Task Demands Predict a Dynamic Switch in the Content of Awake Hippocampal Replay

Summary

Reactivation of hippocampal place cell sequences during behavioral immobility and rest has been linked with both memory consolidation and navigational planning. Yet it remains to be investigated whether these functions are temporally segregated, occurring during different behavioral states. During a self-paced spatial task, awake hippocampal replay occurring either immediately before movement toward a reward location or just after arrival at a reward location preferentially involved cells consistent with the current trajectory. In contrast, during periods of extended immobility, no such biases were evident. Notably, the occurrence of task-focused reactivations predicted the accuracy of subsequent spatial decisions. Additionally, during immobility, but not periods preceding or succeeding movement, grid cells in deep layers of the entorhinal cortex replayed coherently with the hippocampus. Thus, hippocampal reactivations dynamically and abruptly switch between operational modes in response to task demands, plausibly moving from a state favoring navigational planning to one geared toward memory consolidation.

Highlights

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  Place cell replay content varies between periods of task engagement and disengagement

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  Upon arrival/before departure from reward sites, replay depicts task-relevant places

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  No such bias was observed during periods of extended immobility

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  Grid cells from deep MEC were coherent with place cells during extended stops

Abstract

Ólafsdóttir et al. found that, upon arrival at and before departure from reward sites, but not during immobility, hippocampal replay depicts places related to current task demands. Occurrence of task-focused replay predicts decision accuracy. Grid cells were only coherent with replay during immobility.