Cargando…

Contralesional Sensorimotor Network Participates in Motor Functional Compensation in Glioma Patients

BACKGROUND: Some gliomas in sensorimotor areas induce motor deficits, while some do not. Cortical destruction and reorganization contribute to this phenomenon, but detailed reasons remain unclear. This study investigated the differences of the functional connectivity and topological properties in th...

Descripción completa

Detalles Bibliográficos
Autores principales: Fang, Shengyu, Li, Lianwang, Weng, Shimeng, Guo, Yuhao, Zhong, Zhang, Fan, Xing, Jiang, Tao, Wang, Yinyan
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9072743/
https://www.ncbi.nlm.nih.gov/pubmed/35530325
http://dx.doi.org/10.3389/fonc.2022.882313
_version_ 1784701127445446656
author Fang, Shengyu
Li, Lianwang
Weng, Shimeng
Guo, Yuhao
Zhong, Zhang
Fan, Xing
Jiang, Tao
Wang, Yinyan
author_facet Fang, Shengyu
Li, Lianwang
Weng, Shimeng
Guo, Yuhao
Zhong, Zhang
Fan, Xing
Jiang, Tao
Wang, Yinyan
author_sort Fang, Shengyu
collection PubMed
description BACKGROUND: Some gliomas in sensorimotor areas induce motor deficits, while some do not. Cortical destruction and reorganization contribute to this phenomenon, but detailed reasons remain unclear. This study investigated the differences of the functional connectivity and topological properties in the contralesional sensorimotor network (cSMN) between patients with motor deficit and those with normal motor function. METHODS: We retrospectively reviewed 65 patients (32 men) between 2017 and 2020. The patients were divided into four groups based on tumor laterality and preoperative motor status (deficit or non-deficit). Thirty-three healthy controls (18 men) were enrolled after matching for sex, age, and educational status. Graph theoretical measurement was applied to reveal alterations of the topological properties of the cSMN by analyzing resting-state functional MRI. RESULTS: The results for patients with different hemispheric gliomas were similar. The clustering coefficient, local efficiency, transitivity, and vulnerability of the cSMN significantly increased in the non-deficit group and decreased in the deficit group compared to the healthy group (p < 0.05). Moreover, the nodes of the motor-related thalamus showed a significantly increased nodal efficiency and nodal local efficiency in the non-deficit group and decreased in the deficit group compared with the healthy group (p < 0.05). CONCLUSIONS: We posited the existence of two stages of alterations of the preoperative motor status. In the compensatory stage, the cSMN sacrificed stability to acquire high efficiency and to compensate for impaired motor function. With the glioma growing and the motor function being totally damaged, the cSMN returned to a stable state and maintained healthy hemispheric motor function, but with low efficiency.
format Online
Article
Text
id pubmed-9072743
institution National Center for Biotechnology Information
language English
publishDate 2022
publisher Frontiers Media S.A.
record_format MEDLINE/PubMed
spelling pubmed-90727432022-05-07 Contralesional Sensorimotor Network Participates in Motor Functional Compensation in Glioma Patients Fang, Shengyu Li, Lianwang Weng, Shimeng Guo, Yuhao Zhong, Zhang Fan, Xing Jiang, Tao Wang, Yinyan Front Oncol Oncology BACKGROUND: Some gliomas in sensorimotor areas induce motor deficits, while some do not. Cortical destruction and reorganization contribute to this phenomenon, but detailed reasons remain unclear. This study investigated the differences of the functional connectivity and topological properties in the contralesional sensorimotor network (cSMN) between patients with motor deficit and those with normal motor function. METHODS: We retrospectively reviewed 65 patients (32 men) between 2017 and 2020. The patients were divided into four groups based on tumor laterality and preoperative motor status (deficit or non-deficit). Thirty-three healthy controls (18 men) were enrolled after matching for sex, age, and educational status. Graph theoretical measurement was applied to reveal alterations of the topological properties of the cSMN by analyzing resting-state functional MRI. RESULTS: The results for patients with different hemispheric gliomas were similar. The clustering coefficient, local efficiency, transitivity, and vulnerability of the cSMN significantly increased in the non-deficit group and decreased in the deficit group compared to the healthy group (p < 0.05). Moreover, the nodes of the motor-related thalamus showed a significantly increased nodal efficiency and nodal local efficiency in the non-deficit group and decreased in the deficit group compared with the healthy group (p < 0.05). CONCLUSIONS: We posited the existence of two stages of alterations of the preoperative motor status. In the compensatory stage, the cSMN sacrificed stability to acquire high efficiency and to compensate for impaired motor function. With the glioma growing and the motor function being totally damaged, the cSMN returned to a stable state and maintained healthy hemispheric motor function, but with low efficiency. Frontiers Media S.A. 2022-04-22 /pmc/articles/PMC9072743/ /pubmed/35530325 http://dx.doi.org/10.3389/fonc.2022.882313 Text en Copyright © 2022 Fang, Li, Weng, Guo, Zhong, Fan, Jiang and Wang https://creativecommons.org/licenses/by/4.0/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.
spellingShingle Oncology
Fang, Shengyu
Li, Lianwang
Weng, Shimeng
Guo, Yuhao
Zhong, Zhang
Fan, Xing
Jiang, Tao
Wang, Yinyan
Contralesional Sensorimotor Network Participates in Motor Functional Compensation in Glioma Patients
title Contralesional Sensorimotor Network Participates in Motor Functional Compensation in Glioma Patients
title_full Contralesional Sensorimotor Network Participates in Motor Functional Compensation in Glioma Patients
title_fullStr Contralesional Sensorimotor Network Participates in Motor Functional Compensation in Glioma Patients
title_full_unstemmed Contralesional Sensorimotor Network Participates in Motor Functional Compensation in Glioma Patients
title_short Contralesional Sensorimotor Network Participates in Motor Functional Compensation in Glioma Patients
title_sort contralesional sensorimotor network participates in motor functional compensation in glioma patients
topic Oncology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9072743/
https://www.ncbi.nlm.nih.gov/pubmed/35530325
http://dx.doi.org/10.3389/fonc.2022.882313
work_keys_str_mv AT fangshengyu contralesionalsensorimotornetworkparticipatesinmotorfunctionalcompensationingliomapatients
AT lilianwang contralesionalsensorimotornetworkparticipatesinmotorfunctionalcompensationingliomapatients
AT wengshimeng contralesionalsensorimotornetworkparticipatesinmotorfunctionalcompensationingliomapatients
AT guoyuhao contralesionalsensorimotornetworkparticipatesinmotorfunctionalcompensationingliomapatients
AT zhongzhang contralesionalsensorimotornetworkparticipatesinmotorfunctionalcompensationingliomapatients
AT fanxing contralesionalsensorimotornetworkparticipatesinmotorfunctionalcompensationingliomapatients
AT jiangtao contralesionalsensorimotornetworkparticipatesinmotorfunctionalcompensationingliomapatients
AT wangyinyan contralesionalsensorimotornetworkparticipatesinmotorfunctionalcompensationingliomapatients