High-Dimensional Encoding of Movement by Single Neurons in Basal Ganglia Output

Abstract

The Substantia Nigra pars reticulata (SNpr), an output structure of the basal ganglia, has been hypothesized to gate the execution of movements. Previous studies focusing mostly on saccadic eye movements have reported that SNpr neurons are tonically active and either pause or increase their firing during movements, consistent with the gating role. We recorded activity in the SNpr of two monkeys during smooth pursuit and saccadic eye movements. SNpr neurons exhibited highly diverse reaction patterns during pursuit, including frequent increases and decreases in firing rate, uncorrelated responses in different movement directions and in reward conditions resulting in the high dimensional activity of single neurons. These diverse temporal patterns surpassed those in other oculomotor areas in the frontal cortex, basal ganglia, and cerebellum. These results suggest that temporal properties of the responses enrich the coding capacity of the basal ganglia output beyond gating or permitting movement.