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EEG desynchronization during phasic REM sleep suppresses interictal epileptic activity in humans

OBJECTIVE: Rapid eye movement (REM) sleep has a suppressing effect on epileptic activity. This effect might be directly related to neuronal desynchronization mediated by cholinergic neurotransmission. We investigated whether interictal epileptiform discharges (IEDs) and high frequency oscillations—a...

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Autores principales: Frauscher, Birgit, von Ellenrieder, Nicolás, Dubeau, François, Gotman, Jean
Formato: Online Artículo Texto
Lenguaje:English
Publicado: John Wiley and Sons Inc. 2016
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4949560/
https://www.ncbi.nlm.nih.gov/pubmed/27112123
http://dx.doi.org/10.1111/epi.13389
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author Frauscher, Birgit
von Ellenrieder, Nicolás
Dubeau, François
Gotman, Jean
author_facet Frauscher, Birgit
von Ellenrieder, Nicolás
Dubeau, François
Gotman, Jean
author_sort Frauscher, Birgit
collection PubMed
description OBJECTIVE: Rapid eye movement (REM) sleep has a suppressing effect on epileptic activity. This effect might be directly related to neuronal desynchronization mediated by cholinergic neurotransmission. We investigated whether interictal epileptiform discharges (IEDs) and high frequency oscillations—a biomarker of the epileptogenic zone—are evenly distributed across phasic and tonic REM sleep. We hypothesized that IEDs are more suppressed during phasic REM sleep because of additional cholinergic drive. METHODS: Twelve patients underwent polysomnography during long‐term combined scalp‐intracerebral electroencephalography (EEG) recording. After sleep staging in the scalp EEG, we identified segments of REM sleep with rapid eye movements (phasic REM) and segments of REM sleep without rapid eye movements (tonic REM). In the intracerebral EEG, we computed the power in frequencies <30 Hz and from 30 to 500 Hz, and marked IEDs, ripples (>80 Hz) and fast ripples (>250 Hz). We grouped the intracerebral channels into channels in the seizure‐onset zone (SOZ), the exclusively irritative zone (EIZ), and the normal zone (NoZ). RESULTS: Power in frequencies <30 Hz was lower during phasic than tonic REM sleep (p < 0.001), most likely reflecting increased desynchronization. IEDs, ripples and fast ripples, were less frequent during phasic than tonic REM sleep (phasic REM sleep: 39% of spikes, 35% of ripples, 18% of fast ripples, tonic REM sleep: 61% of spikes, 65% of ripples, 82% of fast ripples; p < 0.001). In contrast to ripples in the epileptogenic zone, physiologic ripples were more abundant during phasic REM sleep (phasic REM sleep: 73% in NoZ, 30% in EIZ, 28% in SOZ, tonic REM sleep: 27% in NoZ, 70% in EIZ, 72% in SOZ; p < 0.001). SIGNIFICANCE: Phasic REM sleep has an enhanced suppressive effect on IEDs, corroborating the role of EEG desynchronization in the suppression of interictal epileptic activity. In contrast, physiologic ripples were increased during phasic REM sleep, possibly reflecting REM‐related memory consolidation and dreaming.
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spelling pubmed-49495602016-07-28 EEG desynchronization during phasic REM sleep suppresses interictal epileptic activity in humans Frauscher, Birgit von Ellenrieder, Nicolás Dubeau, François Gotman, Jean Epilepsia Full‐length Original Research OBJECTIVE: Rapid eye movement (REM) sleep has a suppressing effect on epileptic activity. This effect might be directly related to neuronal desynchronization mediated by cholinergic neurotransmission. We investigated whether interictal epileptiform discharges (IEDs) and high frequency oscillations—a biomarker of the epileptogenic zone—are evenly distributed across phasic and tonic REM sleep. We hypothesized that IEDs are more suppressed during phasic REM sleep because of additional cholinergic drive. METHODS: Twelve patients underwent polysomnography during long‐term combined scalp‐intracerebral electroencephalography (EEG) recording. After sleep staging in the scalp EEG, we identified segments of REM sleep with rapid eye movements (phasic REM) and segments of REM sleep without rapid eye movements (tonic REM). In the intracerebral EEG, we computed the power in frequencies <30 Hz and from 30 to 500 Hz, and marked IEDs, ripples (>80 Hz) and fast ripples (>250 Hz). We grouped the intracerebral channels into channels in the seizure‐onset zone (SOZ), the exclusively irritative zone (EIZ), and the normal zone (NoZ). RESULTS: Power in frequencies <30 Hz was lower during phasic than tonic REM sleep (p < 0.001), most likely reflecting increased desynchronization. IEDs, ripples and fast ripples, were less frequent during phasic than tonic REM sleep (phasic REM sleep: 39% of spikes, 35% of ripples, 18% of fast ripples, tonic REM sleep: 61% of spikes, 65% of ripples, 82% of fast ripples; p < 0.001). In contrast to ripples in the epileptogenic zone, physiologic ripples were more abundant during phasic REM sleep (phasic REM sleep: 73% in NoZ, 30% in EIZ, 28% in SOZ, tonic REM sleep: 27% in NoZ, 70% in EIZ, 72% in SOZ; p < 0.001). SIGNIFICANCE: Phasic REM sleep has an enhanced suppressive effect on IEDs, corroborating the role of EEG desynchronization in the suppression of interictal epileptic activity. In contrast, physiologic ripples were increased during phasic REM sleep, possibly reflecting REM‐related memory consolidation and dreaming. John Wiley and Sons Inc. 2016-04-25 2016-06 /pmc/articles/PMC4949560/ /pubmed/27112123 http://dx.doi.org/10.1111/epi.13389 Text en Wiley Periodicals, Inc. © 2016 The Authors. Epilepsia published by Wiley Periodicals, Inc. on behalf of International League Against Epilepsy. This is an open access article under the terms of the Creative Commons Attribution (http://creativecommons.org/licenses/by/4.0/) License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited.
spellingShingle Full‐length Original Research
Frauscher, Birgit
von Ellenrieder, Nicolás
Dubeau, François
Gotman, Jean
EEG desynchronization during phasic REM sleep suppresses interictal epileptic activity in humans
title EEG desynchronization during phasic REM sleep suppresses interictal epileptic activity in humans
title_full EEG desynchronization during phasic REM sleep suppresses interictal epileptic activity in humans
title_fullStr EEG desynchronization during phasic REM sleep suppresses interictal epileptic activity in humans
title_full_unstemmed EEG desynchronization during phasic REM sleep suppresses interictal epileptic activity in humans
title_short EEG desynchronization during phasic REM sleep suppresses interictal epileptic activity in humans
title_sort eeg desynchronization during phasic rem sleep suppresses interictal epileptic activity in humans
topic Full‐length Original Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4949560/
https://www.ncbi.nlm.nih.gov/pubmed/27112123
http://dx.doi.org/10.1111/epi.13389
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