Exploring the Feasibility of Bidirectional Spinal Cord Machine Interface Through Sensing and Stimulation of Axonal Bundles.

Spinal cord injury (SCI) patients experience long-term deficits in motor and sensory functions. While brain-machine interface (BMI) has shown great promise for restoring neurological functions after SCI, spinal cord-machine interface (SCMI) offers unique advantages, such as more defined somatotopy and the compact organization of neural elements in the spinal cord. In the current study, we aim to demonstrate the feasibility of sensing and evoking compound action potentials (CAPs) via electrode implantation in spinal cord axonal bundles, an essential prerequisite for advancing SCMI development. To do so, we designed microelectrode arrays (MEA) optimized for recording and stimulation in the spinal cord. For sensory mapping, the MEAs were inserted into the lumbar dorsal column (i.e., the fasciculus gracilis) to determine somatotopic representations corresponding to tactile stimulation across lower body regions and assess proprioceptive signals with varying hip positions. For stimulations, at the L3 level, we delivered electrical pulses both rostrally, along ascending afferent tracts (dorsal column), and caudally, down descending corticospinal tract. We successfully captured axonal CAPs from the dorsal columns with high spatial precision that corresponded to known dermatomal somatotopy. Proprioceptive changes produced by abduction at the hip resulted in modulation of discharge frequency in the dorsal column axons. We demonstrated that stimulation pulses emitted by a caudally placed electrode could be propagated up the ascending fibers and be intercepted by a rostrally placed electrode array along the same axonal tracts. We also confirmed that electrical pulses can be directed down descending corticospinal tracts resulting in specific activations of lower limb muscles. These findings set a critical groundwork for developing closed-loop, bidirectional SCMI systems capable of sensing and modulating spinal cord activity.