Epidural electrical stimulation of the lumbar spinal cord is currently regaining momentum as a neuromodulation intervention in spinal cord injury (SCI) to modify dysregulated sensorimo-tor 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. PLOS ONE | https://doi.org/10.1371/journal.pone.
Features of the human spinal cord motor control are described using two spinal cord injury models: (i) the spinal cord completely separated from brain motor structures by accidental injury; (ii) the spinal cord receiving reduced and altered supraspinal input due to an incomplete lesion. Systematic studies using surface electrode polyelectromyography were carried out to assess skeletal muscle reflex responses to single and repetitve stimulation in a large number of subjects. In complete spinal cord injured subjects the functional integrity of three different neuronal circuits below the lesion level is demonstrated: first, simple mono- and oligosynaptic reflex arcs and polysynaptic pathways; second, propriospinal interneuron system with their cell in the gray matter and the axons in the white matter of the spinal cord conducting activity between different spinal cord segments; and third, internuncial gray matter neurons with short axons and dense neuron contact within the spinal gray matter. All of these three systems participate continuously in the generation of spinal cord reflex output activating muscles. The integration of these systems and their relative degree of excitation and set-up produces characteristic functions of motor control. In incomplete spinal cord injured patients, the implementation of brain motor control depends on the profile of residual brain descending input and its integration with the functional neuronal circuits below the lesion. Locomotor patterns result from the establishment of a new structural relationship between brain and spinal cord. The functions of this new structural relationship are expressed as an alternative, but characteristic and consistent neurocontrol. The more we know about how the brain governs spinal cord networks, the better we can describe human motor control. On the other hand such knowledge is essential for the restoration of residual functions and for the construction of new cord circuitry to expand the functions of the injured spinal cord.
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