The neural origin of muscle synergies

Evidence suggests that the nervous system controls motor tasks using a low-dimensional modular organization of muscle activation. However, it is not clear if such an organization applies to coordination of human walking, nor how nervous system injury may alter the organization of motor modules and their biomechanical outputs. We first tested the hypothesis that muscle activation patterns during walking are produced through the variable activation of a small set of motor modules. In 20 healthy control subjects, EMG signals from eight leg muscles were measured across a range of walking speeds. Four motor modules identified through nonnegative matrix factorization were sufficient to account for variability of muscle activation from step to step and across speeds. Next, consistent with the clinical notion of abnormal limb flexion-extension synergies post-stroke, we tested the hypothesis that subjects with post-stroke hemiparesis would have altered motor modules, leading to impaired walking performance. In post-stroke subjects (n = 55), a less complex coordination pattern was shown. Fewer modules were needed to account for muscle activation during walking at preferred speed compared with controls. Fewer modules resulted from merging of the modules observed in healthy controls, suggesting reduced independence of neural control signals. The number of modules was correlated to preferred walking speed, speed modulation, step length asymmetry, and propulsive asymmetry. Our results suggest a common modular organization of muscle coordination underlying walking in both healthy and post-stroke subjects. Identification of motor modules may lead to new insight into impaired locomotor coordination and the underlying neural systems.

How rudimentary movements evolve into sophisticated ones during development remains unclear. It is often assumed that the primitive patterns of neural control are suppressed during development, replaced by entirely new patterns. Here we identified the basic patterns of lumbosacral motoneuron activity from multimuscle recordings in stepping neonates, toddlers, preschoolers, and adults. Surprisingly, we found that the two basic patterns of stepping neonates are retained through development, augmented by two new patterns first revealed in toddlers. Markedly similar patterns were observed also in the rat, cat, macaque, and guineafowl, consistent with the hypothesis that, despite substantial phylogenetic distances and morphological differences, locomotion in several animal species is built starting from common primitives, perhaps related to a common ancestral neural network.