Abstract

Spinal cord epidural stimulation (scES) combined with activity-based training can promote motor function recovery in individuals with motor complete spinal cord injury (SCI). The characteristics of motor neuron recruitment, which influence different aspects of motor control, are still unknown when motor function is promoted by scES. Here, we enrolled five individuals with chronic motor complete SCI implanted with an scES unit to study the recruitment order of motor neurons during standing enabled by scES. We recorded high-density electromyography (HD-EMG) signals on the vastus lateralis muscle and inferred the order of recruitment of motor neurons from the relation between amplitude and conduction velocity of the scES-evoked EMG responses along the muscle fibers. Conduction velocity of scES-evoked responses was modulated over time, whereas stimulation parameters and standing condition remained constant, with average values ranging between 3.0 ± 0.1 and 4.4 ± 0.3 m/s. We found that the human spinal circuitry receiving epidural stimulation can promote both orderly (according to motor neuron size) and inverse trends of motor neuron recruitment, and that the engagement of spinal networks promoting rhythmic activity may favor orderly recruitment trends. Conversely, the different recruitment trends did not appear to be related with time since injury or scES implant, nor to the ability to achieve independent knees extension, nor to the conduction velocity values. The proposed approach can be implemented to investigate the effects of stimulation parameters and training-induced neural plasticity on the characteristics of motor neuron recruitment order, contributing to improve mechanistic understanding and effectiveness of epidural stimulation-promoted motor recovery after SCI.NEW & NOTEWORTHY After motor complete spinal cord injury, the human spinal cord receiving epidural stimulation can promote both orderly and inverse trends of motor neuron recruitment. The engagement of spinal networks involved in the generation of rhythmic activity seems to favor orderly recruitment trends.

Highlights

  • Chronic, clinically motor complete spinal cord injury (SCI) disrupts the communication within the nervous system, leading to loss of motor function below the level of injury

  • We studied the recruitment order of motor neurons during standing motor function enabled by spinal cord epidural stimulation (scES) in individuals with chronic motor complete SCI

  • We found that conduction velocity and amplitude of scES-evoked responses were modulated over time, and that this modulation resulted in significant trends of inverse or orderly motor neuron recruitment order

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Summary

Introduction

Clinically motor complete spinal cord injury (SCI) disrupts the communication within the nervous system, leading to loss of motor function below the level of injury. Proof of principle studies have demonstrated that the application of spinal cord epidural stimulation (scES) combined with activitybased training can promote remarkable motor function recovery in this population as well as in individuals with incomplete SCI [4,5,6,7,8]. These studies suggest that scES can modulate the excitability of the spinal circuitry controlling posture and locomotion, so that sensory information can serve as a source of control for generating appropriate motor patterns during standing and stepping.

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