Synergistic Organization of Neural Inputs from Spinal Motor Neurons to Extrinsic and Intrinsic Hand Muscles

Our current understanding of synergistic muscle control is based on the analysis of muscle activities. Modules (synergies) in muscle coordination are extracted from electromyographic (EMG) signal envelopes. Each envelope indirectly reflects the neu-ral drive received by a muscle; therefore, it carries information on the overall activity of the innervating motor neurons. However, it is not known whether the output of spinal motor neurons, whose number is orders of magnitude greater than the muscles they innervate, is organized in a low-dimensional fashion when performing complex tasks. Here, we hypothesized that motor neuron activities exhibit a synergistic organization in complex tasks and therefore that the common input to motor neurons results in a large dimensionality reduction in motor neuron outputs. To test this hypothesis, we factorized the output spike trains of motor neurons innervating 14 intrinsic and extrinsic hand muscles and analyzed the dimensionality of control when healthy individuals exerted isometric forces using seven grip types. We identified four motor neuron syner-gies, accounting for >70% of the variance of the activity of 54.1 +/- 12.9 motor neurons, and we identified four functionally similar muscle synergies. However, motor neuron synergies better discriminated individual finger forces than muscle syner-gies and were more consistent with the expected role of muscles actuating each finger. Moreover, in a few cases, motor neu-rons innervating the same muscle were active in separate synergies. Our findings suggest a highly divergent net neural inputs to spinal motor neurons from spinal and supraspinal structures, contributing to the dimensionality reduction captured by muscle synergies.

Automated summary

The study revealed a synergistic organization in motor neuron activities during complex tasks, leading to a reduction in output dimensionality. By factorizing the output of motor neurons, four motor neuron synergies and four functionally similar muscle synergies were identified. Motor neuron synergies were found to better discriminate individual finger forces compared to muscle synergies and were more consistent with the expected role of muscles in activating each finger.