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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Main Authors: Eric W. Moffet, Ruben Verhagen, Benjamin Jones, Graham Findlay, Elsa Juan, Tom Bugnon, Armand Mensen, Mariel Kalkach Aparicio, Rama Maganti, Aaron F. Struck, Giulio Tononi, Melanie Boly
Format: Article
Language:English
Published: Frontiers Media S.A. 2020-10-01
Series:Frontiers in Systems Neuroscience
Subjects:
Online Access:https://www.frontiersin.org/articles/10.3389/fnsys.2020.549309/full
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author Eric W. Moffet
Eric W. Moffet
Ruben Verhagen
Ruben Verhagen
Ruben Verhagen
Benjamin Jones
Benjamin Jones
Graham Findlay
Graham Findlay
Elsa Juan
Elsa Juan
Elsa Juan
Tom Bugnon
Tom Bugnon
Armand Mensen
Mariel Kalkach Aparicio
Rama Maganti
Aaron F. Struck
Giulio Tononi
Melanie Boly
Melanie Boly
spellingShingle Eric W. Moffet
Eric W. Moffet
Ruben Verhagen
Ruben Verhagen
Ruben Verhagen
Benjamin Jones
Benjamin Jones
Graham Findlay
Graham Findlay
Elsa Juan
Elsa Juan
Elsa Juan
Tom Bugnon
Tom Bugnon
Armand Mensen
Mariel Kalkach Aparicio
Rama Maganti
Aaron F. Struck
Giulio Tononi
Melanie Boly
Melanie Boly
Local Sleep Slow-Wave Activity Colocalizes With the Ictal Symptomatogenic Zone in a Patient With Reflex Epilepsy: A High-Density EEG Study
Frontiers in Systems Neuroscience
high-density EEG
reflex epilepsy
sleep
slow-wave activity
delta power
author_facet Eric W. Moffet
Eric W. Moffet
Ruben Verhagen
Ruben Verhagen
Ruben Verhagen
Benjamin Jones
Benjamin Jones
Graham Findlay
Graham Findlay
Elsa Juan
Elsa Juan
Elsa Juan
Tom Bugnon
Tom Bugnon
Armand Mensen
Mariel Kalkach Aparicio
Rama Maganti
Aaron F. Struck
Giulio Tononi
Melanie Boly
Melanie Boly
author_sort Eric W. Moffet
title 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_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_sort local sleep slow-wave activity colocalizes with the ictal symptomatogenic zone in a patient with reflex epilepsy: a high-density eeg study
publisher Frontiers Media S.A.
series Frontiers in Systems Neuroscience
issn 1662-5137
publishDate 2020-10-01
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.
topic high-density EEG
reflex epilepsy
sleep
slow-wave activity
delta power
url https://www.frontiersin.org/articles/10.3389/fnsys.2020.549309/full
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spelling doaj-d97ad8a6bc404572b6faaba23a6c0ecb2020-11-25T03:59:52ZengFrontiers Media S.A.Frontiers in Systems Neuroscience1662-51372020-10-011410.3389/fnsys.2020.549309549309Local Sleep Slow-Wave Activity Colocalizes With the Ictal Symptomatogenic Zone in a Patient With Reflex Epilepsy: A High-Density EEG StudyEric W. Moffet0Eric W. Moffet1Ruben Verhagen2Ruben Verhagen3Ruben Verhagen4Benjamin Jones5Benjamin Jones6Graham Findlay7Graham Findlay8Elsa Juan9Elsa Juan10Elsa Juan11Tom Bugnon12Tom Bugnon13Armand Mensen14Mariel Kalkach Aparicio15Rama Maganti16Aaron F. Struck17Giulio Tononi18Melanie Boly19Melanie Boly20Department of Neurology, University of Wisconsin-Madison, Madison, WI, United StatesKen and Ruth Davee Department of Neurology, Northwestern University Feinberg School of Medicine, Chicago, IL, United StatesDepartment of Neurology, University of Wisconsin-Madison, Madison, WI, United StatesDepartment of Psychiatry, University of Wisconsin-Madison, Madison, WI, United StatesDepartment of Philosophy, Vrije Universiteit Amsterdam, Amsterdam, NetherlandsDepartment of Neurology, University of Wisconsin-Madison, Madison, WI, United StatesDepartment of Psychiatry, University of Wisconsin-Madison, Madison, WI, United StatesDepartment of Neurology, University of Wisconsin-Madison, Madison, WI, United StatesDepartment of Psychiatry, University of Wisconsin-Madison, Madison, WI, United StatesDepartment of Psychiatry, University of Wisconsin-Madison, Madison, WI, United StatesDepartment of Philosophy, Vrije Universiteit Amsterdam, Amsterdam, NetherlandsDepartment of Psychology, University of Amsterdam, Amsterdam, NetherlandsDepartment of Neurology, University of Wisconsin-Madison, Madison, WI, United StatesDepartment of Psychiatry, University of Wisconsin-Madison, Madison, WI, United StatesDepartment of Psychiatry, University of Wisconsin-Madison, Madison, WI, United StatesDepartment of Psychiatry, University of Wisconsin-Madison, Madison, WI, United StatesDepartment of Neurology, University of Wisconsin-Madison, Madison, WI, United StatesDepartment of Neurology, University of Wisconsin-Madison, Madison, WI, United StatesDepartment of Psychiatry, University of Wisconsin-Madison, Madison, WI, United StatesDepartment of Neurology, University of Wisconsin-Madison, Madison, WI, United StatesDepartment of Psychiatry, University of Wisconsin-Madison, Madison, WI, United StatesBackground: 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.https://www.frontiersin.org/articles/10.3389/fnsys.2020.549309/fullhigh-density EEGreflex epilepsysleepslow-wave activitydelta power