A neuronal population of the primary motor cortex (M1) and of the magnocellular part of red nucleus (Rmg) are origins of major synaptic inputs to spinal motoneurons of forelimb muscles, consisting of a "premotor layer" in the motor processing hierarchy. Since such premotor (PreM) neurons have been shown to project to motor nuclei of multiple muscles, they could conceivably be involved in forming functional modules called "muscle synergies" that subserve dimensionality reduction of a redundant musculoskeletal system. However, evidence is lacking as to whether such descending PreM neurons have different functions, and whether/how muscle synergies are formed through such PreM populations.
To address the issue, we compared muscle projection patterns between M1 and Rmg populations, and then sought any match between the PreM organizations and muscle synergies. A PreM connection was identified based upon functional synaptic linkages using spike triggered averaging; we recorded the single-unit activities of M1 or Rmg neurons concurrently with EMG activities from the 26 forelimb muscles while a macaque monkey performed whole-limb movements (reach-to-grasp of a ball-shaped object, precision grip of pellets, and transportation of pellets to the mouth).
We identified 251 M1 and 90 Rmg neurons, and extracted muscle synergies using non-negative matrix factorization from the EMG signals. Clustering analysis of the PreM connection patterns of the populations revealed distinct neuronal clusters; the Rmg population showed major clusters connecting to muscle sets working as a reciprocally inhibitory circuit (extensor-flexor), and a flexion reflex circuit, whereas the M1 population showed small clusters, each of which largely coalesces muscles for similar joint actions. Despite the distinct neuronal clusters, the muscle clusters of each population correspond similarly to clusters of the extracted muscle synergies. These results indicate each PreM population can provide a neuronal underpinning of muscle synergies in contrasting ways; Rmg organizes the modules by utilizing spinal cord circuitry, whereas M1 achieves them via dedicated direct connections.