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

Abstract 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 inhibi...

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Main Authors: Guoliang Chen, Yansong Li, Zhao Dong, Rongfei Wang, Dengfa Zhao, Ignacio Obeso, Shengyuan Yu
Format: Article
Language:English
Published: BMC 2020-10-01
Series:The Journal of Headache and Pain
Subjects:
N2
P3
Online Access:http://link.springer.com/article/10.1186/s10194-020-01187-2
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spelling doaj-e7eb928cb81449b7ac6c5239ff30a2db2020-11-25T02:49:52ZengBMCThe Journal of Headache and Pain1129-23691129-23772020-10-0121111210.1186/s10194-020-01187-2Response inhibition alterations in migraine: evidence from event-related potentials and evoked oscillationsGuoliang Chen0Yansong Li1Zhao Dong2Rongfei Wang3Dengfa Zhao4Ignacio Obeso5Shengyuan Yu6Medical School of Chinese PLAReward, Competition and Social Neuroscience Lab, Department of Psychology, School of Social and Behavioral SciencesMedical School of Chinese PLAMedical School of Chinese PLAMedical School of Chinese PLAHM Hospitales – Centro Integral en Neurociencias HM CINACMedical School of Chinese PLAAbstract 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.http://link.springer.com/article/10.1186/s10194-020-01187-2MigraineResponse inhibitionERPsN2P3Theta oscillation
collection DOAJ
language English
format Article
sources DOAJ
author Guoliang Chen
Yansong Li
Zhao Dong
Rongfei Wang
Dengfa Zhao
Ignacio Obeso
Shengyuan Yu
spellingShingle Guoliang Chen
Yansong Li
Zhao Dong
Rongfei Wang
Dengfa Zhao
Ignacio Obeso
Shengyuan Yu
Response inhibition alterations in migraine: evidence from event-related potentials and evoked oscillations
The Journal of Headache and Pain
Migraine
Response inhibition
ERPs
N2
P3
Theta oscillation
author_facet Guoliang Chen
Yansong Li
Zhao Dong
Rongfei Wang
Dengfa Zhao
Ignacio Obeso
Shengyuan Yu
author_sort Guoliang Chen
title 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_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_sort response inhibition alterations in migraine: evidence from event-related potentials and evoked oscillations
publisher BMC
series The Journal of Headache and Pain
issn 1129-2369
1129-2377
publishDate 2020-10-01
description Abstract 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.
topic Migraine
Response inhibition
ERPs
N2
P3
Theta oscillation
url http://link.springer.com/article/10.1186/s10194-020-01187-2
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