Prioritized experience replays on a hippocampal predictive map for learning

Proc Natl Acad Sci U S A. 2021 Jan 5;118(1):e2011266118. doi: 10.1073/pnas.2011266118. Epub 2020 Dec 18.

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.

Keywords: hippocampus; learning; place cell; replay; ripple.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Brain / metabolism
  • Brain / physiology
  • Hippocampus / metabolism*
  • Hippocampus / physiology
  • Learning / physiology*
  • Male
  • Memory / physiology
  • Neurons / physiology
  • Place Cells / metabolism
  • Rats
  • Rats, Long-Evans
  • Reinforcement, Psychology
  • Reward
  • Spatial Learning / physiology*