Non-concomitant cortical structural and functional alterations in sensorimotor areas following incomplete spinal cord injury

Abstract

Brain plasticity, including anatomical changes and functional reorganization, is the physiological basis of functional recovery after spinal cord injury (SCI). The correlation between brain anatomical changes and functional reorganization after SCI is unclear. This study aimed to explore whether alterations of cortical structure and network function are concomitant in sensorimotor areas after incomplete SCI. Eighteen patients with incomplete SCI (mean age 40.94 ± 14.10 years old; male:female, 7:11) and 18 healthy subjects (37.33 ± 11.79 years old; male:female, 7:11) were studied by resting state functional magnetic resonance imaging. Gray matter volume (GMV) and functional connectivity were used to evaluate cortical structure and network function, respectively. There was no significant alteration of GMV in sensorimotor areas in patients with incomplete SCI compared with healthy subjects. Intra-hemispheric functional connectivity between left primary somatosensory cortex (BA1) and left primary motor cortex (BA4), and left BA1 and left somatosensory association cortex (BA5) was decreased, as well as inter-hemispheric functional connectivity between left BA1 and right BA4, left BA1 and right BA5, and left BA4 and right BA5 in patients with SCI. Functional connectivity between both BA4 areas was also decreased. The decreased functional connectivity between the left BA1 and the right BA4 positively correlated with American Spinal Injury Association sensory score in SCI patients. The results indicate that alterations of cortical anatomical structure and network functional connectivity in sensorimotor areas were non-concomitant in patients with incomplete SCI, indicating the network functional changes in sensorimotor areas may not be dependent on anatomic structure. The strength of functional connectivity within sensorimotor areas could serve as a potential imaging biomarker for assessment and prediction of sensory function in patients with incomplete SCI. This trial was registered with the Chinese Clinical Trial Registry (registration number: ChiCTR-ROC-17013566).

Keywords: anatomical structure; brain plasticity; functional connectivity; functional magnetic resonance imaging; gray matter volume; imaging biomarker; incomplete spinal cord injury; nerve regeneration; network; neural regeneration; non-concomitant; sensorimotor areas.

Figure 1

Anatomic replicas show the decreased functional connectivity of sensorimotor brain areas in patients with SCI compared with healthy subjects. (A) Normal functional connectivity in healthy subjects; (B) decreased functional connectivity in patients with spinal cord injury. The red nodes represent the seed areas and significantly changed areas of functional connectivity. The yellow lines represent decreased functional connectivity in spinal cord injury patients relative to healthy subjects. BA1L: Left primary somatosensory cortex; BA4L: left primary motor cortex; BA4R: right primary motor cortex; BA5L: left somatosensory association cortex; BA5R: right somatosensory association cortex.

Figure 2

Correlation between functional connectivity (FC) and ASIA sensory score. The decreased FC between the left BA1 and the right BA4 positively correlated with ASIA sensory score in spinal cord injury patients (r = 0.529, P = 0.023; Spearman's rank correlation). FC (BA1L-BA4R): Functional connectivity between left primary somatosensory cortex and right primary motor cortex; ASIA: American Spinal Injury Association.