A shift of brain network hub after spinal cord injury

Kohei Matsubayashi; Munehisa Shinozaki; Junichi Hata; Yuji Komaki; Narihito Nagoshi; Osahiko Tsuji; Kanehiro Fujiyoshi; Masaya Nakamura; Hideyuki Okano

doi:10.3389/fnmol.2023.1245902

A shift of brain network hub after spinal cord injury

Front Mol Neurosci. 2023 Oct 17:16:1245902. doi: 10.3389/fnmol.2023.1245902. eCollection 2023.

Authors

Kohei Matsubayashi¹, Munehisa Shinozaki², Junichi Hata³, Yuji Komaki⁴, Narihito Nagoshi¹, Osahiko Tsuji¹, Kanehiro Fujiyoshi⁵, Masaya Nakamura¹, Hideyuki Okano²

Affiliations

¹ Department of Orthopaedic Surgery, School of Medicine, Keio University, Tokyo, Japan.
² Department of Physiology, School of Medicine, Keio University, Tokyo, Japan.
³ Graduate School of Human Health Sciences, Tokyo Metropolitan University, Tokyo, Japan.
⁴ Live Animal Imaging Center, Central Institute for Experimental Animals, Kanagawa, Japan.
⁵ Department of Orthopaedic Surgery, Murayama Medical Center (NHO), Tokyo, Japan.

Abstract

Background: Spinal 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.

Purpose: We aim to investigate functional connectivity in the brain using rsfMRI after SCI and to determine how brain-network main hubs change over time.

Methods: We 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.

Results: Before 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.

Conclusion: We 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.

Keywords: (rS-fMRI); brain network hubs; corticospinal tract; motor function; network analysis; resting-state functional MRI; spinal cord injury.

Grants and funding

This work was supported by the Japan Agency for Medical Research and Development (AMED: grant nos. JP20bk0104114 and JP15bm0204001 to HO and MN; AMED: grant no. 23bm1123037h0001 to HO and MS).