Encoding of direction and combination of movements by primate putamen neurons

To perform multiple movements in a preprogrammed order, the brain needs to compute both the visuospatial and temporal organization of such multiple movements. Previous studies revealed participation of the parietal and premotor areas in visuospatial processing, and of the supplementary motor and presupplementary motor areas in temporal structuring of multiple movements. In the basal ganglia, on the other hand, relatively little has been known about how the neuronal processing of the visuospatial and temporal structuring of multiple movements occurs. In the present study, monkeys performed combinations of hand movements, either a lever turn-lever turn or lever turn-button press. Combinations of the two movements were performed under visually instructed condition first, then under remembered condition. We found that activity of 43% (30/69) and 60% (42/69) of putamen neurons was selective to the preprogrammed combination of movements and to the direction of the first movement. The neurons preferring remembered condition were mainly observed in the dorsomedial part of the putamen, where most of neurons were also selective to both direction and combination of movements, while those in the ventrolateral part of the putamen were not selective to the instructed and remembered conditions. The results supported a hypothesis that the movement direction-selective and the movement combination-selective neuron activities in the striatum may play an indispensable role in the visuospatial and temporal organization of movements through the cortico-basal ganglia loop system.