Transcutaneous Spinal Stimulation From Adults to Children: A Review

Abstract

Neuromodulation via spinal stimulation is a promising therapy that can augment the neuromuscular capacity for voluntary movements, standing, stepping, and posture in individuals with spinal cord injury (SCI). The spinal locomotor-related neuronal network known as a central pattern generator (CPG) can generate a stepping-like motor output in the absence of movement-related afferent signals from the limbs. Using epidural stimulation (EP) in conjunction with activity-based locomotor training (ABLT), the neural circuits can be neuromodulated to facilitate the recovery of locomotor functions in persons with SCI. Recently, transcutaneous spinal stimulation (scTS) has been developed as a noninvasive alternative to EP. Early studies of scTS at thoracolumbar, coccygeal, and cervical regions have demonstrated its effectiveness in producing voluntary leg movements, posture control, and independent standing and improving upper extremity function in adults with chronic SCI. In pediatric studies, the technology of spinal neuromodulation is not yet widespread. There are a limited number of publications reporting on the use of scTS in children and adolescents with either cerebral palsy, spina bifida, or SCI.

Keywords: motor recovery; neuromodulation; pediatric; spinal cord injury; spinal stimulation; transcutaneous spinal cord stimulation.

Figure 1.

Transcutaneous spinal cord stimulation electrodes placement. Schematic of anode and cathode electrode placements used in studies in adult with spinal cord injury. Stimulating electrodes are placed between spinal process of vertebral column. Cathode electrodes labelled as letter A are placed over cervical spinal cord to primarily facilitate upper extremity motor functions. Electrodes B, C, D, and E are placed over thoracolumbar and coccygeal regions of the vertebral column to facilitate posture and locomotion. The anode electrodes are placed bilaterally on the anterior superior iliac crest or on the abdomen, either side of umbilicus.

Figure 2.

Upright sitting postural control enabled by transcutaneous spinal stimulation. (A) Surface electromyography (EMG) recordings of four trunk muscles in a participant during unsupported quiet sitting without (blue) and with (red) submotor threshold stimulation. 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) Upright sitting and trunk curvature of a participant without (left) and with submotor threshold spinal stimulation (right). Note the improvement in trunk angle (green), upright posture and spinal alignment. (C) Spinal alignment during quiet sitting without (blue) and with (red) spinal stimulation from a single participant. Adapted from Rath M, Vette, AH, Ramasubramaniam S, et al. Trunk stability enabled by noninvasive spinal electrical stimulation after spinal cord injury. J Neurotrauma. 2018;35(21):2540–2553.

Figure 3.

Standing posture control enabled by transcutaneous spinal stimulation (scTS). (A) Electromyography (EMG) activity of the left leg muscles during scTS delivered with a frequency of 15 Hz at incremental intensities over L1 during sitting and standing from a single participant. (B) Participant with T9 (AIS A) injury after 20 sessions standing without assistance with stimulation at T11 at 30 Hz at 40 mA and L1 at 15 Hz at 40 mA. (C) Spinally evoked motor potentials recorded during the indicated stimulation intensities at L1 during sitting and standing. Adapted from Sayenko DG, Rath M, Ferguson AR, et al. Self-assisted standing enabled by non-invasive spinal stimulation after spinal cord injury. J Neurotrauma. 2019;36(9):1435–1450.

Figure 4.

Neural structures activated during spinal stimulation. (A) Based on the location, intensity, pulse shape, and frequency, transcutaneous spinal stimulation may activate various neuronal subtypes along the spinal cord including sensory afferents at the dorsal root entry zone, motor axons, and interneuronal circuitry. FRA = flexor reflex afferent neurons; MN = motor neurons. Adapted from Gerasimenko Y, Gorodnichev R, Moshonkina T, Sayenko D, Gad P, Reggie Edgerton V. Transcutaneous electrical spinal-cord stimulation in humans. Ann Phys Rehabil Med. 2015;58(4):225–231. (B) Analysis of electromyography (EMG) bursting activity of flexor (tibialis anterior [TA]) muscle using time windows corresponding to the monosynaptic (MN; from 20 to 30 ms) and polysynaptic (PL; from 31 to 45 ms) responses during epidural stimulation at 23 Hz. The response to each stimulus was placed to one of the windows according to its latency. Then successive time windows for each sort of the responses were reassembled into one continuous time curve. Adapted from Gerasimenko Y, Daniel O, Regnaux J, Combeaud M, Bussel B. Mechanisms of locomotor activity generation under epidural spinal cord stimulation. In: Dengler R, Kossev A, eds. Sensorimotor Control. NATO Science Series, 1: Life and Behavioural Sciences. 2001;326:164–171.

Figure 5.

Transcutaneous spinal stimulation (scTS) improves motor function in children with cerebral palsy (CP). (A) Patterns of electromyography (EMG) activity during treadmill walking in healthy and in a child with CP before and after scTS with maximal speed and average of 10 movement cycles. The gray filled curves (bottom) represent EMG envelopes of leg muscles in one noninjured participant and in one child with CP before and after treatment. (B) Cathode placement of scTS on the child. Adapted from Solopova IA, Sukhotina IA, Zhvansky DS, et al. Effects of spinal cord stimulation on motor functions in children with cerebral palsy. Neurosci Lett. 2017;639:192–198.