Reduced resting-state brain functional network connectivity and poor regional homogeneity in patients with CADASIL

Abstract Background Cerebral autosomal dominant arteriopathy with subcortical infarcts and leukoencephalopathy (CADASIL) manifests principally as a suite of cognitive impairments, particularly in the executive domain. Executive functioning requires the dynamic coordination of neural activity over la...

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Main Authors: Jingjing Su, Shiyu Ban, Mengxing Wang, Fengchun Hua, Liang Wang, Xin Cheng, Yuping Tang, Houguang Zhou, Yu Zhai, Xiaoxia Du, Jianren Liu
Format: Article
Language:English
Published: BMC 2019-11-01
Series:The Journal of Headache and Pain
Subjects:
Online Access:http://link.springer.com/article/10.1186/s10194-019-1052-6
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author Jingjing Su
Shiyu Ban
Mengxing Wang
Fengchun Hua
Liang Wang
Xin Cheng
Yuping Tang
Houguang Zhou
Yu Zhai
Xiaoxia Du
Jianren Liu
author_facet Jingjing Su
Shiyu Ban
Mengxing Wang
Fengchun Hua
Liang Wang
Xin Cheng
Yuping Tang
Houguang Zhou
Yu Zhai
Xiaoxia Du
Jianren Liu
author_sort Jingjing Su
collection DOAJ
description Abstract Background Cerebral autosomal dominant arteriopathy with subcortical infarcts and leukoencephalopathy (CADASIL) manifests principally as a suite of cognitive impairments, particularly in the executive domain. Executive functioning requires the dynamic coordination of neural activity over large-scale networks. It remains unclear whether changes in resting-state brain functional network connectivity and regional homogeneities (ReHos) underly the mechanisms of executive dysfunction evident in CADASIL patients. Methods In this study, 22 CADASIL patients and 44 matched healthy controls underwent resting-state functional magnetic resonance imaging (fMRI). Independent component analysis (ICA) was used to measure functional brain network connectivity, and ReHos were calculated to evaluate local brain activities. We used seed-based functional connectivity (FC) analyses to determine whether dysfunctional areas (as defined by ReHos) exhibited abnormal FC with other brain areas. Relationships among the mean intra-network connectivity z-scores of dysfunctional areas within functional networks, and cognitive scores were evaluated using Pearson correlation analyses. Results Compared to the controls, CADASIL patients exhibited decreased intra-network connectivity within the bilateral lingual gyrus (LG) and the right cuneus (CU) (thus within the visual network [VIN)], and within the right precuneus (Pcu), inferior frontal gyrus (IFG), and precentral gyrus (thus within the frontal network [FRN]). Compared to the controls, patients also exhibited significantly lower ReHos in the right precuneus and cuneus (Pcu/CU), visual association cortex, calcarine gyri, posterior cingulate, limbic lobe, and weaker FC between the right Pcu/CU and the bilateral parahippocampal gyrus (PHG), and between the right Pcu/CU and the right postcentral gyrus. Notably, the mean connectivity z-scores of the bilateral LG and the right CU within the VIN were positively associated with compromised attention, calculation and delayed recall as revealed by tests of the various cognitive domains explored by the Mini-Mental State Examination. Conclusions The decreases in intra-network connectivity within the VIN and FRN and reduced local brain activity in the posterior parietal area suggest that patients with CADASIL may exhibit dysfunctional visuomotor behaviors (a hallmark of executive function), and that all visual information processing, visuomotor planning, and movement execution may be affected.
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spelling doaj.art-967a6baf2c3744069f486cf0b44da5c72022-12-22T00:33:14ZengBMCThe Journal of Headache and Pain1129-23691129-23772019-11-0120111210.1186/s10194-019-1052-6Reduced resting-state brain functional network connectivity and poor regional homogeneity in patients with CADASILJingjing Su0Shiyu Ban1Mengxing Wang2Fengchun Hua3Liang Wang4Xin Cheng5Yuping Tang6Houguang Zhou7Yu Zhai8Xiaoxia Du9Jianren Liu10Department of Neurology, Shanghai Ninth People’s Hospital, Shanghai Jiao Tong University School of MedicineShanghai Key Laboratory of Magnetic Resonance and Department of Physics, School of Physics and Materials Science, East China Normal UniversityShanghai Key Laboratory of Magnetic Resonance and Department of Physics, School of Physics and Materials Science, East China Normal UniversityPET Center, Huashan Hospital, Fudan UniversityDepartment of Neurology, Huashan Hospital, Fudan UniversityDepartment of Neurology, Huashan Hospital, Fudan UniversityDepartment of Neurology, Huashan Hospital, Fudan UniversityDepartment of Geriatrics Neurology, Huashan Hospital, Fudan UniversityDepartment of Neurology, Shanghai Ninth People’s Hospital, Shanghai Jiao Tong University School of MedicineShanghai Key Laboratory of Magnetic Resonance and Department of Physics, School of Physics and Materials Science, East China Normal UniversityDepartment of Neurology, Shanghai Ninth People’s Hospital, Shanghai Jiao Tong University School of MedicineAbstract Background Cerebral autosomal dominant arteriopathy with subcortical infarcts and leukoencephalopathy (CADASIL) manifests principally as a suite of cognitive impairments, particularly in the executive domain. Executive functioning requires the dynamic coordination of neural activity over large-scale networks. It remains unclear whether changes in resting-state brain functional network connectivity and regional homogeneities (ReHos) underly the mechanisms of executive dysfunction evident in CADASIL patients. Methods In this study, 22 CADASIL patients and 44 matched healthy controls underwent resting-state functional magnetic resonance imaging (fMRI). Independent component analysis (ICA) was used to measure functional brain network connectivity, and ReHos were calculated to evaluate local brain activities. We used seed-based functional connectivity (FC) analyses to determine whether dysfunctional areas (as defined by ReHos) exhibited abnormal FC with other brain areas. Relationships among the mean intra-network connectivity z-scores of dysfunctional areas within functional networks, and cognitive scores were evaluated using Pearson correlation analyses. Results Compared to the controls, CADASIL patients exhibited decreased intra-network connectivity within the bilateral lingual gyrus (LG) and the right cuneus (CU) (thus within the visual network [VIN)], and within the right precuneus (Pcu), inferior frontal gyrus (IFG), and precentral gyrus (thus within the frontal network [FRN]). Compared to the controls, patients also exhibited significantly lower ReHos in the right precuneus and cuneus (Pcu/CU), visual association cortex, calcarine gyri, posterior cingulate, limbic lobe, and weaker FC between the right Pcu/CU and the bilateral parahippocampal gyrus (PHG), and between the right Pcu/CU and the right postcentral gyrus. Notably, the mean connectivity z-scores of the bilateral LG and the right CU within the VIN were positively associated with compromised attention, calculation and delayed recall as revealed by tests of the various cognitive domains explored by the Mini-Mental State Examination. Conclusions The decreases in intra-network connectivity within the VIN and FRN and reduced local brain activity in the posterior parietal area suggest that patients with CADASIL may exhibit dysfunctional visuomotor behaviors (a hallmark of executive function), and that all visual information processing, visuomotor planning, and movement execution may be affected.http://link.springer.com/article/10.1186/s10194-019-1052-6Functional network connectivityRegional homogeneityCADASILResting-state fMRIVisuomotor behaviors
spellingShingle Jingjing Su
Shiyu Ban
Mengxing Wang
Fengchun Hua
Liang Wang
Xin Cheng
Yuping Tang
Houguang Zhou
Yu Zhai
Xiaoxia Du
Jianren Liu
Reduced resting-state brain functional network connectivity and poor regional homogeneity in patients with CADASIL
The Journal of Headache and Pain
Functional network connectivity
Regional homogeneity
CADASIL
Resting-state fMRI
Visuomotor behaviors
title Reduced resting-state brain functional network connectivity and poor regional homogeneity in patients with CADASIL
title_full Reduced resting-state brain functional network connectivity and poor regional homogeneity in patients with CADASIL
title_fullStr Reduced resting-state brain functional network connectivity and poor regional homogeneity in patients with CADASIL
title_full_unstemmed Reduced resting-state brain functional network connectivity and poor regional homogeneity in patients with CADASIL
title_short Reduced resting-state brain functional network connectivity and poor regional homogeneity in patients with CADASIL
title_sort reduced resting state brain functional network connectivity and poor regional homogeneity in patients with cadasil
topic Functional network connectivity
Regional homogeneity
CADASIL
Resting-state fMRI
Visuomotor behaviors
url http://link.springer.com/article/10.1186/s10194-019-1052-6
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