Transcutaneous spinal stimulation in people with and without spinal cord injury: Effect of electrode placement and trains of stimulation on threshold intensity

Abstract

Transcutaneous spinal cord stimulation (TSS) is purported to improve motor function in people after spinal cord injury (SCI). However, several methodology aspects are yet to be explored. We investigated whether stimulation configuration affected the intensity needed to elicit spinally evoked motor responses (sEMR) in four lower limb muscles bilaterally. Also, since stimulation intensity for therapeutic TSS (i.e., trains of stimulation, typically delivered at 15-50 Hz) is sometimes based on the single-pulse threshold intensity, we compared these two stimulation types. In non-SCI participants (n = 9) and participants with a SCI (n = 9), three different electrode configurations (cathode-anode); L1-midline (below the umbilicus), T11-midline and L1-ASIS (anterior superior iliac spine; non-SCI only) were compared for the sEMR threshold intensity using single pulses or trains of stimulation which were recorded in the vastus medialis, medial hamstring, tibialis anterior, medial gastrocnemius muscles. In non-SCI participants, the L1-midline configuration showed lower sEMR thresholds compared to T11-midline (p = 0.002) and L1-ASIS (p < 0.001). There was no difference between T11-midline and L1-midline for participants with SCI (p = 0.245). Spinally evoked motor response thresholds were ~13% lower during trains of stimulation compared to single pulses in non-SCI participants (p < 0.001), but not in participants with SCI (p = 0.101). With trains of stimulation, threshold intensities were slightly lower and the incidence of sEMR was considerably lower. Overall, stimulation threshold intensities were generally lower with the L1-midline electrode configuration and is therefore preferred. While single-pulse threshold intensities may overestimate threshold intensities for therapeutic TSS, tolerance to trains of stimulation will be the limiting factor in most cases.

Keywords: spinal cord injury; transcutaneous spinal stimulation.

FIGURE 1

Experimental setup for transcutaneous spinal stimulation. (a) Shows the two different electrode configurations. The cathode electrode (10 × 5 cm) was placed vertically along the midline at T11 (black) or L1 (red). The anode electrode was placed horizontally along the midline of the abdomen (10 × 5 cm) approximately 3 cm above the pubic symphysis or on both anterior superior iliac spines (ASIS; 5 × 5 cm). (b) Testing position for participants with spinal cord injury: tilt table inclined to 55°. Electromyography (EMG) electrodes were placed bilaterally over the vastus medialis, tibialis anterior, medial gastrocnemius, and medial hamstring muscles. (c) Testing position for non‐SCI participants: suspended in body‐weight support harness. The same EMG set‐up was used. (d) Schematic representation of the stimulation waveform used for single pulses and trains of stimulation. Each pulse contained 10, 40 μs biphasic pulses at 10 kHz; trains were delivered at 20 Hz.

FIGURE 2

Representative spinally evoked motor response (sEMR) for a participant with a spinal cord injury for the single pulses (a) and trains of stimulation (b) for the four muscles on the right side. The electrode configuration used was L1‐midline. Individual traces (gray; single pulses n = 5; trains of stimulation n = 30) and the average waveform (black) are shown. The * indicates the threshold intensity to evoke sEMR for each muscle (see Section 2). The vertical line indicates the timing of the single‐pulse transcutaneous spinal stimulation. Ham, medial hamstring muscle; MG, medial gastrocnemius muscle; TA, tibialis anterior muscle; VM, Vastus medialis muscle.

FIGURE 3

Incidence of a spinally evoked motor response (sEMR) for each muscle group and electrode configuration (blue: T11‐midline; orange: L1‐ASIS; green: L1‐midline). Solid bars to the left of each muscle label represent muscles on the left side of the body; lighter bars to the right of each muscle label represent muscles on the right side of the body. The incidence of sEMR in non‐spinal cord injury participants (n = 9) is shown in panels (a; single pulses) and (c; trains of stimulation). The incidence of sEMR in participants with spinal cord injury (n = 9) is shown in panels (b; single pulses) and (d; trains of stimulation). The L1‐ASIS electrode configuration was not tested in participants with a spinal cord injury. ASIS, anterior superior iliac spines; Ham, medial hamstring muscle; MG, medial gastrocnemius muscle; SCI, spinal cord injury; TA, tibialis anterior muscle; VM, vastus medialis muscle.

FIGURE 4

Intensities at which the first (triangle) and last (circle) spinally evoked motor responses (sEMR) were evoked for each participant for each electrode configuration (blue: T11‐midline; orange: L1‐ASIS; green: L1‐midline). If sEMR were not evoked in all 8 muscles (bilateral vastus medialis, tibialis anterior, medial gastrocnemius and medial hamstring muscles), a number is included to the left of the triangle to indicate the total number of muscles that showed sEMR. The dashed line represents increases in stimulation intensity without recruiting additional sEMR. The ‘x’ symbol indicates the intensity reached in cases where no sEMR was evoked for that experimental condition. ASIS, anterior superior iliac spine; SCI, spinal cord injury.

FIGURE 5

The stimulation threshold intensity (mA) to elicit a spinally evoked motor response (sEMR). Results for non‐spinal cord injury (non‐SCI) participants are in the left panels (a–d) and those for participants with a SCI are in the right panels (e–h). (a, e) Stimulation threshold intensity for single pulses in the left and right legs (all muscles pooled; left sub‐panel) and differences between the right and left legs (right sub‐panel). (b, f) Stimulation threshold intensity in each muscle group (left and right muscles pooled) for each electrode configuration (Blue, T11‐midline; Orange, L1‐ASIS; Green, L1‐midline). (c, g) Rank (out of 8, 1 = first recruited) of the stimulation threshold intensity across muscles (left and right muscles pooled). The count of no response (NR) for each muscle and electrode configuration is displayed at the top of the panel. Black circles indicate group means; error bars standard deviation for all figures except (c) and (g) which display the median and interquartile range. (d, h) Stimulation threshold intensity to evoke sEMR with trains of stimulation for each muscle group (left and right sides pooled), and electrode configurations. ASIS, anterior superior iliac spine; Ham, medial hamstring muscle; MG, medial gastrocnemius muscle; TA, tibialis anterior muscle; VM, vastus medialis muscle.

FIGURE 6

Comparison of stimulation threshold intensity to elicit spinally evoked motor response (sEMR) with single pulses and trains of stimulation. Results for non‐spinal cord injury (non‐SCI) participants are in the left panels (a–d) and those for participants with a SCI are in the right panels (e–h). (a, e) Results, pooled across muscles and sides, where single pulses (●) and trains of stimulation (■) both elicited a sEMR (‘Both’); if trains of stimulation did not elicit sEMR, the highest intensity reached during trains of stimulation (▲) was compared to the stimulation threshold intensity for single pulses (‘Highest intensity for trains’). (b, f) Differences between stimulation threshold intensity for single pulses and trains stimulation of the data depicted in panels A and E: right (♦) and left (◊) side muscles. (c, g) Comparison of stimulation threshold intensity to elicit a sEMR with single pulse pulses (●) and trains of stimulation (■) for each muscle group (left and right sides combined). (d, h) Comparison of threshold stimulation intensity required to elicit a sEMR with single pulses (●) and trains of stimulation (■) for each electrode configuration (Blue, T11‐midline; Orange, L1‐ASIS; Green, L1‐midline). Large symbols and error bars are means and standard deviations. ASIS, anterior superior iliac spine; Ham, medial hamstring muscle; MG, medial gastrocnemius muscle; TA, tibialis anterior muscle; VM, vastus medialis muscle.