Striatal cell-type specific encoding stability and reorganization for agency and habit

Adaptive, goal-directed decision making requires agency, knowledge that an action will cause a particular outcome. For well-practiced routines, agency is relinquished in favor of automatic habits. Here, we used cell-type specific, longitudinal, cellular-resolution, microendoscopic calcium imaging, chemogenetics, instrumental conditioning and a test of behavioral strategy to ask how dorsomedial striatum D1 ⁺ and D2/A2A ⁺ neurons contribute to the formation of agency and habit. We found that DMS D1 ⁺ neurons stably encode actions and variables related to goal-directed v. habitual behavioral strategy, develop encoding of the action-outcome relationship, and are critical for both action-outcome learning and the application of this learned agency for flexible, goal-directed decision making. Conversely, one ensemble of A2A ⁺ neurons transiently encodes actions and behavioral transition variables during early action-outcome learning and another slowly starts to encode actions as routine habits form. Correspondingly, A2A ⁺ neurons are only transiently necessary for initial formation of the action-outcome model underlying agency. Thus, agency is learned through DMS D1 ⁺ and A2A ⁺ neuronal activity and then maintained in DMS D1 ⁺ neurons to support adaptive, goal-directed decision making. Habit formation is associated with reorganization of A2A ⁺ neuronal encoding. These data reveal important insights into the neuronal circuits of learning and decision making.