Spinal cord imaging markers and recovery of standing with epidural stimulation in individuals with clinically motor complete spinal cord injury

Abstract

Spinal cord epidural stimulation (scES) is an intervention to restore motor function in those with severe spinal cord injury (SCI). Spinal cord lesion characteristics assessed via magnetic resonance imaging (MRI) may contribute to understand motor recovery. This study assessed relationships between standing ability with scES and spared spinal cord tissue characteristics at the lesion site. We hypothesized that the amount of lateral spared cord tissue would be related to independent extension in the ipsilateral lower limb. Eleven individuals with chronic, clinically motor complete SCI underwent spinal cord MRI, and were subsequently implanted with scES. Standing ability and lower limb activation patterns were assessed during an overground standing experiment with scES. This assessment occurred prior to any activity-based intervention with scES. Lesion hyperintensity was segmented from T2 axial images, and template-based analysis was used to estimate spared tissue in anterior, posterior, right, and left spinal cord regions. Regression analysis was used to assess relationships between imaging and standing outcomes. Total volume of spared tissue was related to left (p = 0.007), right (p = 0.005), and bilateral (p = 0.011) lower limb extension. Spared tissue in the left cord region was related to left lower limb extension (p = 0.019). A positive trend (p = 0.138) was also observed between right spared cord tissue and right lower limb extension. In this study, MRI measures of spared spinal cord tissue were significantly related to standing outcomes with scES. These preliminary results warrant future investigation of roles of supraspinal input and MRI-detected spared spinal cord tissue on lower limb motor responsiveness to scES.

Keywords: Epidural stimulation; Spinal cord MRI; Spinal cord injury; Spinal cord lesion; Standing.

Conflict of interest statement

Conflict of interest The authors declare no competing interests.

© 2021. The Author(s), under exclusive licence to Springer-Verlag GmbH Germany, part of Springer Nature.

Figures

Fig. 1

Imaging results from two representative research participants. A depicts an individual (A110) who demonstrated more spared cord in all regions and also better scES-promoted standing ability. B represents an individual (A41) who did not show spared cord tissue in the four regions of interest or any ability to achieve independent extension of either lower limb. From left to right: a mid-sagittal T2-weighted image with lesion hyperintensity visible, an axial T2-weighted image with lesion hyperintensity visible, the axial template showing each participant’s aggregated damage with the four regions depicted, and the percentages of spared tissue in these regions corresponding to standing ability with scES on.

Fig. 2

Duration of standing with independent bilateral, left and right lower limb extension is plotted against the amount of spared tissue of representative cord regions. Spinal cord injured individuals graded sensory and motor complete (AIS A) are identified by black circles, and those graded motor complete and sensory incomplete (AIS B) by grey triangles

Fig. 3

Time course of electro-myographic (EMG), kinematic and kinetic data collected from participant A96 during standing overground with epidural stimulation. From bilateral lower limb independent extension, the participant volitionally attempted to perform: A right knee flexion and subsequent extension, while maintaining left lower limb extension: B bilateral lower limb flexion (interrupted by the manual assistance at the knees by the trainer) and subsequent extension. IL iliopsoas; RF rectus femoris; MH medial hamstrings; VL vastus lateralis; TA tibialis anterior; MG medial gastrocnemius. Antero-posterior (Fy) and vertical (Fz) ground reaction force traces are also reported. Electrode configuration (cathodes in black, anodes in red, inactive in white), frequency, pulse width, and intensities applied in Panels A and B are reported for each of the three epidural stimulation programs concurrently applied (P1 to P3). This dataset was collected after 80 sessions (2 h/day; 5 days/week) of stand training with epidural stimulation