Neuromechanical Coupling is Reflected in the Spatial Organization of the Spinal Motoneuron Pools

The anatomy of muscles is complex, so that a given movement can result from the activity of multiple muscle combinations, a concept termed redundancy. The central nervous system must resolve this redundancy to produce coordinated and efficient motion. One proposed mechanism that simplifies motor control is through the neural embedding of musculoskeletal dynamics. We have shown previously that the musculoskeletal anatomy of the upper extremity is organized in functional agonistic and antagonistic groups through mechanical coupling. However, it remains unknown if the neural anatomy of the spinal motoneuron pools somatotopically embeds this musculoskeletal anatomy. Here, we develop a three-dimensional model of the macaque cervical spinal cord and a corresponding OpenSim model of the upper extremity to characterize the structure-function relationship of spinal motoneurons innervating upper limb musculature. We hypothesize that the motoneuron pools of agonistic muscles that perform a coordinated action are located closer together in the spinal cord compared to antagonistic muscles. We used the spinal cord model to quantify the spatial relationship between motoneuron pools, and we used the OpenSim model to quantify the functional relationship between muscles. We used a hierarchical clustering analysis compare the structural and functional relationships. We found that the spatial organization of motoneuron pools in the spinal cord broadly mimics the anatomical relationships between muscle lengths and moment arms. Furthermore, within the same segment, the motoneurons innervating synergistic muscles were located closer to each other than to the motoneurons innervating antagonistic muscles, while across segments the motoneurons innervating specific antagonistic groups of muscles were colocalized. These results suggest that the mechanical coupling of the musculoskeletal system is embedded in the spinal cord anatomy underlying the modular organization of the neural motor control system.