Hippocampal sharp-wave ripples linked to visual episodic recollection in humans

Sharp-wave ripples in the hippocampus

What are the brain mechanisms responsible for episodic memory retrieval? Norman et al. investigated epilepsy patients who had electrodes implanted in the hippocampus and a variety of cortical areas. Using a visual learning paradigm, they examined the temporal relationship between the incidence of hippocampal sharp-wave ripples and recall. Effective encoding of visual information was associated with higher incidence of ripples. Successful recall was preceded by an increased probability of ripples, which were also associated with transient reemergence of activation patterns in higher visual cortical areas. Hippocampal ripples may thus boost recollections during episodic memory retrieval.

Science, this issue p. eaax1030

Structured Abstract

INTRODUCTION

Sharp-wave ripples (SWRs) are rapid bursts of synchronized neuronal activity elicited by the hippocampus. Extensive study of SWRs, mainly in the rodent brain, has linked these bursts to navigation, memory formation, and offline memory consolidation. However, fundamental questions remain regarding the functional meaning of this striking example of network synchrony. Perhaps the most glaring unknown is the relationship between SWRs and conscious cognition. We still do not know what cognitive process, if any, is linked to the emergence of SWRs; to put it simply, we still do not know what an animal thinks about (if anything) when the hippocampus elicits a ripple. Furthermore, the potential role of SWRs in human episodic memory is still largely unknown. Thus, studying this phenomenon in conscious, awake human patients opens a unique window, as it allows direct examination of detailed verbal reports with respect to SWR occurrences.

RATIONALE

We took advantage of the unique ability of humans to communicate verbally about their inner cognitive state to examine the role of SWRs in memory formation and retrieval, using intracranial electrophysiological recordings in patients. This approach allowed us to study free recall, the process of self-initiated, internal generation of memories. It is a uniquely powerful approach because it isolates the process of recall from external stimulation.

RESULTS

Our study revealed three major aspects linking SWRs to human declarative memory. First, the SWR rate during picture viewing (i.e., memory encoding) predicted subjects’ subsequent free-recall performance. Second, a transient increase in SWR rate preceded the verbal report of recall by 1 to 2 s. This increase was content-selective, recapitulating the same picture preferences observed during viewing. Finally, during recollection, high-order visual areas showed content-selective reactivation coupled to SWR emission.

CONCLUSION

By direct recordings of electrophysiological events in the brains of individuals who could inform, in real time, on their cognitive state, we were able to demonstrate and characterize an important role of SWRs in human episodic memory. Our findings point to the involvement of hippocampal SWRs in establishing and triggering spontaneous recollections in the human brain. They implicate SWRs in the process of engraving new memories, and reveal their fundamental contribution in orchestrating the dialogue between memory centers (hippocampus) and high-level representations (cerebral cortex), which underlies the retrieval of these memories. Our study thus highlights the function of SWRs as powerful multitasking signals that contribute both to the encoding and to the spontaneous access and reinstatement of human memories.

Memory reactivation coupled to hippocampal ripples during free recall.

(A) Simultaneous intracranial recordings in hippocampus and cortex. (B) Patients first viewed and then freely recalled photographs of famous faces and places. (C) Rapid hippocampal neuronal bursts (SWRs) were identified (left). When patients freely recalled the images, a transient increase in SWR rate anticipated the onset of recall, dominated by items that generated a higher ripple rate (RR) during viewing (compare red and black lines). (D) Visual areas in the cortex showed SWR-coupled reactivation, recapitulating the content selectivity observed during viewing.

Abstract

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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