PREPARATION FOR MOVEMENT - NEURAL REPRESENTATIONS OF INTENDED DIRECTION IN 3 MOTOR AREAS OF THE MONKEY

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). A minority of cells in each area showed preparatory activity that was weakly modulated by the presence of constant torque loads, but in nearly all such cases the 'loading effects' were not confirmed to the postinstruction interval and therefore did not appear to be 'preparatory' in nature; rather, they appeared merely to reflect the current loading conditions. 5. The average onsets and offsets of directional preparatory activity in the SMA and MC were significantly earlier than those in the putamen. This is consistent with the possibility that some of the preparatory activity in the putamen may arise from corticostriatal inputs to this nucleus from the SMA and/or MC. It should be noted, however, that preparatory neurons in all three motor areas were active simultaneously throughout most of the postinstruction interval. 6. The results of this study indicate that directionally selective preparatory activity is distributed across the SMA, MC, and the putamen. The near absence of preparatory loading effects in all three motor areas suggests that directional preparatory activity, at least in these structures, may not play a significant role in coding for either the dynamics or the muscle activation patterns of preplanned movements. Instead, such activity may be coding for the intended direction of movement at a more abstract level of processing (e.g., trajectory and/or kinematics), independent of the forces that the movement will require.