Hippocampal gamma and sharp wave/ripples mediate bidirectional interactions with cortical networks during sleep

Proc Natl Acad Sci U S A. 2022 Nov;119(44):e2204959119. doi: 10.1073/pnas.2204959119. Epub 2022 Oct 24.

Abstract

Hippocampus-neocortex interactions during sleep are critical for memory processes: Hippocampally initiated replay contributes to memory consolidation in the neocortex and hippocampal sharp wave/ripples modulate cortical activity. Yet, the spatial and temporal patterns of this interaction are unknown. With voltage imaging, electrocorticography, and laminarly resolved hippocampal potentials, we characterized cortico-hippocampal signaling during anesthesia and nonrapid eye movement sleep. We observed neocortical activation transients, with statistics suggesting a quasi-critical regime, may be helpful for communication across remote brain areas. From activity transients, we identified, in a data-driven fashion, three functional networks. A network overlapping with the default mode network and centered on retrosplenial cortex was the most associated with hippocampal activity. Hippocampal slow gamma rhythms were strongly associated to neocortical transients, even more than ripples. In fact, neocortical activity predicted hippocampal slow gamma and followed ripples, suggesting that consolidation processes rely on bidirectional signaling between hippocampus and neocortex.

Keywords: cortical networks; default mode network; gamma oscillations; hippocampus; memory consolidation.

Publication types

  • Research Support, Non-U.S. Gov't
  • Research Support, U.S. Gov't, Non-P.H.S.
  • Research Support, N.I.H., Extramural

MeSH terms

  • Gamma Rhythm
  • Hippocampus / physiology
  • Memory / physiology
  • Memory Consolidation*
  • Neocortex* / physiology
  • Sleep / physiology