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Intrinsic Functional Plasticity of the Sensorimotor Network in Relapsing-Remitting Multiple Sclerosis: Evidence from a Centrality Analysis

BACKGROUND AND PURPOSE: Advanced MRI studies have revealed regional alterations in the sensorimotor cortex of patients with relapsing-remitting multiple sclerosis (RRMS). However, the organizational features underlying the relapsing phase and the subsequent remitting phase have not been directly sho...

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Autores principales: Zhuang, Ying, Zhou, Fuqing, Gong, Honghan.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Public Library of Science 2015
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4482320/
https://www.ncbi.nlm.nih.gov/pubmed/26110420
http://dx.doi.org/10.1371/journal.pone.0130524
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author Zhuang, Ying
Zhou, Fuqing
Gong, Honghan.
author_facet Zhuang, Ying
Zhou, Fuqing
Gong, Honghan.
author_sort Zhuang, Ying
collection PubMed
description BACKGROUND AND PURPOSE: Advanced MRI studies have revealed regional alterations in the sensorimotor cortex of patients with relapsing-remitting multiple sclerosis (RRMS). However, the organizational features underlying the relapsing phase and the subsequent remitting phase have not been directly shown at the functional network or the connectome level. Therefore, this study aimed to characterize MS-related centrality disturbances of the sensorimotor network (SMN) and to assess network integrity and connectedness. METHODS: Thirty-four patients with clinically definite RRMS and well-matched healthy controls participated in the study. Twenty-three patients in the remitting phase underwent one resting-state functional MRI, and 11 patients in the relapsing-remitting phase underwent two different MRIs. We measured voxel-wise centrality metrics to determine direct (degree centrality, DC) and global (eigenvector centrality, EC) functional relationships across the entire SMN. RESULTS: In the relapsing phase, DC was significantly decreased in the bilateral primary motor and somatosensory cortex (M1/S1), left dorsal premotor (PMd), and operculum-integrated regions. However, DC was increased in the peripheral SMN areas. The decrease in DC in the bilateral M1/S1 was associated with the expanded disability status scale (EDSS) and total white matter lesion loads (TWMLLs), suggesting that this adaptive response is related to the extent of brain damage in the rapid-onset attack stage. During the remission process, these alterations in centrality were restored in the bilateral M1/S1 and peripheral SMN areas. In the remitting phase, DC was reduced in the premotor, supplementary motor, and operculum-integrated regions, reflecting an adaptive response due to brain atrophy. However, DC was enhanced in the right M1 and left parietal-integrated regions, indicating chronic reorganization. In both the relapsing and remitting phases, the changes in EC and DC were similar. CONCLUSIONS: The alterations in centrality within the SMN indicate rapid plasticity and chronic reorganization with a biased impairment of specific functional areas in RRMS patients.
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spelling pubmed-44823202015-07-01 Intrinsic Functional Plasticity of the Sensorimotor Network in Relapsing-Remitting Multiple Sclerosis: Evidence from a Centrality Analysis Zhuang, Ying Zhou, Fuqing Gong, Honghan. PLoS One Research Article BACKGROUND AND PURPOSE: Advanced MRI studies have revealed regional alterations in the sensorimotor cortex of patients with relapsing-remitting multiple sclerosis (RRMS). However, the organizational features underlying the relapsing phase and the subsequent remitting phase have not been directly shown at the functional network or the connectome level. Therefore, this study aimed to characterize MS-related centrality disturbances of the sensorimotor network (SMN) and to assess network integrity and connectedness. METHODS: Thirty-four patients with clinically definite RRMS and well-matched healthy controls participated in the study. Twenty-three patients in the remitting phase underwent one resting-state functional MRI, and 11 patients in the relapsing-remitting phase underwent two different MRIs. We measured voxel-wise centrality metrics to determine direct (degree centrality, DC) and global (eigenvector centrality, EC) functional relationships across the entire SMN. RESULTS: In the relapsing phase, DC was significantly decreased in the bilateral primary motor and somatosensory cortex (M1/S1), left dorsal premotor (PMd), and operculum-integrated regions. However, DC was increased in the peripheral SMN areas. The decrease in DC in the bilateral M1/S1 was associated with the expanded disability status scale (EDSS) and total white matter lesion loads (TWMLLs), suggesting that this adaptive response is related to the extent of brain damage in the rapid-onset attack stage. During the remission process, these alterations in centrality were restored in the bilateral M1/S1 and peripheral SMN areas. In the remitting phase, DC was reduced in the premotor, supplementary motor, and operculum-integrated regions, reflecting an adaptive response due to brain atrophy. However, DC was enhanced in the right M1 and left parietal-integrated regions, indicating chronic reorganization. In both the relapsing and remitting phases, the changes in EC and DC were similar. CONCLUSIONS: The alterations in centrality within the SMN indicate rapid plasticity and chronic reorganization with a biased impairment of specific functional areas in RRMS patients. Public Library of Science 2015-06-25 /pmc/articles/PMC4482320/ /pubmed/26110420 http://dx.doi.org/10.1371/journal.pone.0130524 Text en © 2015 Zhuang et al http://creativecommons.org/licenses/by/4.0/ This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are properly credited.
spellingShingle Research Article
Zhuang, Ying
Zhou, Fuqing
Gong, Honghan.
Intrinsic Functional Plasticity of the Sensorimotor Network in Relapsing-Remitting Multiple Sclerosis: Evidence from a Centrality Analysis
title Intrinsic Functional Plasticity of the Sensorimotor Network in Relapsing-Remitting Multiple Sclerosis: Evidence from a Centrality Analysis
title_full Intrinsic Functional Plasticity of the Sensorimotor Network in Relapsing-Remitting Multiple Sclerosis: Evidence from a Centrality Analysis
title_fullStr Intrinsic Functional Plasticity of the Sensorimotor Network in Relapsing-Remitting Multiple Sclerosis: Evidence from a Centrality Analysis
title_full_unstemmed Intrinsic Functional Plasticity of the Sensorimotor Network in Relapsing-Remitting Multiple Sclerosis: Evidence from a Centrality Analysis
title_short Intrinsic Functional Plasticity of the Sensorimotor Network in Relapsing-Remitting Multiple Sclerosis: Evidence from a Centrality Analysis
title_sort intrinsic functional plasticity of the sensorimotor network in relapsing-remitting multiple sclerosis: evidence from a centrality analysis
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4482320/
https://www.ncbi.nlm.nih.gov/pubmed/26110420
http://dx.doi.org/10.1371/journal.pone.0130524
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