Complete representation of action space and value in all striatal pathways

ABSTRACT The dorsal striatum plays a central role in motor and decision programs, such as the selection and execution of particular actions and the evaluation of their outcomes. A standard circuit model has emerged based on the striatal organization where projection neurons with specific molecular and long-range connectivity identities encode discrete and possibly opposing action signals. We used large-scale cell-type specific imaging of calcium signals during motor and decision behaviors to map the activity of individual striatal projection neurons (SPNs) that form the three major output pathways of the striatum – SPNs in the D1+ direct, the A2A+ indirect, and the Oprm1+ patch pathway. We found that during exploration or choice behaviors SPNs showed a pathway-independent representation of the discrete phases and action variables. The tuning of individual SPNs was action and context-dependent, together covering the entire task space, and included pathway-independent representation of decision-variables such as action value in a dynamic choice task. We propose that the three major SPN pathways broadcast in parallel the complete representation of the task space to downstream targets, including task- and phase-specific signals of action value and choice.