Dorsolateral Striatal Task-initiation Bursts Represent Past Experiences More than Future Action Plans

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 (γ50) 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 γ50 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 γ50 power in the DLS. There was no evidence of task-initiation bursts, increased γ50 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.SIGNIFICANCE STATEMENT While it is well-established that the dorsolateral striatum (DLS) plays a critical role in procedural decision-making, open questions remain about the kinds of representations contained in DLS ensemble activity that guide procedural actions. We found that DLS, but not DMS, cell ensembles contained nonlocal representations of past reward locations that appear moments before task-initiation DLS bursts. These retrospective representations were temporally linked to a rise in γ50 power that also preceded the characteristic DLS burst at task-initiation. These results support models of procedural decision-making based on associations between available actions and the current state of the world over models based on planning over action-chains.