Single-trial dynamics of hippocampal spatial representations are modulated by reward value

Abstract

Reward value is known to modulate learning speed in spatial memory tasks, but little is known about its influence on the dynamical changes in hippocampal spatial representations. Here, we monitored the trial-to-trial changes in hippocampal place cell activity during the acquisition of place-reward associations with varying reward size. We show a faster reorganization and stabilization of the hippocampal place map when a goal location is associated with a large reward. The reorganization is driven by both rate changes and the appearance and disappearance of place fields. The occurrence of hippocampal replay activity largely followed the dynamics of changes in spatial representations. Replay patterns became more selectively tuned toward behaviorally relevant experiences over the course of learning via the refined contributions of specific cell subpopulations. These results suggest that high reward value enhances memory retention by accelerating the formation and stabilization of the hippocampal cognitive map and selectively enhancing its reactivation during learning.

Keywords: hippocampus; learning; place cells; replay; reward.