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Disrupted White Matter Functional Connectivity With the Cerebral Cortex in Migraine Patients.

ABSTRACT: Background: In attempts to understand the migraine patients' overall brain functional architecture, blood oxygenation level-dependent (BOLD) signals in the white matter (WM) and gray matter (GM) were considered in the current study. Migraine, a severe and multiphasic brain condition, is characterized by recurrent attacks of headaches. BOLD fluctuations in a resting state exhibit similar temporal and spectral profiles in both WM and GM. It is feasible to explore the functional interactions between WM tracts and GM regions in migraine. Methods: Forty-eight migraineurs without aura (MWoA) and 48 healthy controls underwent resting-state functional magnetic resonance imaging. Pearson's correlations between the mean time courses of 48 white matter (WM) bundles and 82 gray matter (GM) regions were computed for each subject. Two-sample t-tests were performed on the Pearson's correlation coefficients (CC) to compare the differences between the MWoA and healthy controls in the GM-averaged CC of each bundle and the WM-averaged CC of each GM region. Results: The MWoAs exhibited an overall decreased average temporal CC between BOLD signals in 82 GM regions and 48 WM bundles compared with healthy controls, while little was increased. In particular, WM bundles such as left anterior corona radiata, left external capsule and bilateral superior longitudinal fasciculus had significantly decreased mean CCs with GM in MWoA. On the other hand, 16 GM regions had significantly decreased mean CCs with WM in MWoA, including some areas that are parts of the somatosensory regions, auditory cortex, temporal areas, frontal areas, cingulate cortex, and parietal cortex. Conclusion: Decreased functional connections between WM bundles and GM regions might contribute to disrupted functional connectivity between the parts of the pain processing pathway in MWoAs, which indicated that functional and connectivity abnormalities in cortical regions may not be limited to GM regions but are instead associated with functional abnormalities in WM tracts.

SUBMITTER: Qin Z

PROVIDER: S-EPMC8793828 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:Chronic pain has been linked with learning and memory processes and functional changes in brain plasticity in its development and maintenance via neuroimaging studies. However, the principle of reorganization of the migraine brain network as the brain progresses into chronic pain remain poorly understood. Here, using resting-state functional magnetic resonance imaging (rs-fMRI) and graph theory approaches, we aimed to investigate the dynamic dysfunctional connectivity in 108 patients with migraine without aura (MWoA) and 30 gender-matched healthy controls (HC). All patients were divided into 40 groups using a sliding boxcar grouping of subjects in disease duration order. As compared with HC, nonparametric permutation tests were applied for between-group comparisons of functional connectivity strength in each patient group. We focused only on the between-group differences of functional connections in MWoA, and the situation how these different connections were organized along with the changing trend. As the disease duration increased, the presence of chronic headache altered the functional connectivity from the local central nervous system (CNS) to a disruption in the whole-brain networks. These dysfunctional connections integrated into a connected component in relatively longer migraine duration groups, suggesting an abnormal integrated network configuration with ongoing central changes for long-term migraine. Within these between-group differences of the connected component, there were contained a small number of brain regions that had disproportionately numerous connections. Moreover, these brain regions exhibited a tendency to link to each other were organized into a strongly interconnected community. These interconnected brain regions were mainly located in the sensory-discriminative brain areas. Our results exhibited a working model of the central mechanisms of migraine where the brain functional connectivity was altered from the local central nervous system to a densely interconnected center, which may extend our understanding of the role of learning mechanisms which are likely involved in maintenance of chronic pain.

Project description:The existence of "sex phenotype" in migraine is a long-standing scientific question. Fluctuations of female sex hormones contribute to migraine attacks, and women also have enhanced brain activity during emotional processing and their functional brain networks seem to be more vulnerable to migraine-induced disruption compared to men. Periaqueductal grey matter (PAG) is a core region of pain processing and modulation networks with possible sex-related implications in migraine. In our study, sex differences of PAG functional resting-state connectivity were investigated in the interictal state in 32 episodic migraines without aura patients (16 women and 16 men). A significant main effect of sex was detected in PAG connectivity with postcentral, precentral, and inferior parietal gyri, and further differences were found between right PAG and visual areas (superior occipital gyrus, calcarine, and cuneus), supplementary motor area, and mid-cingulum connectivity. In all cases, PAG functional connectivity was stronger in female migraineurs compared to males. However, higher average pain intensity of migraine attacks correlated with stronger connectivity of PAG and middle temporal, superior occipital, and parietal gyri in male migraineurs compared to females. Migraine-related disability is also associated with PAG connectivity but without sex differences. Our results indicate that sex differences in PAG connectivity with brain regions involved in sensory and emotional aspects of pain might contribute to the "sex-phenotype" in migraine. The stronger functional connectivity between PAG and pain processing areas may be a sign of increased excitability of pain pathways even in resting-state in females compared to male migraineurs, which could contribute to female vulnerability for migraine. However, pain intensity experienced by male migraineurs correlated with increased connectivity between PAG and regions involved in the subjective experience of pain and pain-related unpleasantness. The demonstrated sex differences of PAG functional connectivity may support the notion that the female and male brain is differently affected by migraine.

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Disrupted White Matter Functional Connectivity With the Cerebral Cortex in Migraine Patients.

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