Altered effective connectivity in migraine patients during emotional stimuli: a multi-frequency magnetoencephalography study

Abstract Background Migraine is a common and disabling primary headache, which is associated with a wide range of psychiatric comorbidities. However, the mechanisms of emotion processing in migraine are not fully understood yet. The present study aimed to investigate the neural network during neutra...

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Main Authors: Jing Ren, Qun Yao, Minjie Tian, Feng Li, Yueqiu Chen, Qiqi Chen, Jing Xiang, Jingping Shi
Format: Article
Language:English
Published: BMC 2022-01-01
Series:The Journal of Headache and Pain
Subjects:
Online Access:https://doi.org/10.1186/s10194-021-01379-4
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author Jing Ren
Qun Yao
Minjie Tian
Feng Li
Yueqiu Chen
Qiqi Chen
Jing Xiang
Jingping Shi
author_facet Jing Ren
Qun Yao
Minjie Tian
Feng Li
Yueqiu Chen
Qiqi Chen
Jing Xiang
Jingping Shi
author_sort Jing Ren
collection DOAJ
description Abstract Background Migraine is a common and disabling primary headache, which is associated with a wide range of psychiatric comorbidities. However, the mechanisms of emotion processing in migraine are not fully understood yet. The present study aimed to investigate the neural network during neutral, positive, and negative emotional stimuli in the migraine patients. Methods A total of 24 migraine patients and 24 age- and sex-matching healthy controls were enrolled in this study. Neuromagnetic brain activity was recorded using a whole-head magnetoencephalography (MEG) system upon exposure to human facial expression stimuli. MEG data were analyzed in multi-frequency ranges from 1 to 100 Hz. Results The migraine patients exhibited a significant enhancement in the effective connectivity from the prefrontal lobe to the temporal cortex during the negative emotional stimuli in the gamma frequency (30–90 Hz). Graph theory analysis revealed that the migraine patients had an increased degree and clustering coefficient of connectivity in the delta frequency range (1–4 Hz) upon exposure to positive emotional stimuli and an increased degree of connectivity in the delta frequency range (1–4 Hz) upon exposure to negative emotional stimuli. Clinical correlation analysis showed that the history, attack frequency, duration, and neuropsychological scales of the migraine patients had a negative correlation with the network parameters in certain frequency ranges. Conclusions The results suggested that the individuals with migraine showed deviant effective connectivity in viewing the human facial expressions in multi-frequencies. The prefrontal-temporal pathway might be related to the altered negative emotional modulation in migraine. These findings suggested that migraine might be characterized by more universal altered cerebral processing of negative stimuli. Since the significant result in this study was frequency-specific, more independent replicative studies are needed to confirm these results, and to elucidate the neurocircuitry underlying the association between migraine and emotional conditions.
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spelling doaj.art-d7912534167b4a479e19d7b5706e27632022-12-21T19:22:17ZengBMCThe Journal of Headache and Pain1129-23691129-23772022-01-0123111210.1186/s10194-021-01379-4Altered effective connectivity in migraine patients during emotional stimuli: a multi-frequency magnetoencephalography studyJing Ren0Qun Yao1Minjie Tian2Feng Li3Yueqiu Chen4Qiqi Chen5Jing Xiang6Jingping Shi7Department of Neurology, The Affiliated Brain Hospital of Nanjing Medical UniversityDepartment of Neurology, The Affiliated Brain Hospital of Nanjing Medical UniversityDepartment of Neurology, The Affiliated Brain Hospital of Nanjing Medical UniversityDepartment of Neurology, The Affiliated Brain Hospital of Nanjing Medical UniversityDepartment of Neurology, The Affiliated Brain Hospital of Nanjing Medical UniversityMEG Center, The Affiliated Brain Hospital of Nanjing Medical UniversityMEG Center, Division of Neurology, Cincinnati Children’s Hospital Medical CenterDepartment of Neurology, The Affiliated Brain Hospital of Nanjing Medical UniversityAbstract Background Migraine is a common and disabling primary headache, which is associated with a wide range of psychiatric comorbidities. However, the mechanisms of emotion processing in migraine are not fully understood yet. The present study aimed to investigate the neural network during neutral, positive, and negative emotional stimuli in the migraine patients. Methods A total of 24 migraine patients and 24 age- and sex-matching healthy controls were enrolled in this study. Neuromagnetic brain activity was recorded using a whole-head magnetoencephalography (MEG) system upon exposure to human facial expression stimuli. MEG data were analyzed in multi-frequency ranges from 1 to 100 Hz. Results The migraine patients exhibited a significant enhancement in the effective connectivity from the prefrontal lobe to the temporal cortex during the negative emotional stimuli in the gamma frequency (30–90 Hz). Graph theory analysis revealed that the migraine patients had an increased degree and clustering coefficient of connectivity in the delta frequency range (1–4 Hz) upon exposure to positive emotional stimuli and an increased degree of connectivity in the delta frequency range (1–4 Hz) upon exposure to negative emotional stimuli. Clinical correlation analysis showed that the history, attack frequency, duration, and neuropsychological scales of the migraine patients had a negative correlation with the network parameters in certain frequency ranges. Conclusions The results suggested that the individuals with migraine showed deviant effective connectivity in viewing the human facial expressions in multi-frequencies. The prefrontal-temporal pathway might be related to the altered negative emotional modulation in migraine. These findings suggested that migraine might be characterized by more universal altered cerebral processing of negative stimuli. Since the significant result in this study was frequency-specific, more independent replicative studies are needed to confirm these results, and to elucidate the neurocircuitry underlying the association between migraine and emotional conditions.https://doi.org/10.1186/s10194-021-01379-4MigraineMagnetoencephalographyMulti-frequencyEmotional stimuliEffective connectivity
spellingShingle Jing Ren
Qun Yao
Minjie Tian
Feng Li
Yueqiu Chen
Qiqi Chen
Jing Xiang
Jingping Shi
Altered effective connectivity in migraine patients during emotional stimuli: a multi-frequency magnetoencephalography study
The Journal of Headache and Pain
Migraine
Magnetoencephalography
Multi-frequency
Emotional stimuli
Effective connectivity
title Altered effective connectivity in migraine patients during emotional stimuli: a multi-frequency magnetoencephalography study
title_full Altered effective connectivity in migraine patients during emotional stimuli: a multi-frequency magnetoencephalography study
title_fullStr Altered effective connectivity in migraine patients during emotional stimuli: a multi-frequency magnetoencephalography study
title_full_unstemmed Altered effective connectivity in migraine patients during emotional stimuli: a multi-frequency magnetoencephalography study
title_short Altered effective connectivity in migraine patients during emotional stimuli: a multi-frequency magnetoencephalography study
title_sort altered effective connectivity in migraine patients during emotional stimuli a multi frequency magnetoencephalography study
topic Migraine
Magnetoencephalography
Multi-frequency
Emotional stimuli
Effective connectivity
url https://doi.org/10.1186/s10194-021-01379-4
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