Abstract
Neuromodulation via spinal stimulation has been investigated for improving motor function and reducing spasticity after spinal cord injury (SCI) in humans. Despite the reported heterogeneity of outcomes, few investigations have attempted to discern commonalities among individual responses to neuromodulation, especially the impact of stimulation frequencies. Here, we examined how exposure to continuous lumbosacral transcutaneous spinal stimulation (TSS) across a range of frequencies affects robotic torques and EMG patterns during step** in a robotic gait orthosis on a motorized treadmill. We studied nine chronic motor-incomplete SCI individuals (8/1 AIS-C/D, 8 men) during robot-guided step** with body-weight support without and with TSS applied at random frequencies between 1 and up to 100 Hz at a constant, individually selected stimulation intensity below the common motor threshold for posterior root reflexes. The hip and knee robotic torques needed to maintain the predefined step** trajectory and EMG in eight bilateral leg muscles were recorded. We calculated the standardized mean difference between the stimulation conditions grouped into frequency bins and the no stimulation condition to determine changes in the normalized torques and the average EMG envelopes. We found heterogeneous changes in robotic torques across individuals. Agglomerative clustering of robotic torques identified four groups wherein the patterns of changes differed in magnitude and direction depending mainly on the stimulation frequency and stance/swing phase. On one end of the spectrum, the changes in robotic torques were greater with increasing stimulation frequencies (four participants), which coincided with a decrease in EMG, mainly due to the reduction of clonogenic motor output in the lower leg muscles. On the other end, we found an inverted u-shape change in torque over the mid-frequency range along with an increase in EMG, reflecting the augmentation of gait-related physiological (two participants) or pathophysiological (one participant) output. We conclude that TSS during robot-guided step** reveals different frequency-dependent motor profiles among individuals with chronic motor incomplete SCI. This suggests the need for a better understanding and characterization of motor control profiles in SCI when applying TSS as a therapeutic intervention for improving gait.
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The data set submitted to this analysis is available upon reasonable request.
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Acknowledgements
We thank Joy Bruce, Barry McKay, and Brad Farrell for their assistance with data collection.
Funding
This study was supported by NIH NINDS (EB006179), the Shepherd Center Hulse Spinal Cord Injury Lab (SCIL) founding grant, Georgia Institute of Technology Graduate Programs, the Wings for Life—Spinal Cord Research Foundation (WFL-US-07/19:199), and The Yerger NeuroRobotics Research Fund and Wilson Research Foundation affiliated with Methodist Rehabilitation Center, Jackson, MS, USA.
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MJK: data curation, formal analysis, funding acquisition, methodology, software, validation, visualization, writing—original draft, writing—review and editing. JMW: data curation, investigation, methodology, software, validation, writing—review and editing. DSS: formal analysis, methodology, validation, visualization, writing—original draft, writing—review and editing. KET: conceptualization, funding acquisition, investigation, methodology, project administration, resources, supervision, visualization, writing—original draft, writing—review and editing.
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MJK, JMW, and DSS declare no conflicts of interest. KET serves as a consultant for ONWARD Medical BV (Eindhoven, Netherlands).
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Krenn, M.J., White, J.M., Stokic, D.S. et al. Neuromodulation with transcutaneous spinal stimulation reveals different groups of motor profiles during robot-guided step** in humans with incomplete spinal cord injury. Exp Brain Res 241, 365–382 (2023). https://doi.org/10.1007/s00221-022-06521-5
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DOI: https://doi.org/10.1007/s00221-022-06521-5