Differential effects of reward and navigation history on hippocampal forward and reverse replays

Abstract

Sequential firing patterns of place cells along a spatial trajectory are often replayed during sharp wave ripple (SWR) epochs during awake immobility. These brief sequential burst of spikes can occur both in forward and reverse directions. The functional roles and mechanisms underlying these awake replays are not clear. To obtain better insight into this matter, we examined hippocampal replays in a novel spatial sequence memory task. Reward enhances the rate of reverse replays, but it increases the fidelity of forward replays for recently-travelled as well as other alternative trajectories heading toward a rewarding location. This suggests roles of forward and reverse replays in reinforcing representations for all potential rewarding trajectories. We also found more faithful reactivation of place cell sequences for upcoming rewarding trajectories than already rewarded trajectories in forward replays. This suggests a role of forward replays in preferentially reinforcing representations for high-value trajectories. Our results suggest hippocampal forward and reverse replays may contribute to constructing a map of potential navigation trajectories and their associated values ('value map') via distinct mechanisms.