand (like those of language) owe the extension
of their means of action to both the enlargement of their vocabulary (the number of
discrete elements supplied by the related structures of the motor keyboard) and the
development of a syntax (the logic of the sequencing of acts analogous to a phoneme
sequence). Together, they enable the organization of motor phrases or sequences of
activity which have a definite functional utility, i.e., a biological meaning in a given
postural and environmental context. From this point of view, manual and vocal skills
are closely dependent on the generation of programmed sequences, resulting from
temporally ordered brain activity. We may recall, however, that the musculoskeletal
properties of the human hand are not far removed from those of the primate, but this
is not true with regard to oropharyngeal properties. Apes lack the specialized
supralaryngeal vocal tract that is necessary to produce the full range of human
speech sound (Lieberman, 1984). Moreover, it is also impossible to train them to
produce the many sounds that their anatomy could theoretically produce. They seem
unable to produce voluntary vocalization in the absence of affect.
Thus, the idea is that neural mechanisms regulating "voluntary" speech are a
necessary step in the evolutionary process that resulted in human speech. On the
other hand, considering the conservative nature of evolution that must build on what
was already present, consistent evidence is presented suggesting that homologous
neural substrates might exist for the early ontogeny of the hierarchical organization
shared both by manual skills and speech production (Greenfield 1991). Tool-use and
manual proto-language evolved together, both supported by the programming function
of the left frontal region associated with Broca's area.
As paleontologists have suggested (Leroy-Gourhan 1954) hand could have
liberated those cortical areas previously assigned to the control of oral reaching and
grasping skills, and thus made them available for the emission of articulated sound
and the emergence of language? Thus, language would have become the beneficiary
of the operational capacities formerly used for gestural communication (Kimura 1977).
Orolaryngeal motor capabilities, liberated from postural constraints and from the
spatial restrictions which impede skeleto-motor production, thus become a flexible
instrument for the production of kinetic melodies where temporal configurations are
organized and deployed within the impressive framework of generative grammar
(Paillard 1993). In this context, the study of the gestural sign languages used by the
deaf offers interesting prospects. Poizner et al. (1987) indicate that massive damage
to Broca's area and the left prefrontal lobe leads to agrammatisms in sign language
 THE NEUROBIOLOGICAL ROOTS OF RATIONAL THINKING 353

as in spoken language. Kimura (1988), looking at the relationship between aphasia

and manual skills, found difficulties in complex hand movements that paralleled the
syntactical difficulties of aphasic subjects.
We are then led to consider that the development of manual skills would have
guided 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 specifically
used for object manipulation but not for vocal production.
When attempting, however, to establish empirical links between behavioral and
neural development of language and tools, we have to take in consideration the fact
that language and tools are not merely biological phenomena. Both human
environments and human biological endowments contribute to the very foundations of
human culture and, thus, to the appearance of language and tools. Each stage of
neural development opens new ways for certain interactions with the sociocultural
and physical environment, thus influencing both brain and behavior in epigenetic
processes. This must be as true for phylogeny as it is for ontogeny where historical,
cultural and functional constraints intertwined each contributing on present
modularization of human brain functions. Understanding the way in which
environmental constraints may adaptively shape neural structures during the early
development 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 a
goal representation in relation to the increasing versatility of manual skills has
contributed to promote the ability to reason casually about future events and, thus,
created brain functions which together with the symbolism of language could support
rational thinking.

Centre national de la Recherche Scientifique

UPR Neurobiologie et Mouvements, Marseille, France.

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