How do hippocampal replay patterns dynamically change during the spatial learning process

Hideyoshi Igata, Yuji Ikegaya, Takuya Sasaki. Prioritized experience replays on a hippocampal predictive map for learning. Proceedings of the National Academy of Sciences Jan 2021, 118 (1) e2011266118; DOI: 10.1073/pnas.2011266118

Significance

The hippocampus is crucial for spatial learning but their neuronal mechanisms remain unknown. Here, we found that hippocampal cell ensembles preferentially replayed salient reward-related locations as rats learned a new behavioral trajectory for reward. The contents of these hippocampal replays progressively varied with learning. Especially during learning, hippocampal neurons even replayed an optimized path that had never been exploited by the animals. The learning-related hippocampal activity was necessary for the stabilization of spatial behavior. These results suggest prioritized replays of significant experiences on a predictive map by hippocampal neurons.“

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.“

Hideyoshi Igata, Yuji Ikegaya, Takuya Sasaki. Prioritized experience replays on a hippocampal predictive map for learning. Proceedings of the National Academy of Sciences Jan 2021, 118 (1) e2011266118; DOI: 10.1073/pnas.2011266118