Adjustments of Motor Pattern for Load Compensation Via Modulated Activations of Muscle Synergies During Natural Behaviors

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Abstract
It has been suggested that the motor system may circumvent the difficulty of controlling many degrees of freedom in the musculoskeletal apparatus by generating motor outputs through a combination of discrete muscle synergies. How a discretely organized motor system compensates for diverse perturbations has remained elusive. Here, we investigate whether motor responses observed after an inertial-load perturbation can be generated by altering the recruitment of synergies normally used for constructing unperturbed movements. Electromyographic (EMG, 13 muscles) data were collected from the bullfrog hindlimb during natural behaviors before, during, and after the same limb was loaded by a weight attached to the calf. Kinematic analysis reveals the absence of aftereffect on load removal, suggesting that load-related EMG changes were results of immediate motor pattern adjustments. We then extracted synergies from EMGs using the nonnegative matrix factorization algorithm and developed a procedure for assessing the extent of synergy sharing across different loading conditions. Most synergies extracted were found to be activated in all loaded and unloaded conditions. However, for certain synergies, the amplitude, duration, and/or onset time of their activation bursts were up- or down-modulated during loading. Behavioral parameterizations reveal that load-related modulation of synergy activations depended on the behavioral variety (e.g., kick direction and amplitude) and the movement phase performed. Our results suggest that muscle synergies are robust across different dynamic conditions and immediate motor adjustments can be accomplished by modulating synergy activations. An appendix describes the novel procedure we developed, useful for discovering shared and specific features from multiple data sets.