Prioritized memory access explains planning and hippocampal replay

Abstract

To make decisions, animals must evaluate outcomes of candidate choices by accessing memories of relevant experiences. Yet little is known about which experiences are considered or ignored during deliberation, which ultimately governs choice. Here, we propose a normative theory to predict which memories should be accessed at each moment to optimize future decisions. Using nonlocal \"replay\" of spatial locations in hippocampus as a window into memory access, we simulate a spatial navigation task where an agent accesses memories of locations sequentially, ordered by utility: how much extra reward would be earned due to the computation enabling better choices. This prioritization balances two desiderata: the need to evaluate imminent choices, vs. the gain from propagating newly encountered information to predecessor states. We show that this theory offers a unifying account of a range of hitherto disconnected findings in the place cell literature such as the balance of forward and reverse replay, biases in the replayed content, and effects of experience. Accordingly, various types of nonlocal events during behavior and rest are re-interpreted as instances of a single choice evaluation operation, unifying seemingly disparate proposed functions of replay including planning, learning and consolidation, and whose dysfunction may underlie pathologies like rumination and craving.