Stepping-like movements in humans with complete spinal cord injury induced by epidural stimulation of the lumbar cord: electromyographic study of compound muscle action potentials

Abstract

Study design: It has been previously demonstrated that sustained nonpatterned electric stimulation of the posterior lumbar spinal cord from the epidural space can induce stepping-like movements in subjects with chronic, complete spinal cord injury. In the present paper, we explore physiologically related components of electromyographic (EMG) recordings during the induced stepping-like activity. Objectives: To examine mechanisms underlying the stepping-like movements activated by electrical epidural stimulation of posterior lumbar cord structures. Materials and methods: The study is based on the assessment of epidural stimulation to control spasticity by simultaneous recordings of the electromyographic activity of quadriceps, hamstrings, tibialis anterior, and triceps surae. We examined induced muscle responses to stimulation frequencies of 2.2-50 Hz in 10 subjects classified as having a motor complete spinal cord injury (ASIA A and B). We evaluated stimulus-triggered time windows 50 ms in length from the original EMG traces. Stimulus-evoked compound muscle action potentials (CMAPs) were analyzed with reference to latency, amplitude, and shape. Results: Epidural stimulation of the posterior lumbosacral cord recruited lower limb muscles in a segmental-selective way, which was characteristic for posterior root stimulation. A 2.2 Hz stimulation elicited stimulus-coupled CMAPs of short latency which were approximately half that of phasic stretch reflex latencies for the respective muscle groups. EMG amplitudes were stimulus-strength dependent. Stimulation at 5-15 and 25-50 Hz elicited sustained tonic and rhythmic activity, respectively, and initiated lower limb extension or stepping-like movements representing different levels of muscle synergies. All EMG responses, even during burst-style phases were composed of separate stimulus-triggered CMAPs with characteristic amplitude modulations. During burst-style phases, a significant increase of CMAP latencies by about 10 ms was observed. Conclusion: The muscle activity evoked by epidural lumbar cord stimulation as described in the present study was initiated within the posterior roots. These posterior roots muscle reflex responses (PRMRRs) to 2.2 Hz stimulation were routed through monosynaptic pathways. Sustained stimulation at 5-50 Hz engaged central spinal PRMRR components. We propose that repeated volleys delivered to the lumbar cord via the posterior roots can effectively modify the central state of spinal circuits by temporarily combining them into functional units generating integrated motor behavior of sustained extension and rhythmic flexion/extension movements. This study opens the possibility for developing neuroprostheses for activation of inherent spinal networks involved in generating functional synergistic movements using a single electrode implanted in a localized and stable region.

Epidural stimulation: Comparison of the spinal circuits that generate and control locomotion in rats, cats and humans

“…There is a very consistent difference between the evoked potentials in flexor and extensor motor pools in both rats and humans (Gerasimenko et al, 2001;Minassian et al, 2004). For example, monosynaptic responses are prominent in extensor motor pools, whereas the flexor motor pools are activated predominantly polysynaptically in response to ES.…”

Epidural Stimulation Induced Modulation of Spinal Locomotor Networks in Adult Spinal Rats

“…The evoked potentials forming the late response differed in the TA and MG: the progression of the onset delays during consecutive stimuli was evident only in MG. Similarly, long-latency responses were more prominent in flexors than extensors during stimulation-induced stepping in humans (Gerasimenko et al, 2001Minassian et al, 2004) and during stimulation-and quipazine-facilitated stepping in spinal rats . The timing of recovery of weight-bearing stepping highlights the functional significance of the phase-dependent modulation of the late response in TA and MG. As suggested previously , the presence and amplitude of the late, but not middle, response appear to be related to the degree of locomotor recovery after transection.…”

Cervical multisegmental motor responses in healthy subjects

“…9 On the other hand, Gerasimenko 10 reported that such epidural stimulation of the rat spinal cord elicited early, intermediate and late responses in several extensor and flexor muscles in the hind limb. Further, they showed that those early-evoked responses are, in fact, direct stimulation of the spinal cord and not the dorsal roots.…”