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Disruption of Rolandic Gamma-Band Functional Connectivity by Seizures is Associated with Motor Impairments in Children with Epilepsy

Although children with epilepsy exhibit numerous neurological and cognitive deficits, the mechanisms underlying these impairments remain unclear. Synchronization of oscillatory neural activity in the gamma frequency range (>30 Hz) is purported to be a mechanism mediating functional integration wi...

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Autores principales: Ibrahim, George M., Akiyama, Tomoyuki, Ochi, Ayako, Otsubo, Hiroshi, Smith, Mary Lou, Taylor, Margot J., Donner, Elizabeth, Rutka, James T., Snead, O. Carter, Doesburg, Sam M.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Public Library of Science 2012
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3380842/
https://www.ncbi.nlm.nih.gov/pubmed/22737233
http://dx.doi.org/10.1371/journal.pone.0039326
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author Ibrahim, George M.
Akiyama, Tomoyuki
Ochi, Ayako
Otsubo, Hiroshi
Smith, Mary Lou
Taylor, Margot J.
Donner, Elizabeth
Rutka, James T.
Snead, O. Carter
Doesburg, Sam M.
author_facet Ibrahim, George M.
Akiyama, Tomoyuki
Ochi, Ayako
Otsubo, Hiroshi
Smith, Mary Lou
Taylor, Margot J.
Donner, Elizabeth
Rutka, James T.
Snead, O. Carter
Doesburg, Sam M.
author_sort Ibrahim, George M.
collection PubMed
description Although children with epilepsy exhibit numerous neurological and cognitive deficits, the mechanisms underlying these impairments remain unclear. Synchronization of oscillatory neural activity in the gamma frequency range (>30 Hz) is purported to be a mechanism mediating functional integration within neuronal networks supporting cognition, perception and action. Here, we tested the hypothesis that seizure-induced alterations in gamma synchronization are associated with functional deficits. By calculating synchrony among electrodes and performing graph theoretical analysis, we assessed functional connectivity and local network structure of the hand motor area of children with focal epilepsy from intracranial electroencephalographic recordings. A local decrease in inter-electrode phase synchrony in the gamma bands during ictal periods, relative to interictal periods, within the motor cortex was strongly associated with clinical motor weakness. Gamma-band ictal desychronization was a stronger predictor of deficits than the presence of the seizure-onset zone or lesion within the motor cortex. There was a positive correlation between the magnitude of ictal desychronization and impairment of motor dexterity in the contralateral, but not ipsilateral hand. There was no association between ictal desynchronization within the hand motor area and non-motor deficits. This study uniquely demonstrates that seizure-induced disturbances in cortical functional connectivity are associated with network-specific neurological deficits.
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spelling pubmed-33808422012-06-26 Disruption of Rolandic Gamma-Band Functional Connectivity by Seizures is Associated with Motor Impairments in Children with Epilepsy Ibrahim, George M. Akiyama, Tomoyuki Ochi, Ayako Otsubo, Hiroshi Smith, Mary Lou Taylor, Margot J. Donner, Elizabeth Rutka, James T. Snead, O. Carter Doesburg, Sam M. PLoS One Research Article Although children with epilepsy exhibit numerous neurological and cognitive deficits, the mechanisms underlying these impairments remain unclear. Synchronization of oscillatory neural activity in the gamma frequency range (>30 Hz) is purported to be a mechanism mediating functional integration within neuronal networks supporting cognition, perception and action. Here, we tested the hypothesis that seizure-induced alterations in gamma synchronization are associated with functional deficits. By calculating synchrony among electrodes and performing graph theoretical analysis, we assessed functional connectivity and local network structure of the hand motor area of children with focal epilepsy from intracranial electroencephalographic recordings. A local decrease in inter-electrode phase synchrony in the gamma bands during ictal periods, relative to interictal periods, within the motor cortex was strongly associated with clinical motor weakness. Gamma-band ictal desychronization was a stronger predictor of deficits than the presence of the seizure-onset zone or lesion within the motor cortex. There was a positive correlation between the magnitude of ictal desychronization and impairment of motor dexterity in the contralateral, but not ipsilateral hand. There was no association between ictal desynchronization within the hand motor area and non-motor deficits. This study uniquely demonstrates that seizure-induced disturbances in cortical functional connectivity are associated with network-specific neurological deficits. Public Library of Science 2012-06-21 /pmc/articles/PMC3380842/ /pubmed/22737233 http://dx.doi.org/10.1371/journal.pone.0039326 Text en Ibrahim et al. http://creativecommons.org/licenses/by/4.0/ This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are properly credited.
spellingShingle Research Article
Ibrahim, George M.
Akiyama, Tomoyuki
Ochi, Ayako
Otsubo, Hiroshi
Smith, Mary Lou
Taylor, Margot J.
Donner, Elizabeth
Rutka, James T.
Snead, O. Carter
Doesburg, Sam M.
Disruption of Rolandic Gamma-Band Functional Connectivity by Seizures is Associated with Motor Impairments in Children with Epilepsy
title Disruption of Rolandic Gamma-Band Functional Connectivity by Seizures is Associated with Motor Impairments in Children with Epilepsy
title_full Disruption of Rolandic Gamma-Band Functional Connectivity by Seizures is Associated with Motor Impairments in Children with Epilepsy
title_fullStr Disruption of Rolandic Gamma-Band Functional Connectivity by Seizures is Associated with Motor Impairments in Children with Epilepsy
title_full_unstemmed Disruption of Rolandic Gamma-Band Functional Connectivity by Seizures is Associated with Motor Impairments in Children with Epilepsy
title_short Disruption of Rolandic Gamma-Band Functional Connectivity by Seizures is Associated with Motor Impairments in Children with Epilepsy
title_sort disruption of rolandic gamma-band functional connectivity by seizures is associated with motor impairments in children with epilepsy
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3380842/
https://www.ncbi.nlm.nih.gov/pubmed/22737233
http://dx.doi.org/10.1371/journal.pone.0039326
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