Altered functional connectivity between primary motor cortex subregions and the whole brain in patients with incomplete cervical spinal cord injury

Abstract

To investigate the reorganizations of gray matter volume (GMV) in each subregion of primary motor cortex (M1) after incomplete cervical cord injury (ICCI) and to explore the differences in functional connectivity (FC) between the M1 subregions and the whole brain, and further to disclose the potential value of each M1 subregion in motor function rehabilitation of ICCI patients. Eighteen ICCI patients and eighteen age- and gender- matched healthy controls (HCs) were recruited in this study. The 3D high-resolution T1-weighted structural images and resting-state functional magnetic resonance imaging (rs-fMRI) of all subjects were obtained using a 3.0 Tesla MRI system. Based on the Human Brainnetome Atlas, the structural and functional changes of M1 subregions (including A4hf, A6cdl, A4ul, A4t, A4tl, A6cvl) in ICCI patients were analyzed by voxel-based morphometry (VBM) and seed-based FC, respectively. Compared with HCs, no structural changes in the M1 subregions of ICCI patients was detected. However, when compared with HCs, ICCI patients exhibited decreased FC in visual related areas (lingual gyrus, fusiform gyrus) and sensorimotor related areas (primary sensorimotor cortex) when the seeds were located in bilateral A4hf, A4ul, and decreased FC in visual related areas (lingual gyrus, fusiform gyrus) and cognitive related areas (temporal pole) when the seed was located in the left A4t. Moreover, when the seeds were located in the bilateral A6cdl, decreased FC in visual related areas (lingual gyrus, fusiform gyrus, calcarine gyrus) was also observed. Our findings demonstrated that each of the M1 regions had diverse FC reorganizations, which may provide a theoretical basis for the selection of precise stimulation targets, such as transcranial magnetic stimulation (TMS) or transcranial direct current stimulation (tCDS), meanwhile, our results may reveal the possible mechanism of visual feedback and cognitive training to promote motor rehabilitation.

A shift of brain network hub after spinal cord injury

“…Recently, studies using rs-fMRI in SCI have increased. There are many reports in humans ( Choe et al, 2013 ; Hou et al, 2014 , 2016 ; Chisholm et al, 2015 ; Min et al, 2015a , b ; Zhu et al, 2015 ; Oni-Orisan et al, 2016 ; Kaushal et al, 2017 ; Pan et al, 2017 ; Chen et al, 2018 ; Hawasli et al, 2018 ; Ge et al, 2019 ; Karunakaran et al, 2020 ; Li et al, 2020a , b , 2023 ; Park et al, 2020 ; Black et al, 2021 ; Huynh et al, 2021 ; Nakanishi et al, 2021 ; Zheng et al, 2021 , 2022 ; Guo et al, 2022 ; Kim et al, 2022 ; Vallesi et al, 2022 ; Wang et al, 2022 ; Mandloi et al, 2023 ) and several reports in nonhuman primates ( Rao et al, 2014 , 2016 , 2022 ; Wu et al, 2017 ) and rodents ( Seminowicz et al, 2012 ; Matsubayashi et al, 2018 ; Wu et al, 2020 ; Sanganahalli et al, 2021 , 2022 ). The analysis of rs-fMRI in SCI seems to be in its infancy due to differences in the various rs-fMRI analysis methods (seed-based, ICA, graph theory, ReHo, ALFF, etc.)…”

“…( Margulies et al, 2010 ; Lv et al, 2018 ), the timing of imaging, and degree of injury, and the lack of sufficient evidence based on animal experiments. For example, while reports of intra-insular network involvement in pain after SCI show similar tendencies ( Li et al, 2020a , b ; Huynh et al, 2021 ; Mandloi et al, 2023 ), reports of changes in motor cortex connectivity in relation to motor function are inconsistent ( Hou et al, 2014 ; Min et al, 2015a , b ; Zhu et al, 2015 ; Hou et al, 2016 ; Oni-Orisan et al, 2016 ; Rao et al, 2016 ; Kaushal et al, 2017 ; Pan et al, 2017 ; Hawasli et al, 2018 ; Matsubayashi et al, 2018 ; Li et al, 2020a,b ; Park et al, 2020 ; Nakanishi et al, 2021 ; Kim et al, 2022 ; Wang et al, 2022 ). In the present study, network analysis revealed a shift in main hub function from the pyramidal/cortical to the extrapyramidal/subcortical system.…”