Abstract

Sleep is pivotal for memory consolidation. According to two-stage accounts, memory traces are gradually translocated from hippocampus to neocortex during non-rapid-eye-movement (NREM) sleep. Mechanistically, this information transfer is thought to rely on interactions between thalamocortical spindles and hippocampal ripples. To test this hypothesis, we analyzed intracranial and scalp Electroencephalography sleep recordings from pre-surgical epilepsy patients. We first observed a concurrent spindle power increase in hippocampus (HIPP) and neocortex (NC) time-locked to individual hippocampal ripple events. Coherence analysis confirmed elevated levels of hippocampal-neocortical spindle coupling around ripples, with directionality analyses indicating an influence from NC to HIPP. Importantly, these hippocampal-neocortical dynamics were particularly pronounced during long-duration compared to short-duration ripples. Together, our findings reveal a potential mechanism underlying active consolidation, comprising a neocortical-hippocampal-neocortical reactivation loop initiated by the neocortex. This hippocampal-cortical dialogue is mediated by sleep spindles and is enhanced during long-duration hippocampal ripples.

Highlights

  • Information transfer during sleep is thought to rely on systematic interactions of the cardinal nonrapid-eye-movement (NREM) sleep rhythms (Diekelmann and Born, 2010; Klinzing et al, 2019): First, the cortical

  • sharp-wave ripples (SW-Rs) are transient network oscillations in the hippocampal CA1 subfield emerging from recurrent interactions within CA3 and consist of a brief 80–200 Hz ripple-burst superimposed on a sharp wave, with the latter characterized by a peak frequency of ~3 Hz in humans (Axmacher et al, 2008; Helfrich et al, 2019; Jiang et al, 2019a; Norman et al, 2019; Staresina et al, 2015)

  • Results were statistically compared to time-frequency representations (TFRs) obtained from control events, that is, matched ripple-free intervals randomly drawn from NREM sleep

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Summary

Introduction

Information transfer during sleep is thought to rely on systematic interactions of the cardinal nonrapid-eye-movement (NREM) sleep rhythms (Diekelmann and Born, 2010; Klinzing et al, 2019): First, the cortical

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