Interlimb Reflexes Induced by Electrical Stimulation of Cutaneous Nerves after Spinal Cord Injury

Abstract

Whether interlimb reflexes emerge only after a severe insult to the human spinal cord is controversial. Here the aim was to examine interlimb reflexes at rest in participants with chronic (>1 year) spinal cord injury (SCI, n = 17) and able-bodied control participants (n = 5). Cutaneous reflexes were evoked by delivering up to 30 trains of stimuli to either the superficial peroneal nerve on the dorsum of the foot or the radial nerve at the wrist (5 pulses, 300 Hz, approximately every 30 s). Participants were instructed to relax the test muscles prior to the delivery of the stimuli. Electromyographic activity was recorded bilaterally in proximal and distal arm and leg muscles. Superficial peroneal nerve stimulation evoked interlimb reflexes in ipsilateral and contralateral arm and contralateral leg muscles of SCI and control participants. Radial nerve stimulation evoked interlimb reflexes in the ipsilateral leg and contralateral arm muscles of control and SCI participants but only contralateral leg muscles of control participants. Interlimb reflexes evoked by superficial peroneal nerve stimulation were longer in latency and duration, and larger in magnitude in SCI participants. Interlimb reflex properties were similar for both SCI and control groups for radial nerve stimulation. Ascending interlimb reflexes tended to occur with a higher incidence in participants with SCI, while descending interlimb reflexes occurred with a higher incidence in able-bodied participants. However, the overall incidence of interlimb reflexes in SCI and neurologically intact participants was similar which suggests that the neural circuitry underlying these reflexes does not necessarily develop after central nervous system injury.

Combined Supra- and Sub-Lesional Epidural Electrical Stimulation for Restoration of the Motor Functions after Spinal Cord Injury in Mini Pigs

“…The neural networks below and above the injury may form a translesional network, which can reorganize over time in functional neuronal structure involved in the restoration of the motor functions, such as volitional motor control with EES. It is expected that electrical stimulation of the spinal networks above the injury may facilitate the activity of the neuronal circuitry below the injury, particularly when downstream pathways from the brain are unable to effectively grow through the injury and provide required interaction between neural networks above and below the injury [ 33 , 34 , 35 , 36 , 37 ]. The propriospinal system consists of short and long axons that interconnect most of the spinal segments promoting modulation during the execution of the most motor commands [ 75 , 76 ], which appears to be an important component in restoring functions in the absence of sufficient axons directly interacting with the corticospinal tracts.…”

“…The propriospinal network provides coordination between multiple spinal segments and between upper and lower limbs during complex motor patterns like locomotion [ 25 ] and likely involved in the coordination of the sensorimotor information along with activation of the local spinal network for upper and lower extremities for synergistic coordination of motor outcome [ 15 , 16 , 32 ]. Multiple evidence suggests that spinal cord circuitry above and below the SCI could participate in the restoration of the sensorimotor function after SCI [ 33 , 34 , 35 , 36 , 37 ]. At the same time, the effect of spinal cord stimulation applied above or combined stimulation applied above and below SCI remains virtually unknown.…”

Identification of residual descending pathways after human spinal cord injury.

“…One such report recently described modulation of baseline EMG in arm and leg muscles after SCI in response to superficial peroneal and radial nerve stimulation, respectively. Descending interlimb reflexes in response to radial nerve stimulation were reported in just 6% (4 total muscles) of ipsilateral and and 0% contralateral muscles out of 17 participants with cervical SCI (Butler, Godfrey et al 2016). Considering that Butler et al used large pulse trains at higher stimulation intensities than applied here, this discrepancy with the current results appears surprising.…”

“…Recent studies have demonstrated that residual descending influence can be electrically evoked through corticospinal, vestibulospinal, and descending interlimb pathways, however response rates in motor complete SCI individuals has been minimal in muscles innervated by the lumbosacral enlargement (Barthelemy, Willerslev-Olsen et al 2015, Butler, Godfrey et al 2016, Squair, Bjerkefors et al 2016. As discussed by the authors, electrically evoked responses in quiescent muscles may be difficult to obtain even in neurologically intact individuals, with the problem being compounded after SCI.…”

“…However, the consistent nature and extent of facilitation observed in heteronymous muscles when the excitability of the lumbosacral circuitry was altered by transcutaneous spinal stimulation is in contrast to that observed in a similar study in which descending reflexes were identified in quiescent knee and ankle flexor and extensor muscles via modulation of baseline EMG. Under these conditions, less than 25% of all muscles studied demonstrated descending interlimb modulation (Butler, Godfrey et al 2016). As such, it seems more likely that descending interlimb and multisegmental afferent inputs are integrated by pre-motor interneurons, thus modulating the excitability state of the entire motor neuron pool.…”