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

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 1...

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Published inProceedings of the National Academy of Sciences - PNAS Vol. 118; no. 21; p. 1
Main Authors Skelin, Ivan, Zhang, Haoxin, Zheng, Jie, Ma, Shiting, Mander, Bryce A, Kim McManus, Olivia, Vadera, Sumeet, Knight, Robert T, McNaughton, Bruce L, Lin, Jack J
Format Journal Article
LanguageEnglish
Published United States National Academy of Sciences 25.05.2021
Subjects
Activity patterns
Amygdala
Biological Sciences
Consolidation
Cortex (frontal)
Cortex (temporal)
Coupling
Hippocampus
Modulation
Neural networks
Ripples
Sleep
Synchronism
Synchronization
sleep
slow waves
human brain
spindles
sharp wave/ripples
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Summary: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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Author contributions: I.S. designed research; I.S., O.K.M., S.V., and J.J.L. performed research; H.Z., B.A.M., R.T.K., and B.L.M. contributed new reagents/analytic tools; I.S., J.Z., and S.M. analyzed data; I.S. and J.J.L. wrote the paper; R.T.K. helped with data interpretation; and B.L.M. helped in the interpretation of the results.
Edited by György Buzsáki, New York University Langone Medical Center, New York, NY, and approved March 30, 2021 (received for review June 12, 2020)
ISSN:0027-8424
1091-6490
1091-6490
DOI:10.1073/pnas.2012075118