Epidural and transcutaneous spinal cord stimulation facilitates descending inputs to upper-limb motoneurons in monkeys

Abstract

Objective. There is renewed interest in epidural and transcutaneous spinal cord stimulation (SCS) as a therapy following spinal cord injury, both to reanimate paralyzed muscles as well as to potentiate weakened volitional control of movements. However, most work to date has focussed on lumbar SCS for restoration of locomotor function. Therefore, we examined upper-limb muscle responses and modulation of supraspinal-evoked movements by different frequencies of cervical SCS delivered to various epidural and transcutaneous sites in anaesthetized, neurologically intact monkeys. Approach. Epidural SCS was delivered via a novel multielectrode cuff placed around both dorsal and ventral surfaces of the cervical spinal cord, while transcutaneous SCS was delivered using a high carrier frequency through surface electrodes. Main results. Ventral epidural SCS elicited robust movements at lower current intensities than dorsal sites, with evoked motor unit potentials that reliably followed even high-frequency trains. By contrast, the muscle responses to dorsal SCS required higher current intensities and were attenuated throughout the train. However, dorsal epidural SCS and, to a lesser extent, transcutaneous SCS were effective at facilitating supraspinal-evoked responses, especially at intermediate stimulation frequencies. The time- and frequency-dependence of dorsal SCS effects could be explained by a simple model in which transynaptic excitation of motoneurons was gated by prior stimuli through presynaptic mechanisms. Significance. Our results suggest that multicontact electrodes allowing access to both dorsal and ventral epidural sites may be beneficial for combined therapeutic purposes, and that the interaction of direct, synaptic and presynaptic effects should be considered when optimising SCS-assisted rehabilitation.