A comparison of movement-related neuronal activities in cerebellar- and basal ganglia-recipient regions of the macaque thalamus

The ventral lateral (VL) nucleus of the thalamus relays signals from the cerebellum (Cb) and basal ganglia (BG) to primary motor cortex (M1). In primates, glutamatergic Cb efferents from the deep cerebellar nuclei and GABAergic BG efferents from the internal segment of the globus pallidus (GPi) terminate in distinct subregions of VL: the posterior (VLp) and anterior (VLa) divisions, respectively. This anatomical segregation suggests that Cb- and BG-thalamocortical circuits may play distinct roles in motor control, which could be revealed by comparing movement-related activity in VLp and VLa. Here, we recorded single-unit activity from VLp and VLa, identified via electrical stimulation of superior cerebellar peduncle and GPi, during a choice reaction time reaching task. We also recorded from M1, which maintains bidirectional connections with both VLp and VLa. Peri-movement increases in firing began earlier in VLp than in VLa whereas decrease-type responses were more prevalent and prolonged in duration in VLa neurons as compared with VLp and M1. Time-resolved general linear model analysis showed dynamic encoding of task parameters, particularly movement direction, in all three regions. Direction encoding was strongest in M1, moderate in VLp, and weakest in VLa. Direction encoding in VLa also lagged behind that in M1 and VLp. Clustering analysis of direction encoding strength and timing revealed a subpopulation of VLp neurons that encoded direction particularly strongly during the reaction time period. These results highlight a limitation of traditional assumptions that activity characteristics are distributed homogeneously across neural populations and suggest a novel functional organization within VLp neurons.