1. Movement-related neuronal activity in the supplementary motor area (SMA), primary mortor cortex (MC), and putamen was studied in monkeys performing a visuomotor tracking task designed to determine 1) the extent to which neuronal activity in each of these areas represented the direction of visually guided arm movements versus the pattern of muscle activity required to achieve those movements and 2) the relative timing of different types of movement-related activity in these three motor areas. 2. A total of 455 movement-related neurons in the three motor areas were tested with a behavioral paradigm, which dissociated the direction of visually guided elbow movements from the accompanying pattern of muscular activity by the application of opposing and assisting torque loads. The movement-related activity described in this report was collected in the same animals performing the same behavioral paradigm used to study preparatory activity described in the preceding paper. Of the total sample, 87 neurons were located within the arm region of the SMA, 150 within the arm region of the MC, and 218 within the arm region of the putamen. 3. Movement-related cells were classified as 'directional' if they showed an increase in discharge rate predominantly or exclusively during movements in one direction and did not have significant static or dynamic load effects. A cell was classified as 'muscle-like' if its directional movement-related activity was associated with static and/or dynamic load effects whose pattern was similar to that of flexors or extensors of the forearm. Both directional and muscle-like cells were found in all three motor areas. The largest proportion of directional cells was located in the putamen (52%), with significantly smaller proportions in the SMA (38%) and MC (41%). Conversely, a smaller proportion of muscle-like cells was seen in the putamen (24%) than in the SMA (41%) or MC (36%). 4. The time of onset of movememt-related discharge relative to the onset of movement ('lead time') was computed for each cell. On average, SMA neurons discharged significantly earlier (SMA lead times 47 ± 8 ms, mean ± SE) than those in MC (23 ± 6 ms), which in turn were earlier than those in putamen (-33 ± 6 ms). However, the degree of overlap of the distributions of lead times for the three areas was extensive. 5. The directional neurons appeared to code for movement direction per se, independent of the pattern of muscle activations required. Thus, in all three areas, there was evidence of neural processing related to 'high-level' aspects of motor control that are logically antecedent to the final specification of muscle activations. The evidence that movement-related neurons in the SMA tend to discharge earlier than their counterparts in MC and these in turn earlier than those in putamen suggests that there is some degree of sequential processing from the SMA to the MC and thence to the putamen. On the other hand, the existence of both directional neurons and neurons with muscle-like activity patterns in each of these areas and the significant overlap in the timing of movement-related activity of these cells strongly suggest that multiple levels of motor processing proceed in parallel within all three motor structures.
