Abstract
Spatial learning requires remembering and choosing paths to goals. Hippocampal place cells replay spatial paths during immobility in reverse and forward order, offering a potential mechanism. However, how replay supports both goal-directed learning and memory-guided decision making is unclear. We therefore continuously tracked awake replay in the same hippocampal-prefrontal ensembles throughout learning of a spatial alternation task. We found that, during pauses between behavioral trajectories, reverse and forward hippocampal replay supports an internal cognitive search of available past and future possibilities and exhibits opposing learning gradients for prediction of past and future behavioral paths, respectively. Coordinated hippocampal-prefrontal replay distinguished correct past and future paths from alternative choices, suggesting a role in recall of past paths to guide planning of future decisions for spatial working memory. Our findings reveal a learning shift from hippocampal reverse-replay-based retrospective evaluation to forward-replay-based prospective planning, with prefrontal readout of memory-guided paths for learning and decision making.
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•Continuous hippocampal-prefrontal (CA1-PFC) replay tracking during spatial learning•Reverse replay for retrospective evaluation, forward replay for prospective planning•Opposing learning gradients for CA1 reverse- and forward-replay prediction of paths•CA1-PFC replay supports past recall and future decisions for spatial working memory
Shin, Tang, and Jadhav use continuous activity tracking to show that awake CA1 reverse- and forward-replay events predict past and future choices, respectively, with opposing spatial learning gradients. CA1-PFC replay supports recall and planning for spatial working memory tasks.