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

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.