Internal and external contexts drive distinct dynamics in shared action-encoding striatal neurons

Abstract

Animals can initiate movements either in response to external cues or from internal drive, yet how the brain flexibly supports both remains unclear. Disorders such as Parkinsons disease disrupt these modes differently, suggesting distinct underlying mechanisms. Such differences could arise from specialized circuits dedicated to each action mode or from shared neuronal populations that shift their dynamics across contexts. To distinguish between these possibilities, we performed two-photon calcium imaging in the dorsolateral striatum as mice executed the same lever press either spontaneously or in response to a cue, enabling direct comparison of internally and externally triggered actions. Unsupervised clustering revealed subpopulations of neurons modulated during cue, movement, or post-action periods. Critically, the same neurons were tuned to movement across initiation contexts. However, the dynamics of this shared population evolved within distinct "context" and "action" subspaces, even before movement initiation. Both dopamine D1- and D2-receptor-expressing spiny projection neurons contributed to both subspaces, with D1-SPNs more active at the time of the sensory stimulus. These results show that context shapes neural dynamics within a shared movement-encoding population, revealing a context-generalizable striatal code that supports flexible movement initiation across internal and external drives.