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      Functional Alterations in the Posterior Insula and Cerebellum in Migraine Without Aura: A Resting-State MRI Study

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          Abstract

          Background: Hypothesis-driven functional connectivity (FC) analyses have revealed abnormal functional interaction of regions or networks involved in pain processing in episodic migraine patients. We aimed to investigate the resting-state FC patterns in episodic migraine by combining data-driven voxel-wise degree centrality (DC) calculation and seed-based FC analysis.

          Methods: Thirty-nine patients suffering from episodic migraine without aura and 35 healthy controls underwent clinical assessment and functional MRI. DC was analyzed voxel-wise and compared between groups, and FC of regions with DC differences were further examined using a seed-based approach.

          Results: Compared with the control group, the migraine group showed increased and decreased DC in the right posterior insula and left crus I, respectively. Seed-based FC analyses revealed that migraine patients demonstrated increased right posterior insula connections with the postcentral gyrus, supplementary motor area/paracentral lobule, fusiform gyrus and temporal pole. The left crus I showed decreased FC with regions of the default mode network (DMN), including the medial prefrontal cortex (mPFC), angular gyrus, medial and lateral temporal cortex in patients with migraine. Furthermore, pain intensity positively correlated with DC in the right amygdala/parahippocampal gyrus, and migraine frequency negatively correlated with FC between the left crus I and mPFC.

          Conclusion: Patients with episodic migraine without aura have increased FC with the right posterior insula and decreased FC within the DMN, which may underlie disturbed sensory integration and cognitive processing of pain. The left crus I-mPFC connectivity may be a useful biomarker for assessing migraine frequency.

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          Most cited references58

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          The brain's default network: anatomy, function, and relevance to disease.

          Thirty years of brain imaging research has converged to define the brain's default network-a novel and only recently appreciated brain system that participates in internal modes of cognition. Here we synthesize past observations to provide strong evidence that the default network is a specific, anatomically defined brain system preferentially active when individuals are not focused on the external environment. Analysis of connectional anatomy in the monkey supports the presence of an interconnected brain system. Providing insight into function, the default network is active when individuals are engaged in internally focused tasks including autobiographical memory retrieval, envisioning the future, and conceiving the perspectives of others. Probing the functional anatomy of the network in detail reveals that it is best understood as multiple interacting subsystems. The medial temporal lobe subsystem provides information from prior experiences in the form of memories and associations that are the building blocks of mental simulation. The medial prefrontal subsystem facilitates the flexible use of this information during the construction of self-relevant mental simulations. These two subsystems converge on important nodes of integration including the posterior cingulate cortex. The implications of these functional and anatomical observations are discussed in relation to possible adaptive roles of the default network for using past experiences to plan for the future, navigate social interactions, and maximize the utility of moments when we are not otherwise engaged by the external world. We conclude by discussing the relevance of the default network for understanding mental disorders including autism, schizophrenia, and Alzheimer's disease.
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            The human brain is intrinsically organized into dynamic, anticorrelated functional networks.

            During performance of attention-demanding cognitive tasks, certain regions of the brain routinely increase activity, whereas others routinely decrease activity. In this study, we investigate the extent to which this task-related dichotomy is represented intrinsically in the resting human brain through examination of spontaneous fluctuations in the functional MRI blood oxygen level-dependent signal. We identify two diametrically opposed, widely distributed brain networks on the basis of both spontaneous correlations within each network and anticorrelations between networks. One network consists of regions routinely exhibiting task-related activations and the other of regions routinely exhibiting task-related deactivations. This intrinsic organization, featuring the presence of anticorrelated networks in the absence of overt task performance, provides a critical context in which to understand brain function. We suggest that both task-driven neuronal responses and behavior are reflections of this dynamic, ongoing, functional organization of the brain.
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              The International Classification of Headache Disorders, 3rd edition (beta version).

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                Author and article information

                Contributors
                Journal
                Front Behav Neurosci
                Front Behav Neurosci
                Front. Behav. Neurosci.
                Frontiers in Behavioral Neuroscience
                Frontiers Media S.A.
                1662-5153
                06 October 2020
                2020
                : 14
                : 567588
                Affiliations
                [1] 1Department of Radiology, the First Affiliated Hospital of Soochow University , Soochow, China
                [2] 2Institute of Medical Imaging, Soochow University , Soochow, China
                [3] 3Department of Radiology, Tianjin First Central Hospital , Tianjin, China
                [4] 4Department of Neurology, the First Affiliated Hospital of Soochow University , Soochow, China
                Author notes

                Edited by: Zsigmond Tamás Kincses, University of Szeged, Hungary

                Reviewed by: Roberta Messina, Vita-Salute San Raffaele University, Italy; Igor Petrusic, University of Belgrade, Serbia

                *Correspondence: Hongru Zhao snzhaohr@ 123456126.com Lingling Dai dailinglinggood@ 123456126.com

                These authors have contributed equally to this work

                Specialty section: This article was submitted to Pathological Conditions, a section of the journal Frontiers in Behavioral Neuroscience

                Article
                10.3389/fnbeh.2020.567588
                7573354
                33132860
                739cc26e-6ad7-4dab-9972-52a13ccc989d
                Copyright © 2020 Ke, Yu, Zhang, Su, Wang, Hu, Dai, Hu, Zhao and Dai.

                This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.

                History
                : 30 May 2020
                : 19 August 2020
                Page count
                Figures: 3, Tables: 3, Equations: 0, References: 58, Pages: 8, Words: 6577
                Categories
                Behavioral Neuroscience
                Original Research

                Neurosciences
                migraine,functional connectivity,resting-state,degree centrality,functional magnetic resonance imaging

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