Neuromotor Modules Revealed by Intraoperative Direct Electrical Stimulation of the Human Primary Motor Cortex

Muscle synergies extracted from multi-muscle electromyographic (EMG) signals are widely interpreted as fundamental building blocks of motor control which coordinate groups of muscles during movement. Whether EMG-derived muscle synergies represent genuine neurally encoded modules or motor regularities arising from task or biomechanical constraints has been hotly debated, because neurophysiological data that definitively demonstrate the neural basis of muscle synergies in humans has been lacking. Here, we seek to validate the potential neural origin of upper limb muscle synergies by exploiting direct electrical stimulation (DES) of the primary motor cortex (M1) routinely delivered by neurosurgeons during awake craniotomy surgery for glioma excision. Across 13 patients, 69% of the muscle synergies observed during pre-operative voluntary behaviors could be matched to DES-evoked muscle synergies or their combination. Analysis of cortical activity maps of the muscle synergies further revealed that the cortical representations of the sparser muscle synergies were more anterior and distributed, and those of the non-sparse synergies, more posterior and localized. Our results not only provide direct causal evidence arguing for the neural origin of most behavioral muscle synergies in humans, but also demonstrate the existence of two M1 subdivisions with distinct patterns of muscle synergy organization.