Impairments to the multisensory integration brain regions during migraine chronification: correlation with the vestibular dysfunction

ObjectivesMigraine is often combined with vestibular dysfunction, particularly in patients with chronic migraine (CM). However, the pathogenesis of migraine chronification leading to vestibular dysfunction is not fully understood. The current study investigated whether structural or functional impai...

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Main Authors: Liang Dong, Xiaoping Fan, Yulan Fan, Ximao Li, Hui Li, Jiying Zhou
Format: Article
Language:English
Published: Frontiers Media S.A. 2023-07-01
Series:Frontiers in Molecular Neuroscience
Subjects:
Online Access:https://www.frontiersin.org/articles/10.3389/fnmol.2023.1153641/full
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author Liang Dong
Xiaoping Fan
Yulan Fan
Ximao Li
Hui Li
Jiying Zhou
author_facet Liang Dong
Xiaoping Fan
Yulan Fan
Ximao Li
Hui Li
Jiying Zhou
author_sort Liang Dong
collection DOAJ
description ObjectivesMigraine is often combined with vestibular dysfunction, particularly in patients with chronic migraine (CM). However, the pathogenesis of migraine chronification leading to vestibular dysfunction is not fully understood. The current study investigated whether structural or functional impairments to the brain during migraine chronification could be associated with vestibular dysfunction development.MethodsThe eligible participants underwent clinical assessment and magnetic resonance imaging (MRI) scans. Voxel-based morphometry (VBM) determined structural impairment by evaluating alterations in gray matter volume (GMV). Functional impairment was assessed by the mean amplitude of low-frequency fluctuation (mALFF). Furthermore, the resting-state functional connectivity (rsFC) of regions possessing impairment was examined with a seed-based approach. We also analyzed the correlations between altered neuroimaging features with clinical variables and performed multiple linear regression.ResultsEighteen CM patients, 18 episodic migraine (EM) patients, and 18 healthy controls (HCs) were included in this study. A one-way ANOVA indicated the group differences in mALFF. These were located within right supramarginal gyrus (SMG), left angular gyrus (AG), middle frontal gyrus (MFG), left middle occipital gyrus (MOG), right rolandic operculum (Rol) and left superior parietal gyrus (SPG). During rsFC analysis, the CM group had more enhanced rsFC of left SPG with left MOG than the EM and HC groups. The EM group revealed enhanced rsFC of left SPG with left AG than the CM and HC groups. In multiple linear regression, after controlling for age, body mass index (BMI) and disease duration, the rsFC of left SPG with left MOG (β = 48.896, p = 0.021) was found to predict the total Dizziness Handicap Inventory (DHI) score with an explained variance of 25.1%. Moreover, the rsFC of left SPG with left MOG (β = 1.253, p = 0.003) and right SMG (β = −1.571, p = 0.049) were significant predictors of migraine frequency, accounting for a total explained variance of 73.8%.ConclusionThe functional impairments due to migraine chronification are primarily concentrated in the multisensory integration-related brain regions. Additionally, the rsFC of SPG with MOG can predict the frequency of migraine and the degree of vestibular dysfunction. Therefore, these neuroimaging features could be potential mechanisms and therapeutic targets for developing vestibular dysfunction in migraine.
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spelling doaj.art-b61653916c094f92ba5ddd1ffcd3f5742023-07-03T05:21:43ZengFrontiers Media S.A.Frontiers in Molecular Neuroscience1662-50992023-07-011610.3389/fnmol.2023.11536411153641Impairments to the multisensory integration brain regions during migraine chronification: correlation with the vestibular dysfunctionLiang Dong0Xiaoping Fan1Yulan Fan2Ximao Li3Hui Li4Jiying Zhou5Department of Neurology, The First Affiliated Hospital of Chongqing Medical University, Chongqing, ChinaDepartment of Hospice, The First Affiliated Hospital of Chongqing Medical University, Chongqing, ChinaDepartment of Neurology, The First Affiliated Hospital of Chongqing Medical University, Chongqing, ChinaDepartment of Radiology, The First Affiliated Hospital of Chongqing Medical University, Chongqing, ChinaDepartment of Neurology, The First Affiliated Hospital of Chongqing Medical University, Chongqing, ChinaDepartment of Neurology, The First Affiliated Hospital of Chongqing Medical University, Chongqing, ChinaObjectivesMigraine is often combined with vestibular dysfunction, particularly in patients with chronic migraine (CM). However, the pathogenesis of migraine chronification leading to vestibular dysfunction is not fully understood. The current study investigated whether structural or functional impairments to the brain during migraine chronification could be associated with vestibular dysfunction development.MethodsThe eligible participants underwent clinical assessment and magnetic resonance imaging (MRI) scans. Voxel-based morphometry (VBM) determined structural impairment by evaluating alterations in gray matter volume (GMV). Functional impairment was assessed by the mean amplitude of low-frequency fluctuation (mALFF). Furthermore, the resting-state functional connectivity (rsFC) of regions possessing impairment was examined with a seed-based approach. We also analyzed the correlations between altered neuroimaging features with clinical variables and performed multiple linear regression.ResultsEighteen CM patients, 18 episodic migraine (EM) patients, and 18 healthy controls (HCs) were included in this study. A one-way ANOVA indicated the group differences in mALFF. These were located within right supramarginal gyrus (SMG), left angular gyrus (AG), middle frontal gyrus (MFG), left middle occipital gyrus (MOG), right rolandic operculum (Rol) and left superior parietal gyrus (SPG). During rsFC analysis, the CM group had more enhanced rsFC of left SPG with left MOG than the EM and HC groups. The EM group revealed enhanced rsFC of left SPG with left AG than the CM and HC groups. In multiple linear regression, after controlling for age, body mass index (BMI) and disease duration, the rsFC of left SPG with left MOG (β = 48.896, p = 0.021) was found to predict the total Dizziness Handicap Inventory (DHI) score with an explained variance of 25.1%. Moreover, the rsFC of left SPG with left MOG (β = 1.253, p = 0.003) and right SMG (β = −1.571, p = 0.049) were significant predictors of migraine frequency, accounting for a total explained variance of 73.8%.ConclusionThe functional impairments due to migraine chronification are primarily concentrated in the multisensory integration-related brain regions. Additionally, the rsFC of SPG with MOG can predict the frequency of migraine and the degree of vestibular dysfunction. Therefore, these neuroimaging features could be potential mechanisms and therapeutic targets for developing vestibular dysfunction in migraine.https://www.frontiersin.org/articles/10.3389/fnmol.2023.1153641/fullmigrainechronificationvestibular dysfunctionfunctional connectivitymultisensory integrationresting-state functional magnetic resonance
spellingShingle Liang Dong
Xiaoping Fan
Yulan Fan
Ximao Li
Hui Li
Jiying Zhou
Impairments to the multisensory integration brain regions during migraine chronification: correlation with the vestibular dysfunction
Frontiers in Molecular Neuroscience
migraine
chronification
vestibular dysfunction
functional connectivity
multisensory integration
resting-state functional magnetic resonance
title Impairments to the multisensory integration brain regions during migraine chronification: correlation with the vestibular dysfunction
title_full Impairments to the multisensory integration brain regions during migraine chronification: correlation with the vestibular dysfunction
title_fullStr Impairments to the multisensory integration brain regions during migraine chronification: correlation with the vestibular dysfunction
title_full_unstemmed Impairments to the multisensory integration brain regions during migraine chronification: correlation with the vestibular dysfunction
title_short Impairments to the multisensory integration brain regions during migraine chronification: correlation with the vestibular dysfunction
title_sort impairments to the multisensory integration brain regions during migraine chronification correlation with the vestibular dysfunction
topic migraine
chronification
vestibular dysfunction
functional connectivity
multisensory integration
resting-state functional magnetic resonance
url https://www.frontiersin.org/articles/10.3389/fnmol.2023.1153641/full
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AT yulanfan impairmentstothemultisensoryintegrationbrainregionsduringmigrainechronificationcorrelationwiththevestibulardysfunction
AT ximaoli impairmentstothemultisensoryintegrationbrainregionsduringmigrainechronificationcorrelationwiththevestibulardysfunction
AT huili impairmentstothemultisensoryintegrationbrainregionsduringmigrainechronificationcorrelationwiththevestibulardysfunction
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