Functional motor mapping of domestic pig lumbar spinal cord using penetrating microelectrodes.

Abstract

The restoration of standing and walking after spinal cord injury (SCI) remains a top priority for individuals with paraplegia. Despite significant advancements in neuromodulation techniques, challenges such as limited selectivity and inconsistent outcomes highlight the need for innovative approaches. Intraspinal microstimulation (ISMS) has emerged as a promising method for restoring motor function as demonstrated in various preclinical models. This study aimed to investigate the functional neural networks within the ventral lumbar spinal cord of pigs. We explored 134 stimulation sites inside the spinal cord in 13 domestic pigs. Post-mortem magnetic resonance imaging (MRI) revealed the location of microelectrode tips inside the spinal cord. The recorded kinematics and electromyographical muscle activity associated with each microelectrode allowed the creation of a functional map of the neural networks activated with ISMS. In addition, we performed anatomical measurements of the lumbar spine and spinal column. Our results revealed a somatotopic organization of motor networks responsible for distinct movements and muscle activations. Differences in activation patterns were primarily observed along the rostrocaudal axis (P < 0.05), where specific stimulation sites were associated with unique movements and muscle responses. In contrast, no notable variations were seen along the mediolateral or dorsoventral directions. Knee extension (KE) was the most frequently observed movement, occurring in 78% of the stimulated sites in the lumbar enlargement, followed by extensor synergy (Ext Syn, 64%), hip flexion (HF, 50%), ankle flexion (AF, 50%), ankle extension (AE, 43%), and hip extension (HE, 43%). Stimulation along the rostrocaudal axis of the lumbar spinal cord elicited a sequence of movements, beginning with HF in the rostral region and transitioning to KE, AF, AE, and HE in the caudal region across animals. Stimulation in the rostral lumbar enlargement produced stronger normalized EMG signals exceeding 50% of the maximum in vastus lateralis (VL) compared to tibialis anterior (TA) gastrocnemius (GS), gluteus medius (GL), and biceps femoris (BF; P < 0.05). Co-activation, defined as simultaneous activity above 50% of normalized maximum EMG activity, occurred at 27.4% of stimulation sites, resulting in synergistic movements and joint stiffening. The resulting map of spinal cord motor networks is important for improving device design and the efficiency of neuroprosthetic interventions. While motor maps exist for other species, they are absent for domestic pigs, a critical model for preclinical testing of SCI treatments. The functional motor maps provided here serve as a foundation for designing and optimizing intraspinal interventions, advancing their translation to clinical application.