Putaminal activity for simple reactions or self-timed movements

Abstract

To examine the role of basal ganglia-cortical circuits in movement initiation, we trained monkeys to make the same arm movements in two ways-in immediate reaction to a randomly timed external cue (cued movements) and also following a variable delay without an explicit initiation signal (self-timed movements). The two movement types were interleaved and balanced in overall timing to allow a direct comparison of activity before and during the movement. Posterior putaminal neurons generally had phasic, movement-related discharges that were comparable for cued and self-timed movements. On cued movements, neuronal activity increased sharply following cue onset. However, for self-timed movements, there was a slow build-up in activity that preceded the phasic discharge. This slow build-up was time-locked to movement and restricted to a narrow time window hundreds of milliseconds before movement. The difference in premovement activity between cued and self-timed trials was present before the earliest cue-onset times and was not related to any differences in the overall time-to-move between the two types of trials. These features suggest that activity evolving in the basal ganglia-cortical circuitry may drive the initiation of movements by increasing until an activity threshold is exceeded. The activity may increase abruptly in response to an external cue or gradually when the timing of movements is determined by the animals themselves rather than an external cue. In this view, small changes in activity that occur in advance of the much larger perimovement neuronal activity may be an important determinant of when movement occurs. In support of this hypothesis, we found that even for cued movements, faster reaction times were associated with slightly higher levels of activity hundreds of milliseconds before movement.