Dorsolateral striatal task-initiation bursts represent past experiences more than future action plans

Abstract

The dorsolateral striatum (DLS) is involved in learning and executing procedural actions. Cell ensembles in the DLS, but not the dorsomedial striatum (DMS), exhibit a burst of firing at the start of a well-learned action sequence ("task-bracketing"). However, it is currently unclear what information is contained in these bursts. Some theories suggest that these bursts should represent the procedural action sequence itself (that they should be about future action chains), whereas others suggest that they should contain representations of the current state of the world, taking into account primarily past information. In addition, the DLS local field potential shows transient bursts of power in the 50 Hz range (c50) around the time a learned action sequence is initiated. However, it is currently unknown how bursts of activity in DLS cell ensembles and bursts of c50 power in the DLS local field potential are related to each other. We found that DLS bursts at lap initiation in rats represented recently experienced reward locations more than future procedural actions, indicating that task-initiation DLS bursts contain primarily retrospective, rather than prospective, information to guide procedural actions. Furthermore, representations of past reward locations increased during periods of increased c50 power in the DLS. There was no evidence of task-initiation bursts, increased c50 power, or retrospective reward location information in the neighboring dorsomedial striatum. These data support a role for the DLS in model-free theories of procedural decision-making over planned action-chain theories, suggesting that procedural actions derive from representations of the current and recent past.