The functional and structural properties of the dorsolateral frontal lobe and posterior parietal proximal arm representations were studied in macaque monkeys. Physiological mapping of primary motor (MI), dorsal premotor (PMd), and posterior parietal (area 5) cortices was performed in behaving monkeys trained in an instructed-delay reaching task. The parietofrontal corticocorticat connectivities of these same areas were subsequently examined anatomically by means of retrograde tracing techniques. Signal-, set-, movement-, and position-related directional neuronal activities were distributed nonuniformly within the task-related areas in both frontal and parietal cortices. Within the frontal lobe, moving caudally from PMd to the MI, the activity that signals for the visuospatial events leading to target localization decreased, while the activity more directly linked to movement generation increased. Physiological recordings in the superior parietal lobule revealed a gradient-like distribution of functional properties similar to that observed in the frontal lobe. Signal- and set-related activities were encountered more frequently in the intermediate and ventral part of the medial bank of the intraparietal sulcus (IPS), in area MIP. Movement- and position-related activities were distributed more uniformly within the superior parietal lobule (SPL), in both dorsal area 5 and in MIP. Frontal and parietal regions sharing similar functional properties were preferentially connected through their association pathways. As a result of this study, area MIP, and possibly areas MDP and 7m as well, emerge as the parietal nodes by which visual information may be relayed to the frontal lobe arm region. These parietal and frontal areas, along with their association connections, represent a potential cortical network for visual reaching. The architecture of this network is ideal for coding reaching as the result of a combination between visual and somatic information.

The activity of 156 individual arm-related neurons was studied in the premotor cortex (area 6) while monkeys made arm movements of similar directions within different parts of 3-dimensional space. This study was aimed at describing the relationship between premotor cortical cell activity and direction of arm movement and assessing the coordinate system underlying this relationship. We found that the activity of 152 (97.4%) cells varied in an orderly fashion with the direction of movement, in at least some region of the work space. Premotor cortical cells fired most for a given preferred direction and less for other directions of movement. These preferred directions covered the directional continuum in a uniform fashion across the work space. It was found that, as movements of similar directions were made within different parts of the work space, the cells' preferred directions changed their orientation. Although these changes had different magnitudes for different cells, at the population level, they followed closely the changes in orientation of the arm necessary to move the hand from one to another part of the work space. This shift of cells' preferred direction with the orientation of the arm in space has been observed with similar characteristics in the motor cortex (see Caminiti et al., 1990). In both premotor and motor cortices, neuronal movement population vectors provide a good description of movement direction. Unlike the individual cell preferred directions upon which they are based, movement population vectors did not change their spatial orientation across the work space, suggesting that they remain good predictors of movement direction regardless of the region of space in which movements are made. The firing frequency of both premotor and motor cortical neurons varied significantly with the position occupied by the hand in space. These static positional effects were observed in 88.5% of premotor and 91.8% of motor cortical cells. In a second task, monkeys made movements from differing origins to a common end point. This task was performed within 3 different parts of space and was aimed at dissociating movement direction from movement end point. It was found that in both premotor and motor cortices virtually all cells were related to the direction and not to the end point of movement. These data suggest that premotor and motor cortices use common mechanisms for coding arm movement direction. They also provide a basis for understanding the coordinate transformation required to move the hand toward visual targets in space.

How is spatial information for limb movement encoded in the brain? Computational and psychophysical studies suggest that beginning hand position, via-points, and target are specified relative to the body to afford a comparison between the sensory (e. g., kinesthetic) reaf-ferences and the commands that generate limb movement Here we propose that the superior parietal lobule (Brodmann area 5) might represent a substrata for a body-centered positional code. Monkeys made arm movements in different parts of 3D space in a reaction-time task. We found that the activity of area 5 neurons can be related to either the starting point or the final point or combinations of the two. Neural activity is monotonicalty tuned in a body-centered frame of reference, whose coordinates define the azimuth, elevation, and distance of the hand. Each spatial coordinate tends to be encoded in a different sub-population of neurons. This parcellation could be a neural correlate of the psychophysical observation that these spatial parameters are processed in parallel and largely independent of each other in man.

Reaching movements are performed in order to bring the hand to targets of interest. It is widely believed that the distributed cortical network underlying visual reaching transforms the information concerning the spatial location of the target into an appropriate motor command. Modem views decompose this process into sequences of coordinate transformations between infonnational domains. The set of cortical areas and pathways by which the information on target location is relayed from the visual areas of the occipital lobe to the motor areas of the frontal lobe have, so far, been poorly understood. Recent data from different fields of neuroscience offer the basis for a new definition of the cortical system subserving reaching and, at the same time, for a reconsideration of the nature of the underlying visuo-to-motor transformation.

The anatomical and physiological substrata of eye–hand coordina- tion during reaching were studied through combined anatomical and physiological techniques. The association connections of parietal areas V6A and PEc, and those of dorso-rostral (F7) and dorso-caudal (F2) premotor cortex were studied in monkeys, after physiological characterization of the parietal regions where retrograde tracers were injected. The results show that parieto-occipital area V6A is reciprocally connected with F7, and receives a smaller projection from F2. Local parietal projections to V6A arise from areas MIP and, to a lesser extent, 7m, PEa and PEc. On the contrary, parietal area PEc is strongly and reciprocally connected with the part of F2 located close to the pre-central dimple (pre-CD). Local parietal projections to PEc come from a distributed network, including PEa, MIP, PEci and, to a lesser extent, 7m, V6A, 7a and MST. Premotor area F7 receives parietal projections mainly from 7m and V6A, and local frontal projections mainly from F2. On the contrary, premotor area F2 in the pre-CD zone receives parietal inputs from PEc and, to a lesser extent, PEci, while in the peri-arcuate zone F2 receives parietal projections from PEa and MIP. Local frontal projections to F2 pre-CD mostly stem from F4, and, to a lesser extent, from F7 and F3, and CMAd; those addressed to peri-arcuate zone of F2 arise mainly from F5 and, to a lesser extent, from F7, F4, dorsal (CMAd) and ventral (CMAv) cingulate motor areas, pre-supplementary (F6) and supplementary (F3) motor areas. The distribution of association cells in both frontal and parietal cortex was characterized through a spectral analysis that revealed an arrangement of these cells in the form of bands, composed of cell clusters, or ‘columns’. The reciprocal connections linking parietal and frontal cortex might explain the presence of visually related and eye-position signals in premotor cortex, as well as the influence of information about arm position and movement direction in V6A and PEc. The association connections identified in this study might carry sensory as well motor information that presumably provides a basis for a re-entrant signaling. This might be necessary to match retinal-, eye- and hand-related information underlying eye–hand coordination during reaching.