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Widespread ripples synchronize human cortical activity during sleep, waking, and memory recall

Declarative memory encoding, consolidation, and retrieval require the integration of elements encoded in widespread cortical locations. The mechanism whereby such “binding” of different components of mental events into unified representations occurs is unknown. The “binding-by-synchrony” theory prop...

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Autores principales: Dickey, Charles W., Verzhbinsky, Ilya A., Jiang, Xi, Rosen, Burke Q., Kajfez, Sophie, Stedelin, Brittany, Shih, Jerry J., Ben-Haim, Sharona, Raslan, Ahmed M., Eskandar, Emad N., Gonzalez-Martinez, Jorge, Cash, Sydney S., Halgren, Eric
Formato: Online Artículo Texto
Lenguaje:English
Publicado: National Academy of Sciences 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9282280/
https://www.ncbi.nlm.nih.gov/pubmed/35867767
http://dx.doi.org/10.1073/pnas.2107797119
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author Dickey, Charles W.
Verzhbinsky, Ilya A.
Jiang, Xi
Rosen, Burke Q.
Kajfez, Sophie
Stedelin, Brittany
Shih, Jerry J.
Ben-Haim, Sharona
Raslan, Ahmed M.
Eskandar, Emad N.
Gonzalez-Martinez, Jorge
Cash, Sydney S.
Halgren, Eric
author_facet Dickey, Charles W.
Verzhbinsky, Ilya A.
Jiang, Xi
Rosen, Burke Q.
Kajfez, Sophie
Stedelin, Brittany
Shih, Jerry J.
Ben-Haim, Sharona
Raslan, Ahmed M.
Eskandar, Emad N.
Gonzalez-Martinez, Jorge
Cash, Sydney S.
Halgren, Eric
author_sort Dickey, Charles W.
collection PubMed
description Declarative memory encoding, consolidation, and retrieval require the integration of elements encoded in widespread cortical locations. The mechanism whereby such “binding” of different components of mental events into unified representations occurs is unknown. The “binding-by-synchrony” theory proposes that distributed encoding areas are bound by synchronous oscillations enabling enhanced communication. However, evidence for such oscillations is sparse. Brief high-frequency oscillations (“ripples”) occur in the hippocampus and cortex and help organize memory recall and consolidation. Here, using intracranial recordings in humans, we report that these ∼70-ms-duration, 90-Hz ripples often couple (within ±500 ms), co-occur (≥ 25-ms overlap), and, crucially, phase-lock (have consistent phase lags) between widely distributed focal cortical locations during both sleep and waking, even between hemispheres. Cortical ripple co-occurrence is facilitated through activation across multiple sites, and phase locking increases with more cortical sites corippling. Ripples in all cortical areas co-occur with hippocampal ripples but do not phase-lock with them, further suggesting that cortico-cortical synchrony is mediated by cortico-cortical connections. Ripple phase lags vary across sleep nights, consistent with participation in different networks. During waking, we show that hippocampo-cortical and cortico-cortical coripples increase preceding successful delayed memory recall, when binding between the cue and response is essential. Ripples increase and phase-modulate unit firing, and coripples increase high-frequency correlations between areas, suggesting synchronized unit spiking facilitating information exchange. co-occurrence, phase synchrony, and high-frequency correlation are maintained with little decrement over very long distances (25 cm). Hippocampo-cortico-cortical coripples appear to possess the essential properties necessary to support binding by synchrony during memory retrieval and perhaps generally in cognition.
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spelling pubmed-92822802022-07-15 Widespread ripples synchronize human cortical activity during sleep, waking, and memory recall Dickey, Charles W. Verzhbinsky, Ilya A. Jiang, Xi Rosen, Burke Q. Kajfez, Sophie Stedelin, Brittany Shih, Jerry J. Ben-Haim, Sharona Raslan, Ahmed M. Eskandar, Emad N. Gonzalez-Martinez, Jorge Cash, Sydney S. Halgren, Eric Proc Natl Acad Sci U S A Biological Sciences Declarative memory encoding, consolidation, and retrieval require the integration of elements encoded in widespread cortical locations. The mechanism whereby such “binding” of different components of mental events into unified representations occurs is unknown. The “binding-by-synchrony” theory proposes that distributed encoding areas are bound by synchronous oscillations enabling enhanced communication. However, evidence for such oscillations is sparse. Brief high-frequency oscillations (“ripples”) occur in the hippocampus and cortex and help organize memory recall and consolidation. Here, using intracranial recordings in humans, we report that these ∼70-ms-duration, 90-Hz ripples often couple (within ±500 ms), co-occur (≥ 25-ms overlap), and, crucially, phase-lock (have consistent phase lags) between widely distributed focal cortical locations during both sleep and waking, even between hemispheres. Cortical ripple co-occurrence is facilitated through activation across multiple sites, and phase locking increases with more cortical sites corippling. Ripples in all cortical areas co-occur with hippocampal ripples but do not phase-lock with them, further suggesting that cortico-cortical synchrony is mediated by cortico-cortical connections. Ripple phase lags vary across sleep nights, consistent with participation in different networks. During waking, we show that hippocampo-cortical and cortico-cortical coripples increase preceding successful delayed memory recall, when binding between the cue and response is essential. Ripples increase and phase-modulate unit firing, and coripples increase high-frequency correlations between areas, suggesting synchronized unit spiking facilitating information exchange. co-occurrence, phase synchrony, and high-frequency correlation are maintained with little decrement over very long distances (25 cm). Hippocampo-cortico-cortical coripples appear to possess the essential properties necessary to support binding by synchrony during memory retrieval and perhaps generally in cognition. National Academy of Sciences 2022-07-07 2022-07-12 /pmc/articles/PMC9282280/ /pubmed/35867767 http://dx.doi.org/10.1073/pnas.2107797119 Text en Copyright © 2022 the Author(s). Published by PNAS. https://creativecommons.org/licenses/by-nc-nd/4.0/This open access article is distributed under Creative Commons Attribution-NonCommercial-NoDerivatives License 4.0 (CC BY-NC-ND) (https://creativecommons.org/licenses/by-nc-nd/4.0/) .
spellingShingle Biological Sciences
Dickey, Charles W.
Verzhbinsky, Ilya A.
Jiang, Xi
Rosen, Burke Q.
Kajfez, Sophie
Stedelin, Brittany
Shih, Jerry J.
Ben-Haim, Sharona
Raslan, Ahmed M.
Eskandar, Emad N.
Gonzalez-Martinez, Jorge
Cash, Sydney S.
Halgren, Eric
Widespread ripples synchronize human cortical activity during sleep, waking, and memory recall
title Widespread ripples synchronize human cortical activity during sleep, waking, and memory recall
title_full Widespread ripples synchronize human cortical activity during sleep, waking, and memory recall
title_fullStr Widespread ripples synchronize human cortical activity during sleep, waking, and memory recall
title_full_unstemmed Widespread ripples synchronize human cortical activity during sleep, waking, and memory recall
title_short Widespread ripples synchronize human cortical activity during sleep, waking, and memory recall
title_sort widespread ripples synchronize human cortical activity during sleep, waking, and memory recall
topic Biological Sciences
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9282280/
https://www.ncbi.nlm.nih.gov/pubmed/35867767
http://dx.doi.org/10.1073/pnas.2107797119
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