Abstract
Hippocampal cells are central to spatial and predictive representations, and experience replays by place cells are crucial for learning and memory. Nonetheless, how hippocampal replay patterns dynamically change during the learning process remains to be elucidated. Here, we designed a spatial task in which rats learned a new behavioral trajectory for reward. We found that as rats updated their behavioral strategies for a novel salient location, hippocampal cell ensembles increased theta-sequences and sharp wave ripple-associated synchronous spikes that preferentially replayed salient locations and reward-related contexts in reverse order. The directionality and contents of the replays progressively varied with learning, including an optimized path that had never been exploited by the animals, suggesting prioritized replays of significant experiences on a predictive map. Online feedback blockade of sharp wave ripples during a learning process inhibited stabilizing optimized behavior. These results implicate learning-associated experience replays that act to learn and reinforce specific behavioral strategies.
Highlights
| | | | hippocampus replay place cell learning ripple observations have demonstrated that the receipt of reward or novel experiences leads to increased rates of sharp wave ripples (SWRs) and coordinated reactivation of place cells [6, 14], and increased reward leads to increased reverse replays [4, 15]
In addition to these map representations, hippocampal place cells that encode animals’ past or future trajectories are sequentially activated during sharp wave ripples (SWRs) within a short time window (∼100 ms) in a phenomenon known as “place cell replays” [3,4,5]
The frequencies of synchronous events and SWRs in the learning and postlearning phases were quantified by the hierarchical Bayesian modeling with Markov chain Monte Carlo (MCMC) methods to take differences in the number of trials and events across individual rats into account (SI Appendix, Fig. S6E). We found that these events became noticeably higher in the open field and goal area compared with the prelearning phase (Fig. 3 B–D and SI Appendix, Fig. S7J)
Summary
| | | | hippocampus replay place cell learning ripple observations have demonstrated that the receipt of reward or novel experiences leads to increased rates of SWRs and coordinated reactivation of place cells [6, 14], and increased reward leads to increased reverse replays [4, 15]. When agents encounter a prediction error, such as a change in reward, experience replays may be an efficient mechanism for the evaluation of their experienced action–outcome associations by providing a solution to the temporal credit assignment problem, which is helpful to update their behavioral policy to maximize future reward [12, 13].
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