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Authors & Affiliations
Ugurcan Mugan, Samantha L. Hoffman, A. David Redish
Abstract
Studies suggest that adaptive behaviors arise from multiple decision systems in the brain, and spatial complexity affects these processes. Three regions are hypothesized to make distinct contributions: hippocampus (HC) — encoding state-space and enabling flexible behaviors, dorsolateral striatum (DLS) — encoding action-chains and enabling automated behaviors, and prefrontal cortex (mPFC) — encoding task-space and strategy-setting. We simultaneously recorded across these regions, and in a separate cohort we chemogenetically inhibited mPFC on a rule-switch task, the left/right/alternation foraging task, where we parametrically varied the environment complexity. Hippocampal time-compressed sequential representations of future positions during theta increased during deliberation and were longer and more prominent in complex environments. In contrast, task-bracketing by DLS ensembles were most prominent in simple environments. Furthermore, task-bracketing was inversely correlated with HC sequence coherence/length in simple environments. In complex environments, DLS ensembles represented multiple action-boundaries aligned to intermediate, distributed decision-points (subgoals). mPFC representations encoded strategy and could be used to predict the length of hippocampal theta sequences. However, the coupling between mPFC and HC state was over longer behaviorally-relevant time scales, implying a role for mPFC in longer-timescale strategy determinations. mPFC changed its firing patterns before HC and DLS around rule switches, further buttressing mPFC’s role in strategy-setting. Inactivation of mPFC with inhibitory DREADDs decreased deliberative behaviors and impaired the ability to recognize task rules and stability, thereby causing acute and long-term performance deficits.Thus, our data show that environmental structure impacts task-relevant representations in HC, DLS, and mPFC, and reveals its impact on the underlying decision-making mechanisms.