Neural coding of arm and hand actions is spatially organized in motor cortex

Abstract

Primate motor cortex (M1) contains distinct zones with dense projections to the spinal circuits of arm and hand muscles making them critical substrates for manual behavior. But how does neural activity encoding manual actions map in space and time onto these zones? We addressed this question by recording single unit activity (n=1,573) throughout M1 in two macaque monkeys performing a reach-to-grasp task. Recordings were made with linear electrode arrays that were registered to detailed motor maps obtained with intracortical microstimulation. When units were grouped by somatotopic location, the time-resolved profiles from the arm and hand zones closely resembled time-lagged versions of the corresponding muscle activity. Thus, activity in both M1 zones differentiated between task phases and target objects. Unlike the arm and hand muscles, however, neural activity did not differ significantly between M1 arm and hand zones. In contrast, examining the spatial organization of neural selectivity for task phase revealed clear functional distinctions: reach-selectivity was stronger in the arm zone than in the hand zone and manipulate-selectivity was stronger in the hand zone than in the arm zone. Similarly, task condition decoding from hand zone activity was more accurate than from arm zone activity. Our findings collectively show that the encoding of reach-to-grasp movements is spatially clustered within the M1 forelimb representation and that the clusters are selective for function. These distinctions are graded rather than categorical, but they reveal tighter coupling between the spatio-temporal organization of M1 single unit activity and underlying cortical structure than generally assumed.