Common neural structures activated by epidural and transcutaneous lumbar spinal cord stimulation: Elicitation of posterior root-muscle reflexes.

Ursula S Hofstoetter,Heinrich Binder,Brigitta Freundl,Karen Minassian,Norbert Weidner

doi:10.1371/journal.pone.0192013

Abstract

Epidural electrical stimulation of the lumbar spinal cord is currently regaining momentum as a neuromodulation intervention in spinal cord injury (SCI) to modify dysregulated sensorimotor functions and augment residual motor capacity. There is ample evidence that it engages spinal circuits through the electrical stimulation of large-to-medium diameter afferent fibers within lumbar and upper sacral posterior roots. Recent pilot studies suggested that the surface electrode-based method of transcutaneous spinal cord stimulation (SCS) may produce similar neuromodulatory effects as caused by epidural SCS. Neurophysiological and computer modeling studies proposed that this noninvasive technique stimulates posterior-root fibers as well, likely activating similar input structures to the spinal cord as epidural stimulation. Here, we add a yet missing piece of evidence substantiating this assumption. We conducted in-depth analyses and direct comparisons of the electromyographic (EMG) characteristics of short-latency responses in multiple leg muscles to both stimulation techniques derived from ten individuals with SCI each. Post-activation depression of responses evoked by paired pulses applied either epidurally or transcutaneously confirmed the reflex nature of the responses. The muscle responses to both techniques had the same latencies, EMG peak-to-peak amplitudes, and waveforms, except for smaller responses with shorter onset latencies in the triceps surae muscle group and shorter offsets of the responses in the biceps femoris muscle during epidural stimulation. Responses obtained in three subjects tested with both methods at different time points had near-identical waveforms per muscle group as well as same onset latencies. The present results strongly corroborate the activation of common neural input structures to the lumbar spinal cord—predominantly primary afferent fibers within multiple posterior roots—by both techniques and add to unraveling the basic mechanisms underlying electrical SCS.

Highlights

Epidural spinal cord stimulation (SCS) is generally known as a neuromodulatory therapy for the relief of chronic, intractable pain of the trunk and limbs [1,2,3]
SCS has experienced a resurgence of interest in spinal cord injury (SCI) research and neurorehabilitation following promising studies that demonstrated the alleviation of severe lower-limb spasticity [13], the generation of motor output underlying lower-limb extension [14] and standing [15,16], the generation [17,18,19] or augmentation [15,20,21,22] of rhythmic and locomotor-like lower-limb activity, and studies that rediscovered the effect of enabling some volitional movements [23] in otherwise paralyzed legs [12,15,24,25,26] when the stimulation was applied over the lumbar spinal cord
We considered recordings during epidural SCS with the bipolar electrode combinations of 0–3+ and 0+3, i.e., with either the most rostral or most caudal contact of the 3487A lead selected as the stimulating cathode (‘–’), as these two settings were routinely tested in all patients

Summary

Introduction

Epidural spinal cord stimulation (SCS) is generally known as a neuromodulatory therapy for the relief of chronic, intractable pain of the trunk and limbs [1,2,3]. The prevailing view is that, depending on the applied SCS parameters [12,30,31], the stimulation-induced afferent input transsynaptically recruits various spinal reflex circuits [12,29,32], circuits involved in the regulation of proprioceptive input and motoneuronal excitability [13,33], and rhythm and pattern generating neural networks [19,30,34]. A recent functional neuroanatomical study of the swine lumbar spinal cord demonstrated that in a large animal model with closer similarity to human vertebral morphometry, an epidural electrode position in proximity to the roots is a critical factor to evoke responses in the hindlimb muscles [37]

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