Trunk Stability Enabled by Noninvasive Spinal Electrical Stimulation after Spinal Cord Injury

Abstract

Electrical neuromodulation of spinal networks improves the control of movement of the paralyzed limbs after spinal cord injury (SCI). However, the potential of noninvasive spinal stimulation to facilitate postural trunk control during sitting in humans with SCI has not been investigated. We hypothesized that transcutaneous electrical stimulation of the lumbosacral enlargement can improve trunk posture. Eight participants with non-progressive SCI at C3-T9, American Spinal Injury Association Impairment Scale (AIS) A or C, performed different motor tasks during sitting. Electromyography of the trunk muscles, three-dimensional kinematics, and force plate data were acquired. Spinal stimulation improved trunk control during sitting in all tested individuals. Stimulation resulted in elevated activity of the erector spinae, rectus abdominis, and external obliques, contributing to improved trunk control, more natural anterior pelvic tilt and lordotic curve, and greater multi-directional seated stability. During spinal stimulation, the center of pressure (COP) displacements decreased to 1.36 ± 0.98 mm compared with 4.74 ± 5.41 mm without stimulation (p = 0.0156) in quiet sitting, and the limits of stable displacement increased by 46.92 ± 35.66% (p = 0.0156), 36.92 ± 30.48% (p = 0.0156), 54.67 ± 77.99% (p = 0.0234), and 22.70 ± 26.09% (p = 0.0391) in the forward, backward, right, and left directions, respectively. During self-initiated perturbations, the correlation between anteroposterior arm velocity and the COP displacement decreased from r = 0.5821 (p = 0.0007) without to r = 0.5115 (p = 0.0039) with stimulation, indicating improved trunk stability. These data demonstrate that the spinal networks can be modulated transcutaneously with tonic electrical spinal stimulation to physiological states sufficient to generate a more stable, erect sitting posture after chronic paralysis.

Keywords: neuromodulation; paralysis; seated posture; transcutaneous electrical spinal cord stimulation; trunk stability and control.

Conflict of interest statement

V.R.E., Y.P.G., and J.B., researchers on the study team, hold shareholder interest in NeuroRecovery Technologies. They hold certain inventorship rights on intellectual property licensed by the regents of the University of California to NeuroRecovery Technologies and its subsidiaries. The other authors have nothing to disclose.

Figures

FIG. 1.

(A) Schematic representing the experimental design protocol and interventions. Eight individuals were tested in a single experimental session without and in the presence of transcutaneous electrical spinal cord stimulation. (B) Testing room layout and experimental setup. (C) Representative participant (P5) without (left) and with submotor threshold spinal stimulation (right). Note the decrease in trunk curvature (orange), increase in trunk angle (green), and improvement in upright sitting posture and spinal alignment. Key anatomical landmarks are shown without (blue) and with stimulation (red).

FIG. 2.

(A) Schematic representing the filtering of the trunk muscle's electromyography (EMG) time series. Note that for the linear adaptive filter, the reference signal was the sum of the T11 and L1 stimulation signals. (B) Representative raw unfiltered (left) and filtered (right) EMG sample from P1 without (light blue) and with (light red) the presence of stimulation. (C) Zoomed in, 50 ms sample of raw unfiltered (left) and filtered (right) EMG without (light blue) and with (light red) stimulation. The orange and green dashed lines indicate the enlarged segments without and with stimulation, respectively.

FIG. 3.

Acute effects of submotor threshold spinal stimulation on center of pressure (COP) parameters during unsupported quiet sitting for eight participants. (A) Normalized COP excursion density for all eight participants with their eyes open without (left) and with submotor threshold spinal stimulation (right). The density indicates time spent at each position for all participants. Below, a scattergram between the erector spinae at the T7 level (E-T7) and external obliques (Obl) without and with stimulation in one representative participant (P2) is shown. (B) Mean amplitude and standard deviation of mean COP displacement (left) and mean COP acceleration (right) without (blue) and with (red) stimulation; A two tailed nonparametric Wilcoxon signed-rank test was used for assessing differences between stimulation conditions; n = 8, *statistical significance, α < 0.05. A lower COP amplitude and acceleration are indicative of better control. (C) Mean electromyography (EMG) between stimulation conditions of E-T7, erector spinae at the L-3 level (E-L3), Obl, rectus abdominus (RA), and rectus femoris (RF). Note the significant change in activity of E-T7, E-L3, and Obl; two tailed nonparametric Wilcoxon signed-rank test in which n = 7 and α < 0.05. P3 was omitted from EMG calculations because of the neurological level of injury of T9. Note that there is no significant change in the RF.

FIG. 4.

Characteristics of spinal stimulation during quiet sitting. (A) Electromyography (EMG) recordings of four trunk muscles from a representative participant (P2) without (blue) and with (red) submotor threshold stimulation during unsupported quiet sitting. The external obliques (Obl), rectus abdominis (RA), erector spinae at levels T7 (E-T7) and L3 (E-L3), and rectus femoris (RF) are shown. (B) Spinal alignment (left), mean trunk curvature (middle), and trunk angle (right) during quiet sitting without (blue) and with (red) spinal stimulation. A 5 sec window was used (4–9 sec after trial onset) to determine the mean trunk curvature, horizontal distance between the hip (anterior-superior iliac crest), and maximal trunk displacement during quiet upright sitting. The pelvis is assumed to be fixed at the origin. Higher values in trunk curvature indicate a decrease in trunk extension and more kyphotic (C-shaped) sitting. Higher values of trunk angle indicate more upright sitting. Individual data for all participants are shown via symbols. *statistical significance, two-tailed nonparametric Wilcoxon signed-rank test, in which n = 8 and α < 0.05.

FIG. 5.

Acute effects of submotor threshold spinal stimulation on the limits of stability (LoS) during the “octagon” multi-directional leaning test. (A) Density plot of the center of pressure (COP) excursions during the “octagon” test for a representative participant (P2) without (left) and with (right) spinal stimulation. The distribution of directional displacement events, occurrence of a magnitude of displacement binned into uniform time windows, is shown in both the mediolateral (M-L) direction above each density plot and in the anteroposterior (A-P) direction to the right of each density plot. Note the distribution of the bins; the presence of spinal stimulation results in a more normal distribution of movement. (B) The M-L and A-P time series, with positive values representing the directions right and forward, and negative values representing the directions left and backward. The pooled percent increases in the LoS in the presence of spinal stimulation compared with no stimulation for all participants (n = 8) are shown to the right of each time series plot. Note the significant increase in all leaning directions. *statistical significance; two tailed nonparametric Wilcoxon signed-rank test in which n = 8 and α < 0.05.

FIG. 6.

Acute effects of submotor threshold spinal stimulation on the limits of stability (LoS) during the “octagon” multi-directional leaning. (A) Three-dimensional joint kinematics showing the spinal alignment during directional leaning without (blue) and with (red) spinal stimulation in a representative participant (P6): leaning in the anteroposterior (A-P) direction (top) and mediolateral (M-L) direction (bottom). Note three-dimensional joint kinematics during the averaged start and extreme forward, backward, right, and left positions. The pelvis is assumed to be fixed at the origin. (B) Electromyographic (EMG) data from a representative participant without (blue) and with (red) stimulation for four trunk muscles in the forward, backward, right, and left directions. The external obliques (Obl), rectus abdominis (RA), erector spinae at levels T7 (E-T7) and L3 (E-L3), and rectus femoris (RF) are shown. Note the change in magnitude of muscle activity. (C) The change in trunk curvature in the presence of stimulation during the A-P (left) and M-L (right) directions (n = 8, α < 0.05). A decrease in trunk curvature indicates more upright neutral spinal alignment. ‡statistical significance. The mean EMG activity levels and their standard deviations during each directional leaning without (blue) and with (red) spinal stimulation are shown (n = 7, α < 0.05, P3 was omitted from EMG calculations because of an NLI of T9). *statistical significance between the corresponding values during quiet sitting and leaning in the indicated direction.

FIG. 7.

Acute effects of transcutaneous spinal stimulation on the anteroposterior center of pressure (COP) excursion during the self-initiated perturbation (SiP) test. (A) Self-initiated perturbation. Below, the average electromyographic activity of the anterior deltoid (AD), rectus femoris (RF), rectus abdominis (RA), and erector spinae at level T7 (E-T7) along with the anteroposterior (A-P) COP displacement of one representative participant (P2) without (left) and with (right) spinal stimulation is shown. Individual (colored traces) as well as the average COP displacements (black trace) are shown. The magnitude of average anterior (green) and posterior (yellow) displacement are shown. (B) Pooled electromyography activity (EMG) of the E-T7, RF, and RA during the self-initiated perturbation without (blue) and with (red) stimulation. Note the change in EMG activity in the indicated muscles. *statistical significance between the mean EMG with stimulation and the mean EMG without stimulation. (C) Mean angular arm velocity versus A-P COP for all trials. Note the increase in arm velocity with stimulation (red) compared with without stimulation (blue) (n = 6, α < 0.05).