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

Cortical disexcitability Delta oscillation ERPs Migraine N2 P3 Response inhibition Theta oscillation

Journal

The journal of headache and pain
ISSN: 1129-2377
Titre abrégé: J Headache Pain
Pays: England
ID NLM: 100940562

Informations de publication

Date de publication:
02 Oct 2020
Historique:
received: 01 08 2020
accepted: 24 09 2020
entrez: 3 10 2020
pubmed: 4 10 2020
medline: 22 12 2020
Statut: epublish

Résumé

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. 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. 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. 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.

Sections du résumé

BACKGROUND 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 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 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 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.

Identifiants

pubmed: 33008328
doi: 10.1186/s10194-020-01187-2
pii: 10.1186/s10194-020-01187-2
pmc: PMC7531083
doi:

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

119

Subventions

Organisme : National Natural Science Foundation of China
ID : 81671077, 81600952, 81771180, 81771200, 81901134 and 81901145
Organisme : National Natural Science Foundation of China
ID : 31600929
Organisme : Beijing Natural Science Foundation Essential Research Project
ID : Z170002
Organisme : Fundamental Research Funds for the Central Universities
ID : 010914380002
Organisme : ISCIII- Miguel Servet funding
ID : CP18/00038

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Auteurs

Guoliang Chen (G)

Medical School of Chinese PLA, Beijing, China.
Department of Neurology, The first Medical Center, Chinese PLA General Hospital, Fuxing Road 28, Haidian District, Beijing, 100853, China.
Department of Psychiatry, The 967th Hospital of Joint Logistic Support Force of PLA, Dalian, China.

Yansong Li (Y)

Reward, Competition and Social Neuroscience Lab, Department of Psychology, School of Social and Behavioral Sciences, 210023, Nanjing, China.
Institute for Brain Sciences, Nanjing University, 210023, Nanjing, China.

Zhao Dong (Z)

Medical School of Chinese PLA, Beijing, China.
Department of Neurology, The first Medical Center, Chinese PLA General Hospital, Fuxing Road 28, Haidian District, Beijing, 100853, China.

Rongfei Wang (R)

Medical School of Chinese PLA, Beijing, China.
Department of Neurology, The first Medical Center, Chinese PLA General Hospital, Fuxing Road 28, Haidian District, Beijing, 100853, China.

Dengfa Zhao (D)

Medical School of Chinese PLA, Beijing, China.
Department of Neurology, The first Medical Center, Chinese PLA General Hospital, Fuxing Road 28, Haidian District, Beijing, 100853, China.

Ignacio Obeso (I)

HM Hospitales - Centro Integral en Neurociencias HM CINAC, Móstoles, Madrid, Spain.

Shengyuan Yu (S)

Medical School of Chinese PLA, Beijing, China. yusy1963@126.com.
Department of Neurology, The first Medical Center, Chinese PLA General Hospital, Fuxing Road 28, Haidian District, Beijing, 100853, China. yusy1963@126.com.

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