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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...
Autores principales: | , , , , , , , , , , , , |
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Formato: | Online Artículo Texto |
Lenguaje: | English |
Publicado: |
National Academy of Sciences
2022
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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. |
format | Online Article Text |
id | pubmed-9282280 |
institution | National Center for Biotechnology Information |
language | English |
publishDate | 2022 |
publisher | National Academy of Sciences |
record_format | MEDLINE/PubMed |
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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