The respective activation and silencing of striatal direct and indirect pathway neurons support behavior encoding

Abstract

Abstract The basal ganglia are known to control actions and modulate movements. Neuronal activity in the two efferent pathways of the dorsal striatum is critical for appropriate behavioral control. Previous evidence has led to divergent conclusions on the respective engagement of both pathways during actions. Using calcium imaging to evaluate how neurons in the direct and indirect pathways encode behaviors during self-paced spontaneous explorations in an open field, we observed that the two striatal pathways exhibit distinct tuning properties. Supervised learning algorithms revealed 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 with congruent activations in the direct pathway encoding multiple accessible behaviors in a given context, and in the indirect pathway encoding the suppression of competing behaviors. This model reconciles previous conflicting conclusions on motor encoding in the striatum.