Recruitment of Upper-Limb Motoneurons with Epidural Electrical Stimulation of the Primate Cervical Spinal Cord

Abstract

Epidural electrical stimulation (EES) of lumbosacral sensorimotor circuits improves leg motor control in animals and humans with spinal cord injury (SCI). Upper-limb motor control involves similar circuits, located in the cervical spinal cord, suggesting that EES could also improve arm and hand movements after quadriplegia. However, the ability of cervical EES to selectively modulate specific upper-limb motor nuclei remains unclear. Here, we combined a realistic computational model of EES of the cervical spinal cord with experiments in macaque monkeys to explore the mechanisms of this modulation and characterize the recruitment selectivity of cervical stimulation interfaces. Our results indicate that interfaces with lateral electrodes can target individual posterior roots and achieve selective modulation of arm motoneurons via the direct recruitment of pre-synaptic pathways. Intraoperative recordings suggested similar properties in humans. These results provide a framework for the design of neuro-technologies to improve arm and hand control in humans with quadriplegia.

Mapping of the Spinal Sensorimotor Network by Transvertebral and Transcutaneous Spinal Cord Stimulation

“…However, some exceptions to this rule exist; for example, the neuronal pool for TA is rostral to the ones for GM and SOL although all these muscles are located on the shin and act to the ankle joint as a flexor and extensor, respectively ( Nicolopoulos-Stournaras and Iles, 1983 ; Mohan et al, 2015 ; Wenger et al, 2016 ). A similar shift in motoneuron pools can be observed for the vastus and hamstrings groups ( Watson et al, 2009 ; Mohan et al, 2015 ; Wenger et al, 2016 ) or for the forelimb biceps and triceps motoneurons ( McKenna et al, 2000 ; Greiner et al, 2020 ). This may reflect the embryonic and phylogenetic origin of the TA and quadriceps group from the dorsal muscle mass and the origin of the SOL, GM, and hamstring group from the ventral one ( Diogo et al, 2016 ).…”

Sensory restoration by epidural stimulation of the lateral spinal cord in upper-limb amputees

“…As such, we could not determine the exact spatial arrangement of the implanted SCS electrodes relative to target neural structures. Several research groups have developed highly detailed computational modeling techniques to study how the electric fields generated in SCS interact with neural structures ( Capogrosso et al, 2013 ; Greiner et al, 2020 ; Lempka et al, 2015 ). These techniques could potentially help illuminate the specific neural targets and pathways that were activated in this study.…”

“…However, we observed little to no effect of increasing stimulation amplitude on percept area. It is possible that the anatomical distance between adjacent spinal roots reduces this effect ( Greiner et al, 2020 ). Additionally, it is currently unknown whether there is strong somatotopic organization of the fanned-out dorsal rootlets where they enter the spinal cord (i.e.…”

Epidural Electrical Stimulation of the Cervical Dorsal Roots Restores Voluntary Upper Limb Control in Paralyzed Monkeys

“…Our previous work showed that stimulation of a single dorsal root will mainly recruit motoneurons located in the corresponding segment 29,30 . Therefore, we designed a spinal interface that could target each of the roots independently by placing contacts on the lateral aspect of the cord to target the entry zone of each individual root 29 . Since each monkey possessed a unique anatomy, we tailored the design Monkeys were trained to reach for, grasp, and pull a target object placed at the end effector of a robotic arm.…”