Effect of epidural stimulation of the lumbosacral spinal cord on voluntary movement, standing, and assisted stepping after motor complete paraplegia: a case study

Abstract

Background: Repeated periods of stimulation of the spinal cord and training increased the ability to control movement in animal models of spinal cord injury. We hypothesised that tonic epidural spinal cord stimulation can modulate spinal circuitry in human beings into a physiological state that enables sensory input from standing and stepping movements to serve as a source of neural control to undertake these tasks.

Methods: A 23-year-old man who had paraplegia from a C7-T1 subluxation as a result of a motor vehicle accident in July 2006, presented with complete loss of clinically detectable voluntary motor function and partial preservation of sensation below the T1 cord segment. After 170 locomotor training sessions over 26 months, a 16-electrode array was surgically placed on the dura (L1-S1 cord segments) in December 2009, to allow for chronic electrical stimulation. Spinal cord stimulation was done during sessions that lasted up to 250 min. We did 29 experiments and tested several stimulation combinations and parameters with the aim of the patient achieving standing and stepping.

Findings: Epidural stimulation enabled the man to achieve full weight-bearing standing with assistance provided only for balance for 4·25 min. The patient achieved this standing during stimulation using parameters identified as specific for standing while providing bilateral load-bearing proprioceptive input. We also noted locomotor-like patterns when stimulation parameters were optimised for stepping. Additionally, 7 months after implantation, the patient recovered supraspinal control of some leg movements, but only during epidural stimulation.

Interpretation: Task-specific training with epidural stimulation might reactivate previously silent spared neural circuits or promote plasticity. These interventions could be a viable clinical approach for functional recovery after severe paralysis.

Funding: National Institutes of Health and Christopher and Dana Reeve Foundation.

Conflict of interest statement

Conflicts of interest

No authors have any conflicts of interest.

Copyright © 2011 Elsevier Ltd. All rights reserved.

Figures

Figure 1. Lower extremity EMG activity during standing and stepping with body weight support prior to implantation

These data demonstrate that intensive training did not result in significant changes in efferent motor patterns. (a) Standing and (b) stepping with body weight support and manual facilitation on a treadmill prior to implantation. (c) Mean EMG amplitude for standing (solid symbols) and stepping (open symbols) across three different time points (0, 66, and 170 step training sessions). Left (L) and right (R) side muscles: rectus femoris (RF), vastus lateralis (VL), medial hamstrings (MH), tibialis anterior (TA), soleus (Sol), and medial gastrocnemius (MG). FSCAN is ground reaction force data.

Figure 2. Lower extremity EMG activity with epidural stimulation of the lumbosacral segments during standing

These data demonstrate that the output of the spinal circuitry is modulated by the proprioceptive input during standing without manual facilitation when sufficient epidural stimulation is present. (a) EMG activity increases in amplitude and becomes more constant bilaterally in most muscles as stimulation is increased in strength from 1–8V (15Hz) with a constant level of body weight support (65% BWS; 585/900N BWS). (b) Reducing body weight support from 45% to 5% (405/900 N to 45/900N) and with constant stimulation (8V, 15Hz) changed the EMG amplitudes and oscillatory patterns differently among muscles. Array diagram illustrates the stimulation configuration; anode electrodes are black and cathode electrodes are gray. Left (L) and right (R) side muscles: rectus femoris (RF), medial hamstrings (MH), tibialis anterior (TA), and medial gastrocnemius (MG). Stim indicates the stimulation intensity. Interpulse interval depicting stimulation frequency is shown at the bottom of graph a. Refer to Supplementary Video 1.

Figure 3. Lower extremity EMG activity during sitting and standing with and without epidural stimulation

There was little or no EMG activity without stimulation during sitting or standing. With increasing levels of epidural stimulation, EMG amplitudes were modulated in a tonic pattern while the subject remained sitting. During the transition from sitting to standing, amplitudes and patterns of EMG were modulated in all recorded muscles. Transition (white) from sitting (gray) to standing (yellow) with (a) no stimulation, (b) rostral (spinal segments L1-L2) stimulation (4–7.5V, 15Hz), and (c) caudal (spinal segments L4-S1) stimulation (4–7.5V, 15Hz). (d) Averaged mean EMG amplitude responses on the right side during sitting and standing with no stimulation (○), and rostral ( ) and caudal ( ) stimulation at 7.5V, 15Hz. (e) Kinematic representation of sitting to standing transition with caudal stimulation (illustration at 10 frames per sec) (Supplementary Video 2). Array diagram illustrates the stimulation configuration; anode electrodes are black and cathode electrodes are gray. Right (R) side muscles: fine wire: iliopsoas (IL); surface EMG: vastus lateralis (VL), medial hamstrings (MH), tibialis anterior (TA), soleus (Sol), and medial gastrocnemius (MG). Stim indicates the stimulation intensity. Interpulse interval depicting stimulation frequency is shown at the bottom of graphs b and c.

Figure 4. Lower extremity EMG activity with epidural stimulation during continuous full weight-bearing standing

(a) EMG activity with epidural stimulation (7.5V, 15Hz) of the lumbosacral segments during weight shifting. Center of gravity displacement in the sagittal plane depicting backward (B) and forward (F) shifts shown under the schematic diagram of the movement. (b) EMG activity with epidural stimulation (9V, 25Hz) during the transition from manually facilitated weight-bearing standing (gray) to full weight-bearing standing without manual facilitation (white). Red line indicates 3 second count down by the subject to initiation of standing without manual facilitation (Supplementary Video 3). Left (L) and right (R) side muscles: vastus lateralis (VL), medial hamstrings (MH), tibialis anterior (TA), soleus (Sol), and medial gastrocnemius (MG). Array diagram illustrates the stimulation configuration; anode electrodes are black and cathode electrodes are gray. Stim indicates the stimulation intensity. Interpulse interval depicting stimulation frequency is shown at the bottom of each graph.

Figure 5. Lower extremity EMG activity during standing and stepping with body weight support and manual facilitation with and without epidural stimulation of lumbosacral segments

The EMG patterns were modified by stimulation and by different patterns of sensory input. EMG activity during (a) manually facilitated stepping (50% BWS, 450/900N, 1.07 m/s) without stimulation, (b) standing with 25% BWS (225/900N) and with epidural stimulation (7.5 V, 30 Hz) and (c) manually facilitated stepping (50% BWS, 450/900N, 1.07 m/s) with epidural stimulation (7.5V, 30 Hz). Shaded area indicates one full step of the right leg. (d) Mean EMG activity for the medial hamstrings (MH) during stepping without stimulation ( ) and with stimulation ( ) (a and c respectively) and stepping after 170 step training sessions prior to implantation ( ) (Figure 1b). The horizontal lines represent the baseline variation in the noise of each signal. Left (L) and right (R) side muscles: vastus lateralis (VL), medial hamstrings (MH), tibialis anterior (TA), and medial gastrocnemius (MG). Load is load cell reading in Newtons (N). Sagittal joint angles for the left (L Hip) and right (R Hip) hip joint. Stance phase represented by left (L FS) and right (R FS) footswitches. Array diagram illustrates the stimulation configuration; anode electrodes are black and cathode electrodes are gray. Stim indicates the stimulation intensity. Interpulse interval depicting stimulation frequency is shown at the bottom of graph c.

Figure 6. EMG activity during voluntary leg movements in a supine position

Supraspinal control of leg movements only occurred during epidural stimulation. EMG and kinematics are shown for three different movement commands with (4V, 30Hz) and without stimulation. At the bottom of each graph the black bar (and gray shading within graph) indicates the “up” command for (a) left leg flexion, (b) left toe extension, and (c) left ankle dorsiflexion. The white bar (and no shading within graph) indicates the command to relax. Left and right EMG are shown to emphasize the isolated control of the left side following the command. There was a delay observed between the onset of the EMG activation in some muscles relative to the “up” command, while the termination of the activation often occurred prior to the command to relax. Intercostal (IC) EMG activation occurred as the subject inhaled during the performance of the voluntary leg movement. (d) Kinematic representation of leg movement (graph a) with and without epidural stimulation (illustrated at 10 frames per second). Left (L) and right (R) side muscles: fine wire: extensor hallucis longus (EHL), extensor digitorum longus (EDL), iliopsoas (IL); surface EMG: soleus (Sol), tibialis anterior (TA), peroneus longus (PL), vastus lateralis (VL), medial hamstrings (MH), adductor magnus (AD), gluteus maximus (GL), erector spinae (ES), rectus abdominus (AB), and intercostals (IC). Sagittal joint angles for the toe (1st metatarsal relative to foot), ankle, knee and hip joints. Array diagram illustrates the stimulation configuration; anode electrodes are black and cathode electrodes are gray. Stim indicates the stimulation intensity. Interpulse interval depicting stimulation frequency is shown at the bottom of graph a. Supplementary Videos 4 and 5 show voluntary control attempts with and without stimulation, respectively.