Complementary coding of behaviors in striatal pathways supports a dual selection-suppression function

Abstract

The basal ganglia are known to control actions and modulate movements. Neuronal activity in the two efferent pathways of the dorsal striatum, a major input to the basal ganglia, is critical for appropriate behavioral control. Previous evidence has led to divergent conclusions on the respective engagement of both pathways during actions. We used calcium imaging to evaluate how neurons in the direct and indirect pathways in the dorsal striatum encode behaviors during self-paced spontaneous explorations in an open field. We observed that the two striatal pathways exhibit distinct tuning properties during spontaneous behaviors. We applied supervised learning algorithms and found that direct pathway neurons encode behaviors through their activation, whereas indirect pathway neurons exhibit behavior-specific silencing. These properties remain stable for weeks. Our findings highlight a complementary encoding of behaviors in the two striatal pathways that supports an updated model, reconciling previous conflicting conclusions on motor encoding in the striatum.