**Cognitive Integration in the Human Primary Sensory and Motor Areas: An Overview**

Jozina B. De Graaf1 and Mireille Bonnard2

*1Institute of Movement Sciences 2Mediterranean Institute for Cognitive Neuroscience CNRS – Aix-Marseille University, Marseille, France* 

#### **1. Introduction**

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Although many different definitions of cognition exist, there is a general acceptance that cognition can be defined as a higher function with respect to both the primary stages of sensory information processing and the final stage of motor output. This idea has been the basis of many well known psychological models where one can identify "input boxes" (i.e., visual, auditory, somatosensory information), and "output boxes" (i.e., motor commands), with, intermediate, high level (attention, language, memory, …) and low-level (motor intention, preparation) cognitive functions (see, for instance, the information processing model of Smidt and Lee (2005), or the model for central representation of goal-directed movements of Jeannerod (1990)).

Although these models are, without doubt, well suited to the study of cognitive processes from a psychological standpoint, they are not very helpful from a neuroscientific point of view. Indeed, ever since the very first investigations into the functioning of the living brain, the main aim has been to localize cognitive functions into the cortical structures of the brain. There exist at least **two** problems related to this approach. Firstly, and this is not a recent objection (e.g., Posner and Raichle (1998) page 16), it is doubtful whether the cognitive functions as presently conceived have a meaning for the brain. Let us take for example the so-called "eye-hand coordination". This "function" is much studied today and many publications report attempts to localize it in the brain. But, for a normally developed brain, this is not a specific function which is needed at specific moments and which is necessarily implemented in a specific brain structure. All input is continuously put in relation with each other as a function of the particular output. It seems more likely that eye-hand coordination is controlled in a continuous, implicit and distributed way. It is pertinent here to mention the ecological approach of perception (Gibson, 1986). This approach is based on the concept of "affordance" that characterizes the object of perception as a whole of many possible actions and interactions, and is in rupture with the cognitive approach. Indeed, according to the latter approach, the brain organizes the perception of the world, whereas in the ecological approach, the world organizes the perception: The role of the brain is to extract the information presented by the world. This theory suggests that the traditional approach of studying cerebral functioning is not very appropriate: the cognitive functions that we define do not have much sense for the brain and, what's more, we generally put subjects in

Cognitive Integration in the Human Primary Sensory and Motor Areas: An Overview 109

who established the well-known cerebral map based on the cytoarchitecture of the different regions of the cortex. Each region of the cortex containing the same cellular organization was attributed the same number, ranging from 1 to 52. Brodmann's assumption was that a given anatomical organization must correspond to a particular function. For instance, Brodmann's area 17, which receives information from a thalamic nucleus which in turn receives projections from the retina, is called the primary visual cortex; Brodmann's areas 41 and 42 form the primary auditory cortex; Brodmann's areas 1 to 3 form the primary somatosensory cortex; Brodmann's area 4 globally corresponds to the primary motor cortex. It is important to note that the Brodmann classification is based on adult brains and so were anatomically and neurophysiologically fully developed. It has been shown that the cytoarchitecture of the sensorimotor cortex is subject to considerable modifications from birth (or even before) until the age of 20 (Shumeiko, 1998). Today, it is not clear how the

The primary sensory areas differ from other cortical areas mainly by the thickness of layer 4. Whatever the cortical structure, this layer receives sensory information. For instance, the axons from the optical radiation primarily project onto neurons of the fourth layer of V1. M1 has a fourth layer that is clearly thinner than S1, indicating that it receives less sensory information. However, M1 does receive some sensory input in layers 1 to 4, not only from cortical sensory areas but also directly from the thalamus. Also, several secondary motor areas, such as the premotor (PM), supplementary motor (SMA) and cingular motor areas, project directly onto M1 (Dum & Strick, 2002). Concerning the efferent fibers of M1, layer 5 contains the so-called "Cells of Betz" (large pyramidal neurons), visible with only little optical enlargement. Part of the corticospinal tract finds its origin in these pyramidal neurons. This tract consists of well myelinated axons which directly descend into the spinal cord. Some of these axons even project directly onto the motoneurons of the distal muscles without passing by interneurons (Maier et al., 2002). M1 also sends small efferent axons

The primary cortical areas represent the information coming from (or going to) the periphery according to a topological principle, i.e., retinotopic for V1, tonotopic for A1, and somatotopic for S1 and M1. These "maps" were long considered as stable and definitive once the neural functions are fully developed. We now know that this is not correct. Without elaborating on this huge research domain, we will give some examples involving M1 and S1 which show that these topologic maps are highly flexible and constantly re-

We begin with some basic details concerning the somatotopy of M1. In a normal subject, M1 shows a rather global somatotopic organization in a medial-lateral direction, representing the leg, back, arm, hand and face (Penfield & Boldrey, 1937). This rather fine somatotopic organization seems to reflect a "basic" organization that exists when the subject is passive. However, when engaged in a task, within each sub-area, we can identify a distributed representation adapted to the requirements of the task. This has been shown by Sanes and colleagues (1995) in an fMRI study. They asked subjects to make flexion/extension movements with different fingers (one at a time) or with the wrist. For each movement, they found multiple activation sites in the arm area of M1. Moreover, these sites showed an important overlap. These results, which have since been confirmed by other studies (see

cytoarchitecture of the cortex depends on its *functional* development.

from layers 5 and 6 to other cortical areas.

actualized.

**2.2 Flexibility and plasticity of the primary cortical areas** 

environments which are too artificial in order to study brain functioning. However, since in their opinion perception is "direct", Gibson and his successors have largely ignored the brain and have, therefore, not contributed to the understanding of brain functioning. Although there is much more to say on this subject, we will not develop this point any further in the present chapter.

The second drawback with the cognitive approach is the fact that cognition has mainly been sought outside the primary cortical areas. Indeed, since the above-mentioned cognitive models localize cognition between the input and the output, cognition is necessarily located in the secondary and associative cortical areas. For a long time, the primary motor area has been considered as a simple "execution area" of which the neuronal activity reflects the immediate output to the muscles. In the same way, the primary sensory areas are often presumed to simply transfer sensory information to higher order cognitive systems. For the same reason, studies concerned with the functioning of the secondary and associative areas do not really take into account the direct projections of the nervous system to peripheral structures.

In this chapter, we aim to show that the hierarchical and modular vision of brain functioning is no longer defendable. Cognition emerges from the interaction between regions that are distributed over the whole brain, including the primary cortical areas. After a brief review of the anatomy of the primary somatosensory (S1) and motor (M1) areas, we will develop arguments in favor of this hypothesis. We will mention the highly flexible functional organization of the primary sensorimotor cortical areas. We will show that the neuronal activity of S1 depends on the environmental and cognitive context, i.e., on the value of the stimulus at a given moment. Then, we will show that M1 is much more than a simple transmission area between the non-primary motor areas and the spinal cord. Indeed, M1 is active in tasks without any motor output and the M1 neuronal activity depends on the context in which a motor output is produced and can be adapted and modified in real time. We will end with an example of a clinical implication of this hypothesis, concerning phantom limb sensations in patients with upper limb amputations.
