4.8 Article

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

Publisher

NATL ACAD SCIENCES
DOI: 10.1073/pnas.2012075118

Keywords

sharp wave; ripples; slow waves; spindles; sleep; human brain

Funding

  1. Extreme Science and Engineering Discovery Environment Support Grant [IBN180014]
  2. NSF [1631465]
  3. Defense Advanced Research Projects Agency [HR0011-18-2-0021]
  4. NIH [1U19NS107609-01]
  5. National Institute of Neurological Disorders and Stroke (NINDS) [NS21135]
  6. NINDS [U01-NS108916]
  7. Roneet Carmell Memorial Endowment Fund

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Studies suggest that during sleep, hippocampal sharp-wave ripples and other neural activities can modulate widespread high-frequency activity, predicting coordinated activity between different brain regions. These findings imply a mechanism where hippocampal and cortical slow-wave synchronization supports memory consolidation.
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 to 150 Hz), subcortical/cortical slow-wave activity (SWA, 0.5 to 4 Hz), and sleep spindles (SP, 7 to 15 Hz). However, the precise role of these interactions in synchronizing subcortical/cortical neuronal activity is unclear. Here, we leverage intracranial electrophysiological recordings from the human hippocampus, amygdala, and 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 to 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 SWA or SP. Finally, local cortical SWA phase offsets and SWR amplitudes predicted functional connectivity between the frontal and temporal cortex during individual SWRs. 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.

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