Hippocampal sharp-wave ripples (SWRs) constitute one of the most synchronized activation events in the brain and play a critical role in offline memory consolidation. Yet their cognitive content and function during awake, conscious behavior remains unclear. We directly examined this question using intracranial recordings in human patients engaged in episodic free recall of previously viewed photographs. Our results reveal a content-selective increase in hippocampal ripple rate emerging 1 to 2 seconds prior to recall events. During recollection, high-order visual areas showed pronounced SWR-coupled reemergence of activation patterns associated with recalled content. Finally, the SWR rate during encoding predicted subsequent free-recall performance. These results point to a role for hippocampal SWRs in triggering spontaneous recollections and orchestrating the reinstatement of cortical representations during free episodic memory retrieval.

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http://dx.doi.org/10.1126/science.aax1030DOI Listing

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Article Synopsis
  • Systems consolidation during sleep involves the interaction between hippocampal sharp-wave ripples (SWRs) and neocortical UP/DOWN states, though the exact coupling mechanisms are still unclear.
  • Research using mouse models shows that there is a precise bidirectional relationship between hippocampal activity and neocortical states, particularly in deep sleep where the retrosplenial cortex (RSC) plays a significant role.
  • The study proposes a model where the hippocampus and RSC interact as weakly coupled, excitable systems that can influence each other, suggesting RSC may help transmit SWRs to neocortex areas by triggering DOWN states.
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