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Response inhibition alterations in migraine: evidence from event-related potentials and evoked oscillations

BACKGROUND: Migraine is characterized by a hypersensitivity to environmental stimulation which climaxes during headache attacks but persists during attack-free period. Despite ongoing debates about the nature of the mechanisms giving rise to this abnormality, the presence of deficient inhibitory cor...

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Autores principales: Chen, Guoliang, Li, Yansong, Dong, Zhao, Wang, Rongfei, Zhao, Dengfa, Obeso, Ignacio, Yu, Shengyuan
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Springer Milan 2020
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7531083/
https://www.ncbi.nlm.nih.gov/pubmed/33008328
http://dx.doi.org/10.1186/s10194-020-01187-2
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author Chen, Guoliang
Li, Yansong
Dong, Zhao
Wang, Rongfei
Zhao, Dengfa
Obeso, Ignacio
Yu, Shengyuan
author_facet Chen, Guoliang
Li, Yansong
Dong, Zhao
Wang, Rongfei
Zhao, Dengfa
Obeso, Ignacio
Yu, Shengyuan
author_sort Chen, Guoliang
collection PubMed
description BACKGROUND: Migraine is characterized by a hypersensitivity to environmental stimulation which climaxes during headache attacks but persists during attack-free period. Despite ongoing debates about the nature of the mechanisms giving rise to this abnormality, the presence of deficient inhibitory cortical processes has been proposed to be one possible mechanism underlying its pathogenesis. Empirical evidence supporting this claim is mainly based on previous accounts showing functional cortical disexcitability in the sensory domain. Considering that a general inhibitory control process can play an important role across early to later stage of information processing, this may indicate the important role other dimensions of inhibitory control can play in migraine disability. The present study examined the pathophysiological features of inhibitory control that takes place during suppression of prepotent responses in migraineurs. METHODS: Twenty-two patients with migraine without aura (mean age = 30.86 ± 5.69 years; 19 females) during the interictal period and 25 healthy controls (mean age = 30.24 ± 3.52 years; 18 females) were recruited. We used a stop signal task in combination with event-related potentials (ERPs) to examine participants’ neural activity supporting response inhibition. RESULTS: Behaviorally, migraineurs exhibited prolonged stop signal reaction times relative to healthy controls. At the neural level, the amplitude of the stop-N2 over fronto-central, central and centro-parietal scalp regions, a component of the ERPs related to conflict monitoring during early, non-motoric stages of inhibition, was significantly increased in migraineurs. Meanwhile, the amplitude of the stop-P3 over central and centro-parietal scalp regions, a component of the ERPs reflecting late-stage inhibition of the motor system and cognitive evaluation of motor inhibition, was also significantly increased in migraineurs. Ultimately, our time-frequency analysis further revealed increased delta activity in migraineurs. CONCLUSIONS: Consistent with the theory that alterations in cognitive cortical processes are a key signature of migraine, our findings revealed an abnormal state of suppressing prepotent responses in migraineurs, which can be attributed to cortical disexcitability of the pre-frontal executive network and centro-parietal sensorimotor network. These novel findings extend to show the existence of dysfunctional inhibition control that occurs during suppression of prepotent responses in migraneurs.
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spelling pubmed-75310832020-10-05 Response inhibition alterations in migraine: evidence from event-related potentials and evoked oscillations Chen, Guoliang Li, Yansong Dong, Zhao Wang, Rongfei Zhao, Dengfa Obeso, Ignacio Yu, Shengyuan J Headache Pain Research Article BACKGROUND: Migraine is characterized by a hypersensitivity to environmental stimulation which climaxes during headache attacks but persists during attack-free period. Despite ongoing debates about the nature of the mechanisms giving rise to this abnormality, the presence of deficient inhibitory cortical processes has been proposed to be one possible mechanism underlying its pathogenesis. Empirical evidence supporting this claim is mainly based on previous accounts showing functional cortical disexcitability in the sensory domain. Considering that a general inhibitory control process can play an important role across early to later stage of information processing, this may indicate the important role other dimensions of inhibitory control can play in migraine disability. The present study examined the pathophysiological features of inhibitory control that takes place during suppression of prepotent responses in migraineurs. METHODS: Twenty-two patients with migraine without aura (mean age = 30.86 ± 5.69 years; 19 females) during the interictal period and 25 healthy controls (mean age = 30.24 ± 3.52 years; 18 females) were recruited. We used a stop signal task in combination with event-related potentials (ERPs) to examine participants’ neural activity supporting response inhibition. RESULTS: Behaviorally, migraineurs exhibited prolonged stop signal reaction times relative to healthy controls. At the neural level, the amplitude of the stop-N2 over fronto-central, central and centro-parietal scalp regions, a component of the ERPs related to conflict monitoring during early, non-motoric stages of inhibition, was significantly increased in migraineurs. Meanwhile, the amplitude of the stop-P3 over central and centro-parietal scalp regions, a component of the ERPs reflecting late-stage inhibition of the motor system and cognitive evaluation of motor inhibition, was also significantly increased in migraineurs. Ultimately, our time-frequency analysis further revealed increased delta activity in migraineurs. CONCLUSIONS: Consistent with the theory that alterations in cognitive cortical processes are a key signature of migraine, our findings revealed an abnormal state of suppressing prepotent responses in migraineurs, which can be attributed to cortical disexcitability of the pre-frontal executive network and centro-parietal sensorimotor network. These novel findings extend to show the existence of dysfunctional inhibition control that occurs during suppression of prepotent responses in migraneurs. Springer Milan 2020-10-02 /pmc/articles/PMC7531083/ /pubmed/33008328 http://dx.doi.org/10.1186/s10194-020-01187-2 Text en © The Author(s) 2020 Open AccessThis 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 licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence 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 licence, visit http://creativecommons.org/licenses/by/4.0/. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated in a credit line to the data.
spellingShingle Research Article
Chen, Guoliang
Li, Yansong
Dong, Zhao
Wang, Rongfei
Zhao, Dengfa
Obeso, Ignacio
Yu, Shengyuan
Response inhibition alterations in migraine: evidence from event-related potentials and evoked oscillations
title Response inhibition alterations in migraine: evidence from event-related potentials and evoked oscillations
title_full Response inhibition alterations in migraine: evidence from event-related potentials and evoked oscillations
title_fullStr Response inhibition alterations in migraine: evidence from event-related potentials and evoked oscillations
title_full_unstemmed Response inhibition alterations in migraine: evidence from event-related potentials and evoked oscillations
title_short Response inhibition alterations in migraine: evidence from event-related potentials and evoked oscillations
title_sort response inhibition alterations in migraine: evidence from event-related potentials and evoked oscillations
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7531083/
https://www.ncbi.nlm.nih.gov/pubmed/33008328
http://dx.doi.org/10.1186/s10194-020-01187-2
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