A shift of brain network hub after spinal cord injury

BackgroundSpinal cord injury (SCI) causes severe sequelae and significant social loss, depending on the extent of the damage. Most previous studies have focused on the pathology of the spinal cord to develop treatments for SCI. However, it is now known that the brain, which is not directly damaged,...

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Main Authors: Kohei Matsubayashi, Munehisa Shinozaki, Junichi Hata, Yuji Komaki, Narihito Nagoshi, Osahiko Tsuji, Kanehiro Fujiyoshi, Masaya Nakamura, Hideyuki Okano
Format: Article
Language:English
Published: Frontiers Media S.A. 2023-10-01
Series:Frontiers in Molecular Neuroscience
Subjects:
Online Access:https://www.frontiersin.org/articles/10.3389/fnmol.2023.1245902/full
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author Kohei Matsubayashi
Munehisa Shinozaki
Junichi Hata
Yuji Komaki
Narihito Nagoshi
Osahiko Tsuji
Kanehiro Fujiyoshi
Masaya Nakamura
Hideyuki Okano
author_facet Kohei Matsubayashi
Munehisa Shinozaki
Junichi Hata
Yuji Komaki
Narihito Nagoshi
Osahiko Tsuji
Kanehiro Fujiyoshi
Masaya Nakamura
Hideyuki Okano
author_sort Kohei Matsubayashi
collection DOAJ
description BackgroundSpinal cord injury (SCI) causes severe sequelae and significant social loss, depending on the extent of the damage. Most previous studies have focused on the pathology of the spinal cord to develop treatments for SCI. However, it is now known that the brain, which is not directly damaged, also undergoes morphological changes after spinal cord injury, which could affect natural recovery and treatment. In recent years, magnetic resonance imaging (MRI) has been developed to analyze functional changes in the brain. Resting-state functional MRI (rsfMRI), which captures brain activity at rest, can calculate functional connections between brain areas and identify central hubs by network analysis.PurposeWe aim to investigate functional connectivity in the brain using rsfMRI after SCI and to determine how brain-network main hubs change over time.MethodsWe evaluated rsfMRI in 10 mice of the contusional SCI model and calculated connectivity using graph theory. We evaluated “centrality,” a representative parameter of network analysis. The subtype of centrality was degree centrality, which indicates the hub function of a single area. The five times of rsfMRI were performed in each individual mouse: before injury and at 1, 3, 7, and 14 weeks post-injury.ResultsBefore the injury, the degree centralities of the primary and secondary motor cortex were high, suggesting that these motor cortices served as main hubs for motor function. After SCI, the hub function of the motor cortices decreased by 14 weeks. In contrast, hub function in the external capsule and the putamen comparatively increased with time after injury, suggesting that the extrapyramidal/subcortical system, which runs the ventral side of the spinal cord and remains after injury in this model, becomes dominant.ConclusionWe demonstrated the shift of the brain network hub after SCI. The results of this study provide basic information for understanding brain network changes after SCI and would be useful for treatment selection and evaluation of its efficacy in SCI patients.
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spelling doaj.art-7ccf44f6b7274b5e8d7e5839e798d2a02023-10-17T08:40:48ZengFrontiers Media S.A.Frontiers in Molecular Neuroscience1662-50992023-10-011610.3389/fnmol.2023.12459021245902A shift of brain network hub after spinal cord injuryKohei Matsubayashi0Munehisa Shinozaki1Junichi Hata2Yuji Komaki3Narihito Nagoshi4Osahiko Tsuji5Kanehiro Fujiyoshi6Masaya Nakamura7Hideyuki Okano8Department of Orthopaedic Surgery, School of Medicine, Keio University, Tokyo, JapanDepartment of Physiology, School of Medicine, Keio University, Tokyo, JapanGraduate School of Human Health Sciences, Tokyo Metropolitan University, Tokyo, JapanLive Animal Imaging Center, Central Institute for Experimental Animals, Kanagawa, JapanDepartment of Orthopaedic Surgery, School of Medicine, Keio University, Tokyo, JapanDepartment of Orthopaedic Surgery, School of Medicine, Keio University, Tokyo, JapanDepartment of Orthopaedic Surgery, Murayama Medical Center (NHO), Tokyo, JapanDepartment of Orthopaedic Surgery, School of Medicine, Keio University, Tokyo, JapanDepartment of Physiology, School of Medicine, Keio University, Tokyo, JapanBackgroundSpinal cord injury (SCI) causes severe sequelae and significant social loss, depending on the extent of the damage. Most previous studies have focused on the pathology of the spinal cord to develop treatments for SCI. However, it is now known that the brain, which is not directly damaged, also undergoes morphological changes after spinal cord injury, which could affect natural recovery and treatment. In recent years, magnetic resonance imaging (MRI) has been developed to analyze functional changes in the brain. Resting-state functional MRI (rsfMRI), which captures brain activity at rest, can calculate functional connections between brain areas and identify central hubs by network analysis.PurposeWe aim to investigate functional connectivity in the brain using rsfMRI after SCI and to determine how brain-network main hubs change over time.MethodsWe evaluated rsfMRI in 10 mice of the contusional SCI model and calculated connectivity using graph theory. We evaluated “centrality,” a representative parameter of network analysis. The subtype of centrality was degree centrality, which indicates the hub function of a single area. The five times of rsfMRI were performed in each individual mouse: before injury and at 1, 3, 7, and 14 weeks post-injury.ResultsBefore the injury, the degree centralities of the primary and secondary motor cortex were high, suggesting that these motor cortices served as main hubs for motor function. After SCI, the hub function of the motor cortices decreased by 14 weeks. In contrast, hub function in the external capsule and the putamen comparatively increased with time after injury, suggesting that the extrapyramidal/subcortical system, which runs the ventral side of the spinal cord and remains after injury in this model, becomes dominant.ConclusionWe demonstrated the shift of the brain network hub after SCI. The results of this study provide basic information for understanding brain network changes after SCI and would be useful for treatment selection and evaluation of its efficacy in SCI patients.https://www.frontiersin.org/articles/10.3389/fnmol.2023.1245902/fullspinal cord injurynetwork analysiscorticospinal tractmotor functionbrain network hubsresting-state functional MRI
spellingShingle Kohei Matsubayashi
Munehisa Shinozaki
Junichi Hata
Yuji Komaki
Narihito Nagoshi
Osahiko Tsuji
Kanehiro Fujiyoshi
Masaya Nakamura
Hideyuki Okano
A shift of brain network hub after spinal cord injury
Frontiers in Molecular Neuroscience
spinal cord injury
network analysis
corticospinal tract
motor function
brain network hubs
resting-state functional MRI
title A shift of brain network hub after spinal cord injury
title_full A shift of brain network hub after spinal cord injury
title_fullStr A shift of brain network hub after spinal cord injury
title_full_unstemmed A shift of brain network hub after spinal cord injury
title_short A shift of brain network hub after spinal cord injury
title_sort shift of brain network hub after spinal cord injury
topic spinal cord injury
network analysis
corticospinal tract
motor function
brain network hubs
resting-state functional MRI
url https://www.frontiersin.org/articles/10.3389/fnmol.2023.1245902/full
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