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

doi:10.1016/S0140-6736(11)60547-3

The Lancet

Volume 377, Issue 9781, 4–10 June 2011, Pages 1938-1947

https://doi.org/10.1016/S0140-6736(11)60547-3 Get rights and content

Summary

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.

Introduction

The mammalian spinal cord can generate locomotor output in the absence of input from the brain1, 2, 3 by central pattern generation.4, 5, 6 Cats with complete transection of the spinal cord (spinal cats) can stand and step when sensory input is provided to the lumbosacral pattern generator circuitry.7, 8, 9 Spinal cats can learn to stand, fully supporting their hindquarters, and to step at a range of speeds and load-bearing levels with task-specific training. Adult spinally transected rats can step only with a combination of interventions of locomotor training, pharmacological intervention, and epidural stimulation.10, 11 This evidence led to the hypothesis that if similar spinal circuits exist in human beings, then electrically stimulating the lumbosacral spinal cord epidurally coupled with intense training could facilitate standing and stepping in patients with a clinically motor complete spinal cord injury (SCI).

Improvements in walking have been achieved with intense locomotor training in patients with SCI who have detectable voluntary movement of the legs12, 13, 14 but not in those with clinically motor complete SCI.15, 16, 17 Rhythmic efferent activity timed to the step cycle can occur during manually facilitated stepping, and bilateral tonic activity can occur during partial weight-bearing standing after a clinically motor complete SCI. Rhythmic and tonic motor patterns of the legs have been induced with18, 19, 20, 21, 22 and without23, 24, 25 epidural stimulation in patients with clinically motor complete SCI while lying supine. This finding suggests that spinal circuitry for locomotion is present in human beings but that human beings cannot functionally complete these tasks without some crucial level of excitability from supraspinal centres that are present after incomplete SCI.

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. We tested this hypothesis by epidural stimulation of the dura of a man with paraplegia who had clinically motor complete SCI.

Section snippets

Clinical characteristics before implantation

A 23-year-old man, who was hit by a motor vehicle in July 2006, 3·4 years before implantation in December 2009, was included in this study. Neurological examination at hospital admission revealed paraplegia from a C7–T1 subluxation with injury to the lower cervical and upper thoracic spinal cord. The patient was able to do weak voluntary contraction of the triceps and intrinsic hand muscles but he had no contraction of trunk or leg muscles. He received emergency treatment after the accident;

Results

The mean total duration of stimulation was 54 min (SD 13) per session. The patient was always aware of the presence of the stimulation. The most common sensation was a tingling feeling localised to the electrode implantation site and in those muscles that were targeted for activation. Paraesthesia also routinely occurred in the trunk, hips, and legs and varied according to the stimulation intensity; however, these sensations never reached a level of substantial discomfort or pain and never

Discussion

With an epidurally implanted electrode array, we modulated the physiological state of the spinal circuitry to enable full weight-bearing standing in a patient with a chronic clinically motor complete SCI. This phenomenon was observed on the first attempt at standing. Epidural stimulation did not induce standing by directly activating motor pools, but enabled motor function by stimulating afferent fibres in the dorsal root and engaging populations of interneurons that integrated load-bearing

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

Summary

Background

Methods

Findings

Interpretation

Funding

Introduction

Section snippets

Clinical characteristics before implantation

Results

Discussion

Exp Neurol

Brain Res Rev

Brain Res

Lancet

Brain Res Rev

Hum Mov Sci

Neurobiological bases of rhythmic motor acts in vertebrates

Science

Central pattern generators for locomotion, with special reference to vertebrates

Ann Rev Neurosci

The motor infrastructure: from ion channels to neuronal networks

Nat Rev Neurosci

On the central generation of locomotion in the low spinal cat

Exp Brain Res

Locomotor capacity attributable to step training versus spontaneous recovery after spinalization in adult cats

J Neurophysiol

Full weight-bearing hindlimb standing following stand training in the adult spinal cat

J Neurophysiol

Transformation of nonfunctional spinal circuits into functional states after the loss of brain input

Nat Neurosci

Step training reinforces specific spinal locomotor circuitry in adult spinal rats

J Neurosci

Laufband locomotion with body weight support improved walking in persons with severe spinal cord injuries

Paraplegia

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