Coupling between slow-waves and sharp-wave ripples organizes distributed neural activity during sleep in humans

Abstract:

Hippocampal-dependent memory consolidation during sleep is hypothesized to depend on the synchronization of distributed neuronal ensembles, organized by the hippocampal sharp-wave ripples (SWRs, 80-150 Hz) and subcortical/cortical slow-waves (0.5-4 Hz). However, the precise role of SWR-slow-wave interactions in synchronizing subcortical/cortical neuronal activity is unclear. Here, we leverage intracranial electrophysiological recordings from the human hippocampus, amygdala, temporal and frontal cortices, to examine activity modulation and cross-regional coordination during SWRs. Hippocampal SWRs are associated with widespread modulation of high frequency activity (HFA; 70-200 Hz) a measure of local neuronal activation. This peri-SWR HFA modulation is predicted by the coupling between hippocampal SWRs and local subcortical/cortical slow-waves. Finally, local cortical slow-wave phase offsets during SWRs predicted functional connectivity between the frontal and temporal cortex. These findings suggest a selection mechanism wherein hippocampal SWR and cortical slow-wave synchronization governs the transient engagement of distributed neuronal populations supporting hippocampal-dependent memory consolidation.

Authors:

  • Ivan Skelin

  • Haoxin Zhang

  • Jie Zheng

  • Shiting Ma

  • Bryce A Mander

  • Olivia Kim Mcmanus

  • Sumeet Vadera

  • Robert T Knight

  • Bruce L McNaughton

  • Jack J Lin

Date: 2020

DOI: https://doi.org/10.1101/2020.05.24.113480

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