Role of primate basal ganglia and frontal cortex in the internal generation of movements

SummaryThis study is a part of a project investigating neuronal activity in the basal ganglia and frontal cortex and describes externally and internally induced preparatory activity in the supplementary motor area (SMA), which forms a closed neuronal loop with the striatum. Monkeys made self-initiated arm reaching movements toward a constant target in the absence of phasic external stimuli. In separate blocks of trials, animals performed in a delayed go no-go task in which an instruction cue prepared for subsequent movement or no-movement to a trigger stimulus. A total of 328 neurons were tested in the delay task. Of these, 91 responded transiently to the instruction light with a median latency of 262 ms. Three quarters of these responses were restricted to the instruction preparing for arm movement, as opposed to with-holding it, and thus may be involved in movement preparation processes. Sustained activation during the instruction-trigger interval was found for 67 neurons and occurred nearly exclusively in movement trials. Activation usually increased gradually after the cue and ended abruptly upon movement onset and thus could be related to the setting and maintenance of processes underlying the preparation of movement. Time-locked responses to the trigger stimulus were found in 38 neurons and were usually restricted to movement trials (median latency 80 ms). Activity time-locked to movement execution occurred in 67 neurons, beginning up to 252 ms before movement onset. A total of 266 neurons were tested with self-initiated arm movements. Of these, 43 showed premovement activity beginning 610–3030 ms before movement onset (median 1430 ms). The activity increased slowly and reached its peak at 370 ms before movement onset. It ended before movement onset or continued until the arm began to move or reached the target. This activity appears to reflect neuronal processes related to the internal generation of movements. Two thirds of activations preceding self-initiated movements occurred in neurons not activated before externally instructed movements, suggesting a selectivity for the internal generation process. Activity related to the execution of self-initiated movements occurred in 67 neurons: it began during and up to 420 ms before movement onset and was usually not associated with pre-movement activity. Most of these neurons were also activated with stimulus-triggered movements, suggesting a lack of selectivity for the execution of self-initiated movements. In comparison with the striatum, more SMA neurons showed preparatory activity preceding externally instructed movements (transient 27% vs 16%, sustained 20% vs 12%) and self-initiated movements (16% vs 11%). Whereas transient responses showed similar latencies and durations in the two structures, sustained preparatory activity preceding externally instructed or self-initiated movements began and reached its peak earlier in SMA compared to striatal neurons. However, due to the long durations, sustained activation largely overlapped in the two structures, and thus essentially occurred simultaneously. Instruction-induced or internally generated preparatory activity may originate outside of the SMA and striatum or may derive from activity reverberating in cortico-basal ganglia loops, possibly in conjunction with other, closely associated cortical and subcortical structures. These data would favor a conjoint role for SMA and striatum in the internal generation of individual behavioral acts and the preparation of behavioral reactions.