The hippocampus has long been known to be involved in spatial navigational learning in rodents, and in memory for events in rodents, primates and humans. A unifying property of both navigation and event memory is a requirement for dealing with temporally sequenced information. Reactivation of temporally sequenced memories for previous behavioural experiences has been reported in sleep in rats. Here we report that sequential replay occurs in the rat hippocampus during awake periods immediately after spatial experience. This replay has a unique form, in which recent episodes of spatial experience are replayed in a temporally reversed order. This replay is suggestive of a role in the evaluation of event sequences in the manner of reinforcement learning models. We propose that such replay might constitute a general mechanism of learning and memory.

Effective navigation requires planning extended routes to remembered goal locations. Hippocampal place cells have been proposed to play a role in navigational planning but direct evidence has been lacking. Here, we show that prior to goal-directed navigation in an open arena, the hippocampus generates brief sequences encoding spatial trajectories strongly biased to progress from the subject’s current location to a known goal location. These sequences predict immediate future behavior, even in cases when the specific combination of start and goal locations is novel. These results suggest that hippocampal sequence events previously characterized in linearly constrained environments as ‘replay’ are also capable of supporting a goal-directed, trajectory-finding mechanism, which identifies important places and relevant behavioral paths, at specific times when memory retrieval is required, and in a manner which could be used to control subsequent navigational behavior.

Summary Hippocampal replays are episodes of sequential place cell activity during sharp wave ripple oscillations (SWRs). Conflicting hypotheses implicate awake replay in learning from rewards, and in memory retrieval for decision-making. Further, awake replays can be forwards, in the same order as experienced, or reverse, in the opposite order. However, while the presence or absence of reward has been reported to modulate SWR rate, the effect of reward changes on replay, and on replay direction in particular, have not been examined. Here we report divergence in the response of forwards and reverse replays to changing reward. While both classes of replays were observed at reward locations, only reverse replays increased their rate at increased reward, or decreased their rate at decreased reward, while forward replays were unchanged. These data demonstrate a unique relationship between reverse replay and reward processing, and point to a functional distinction between different directions of replay.