Altered Brain Functional Network in Parkinson Disease With Rapid Eye Movement Sleep Behavior Disorder

Background and Objective: Parkinson disease (PD) with rapid eye movement (REM) sleep behavior disorder (PD-RBD) tend to be a distinct phenotype with more severe clinical characteristics and pathological lesion when compared with PD without RBD (PD-nRBD). However, the pathological mechanism underlyin...

Full description

Bibliographic Details
Main Authors: Jiao Li, Qiaoling Zeng, Wen Zhou, Xiangwei Zhai, Chao Lai, Junlan Zhu, Shuwen Dong, Zhijian Lin, Guanxun Cheng
Format: Article
Language:English
Published: Frontiers Media S.A. 2020-10-01
Series:Frontiers in Neurology
Subjects:
Online Access:https://www.frontiersin.org/articles/10.3389/fneur.2020.563624/full
_version_ 1819063512666734592
author Jiao Li
Qiaoling Zeng
Wen Zhou
Xiangwei Zhai
Chao Lai
Junlan Zhu
Shuwen Dong
Zhijian Lin
Guanxun Cheng
author_facet Jiao Li
Qiaoling Zeng
Wen Zhou
Xiangwei Zhai
Chao Lai
Junlan Zhu
Shuwen Dong
Zhijian Lin
Guanxun Cheng
author_sort Jiao Li
collection DOAJ
description Background and Objective: Parkinson disease (PD) with rapid eye movement (REM) sleep behavior disorder (PD-RBD) tend to be a distinct phenotype with more severe clinical characteristics and pathological lesion when compared with PD without RBD (PD-nRBD). However, the pathological mechanism underlying PD-RBD remains unclear. We aim to use the resting-state functional magnetic resonance imaging (rs-fMRI) to explore the mechanism of PD-RBD from the perspective of internal connectivity networks.Materials and Methods: A total of 92 PD patients and 20 age and sex matched normal controls (NC) were included. All participants underwent rs-fMRI scan and clinical assessment. According to the RBD screening questionnaire (RBDSQ), PD patients were divided into two groups: PD with probable RBD (PD-pRBD) and PD without probable RBD (PD-npRBD). The whole brain was divided into 90 regions using automated anatomic labeling atlas. Functional network of each subject was constructed according to the correlation of rs-fMRI blood oxygenation level dependent signals in any two brain regions and network metrics were analyzed using graph theory approaches. Network properties among three groups were compared and correlation analysis was made using distinguishing network metrics and RBDSQ scores.Results: We found both PD-pRBD and PD-npRBD patients existed small-world characteristics. PD-pRBD showed a wider range of nodal property changes in neocortex and limbic system than PD-npRBD patients when compared with NC. Besides, PD-pRBD showed significant enhanced nodal efficiency in the bilateral thalamus and betweenness centrality in the left insula, but, reduced betweenness centrality in the right dorsolateral superior frontal gyrus when compared with PD-npRBD. Moreover, nodal efficiency in the bilateral thalamus were positively correlated with RBDSQ scores.Conclusions: Both NC and PD patients displayed small-world properties and indiscriminate global measure but PD-pRBD showed more extensive changes of nodal properties than PD-npRBD. The increased centrality role in the bilateral thalamus and the left insula, and disruption in the right dorsolateral superior frontal gyrus may play as a key role in underlying pathogenesis of PD-RBD.
first_indexed 2024-12-21T15:15:51Z
format Article
id doaj.art-cee15b2135a34dc3b60e2aad7764920b
institution Directory Open Access Journal
issn 1664-2295
language English
last_indexed 2024-12-21T15:15:51Z
publishDate 2020-10-01
publisher Frontiers Media S.A.
record_format Article
series Frontiers in Neurology
spelling doaj.art-cee15b2135a34dc3b60e2aad7764920b2022-12-21T18:59:10ZengFrontiers Media S.A.Frontiers in Neurology1664-22952020-10-011110.3389/fneur.2020.563624563624Altered Brain Functional Network in Parkinson Disease With Rapid Eye Movement Sleep Behavior DisorderJiao Li0Qiaoling Zeng1Wen Zhou2Xiangwei Zhai3Chao Lai4Junlan Zhu5Shuwen Dong6Zhijian Lin7Guanxun Cheng8Department of Medical Imaging, Peking University Shenzhen Hospital, Shenzhen, ChinaDepartment of Medical Imaging, Peking University Shenzhen Hospital, Shenzhen, ChinaDepartment of Medical Imaging, Peking University Shenzhen Hospital, Shenzhen, ChinaDepartment of Medical Imaging, Peking University Shenzhen Hospital, Shenzhen, ChinaDepartment of Medical Imaging, Peking University Shenzhen Hospital, Shenzhen, ChinaDepartment of Medical Imaging, Peking University Shenzhen Hospital, Shenzhen, ChinaDepartment of Medical Imaging, Peking University Shenzhen Hospital, Shenzhen, ChinaDepartment of Neurology, Peking University Shenzhen Hospital, Shenzhen, ChinaDepartment of Medical Imaging, Peking University Shenzhen Hospital, Shenzhen, ChinaBackground and Objective: Parkinson disease (PD) with rapid eye movement (REM) sleep behavior disorder (PD-RBD) tend to be a distinct phenotype with more severe clinical characteristics and pathological lesion when compared with PD without RBD (PD-nRBD). However, the pathological mechanism underlying PD-RBD remains unclear. We aim to use the resting-state functional magnetic resonance imaging (rs-fMRI) to explore the mechanism of PD-RBD from the perspective of internal connectivity networks.Materials and Methods: A total of 92 PD patients and 20 age and sex matched normal controls (NC) were included. All participants underwent rs-fMRI scan and clinical assessment. According to the RBD screening questionnaire (RBDSQ), PD patients were divided into two groups: PD with probable RBD (PD-pRBD) and PD without probable RBD (PD-npRBD). The whole brain was divided into 90 regions using automated anatomic labeling atlas. Functional network of each subject was constructed according to the correlation of rs-fMRI blood oxygenation level dependent signals in any two brain regions and network metrics were analyzed using graph theory approaches. Network properties among three groups were compared and correlation analysis was made using distinguishing network metrics and RBDSQ scores.Results: We found both PD-pRBD and PD-npRBD patients existed small-world characteristics. PD-pRBD showed a wider range of nodal property changes in neocortex and limbic system than PD-npRBD patients when compared with NC. Besides, PD-pRBD showed significant enhanced nodal efficiency in the bilateral thalamus and betweenness centrality in the left insula, but, reduced betweenness centrality in the right dorsolateral superior frontal gyrus when compared with PD-npRBD. Moreover, nodal efficiency in the bilateral thalamus were positively correlated with RBDSQ scores.Conclusions: Both NC and PD patients displayed small-world properties and indiscriminate global measure but PD-pRBD showed more extensive changes of nodal properties than PD-npRBD. The increased centrality role in the bilateral thalamus and the left insula, and disruption in the right dorsolateral superior frontal gyrus may play as a key role in underlying pathogenesis of PD-RBD.https://www.frontiersin.org/articles/10.3389/fneur.2020.563624/fullParkinson diseaseREM sleep behavior disorderresting-state functional magnetic resonance imagingfunctional networkgraph theory
spellingShingle Jiao Li
Qiaoling Zeng
Wen Zhou
Xiangwei Zhai
Chao Lai
Junlan Zhu
Shuwen Dong
Zhijian Lin
Guanxun Cheng
Altered Brain Functional Network in Parkinson Disease With Rapid Eye Movement Sleep Behavior Disorder
Frontiers in Neurology
Parkinson disease
REM sleep behavior disorder
resting-state functional magnetic resonance imaging
functional network
graph theory
title Altered Brain Functional Network in Parkinson Disease With Rapid Eye Movement Sleep Behavior Disorder
title_full Altered Brain Functional Network in Parkinson Disease With Rapid Eye Movement Sleep Behavior Disorder
title_fullStr Altered Brain Functional Network in Parkinson Disease With Rapid Eye Movement Sleep Behavior Disorder
title_full_unstemmed Altered Brain Functional Network in Parkinson Disease With Rapid Eye Movement Sleep Behavior Disorder
title_short Altered Brain Functional Network in Parkinson Disease With Rapid Eye Movement Sleep Behavior Disorder
title_sort altered brain functional network in parkinson disease with rapid eye movement sleep behavior disorder
topic Parkinson disease
REM sleep behavior disorder
resting-state functional magnetic resonance imaging
functional network
graph theory
url https://www.frontiersin.org/articles/10.3389/fneur.2020.563624/full
work_keys_str_mv AT jiaoli alteredbrainfunctionalnetworkinparkinsondiseasewithrapideyemovementsleepbehaviordisorder
AT qiaolingzeng alteredbrainfunctionalnetworkinparkinsondiseasewithrapideyemovementsleepbehaviordisorder
AT wenzhou alteredbrainfunctionalnetworkinparkinsondiseasewithrapideyemovementsleepbehaviordisorder
AT xiangweizhai alteredbrainfunctionalnetworkinparkinsondiseasewithrapideyemovementsleepbehaviordisorder
AT chaolai alteredbrainfunctionalnetworkinparkinsondiseasewithrapideyemovementsleepbehaviordisorder
AT junlanzhu alteredbrainfunctionalnetworkinparkinsondiseasewithrapideyemovementsleepbehaviordisorder
AT shuwendong alteredbrainfunctionalnetworkinparkinsondiseasewithrapideyemovementsleepbehaviordisorder
AT zhijianlin alteredbrainfunctionalnetworkinparkinsondiseasewithrapideyemovementsleepbehaviordisorder
AT guanxuncheng alteredbrainfunctionalnetworkinparkinsondiseasewithrapideyemovementsleepbehaviordisorder