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Local Sleep Slow-Wave Activity Colocalizes With the Ictal Symptomatogenic Zone in a Patient With Reflex Epilepsy: A High-Density EEG Study

Background: Slow-wave activity (SWA) during non-rapid eye movement (NREM) sleep reflects synaptic potentiation during preceding wakefulness. Epileptic activity may induce increases in state-dependent SWA in human brains, therefore, localization of SWA may prove useful in the presurgical workup of ep...

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Autores principales: Moffet, Eric W., Verhagen, Ruben, Jones, Benjamin, Findlay, Graham, Juan, Elsa, Bugnon, Tom, Mensen, Armand, Aparicio, Mariel Kalkach, Maganti, Rama, Struck, Aaron F., Tononi, Giulio, Boly, Melanie
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2020
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7609881/
https://www.ncbi.nlm.nih.gov/pubmed/33192347
http://dx.doi.org/10.3389/fnsys.2020.549309
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author Moffet, Eric W.
Verhagen, Ruben
Jones, Benjamin
Findlay, Graham
Juan, Elsa
Bugnon, Tom
Mensen, Armand
Aparicio, Mariel Kalkach
Maganti, Rama
Struck, Aaron F.
Tononi, Giulio
Boly, Melanie
author_facet Moffet, Eric W.
Verhagen, Ruben
Jones, Benjamin
Findlay, Graham
Juan, Elsa
Bugnon, Tom
Mensen, Armand
Aparicio, Mariel Kalkach
Maganti, Rama
Struck, Aaron F.
Tononi, Giulio
Boly, Melanie
author_sort Moffet, Eric W.
collection PubMed
description Background: Slow-wave activity (SWA) during non-rapid eye movement (NREM) sleep reflects synaptic potentiation during preceding wakefulness. Epileptic activity may induce increases in state-dependent SWA in human brains, therefore, localization of SWA may prove useful in the presurgical workup of epileptic patients. We analyzed high-density electroencephalography (HDEEG) data across vigilance states from a reflex epilepsy patient with a clearly localizable ictal symptomatogenic zone to provide a proof-of-concept for the testability of this hypothesis. Methods: Overnight HDEEG recordings were obtained in the patient during REM sleep, NREM sleep, wakefulness, and during a right facial motor seizure then compared to 10 controls. After preprocessing, SWA (i.e., delta power; 1–4 Hz) was calculated at each channel. Scalp level and source reconstruction analyses were computed. We assessed for statistical differences in maximum SWA between the patient and controls within REM sleep, NREM sleep, wakefulness, and seizure. Then, we completed an identical statistical comparison after first subtracting intrasubject REM sleep SWA from that of NREM sleep, wakefulness, and seizure SWA. Results: The topographical analysis revealed greater left hemispheric SWA in the patient vs. controls in all vigilance states except REM sleep (which showed a right hemispheric maximum). Source space analysis revealed increased SWA in the left inferior frontal cortex during NREM sleep and wakefulness. Ictal data displayed poor source-space localization. Comparing each state to REM sleep enhanced localization accuracy; the most clearly localizing results were observed when subtracting REM sleep from wakefulness. Conclusion: State-dependent SWA during NREM sleep and wakefulness may help to identify aspects of the potential epileptogenic zone. Future work in larger cohorts may assess the clinical value of sleep SWA to help presurgical planning.
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spelling pubmed-76098812020-11-13 Local Sleep Slow-Wave Activity Colocalizes With the Ictal Symptomatogenic Zone in a Patient With Reflex Epilepsy: A High-Density EEG Study Moffet, Eric W. Verhagen, Ruben Jones, Benjamin Findlay, Graham Juan, Elsa Bugnon, Tom Mensen, Armand Aparicio, Mariel Kalkach Maganti, Rama Struck, Aaron F. Tononi, Giulio Boly, Melanie Front Syst Neurosci Neuroscience Background: Slow-wave activity (SWA) during non-rapid eye movement (NREM) sleep reflects synaptic potentiation during preceding wakefulness. Epileptic activity may induce increases in state-dependent SWA in human brains, therefore, localization of SWA may prove useful in the presurgical workup of epileptic patients. We analyzed high-density electroencephalography (HDEEG) data across vigilance states from a reflex epilepsy patient with a clearly localizable ictal symptomatogenic zone to provide a proof-of-concept for the testability of this hypothesis. Methods: Overnight HDEEG recordings were obtained in the patient during REM sleep, NREM sleep, wakefulness, and during a right facial motor seizure then compared to 10 controls. After preprocessing, SWA (i.e., delta power; 1–4 Hz) was calculated at each channel. Scalp level and source reconstruction analyses were computed. We assessed for statistical differences in maximum SWA between the patient and controls within REM sleep, NREM sleep, wakefulness, and seizure. Then, we completed an identical statistical comparison after first subtracting intrasubject REM sleep SWA from that of NREM sleep, wakefulness, and seizure SWA. Results: The topographical analysis revealed greater left hemispheric SWA in the patient vs. controls in all vigilance states except REM sleep (which showed a right hemispheric maximum). Source space analysis revealed increased SWA in the left inferior frontal cortex during NREM sleep and wakefulness. Ictal data displayed poor source-space localization. Comparing each state to REM sleep enhanced localization accuracy; the most clearly localizing results were observed when subtracting REM sleep from wakefulness. Conclusion: State-dependent SWA during NREM sleep and wakefulness may help to identify aspects of the potential epileptogenic zone. Future work in larger cohorts may assess the clinical value of sleep SWA to help presurgical planning. Frontiers Media S.A. 2020-10-21 /pmc/articles/PMC7609881/ /pubmed/33192347 http://dx.doi.org/10.3389/fnsys.2020.549309 Text en Copyright © 2020 Moffet, Verhagen, Jones, Findlay, Juan, Bugnon, Mensen, Aparicio, Maganti, Struck, Tononi and Boly. http://creativecommons.org/licenses/by/4.0/ This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
spellingShingle Neuroscience
Moffet, Eric W.
Verhagen, Ruben
Jones, Benjamin
Findlay, Graham
Juan, Elsa
Bugnon, Tom
Mensen, Armand
Aparicio, Mariel Kalkach
Maganti, Rama
Struck, Aaron F.
Tononi, Giulio
Boly, Melanie
Local Sleep Slow-Wave Activity Colocalizes With the Ictal Symptomatogenic Zone in a Patient With Reflex Epilepsy: A High-Density EEG Study
title Local Sleep Slow-Wave Activity Colocalizes With the Ictal Symptomatogenic Zone in a Patient With Reflex Epilepsy: A High-Density EEG Study
title_full Local Sleep Slow-Wave Activity Colocalizes With the Ictal Symptomatogenic Zone in a Patient With Reflex Epilepsy: A High-Density EEG Study
title_fullStr Local Sleep Slow-Wave Activity Colocalizes With the Ictal Symptomatogenic Zone in a Patient With Reflex Epilepsy: A High-Density EEG Study
title_full_unstemmed Local Sleep Slow-Wave Activity Colocalizes With the Ictal Symptomatogenic Zone in a Patient With Reflex Epilepsy: A High-Density EEG Study
title_short Local Sleep Slow-Wave Activity Colocalizes With the Ictal Symptomatogenic Zone in a Patient With Reflex Epilepsy: A High-Density EEG Study
title_sort local sleep slow-wave activity colocalizes with the ictal symptomatogenic zone in a patient with reflex epilepsy: a high-density eeg study
topic Neuroscience
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7609881/
https://www.ncbi.nlm.nih.gov/pubmed/33192347
http://dx.doi.org/10.3389/fnsys.2020.549309
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