Ipsi- and Contralateral Oligo- and Polysynaptic Reflexes in Humans Revealed by Low-Frequency Epidural Electrical Stimulation of the Lumbar Spinal Cord.

Ursula S Hofstoetter,Peter Lackner,Brigitta Freundl,Simon M Danner,Karen Minassian,Heinrich Binder

doi:10.3390/brainsci11010112

Abstract

Epidural electrical stimulation (EES) applied over the human lumbosacral spinal cord provides access to afferent fibers from virtually all lower-extremity nerves. These afferents connect to spinal networks that play a pivotal role in the control of locomotion. Studying EES-evoked responses mediated through these networks can identify some of their functional components. We here analyzed electromyographic (EMG) responses evoked by low-frequency (2–6 Hz) EES derived from eight individuals with chronic, motor complete spinal cord injury. We identified and separately analyzed three previously undescribed response types: first, crossed reflexes with onset latencies of ~55 ms evoked in the hamstrings; second, oligosynaptic reflexes within 50 ms post-stimulus superimposed on the monosynaptic posterior root-muscle reflexes in the flexor muscle tibialis anterior, but with higher thresholds and no rate-sensitive depression; third, polysynaptic responses with variable EMG shapes within 50–450 ms post-stimulus evoked in the tibialis anterior and triceps surae, some of which demonstrated consistent changes in latencies with graded EES. Our observations suggest the activation of commissural neurons, lumbar propriospinal interneurons, and components of the late flexion reflex circuits through group I and II proprioceptive afferent inputs. These potential neural underpinnings have all been related to spinal locomotion in experimental studies.

Highlights

A growing number of studies have demonstrated that epidural electrical stimulation (EES) can engage spinal neural circuits to enable overground walking in individuals with severe spinal cord injury (SCI) [1,2,3,4]
EES studies in individuals with SCI have revealed the elicitation of monosynaptic spinal reflexes, termed posterior root-muscle (PRM) reflexes according to their initiation and detection sites [21,22,23], the activation of premotoneuronal inhibitory circuits [24], the recruitment of a flexion synergy exploited for facilitating the swing phase for walking [1], and the generation of rhythmic activities resembling the output of central pattern generators observed in experimental animals [25,26,27]
Unilateral stimulation of lumbar posterior roots was corroborated by the low thresholds of the ipsilateral monosynaptic PRM reflexes in rectus femoris (RF) and the 2.7–6.0 times higher thresholds or absence of contralateral monosynaptic PRM reflexes in the thigh muscle groups (Table 2)

Summary

Introduction

A growing number of studies have demonstrated that epidural electrical stimulation (EES) can engage spinal neural circuits to enable overground walking in individuals with severe spinal cord injury (SCI) [1,2,3,4]. EES studies in individuals with SCI have revealed the elicitation of monosynaptic spinal reflexes, termed posterior root-muscle (PRM) reflexes according to their initiation and detection sites [21,22,23], the activation of premotoneuronal inhibitory circuits [24], the recruitment of a flexion synergy exploited for facilitating the swing phase for walking [1], and the generation of rhythmic activities resembling the output of central pattern generators observed in experimental animals [25,26,27]. Latelatency responses succeeding a monosynaptic PRM reflex in the hamstrings muscle group (Ham), evoked by 2-Hz EES in an individual with motor-complete SCI, were exemplarily shown in [6]

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Results

Conclusion