Massimo Matelli

Functional organization of inferior area 6 in the macaque monkey

SummaryTwo series of experiments are reported in this paper. The first concerns the movement representation in the macaque inferior area 6, the second the functional properties of neurons located in the caudal part of this area (histochemical area F4). By combining single neuron recording and intracortical microstimulation, we found that inferior area 6 is somatotopically organized. The axio-proximal movements are represented caudally, the distal movements are represented near the arcuate sulcus. The mouth field is located laterally, the hand field medially. There is no leg field. A comparison between neuron properties and histochemical characteristics of inferior area 6 showed that the proximal movements representation includes most of area F4, whereas the distal movements representation corresponds to area F5 and to the rostral part of F4. Neurons located in that part of F4 where proximal movements are represented respond very well to tactile stimuli. They have large receptive fields mostly located on the face and on the upper part of the body. A large number of these neurons respond to visual stimuli. Objects approaching the animal are particularly effective. The tactile and the visual receptive fields are in register. The most represented movements are reaching movements, movements bringing the hand to the mouth or to the body and facial movements. There is a congruence between location of visual fields and preferred arm movements. It is argued that the receptive field arrangement and the response properties are more complex in area F4 than in the primary motor cortex and that area F4 neurons are involved in the control of arm movements towards different space sectors.

THE ORGANIZATION OF THE CORTICAL MOTOR SYSTEM : NEW CONCEPTS

A series of recent anatomical and functional data has radically changed our view on the organization of the motor cortex in primates. In the present article we present this view and discuss its fundamental principles. The basic principles are the following: (a) the motor cortex, defined as the agranular frontal cortex, is formed by a mosaic of separate areas, each of which contains an independent body movement representation, (b) each motor area plays a specific role in motor control, based on the specificity of its cortical afferents and descending projections, (c) in analogy to the motor cortex, the posterior parietal cortex is formed by a multiplicity of areas, each of which is involved in the analysis of particular aspects of sensory information. There are no such things as multipurpose areas for space or body schema and (d) the parieto-frontal connections form a series of segregated anatomical circuits devoted to specific sensorimotor transformations. These circuits transform sensory information into action. They represent the basic functional units of the motor system. Although these conclusions mostly derive from monkey experiments, anatomical and brain-imaging evidence suggest that the organization of human motor cortex is based on the same principles. Possible homologies between the motor cortices of humans and non-human primates are discussed.

Localization of grasp representations in humans by PET: 1. Observation versus execution

Positron emission tomography (PET) was used to localize brain regions that are active during the observation of grasping movements. Normal, right-handed subjects were tested under three conditions. In the first, they observed grasping movements of common objects performed by the experimenter. In the second, they reached and grasped the same objects. These two conditions were compared with a third condition consisting of object observation. On the basis of monkey data, it was hypothesized that during grasping observation, activations should be present in the region of the superior temporal sulcus (STS) and in inferior area 6. The findings in humans demonstrated that grasp observation significantly activates the cortex of the middle temporal gyrus including that of the adjacent superior temporal sulcus (Brodmanns area 21) and the caudal part of the left inferior frontal gyrus (Brodmanns area 45). The possible functional homologies between these areas and the monkey STS region and frontal area F5 are discussed.

Afferent properties of periarcuate neurons in macaque monkeys. II. Visual responses

The visual response of single neurons of the periarcuate cortex have been studied in the macaque monkey. Two sets of neurons responding to visual stimuli have been found. The first set, located rostral to the arcuate sulcus, was formed by units that could be activated by stimuli presented far from the animal. These neurons had large receptive fields and were neither orientation nor direction selective. The second set, found predominantly caudal to the arcuate sulcus, was formed by units that were maximally or even exclusively activated by stimuli presented in the space immediately around the animal. These neurons were bimodal, responding also to somatosensory stimuli. According to the location of their visual responding regions the bimodal neurons were subdivided into pericutaneous (54%) and distant peripersonal neurons (46%). The former responded best to stimuli presented a few centimeters from the skin, the latter to stimuli within the animals reaching distance. The visual responding regions were spatially related to the tactile fields. It is argued that neurons with a receptive field consisting of several responding areas, some in one sensory modality, some in another, have a praxic function and that they are involved in organizing sequences of movements.

Patterns of cytochrome oxidase activity in the frontal agranular cortex of the macaque monkey

The laminar pattern of cytochrome oxidase activity was studied in the agranular frontal cortex (area 4-6 complex) of the macaque monkey. The cortex, stained with this method, showed 6 stripes of different enzymatic activity. On the basis of their characteristics and of the presence of highly active cells, the agranular frontal cortex could be parcellated in 5 areas (F1-F5). F1 very likely corresponds to area FA of von Bonin and Bailey. Rostral to F1 two large regions could be distinguished, one located medial to the spur of the arcuate sulcus and its imaginary caudal extension, the other laterally. The superior region was formed by areas F2 and F3. The first was located on the dorsomedial cortical surface, the other on the mesial surface. F3 possibly corresponds to the supplementary motor area. The inferior region was formed by areas F4 and F5. The rostral area (F5) showed transition characteristics that rendered it somehow similar to the prefrontal areas. It may correspond to the cytoarchitectonic area FCBm. The cytocrome oxidase technique is a useful means of parcellating the agranular frontal cortex and may greatly help in physiological and behavioral experiments.

Functional neuroanatomy of the primate isocortical motor system

The concept of the primate motor cortex based on the cytoarchitectonic subdivision into areas 4 and 6 according to Brodmann or the functional subdivision into primary motor, supplementary motor, and lateral premotor cortex has changed in recent years. Instead, this cortical region is now regarded as a complex mosaic of different areas. This review article gives an overview of the structure and function of the isocortical part of the motor cortex in the macaque and human brain. In the macaque monkey, the primary motor cortex (Brodmann’s area 4 or area F1) with its giant pyramidal or Betz cells lies immediately anterior to the central sulcus. The non-primary motor cortex (Brodmann’s area 6) lies further rostrally and can be subdivided into three groups of areas: the supplementary motor areas ”SMA proper” (area F3) and ”pre-SMA” (area F6) on the mesial cortical surface, the dorsolateral premotor cortex (areas F2 and F7) on the dorsolateral convexity, and the ventrolateral premotor cortex (areas F4 and F5) on the ventrolateral convexity. The primary motor cortex is mainly involved in controlling kinematic and dynamic parameters of voluntary movements, whereas non-primary motor areas are more related to preparing voluntary movements in response to a variety of internal or external cues. Since a structural map of the human isocortical motor system as detailed as in the macaque is not yet available, homologies between the two species have not been firmly established. There is increasing evidence, however, that a similar organizational principle (i.e., primary motor cortex, supplementary motor areas, dorso- and ventrolateral premotor cortex) also exists in humans. Imaging studies have revealed that functional gradients can be discerned within the human non-primary motor cortex. More rostral cortical regions are active when a motor task is nonroutine, whereas more routine motor actions engage more caudal areas.

Largely segregated parietofrontal connections linking rostral intraparietal cortex (areas AIP and VIP) and the ventral premotor cortex (areas F5 and F4).

Abstract Two functionally different cortical areas are located in the rostral part of the intraparietal sulcus (IP): the ventral intraparietal area (VIP), along the fundus of the sulcus, and the anterior intraparietal area (AIP), rostral in the lateral bank. VIP and AIP have functional properties comparable to those of the ventral premotor areas, F4 and F5, respectively. The aim of this study was to establish whether these intraparietal and premotor areas have direct and specific anatomical connections. Neural tracers were injected in F4, F5, and AIP in three macaque monkeys. The results showed that F4 and F5 are targets of strong projections from VIP and AIP, respectively, and that the linkage between F5 and AIP is highly selective. These data support the notion that parietofrontal connections selectively link areas displaying similar functional properties and form largely segregated anatomical circuits. Each of these circuits is possibly dedicated to specific aspects of sensorimotor transformations. In particular, the AIP-F5 circuit should play a crucial role in visuomotor transformation for grasping, the VIP-F4 circuit is possibly involved in peripersonal space coding for movement.

Superior Area 6 Afferents From the Superior Parietal Lobule in the Macaque Monkey

Superior area 6 of the macaque monkey frontal cortex is formed by two cytoarchitectonic areas: F2 and F7. In the present experiment, we studied the input from the superior parietal lobule (SPL) to these areas by injecting retrograde neural tracers into restricted parts of F2 and F7. Additional injections of retrograde tracers were made into the spinal cord to define the origin of corticospinal projections from the SPL. The results are as follows: 1) The part of F2 located around the superior precentral dimple (F2 dimple region) receives its main input from areas PEc and PEip (PE intraparietal, the rostral part of area PEa of Pandya and Seltzer, [1982] J. Comp. Neurol. 204:196–210). Area PEip was defined as that part of area PEa that is the source of corticospinal projections. 2) The ventrorostral part of F2 is the target of strong projections from the medial intraparietal area (area MIP) and from the dorsal part of the anterior wall of the parietooccipital sulcus (area V6A). 3) The ventral and caudal parts of F7 receive their main parietal input from the cytoarchitectonic area PGm of the SPL and from the posterior cingulate cortex. 4) The dorsorostral part of F7, which is also known as the supplementary eye field, is not a target of the SPL, but it receives mostly afferents from the inferior parietal lobule and from the temporal cortex. It is concluded that at least three separate parietofrontal circuits link the superior parietal lobule with the superior area 6. Considering the functional properties of the areas that form these circuits, it is proposed that the PEc/PEip‐F2 dimple region circuit is involved in controlling movements on the basis of somatosensory information, which is the traditional role proposed for the whole dorsal premotor cortex. The two remaining circuits appear to be involved in different aspects of visuomotor transformations. J. Comp. Neurol. 402:327–352, 1998.

Space coding by premotor cortex

SummaryMany neurons in inferior area 6, a cortical premotor area, respond to visual stimuli presented in the space around the animal. We were interested to learn whether the receptive fields of these neurons are coded in retinotopic or in body-centered coordinates. To this purpose we recorded single neurons from inferior area 6 (F4 sector) in a monkey trained to fixate a light and detect its dimming. During fixation visual stimuli were moved towards the monkey both within and outside the neuronss receptive field. The fixation point was then moved and the neuron retested with the monkeys gaze deviated to the new location. The results showed that most inferior area 6 visual neurons code the stimulus position in spatial and not in retinal coordinates. It is proposed that these visual neurons are involved in generating the stable body-centered frame of reference necesary for programming visually guided movements.

The cortical connections of area V6: an occipito-parietal network processing visual information

The aim of this work was to study the cortical connections of area V6 by injecting neuronal tracers into different retinotopic representations of this area. To this purpose, we first functionally recognized V6 by recording from neurons of the parieto‐occipital cortex in awake macaque monkeys. Penetrations with recording syringes were performed in the behaving animals in order to inject tracers exactly at the recording sites. The tracers were injected into the central or peripheral field representation of V6 in different hemispheres. Irrespective of whether injections were made in the centre or periphery, area V6 showed reciprocal connections with areas V1, V2, V3, V3A, V4T, the middle temporal area /V5 (MT/V5), the medial superior temporal area (MST), the medial intraparietal area (MIP), the ventral intraparietal area (VIP), the ventral part of the lateral intraparietal area and the ventral part of area V6A (V6AV). No labelled cells or terminals were found in the inferior temporal, mesial and frontal cortices. The connections of V6 with V1, and with all the retinotopically organized prestriate areas, were organized retinotopically. The connection of V6 with MIP suggests a visuotopic organization for this latter. Labelling in V6A and VIP after either central or peripheral V6 injections was very similar in location and extent, as expected on the basis of the nonretinotopic organization of these areas. We suggest that V6 plays a pivotal role in the dorsal visual stream, by distributing the visual information coming from the occipital lobe to the sensorimotor areas of the parietal cortex. Given the functional characteristics of the cells of this network, we suggest that it could perform the fast form and motion analyses needed for the visual guiding of arm movements as well as their coordination with the eyes and the head.