Forelimb force direction and magnitude independently controlled by spinal modules in the macaque

Significance Studies in frogs and rodents have shown that to deal with the complexity of controlling all the muscles in the body the brain can activate sets of neurons in the spinal cord with a single signal. Here, we provide confirmation of a similar system of “modular” output in nonhuman primates. Costimulation at two spinal sites resulted in force field directionality that was the linear sum of the fields from each site. However, unlike the frog and rodent, the magnitude of the force vectors was greater than the simple sum (supralinear). Thus, while force direction in primates is controlled by the linear sum of modular output, force amplitude might be adjusted by additional sources shared by those modules. Modular organization of the spinal motor system is thought to reduce the cognitive complexity of simultaneously controlling the large number of muscles and joints in the human body. Although modular organization has been confirmed in the hindlimb control system of several animal species, it has yet to be established in the forelimb motor system or in primates. Expanding upon experiments originally performed in the frog lumbar spinal cord, we examined whether costimulation of two sites in the macaque monkey cervical spinal cord results in motor activity that is a simple linear sum of the responses evoked by stimulating each site individually. Similar to previous observations in the frog and rodent hindlimb, our analysis revealed that in most cases (77% of all pairs) the directions of the force fields elicited by costimulation were highly similar to those predicted by the simple linear sum of those elicited by stimulating each site individually. A comparable simple summation of electromyography (EMG) output, especially in the proximal muscles, suggested that this linear summation of force field direction was produced by a spinal neural mechanism whereby the forelimb motor output recruited by costimulation was also summed linearly. We further found that the force field magnitudes exhibited supralinear (amplified) summation, which was also observed in the EMG output of distal forelimb muscles, implying a novel feature of primate forelimb control. Overall, our observations support the idea that complex movements in the primate forelimb control system are made possible by flexibly combined spinal motor modules.