Abnormal Thalamo–Cortical Interactions in Overlapping Communities of Migraine: An Edge Functional Connectivity Study

Author:

Dai Wei1ORCID,Qiu Enchao2,Lin Xiaoxue1,Zhang Shuhua1,Zhang Mingjie1,Han Xun1,Jia Zhihua1,Su Hui1,Bian Xiangbing3,Zang Xiao3,Li Meng3,Zhang Qingkui1,Ran Ye1,Gong Zihua1,Wang Xiaolin1,Wang Rongfei1,Tian Lixia4ORCID,Dong Zhao1ORCID,Yu Shengyuan1ORCID

Affiliation:

1. Department of Neurology First Medical Center of Chinese PLA General Hospital Beijing China

2. Department of Neurology Thomas Jefferson University Philadelphia PA USA

3. Department of Radiology First Medical Center of Chinese PLA General Hospital Beijing China

4. School of Computer and Information Technology Beijing Jiaotong University Beijing China

Abstract

ObjectiveMigraine has been demonstrated to exhibit abnormal functional connectivity of large‐scale brain networks, which is closely associated with its pathophysiology and has not yet been explored by edge functional connectivity. We used an edge‐centric approach combined with motif analysis to evaluate higher‐order communication patterns of brain networks in migraine.MethodsWe investigated edge‐centric metrics in 108 interictal migraine patients and 71 healthy controls. We parcellated the brain into networks using independent component analysis. We applied edge graph construction, k‐means clustering, community overlap detection, graph‐theory‐based evaluations, and clinical correlation analysis. We conducted motif analysis to explore the interactions among regions, and a classification model to test the specificity of edge‐centric results.ResultsThe normalized entropy of lateral thalamus was significantly increased in migraine, which was positively correlated with the baseline headache duration, and negatively correlated with headache duration reduction following preventive medications at 3‐month follow‐up. Network‐wise entropy of the sensorimotor network was significantly elevated in migraine. The community similarity between lateral thalamus and postcentral gyrus was enhanced in migraine. Migraine patients showed overrepresented L‐shape and diverse motifs, and underrepresented forked motifs with lateral thalamus serving as the reference node. Furthermore, migraine patients presented with overrepresented L‐shape triads, where the postcentral gyrus shared different edges with the lateral thalamus. The classification model showed that entropy of the lateral thalamus had the highest discriminative power, with an area under the curve of 0.86.InterpretationOur findings indicated an abnormal higher‐order thalamo–cortical communication pattern in migraine patients. The thalamo–cortical–somatosensory disturbance of concerted working may potentially lead to aberrant information flow and deficit pain processing of migraine. ANN NEUROL 2023;94:1168–1181

Funder

National Natural Science Foundation of China

International Headache Society

Publisher

Wiley

Subject

Neurology (clinical),Neurology

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