Transspinal stimulation increases motoneuron output of multiple segments in human spinal cord injury

Abstract

Targeted neuromodulation strategies that strengthen neuronal activity are in great need for restoring sensorimotor function after chronic spinal cord injury (SCI). In this study, we established changes in the motoneuron output of individuals with and without SCI after repeated noninvasive transspinal stimulation at rest over the thoracolumbar enlargement, the spinal location of leg motor circuits. Cases of motor incomplete and complete SCI were included to delineate potential differences when corticospinal motor drive is minimal. All 10 SCI and 10 healthy control subjects received daily monophasic transspinal stimuli of 1-ms duration at 0.2 Hz at right soleus transspinal evoked potential (TEP) subthreshold and suprathreshold intensities at rest. Before and two days after cessation of transspinal stimulation, we determined changes in TEP recruitment input-output curves, TEP amplitude at stimulation frequencies of 0.1, 0.125, 0.2, 0.33 and 1.0 Hz, and TEP postactivation depression upon transspinal paired stimuli at interstimulus intervals of 60, 100, 300, and 500 ms. TEPs were recorded at rest from bilateral ankle and knee flexor/extensor muscles. Repeated transspinal stimulation increased the motoneuron output over multiple segments. In control and complete SCI subjects, motoneuron output increased for knee muscles, while in motor incomplete SCI subjects motoneuron output increased for both ankle and knee muscles. In control subjects, TEPs homosynaptic and postactivation depression were present at baseline, and were potentiated for the distal ankle or knee flexor muscles. TEPs homosynaptic and postactivation depression at baseline depended on the completeness of the SCI, with minimal changes observed after transspinal stimulation. These results indicate that repeated transspinal stimulation increases spinal motoneuron responsiveness of ankle and knee muscles in the injured human spinal cord, and thus can promote motor recovery. This noninvasive neuromodulation method is a promising modality for promoting functional neuroplasticity after SCI.

Repeated transspinal stimulation decreases soleus H-reflex excitability and restores spinal inhibition in human spinal cord injury

“…Individuals with motor complete SCI were included in order to assess potential changes in presence of minimal descending inputs. Both SCI and healthy control subjects participated in a previous study [10], and are identified here with the same code.…”

“…A single reusable self-adhered cathode electrode (10.2 × 5.1 cm 2 , Uni-Patch, Massachusetts, USA) was placed at T10 equally spaced along the vertebrae ending at L1-2. Two interconnected electrodes (anode, same type as the cathode) were placed on either side of the abdominal muscles or iliac crests depending on each subject’s reported level of comfort or if stimulation caused bladder discomfort [7,8,10,17,18]. Stimulation was delivered by a constant current stimulator (DS7A or DS7AH, Digitimer, Welwyn Garden City, UK) that was triggered by Spike 2 scripts (Cambridge Electronics Design Ltd., Cambridge, UK).…”

“…Knee and hip joints were flexed at 30°, ankles were supported in a neutral position, and legs were maintained in midline via external support. Similar to stimulation parameters we have previously used [10,17], transspinal stimulation was delivered as a 1-ms single monophasic square pulse at 0.2 Hz based on the postulated interactions between the motor evoked potentials and TEPs [18], and between the soleus H reflex and TEPs [7,11] at the spinal cord. Individuals with SCI received a total of 16.6 ± 1 stimulation sessions for an average of 60 ± 2 min per session (Table 1).…”

“…Stimulation of the primary motor cortex, spinal cord, peripheral nerve(s), and muscle(s) has been employed to improve sensorimotor function after spinal cord injury (SCI) [1–6]. Transcutaneous spinal cord (termed here transspinal) stimulation delivered via single monophasic pulses generates transspinal evoked potentials (TEPs) simultaneously in both legs of individuals with and without SCI that have distinct characteristics regarding their latency, duration, shape, and spinal integration [7–10]. We have recently demonstrated that TEPs summate in surface electromyogram (EMG) with spinal (H reflex) and peripheral (M wave) responses [11], supporting for a specific control of transspinal stimulation on spinal proprioceptive neuronal pathways.…”

“…Specifically, the soleus TEP summates with the soleus H reflex when these two action potentials interact at the peripheral nerve axons [11], while at long stimulation delays the H reflex is depressed or completely abolished [7,11]. A single session of transspinal stimulation decreased ankle clonus and spasticity in a few cases of incomplete or complete SCI [12–14], while multiple sessions improved responsiveness of motoneurons spanning multiple spinal segments after SCI in humans [10].…”