M. D. Crutcher

The central theme of the "segregated circuits" hypothesis is that structural convergence and functional integration occurs within, rather than between, each of the identified circuits. Admittedly, the anatomical evidence upon which this scheme is based remains incomplete. The hypothesis continues to be predicated largely on comparisons of anterograde and retrograde labeling studies carried out in different sets of animals. Only in the case of the "motor" circuit has evidence for the continuity of the loop been demonstrated directly in individual subjects; for the other circuits, such continuity is inferred from comparisons of data on different components of each circuit obtained in separate experiments. Because of the marked compression of pathways leading from cortex through basal ganglia to thalamus, comparisons of projection topography across experimental subjects may be hazardous. Definitive tests of the hypothesis of maintained segregation await additional double- and multiple-label tract-tracing experiments wherein the continuity of one circuit, or the segregation of adjacent circuits, can be examined directly in individual subjects. It is worthy of note, however, that the few studies to date that have employed this methodology have generated results consistent with the segregated circuits hypothesis. Moreover, single cell recordings in behaving animals have shown striking preservation of functional specificity at the level of individual neurons throughout the "motor" and "oculomotor" circuits. It is difficult to imagine how such functional specificity could be maintained in the absence of strict topographic specificity within the sequential projections that comprise these two circuits. This is not to say, however, that we expect the internal structure of functional channels (e.g., the "arm" channel within the "motor" circuit) to have cable-like, point-to-point topography. When the grain of analysis is sufficiently fine, anatomical studies have shown repeatedly that the terminal fields of internuclear projections (e.g., to striatum, pallidum, nigra, thalamus, etc.) often appear patchy and highly divergent, suggesting that neighboring groups of projection cells tend to influence interdigitating clusters of postsynaptic neurons. While more intricate and complex than simple point-to-point topography, however, this type arrangement should also be capable of maintaining functional specificity. As discussed briefly above, it is not yet clear to what extent the inputs to the "motor" circuit from the different precentral motor fields (e.g., MC, SMA, APA) are integrated in their passage through the circuit. It now appears that at the level of the putamen such inputs remain segregated.(ABSTRACT TRUNCATED AT 400 WORDS)

1. The purpose of this study was to compare the functional properties of neurons in three interrelated motor areas that have been implicated in the planning and execution of visually guided limb movements. All three structures, the supplementary motor area (SMA), primary motor cortex (MC), and the putamen, are components of the basal ganglia-thalamocortical "motor circuit." The focus of this report is on neuronal activity related to the preparation for movement. 2. Five rhesus monkeys were trained to perform a visuomotor step-tracking task in which elbow movements were made both with and without prior instruction concerning the direction of the forthcoming movement. To dissociate the direction of preparatory set (and limb movement) from the task-related patterns of tonic (and phasic) muscular activation, some trials included the application of a constant torque load that either opposed or assisted the movements required by the behavioral paradigm. Single-cell activity was recorded from the arm regions of the SMA, MC, and putamen contralateral to the working arm. 3. A total of 741 task-related neurons were studied, including 222 within the SMA, 202 within MC, and 317 within the putamen. Each area contained substantial proportions of neurons that manifested preparatory activity, i.e., cells that showed task-related changes in discharge rate during the postinstruction (preparatory) interval. The SMA contained a larger proportion of such cells (55%) than did MC (37%) or the putamen (33%). The proportion of cells showing only preparatory activity was threefold greater in the SMA (32%) than in MC (11%). In all three areas, cells that showed only preparatory activity tended to be located more rostrally than cells with movement-related activity. Within the arm region of the SMA, the distribution of sites from which movements were evoked by microstimulation showed just the opposite tendency: i.e., microexcitable sites were largely confined to the caudal half of this region. 4. The majority of cells with task-related preparatory activity showed selective activation in anticipation of elbow movements in a particular direction (SMA, 86%; MC, 87%; putamen, 78%), and in most cases the preparatory activity was found to be independent of the loading conditions (80% in SMA, 83% in MC, and 84% in putamen).(ABSTRACT TRUNCATED AT 400 WORDS)

Neuronal relations to active movements of individual body parts and neuronal responses to somatosensory stimulation were studied in the external (GPe) and internal (GPi) segments of the globus pallidus (GP) and the subthalamic nucleus (STN) of awake monkeys. In GPe (n = 249), GPi (n = 151), and STN (n = 153), 47, 29, and 28% of the cells, respectively, discharged in relation to active arm movements, 10, 11, and 15% to leg movements, and 22, 22, and 18% to orofacial movements. Of the neurons whose activity was related to arm movements, 26, 16, and 21% in GPe, GPi, and STN, respectively, discharged in relation to movements of distal parts of the limb. Of cells whose discharge was related to active limb movements, 37, 22, and 20% in GPe, GPi, and STN, respectively, also responded to passive joint rotation, which was usually specific in terms of joint and direction of movement. Only a small percentage of cells responded to muscle or joint palpation, tendon taps, or cutaneous stimulation. Short-latency, direction-specific neuronal responses to load perturbations confirmed the existence of proprioceptive driving. In both GPe and GPi, leg movement-related neurons were centrally located in the rostrocaudal and dorsoventral dimensions. In contrast, arm movement-related cells were found throughout the entire rostrocaudal extent of both segments, although in greater numbers caudally. In the central portions they were situated largely inferior and lateral to leg movement-related neurons. Neurons related to orofacial movements were largely confined to the caudal halves of both segments, where they were located largely ventral to arm movement-related cells. The STN cells whose activity was related to leg movements were observed largely in the central portions of the nucleus in the rostrocaudal and mediolateral dimensions. Cells whose activity was related to arm movements were found throughout the rostrocaudal extent of the nucleus, but were most numerous at the rostral and caudal poles. Neurons related to movements of the facial musculature and to licking and chewing movements were distributed over the entire rostrocaudal extent of the nucleus, where they generally occupied the ventrolateral regions. In all three nuclei, neurons with similar functional properties were sometimes clustered together. Within the arm and leg areas, however, there was no clear evidence for a simple organization of clusters related to different parts of the limb. These studies provide further evidence for a role of the basal ganglia in the control of limb movements.(ABSTRACT TRUNCATED AT 400 WORDS)

1. This study was designed to determine whether the supplementary motor area (SMA), the primary motor cortex (MC), and the putamen, all of which are components of the basal ganglia-thalamocortical “motor circuit,” contain neural representations of the target or goal of a movement, independent of specific features of the movement itself. Four rhesus monkeys were trained to perform two visuomotor delayed step-tracking tasks in which the subject used a cursor to track targets on a display screen by making flexion and extension movements of the elbow. Single-cell activity was recorded from the SMA, MC, and putamen while the monkeys performed the two tasks. In the Standard task, the cursor and the forearm moved in the same direction. The Cursor/Limb Inversion task was identical to the Standard task except that there was an inverse relationship between the directions of movement of the forearm and cursor. Together, these tasks dissociated the spatial features of the target or goal of the movement from those of the movement itself. Both tasks also included features that made it possible to distinguish neuronal activity related to the preparation for movement from that related to movement execution. A total of 554 directionally selective, task-related neurons were tested with both tasks (SMA, 207; MC, 198; putamen, 149). 2. Two types of directionally selective preparatory activity were seen in each motor area. Cells with target-dependent preparatory activity showed selective discharge prior to all preplanned movements of the cursor toward one of the side targets (right or left), irrespective of whether the limb movement involved extension or flexion of the elbow. Comparable proportions of target-dependent preparatory cells were seen in the SMA (36%), MC (40%), and putamen (38%). Cells with limb-dependent preparatory activity showed selective discharge prior to all preplanned elbow movements in a particular direction (extension or flexion), irrespective of whether the target to which the cursor was moved was located on the right or left side of the display. The SMA contained a higher proportion of limb-dependent preparatory cells (40%) than either MC (15%) or putamen (9%). 3. Two types of directionally selective movement-related activity were also seen in each motor area.(ABSTRACT TRUNCATED AT 400 WORDS)