Striatal activity maintains a short-term action-outcome memory to guide future choice

ABSTRACT Adaptive behavior requires animals to use the outcomes of recent actions (action-outcomes) to guide future decisions. While the striatum is critical for decision-making, it is currently unclear how it is involved in the storage and retrieval of short-term associative memories. Here, we implemented a head-fixed memory-guided decision-making task in which mice use the outcome of a previous choice to determine whether to repeat or switch their next action. We show that dopamine fluctuations in the ventrolateral striatum are modulated by reward receipt or omission and recent outcome history, while the activity of direct and indirect pathway striatal projection neurons encodes recent action-outcome associations and predicts future switch/repeat choices. Closed-loop optogenetic activation and inhibition of direct and indirect pathway neurons during either the action-outcome association period or the delay preceding the next choice bidirectionally biased future actions away from those favored by reward history. Together, these findings suggest that striatal activity maintains a short-term action-outcome associative memory that links completed actions to future motor plans during adaptive decision-making.