Hippocampal replay repairs the cognitive map for flexible planning

Abstract

Hippocampal replay is structured: prospective replay typically precedes retrospective replay, each aligns with the animal's future and past paths, and replay sometimes targets abandoned goals. We propose that replay repairs the cognitive map. A map that supports efficient planning precomputes expected paths; because plans terminate at the goal, the goal is part of the structure it represents. Every goal change therefore leaves the map incorrect and requires two repairs: one for the goal adopted, one for the goal left behind. The larger is expressed first, and the path each takes determines what it depicts, accounting for replay's ordering, direction, and paradoxical content. The model also generates the predictions that this ordering should invert when past and future paths converge. Recordings from rats foraging in an open arena confirm this: replay order is not as fixed as previously believed, but varies with trajectory geometry and the proximity of the abandoned goal.