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Wake slow waves in focal human epilepsy impact network activity and cognition

Slow waves of neuronal activity are a fundamental component of sleep that are proposed to have homeostatic and restorative functions. Despite this, their interaction with pathology is unclear and there is only indirect evidence of their presence during wakefulness. Using intracortical recordings fro...

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Autores principales: Sheybani, Laurent, Vivekananda, Umesh, Rodionov, Roman, Diehl, Beate, Chowdhury, Fahmida A., McEvoy, Andrew W., Miserocchi, Anna, Bisby, James A., Bush, Daniel, Burgess, Neil, Walker, Matthew C.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Nature Publishing Group UK 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10689494/
https://www.ncbi.nlm.nih.gov/pubmed/38036557
http://dx.doi.org/10.1038/s41467-023-42971-3
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author Sheybani, Laurent
Vivekananda, Umesh
Rodionov, Roman
Diehl, Beate
Chowdhury, Fahmida A.
McEvoy, Andrew W.
Miserocchi, Anna
Bisby, James A.
Bush, Daniel
Burgess, Neil
Walker, Matthew C.
author_facet Sheybani, Laurent
Vivekananda, Umesh
Rodionov, Roman
Diehl, Beate
Chowdhury, Fahmida A.
McEvoy, Andrew W.
Miserocchi, Anna
Bisby, James A.
Bush, Daniel
Burgess, Neil
Walker, Matthew C.
author_sort Sheybani, Laurent
collection PubMed
description Slow waves of neuronal activity are a fundamental component of sleep that are proposed to have homeostatic and restorative functions. Despite this, their interaction with pathology is unclear and there is only indirect evidence of their presence during wakefulness. Using intracortical recordings from the temporal lobe of 25 patients with epilepsy, we demonstrate the existence of local wake slow waves (LoWS) with key features of sleep slow waves, including a down-state of neuronal firing. Consistent with a reduction in neuronal activity, LoWS were associated with slowed cognitive processing. However, we also found that LoWS showed signatures of a homeostatic relationship with interictal epileptiform discharges (IEDs): exhibiting progressive adaptation during the build-up of network excitability before an IED and reducing the impact of subsequent IEDs on network excitability. We therefore propose an epilepsy homeostasis hypothesis: that slow waves in epilepsy reduce aberrant activity at the price of transient cognitive impairment.
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spelling pubmed-106894942023-12-02 Wake slow waves in focal human epilepsy impact network activity and cognition Sheybani, Laurent Vivekananda, Umesh Rodionov, Roman Diehl, Beate Chowdhury, Fahmida A. McEvoy, Andrew W. Miserocchi, Anna Bisby, James A. Bush, Daniel Burgess, Neil Walker, Matthew C. Nat Commun Article Slow waves of neuronal activity are a fundamental component of sleep that are proposed to have homeostatic and restorative functions. Despite this, their interaction with pathology is unclear and there is only indirect evidence of their presence during wakefulness. Using intracortical recordings from the temporal lobe of 25 patients with epilepsy, we demonstrate the existence of local wake slow waves (LoWS) with key features of sleep slow waves, including a down-state of neuronal firing. Consistent with a reduction in neuronal activity, LoWS were associated with slowed cognitive processing. However, we also found that LoWS showed signatures of a homeostatic relationship with interictal epileptiform discharges (IEDs): exhibiting progressive adaptation during the build-up of network excitability before an IED and reducing the impact of subsequent IEDs on network excitability. We therefore propose an epilepsy homeostasis hypothesis: that slow waves in epilepsy reduce aberrant activity at the price of transient cognitive impairment. Nature Publishing Group UK 2023-11-30 /pmc/articles/PMC10689494/ /pubmed/38036557 http://dx.doi.org/10.1038/s41467-023-42971-3 Text en © The Author(s) 2023 https://creativecommons.org/licenses/by/4.0/Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons license and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) .
spellingShingle Article
Sheybani, Laurent
Vivekananda, Umesh
Rodionov, Roman
Diehl, Beate
Chowdhury, Fahmida A.
McEvoy, Andrew W.
Miserocchi, Anna
Bisby, James A.
Bush, Daniel
Burgess, Neil
Walker, Matthew C.
Wake slow waves in focal human epilepsy impact network activity and cognition
title Wake slow waves in focal human epilepsy impact network activity and cognition
title_full Wake slow waves in focal human epilepsy impact network activity and cognition
title_fullStr Wake slow waves in focal human epilepsy impact network activity and cognition
title_full_unstemmed Wake slow waves in focal human epilepsy impact network activity and cognition
title_short Wake slow waves in focal human epilepsy impact network activity and cognition
title_sort wake slow waves in focal human epilepsy impact network activity and cognition
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10689494/
https://www.ncbi.nlm.nih.gov/pubmed/38036557
http://dx.doi.org/10.1038/s41467-023-42971-3
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