Stability of muscle synergies for voluntary actions after cortical stroke in humans

TLDR

Voluntary movements depend on the integration of motor cortical areas and spinal circuits, yet how the motor cortices generate descending signals remains unclear after four decades of research. The authors hypothesize that motor cortices select and activate fixed muscle synergies specified by spinal or brainstem networks. To test this, EMGs were recorded from 12–16 upper‑arm and shoulder muscles in both the unaffected and stroke‑affected arms of patients with moderate‑to‑severe unilateral ischemic lesions in frontal motor cortical areas. Nonnegative matrix factorization of these EMGs showed that in 7 of 8 patients the muscle synergy compositions were remarkably similar between arms, supporting the idea that cortical signals flexibly combine synergies defined by spinal/brainstem networks and suggesting a rehabilitation focus on altered synergy activations.

Abstract

Production of voluntary movements relies critically on the functional integration of several motor cortical areas, such as the primary motor cortex, and the spinal circuitries. Surprisingly, after almost 40 years of research, how the motor cortices specify descending neural signals destined for the downstream interneurons and motoneurons has remained elusive. In light of the many recent experimental demonstrations that the motor system may coordinate muscle activations through a linear combination of muscle synergies, we hypothesize that the motor cortices may function to select and activate fixed muscle synergies specified by the spinal or brainstem networks. To test this hypothesis, we recorded electromyograms (EMGs) from 12-16 upper arm and shoulder muscles from both the unaffected and the stroke-affected arms of stroke patients having moderate-to-severe unilateral ischemic lesions in the frontal motor cortical areas. Analyses of EMGs using a nonnegative matrix factorization algorithm revealed that in seven of eight patients the muscular compositions of the synergies for both the unaffected and the affected arms were strikingly similar to each other despite differences in motor performance between the arms, and differences in cerebral lesion sizes and locations between patients. This robustness of muscle synergies that we observed supports the notion that descending cortical signals represent neuronal drives that select, activate, and flexibly combine muscle synergies specified by networks in the spinal cord and/or brainstem. Our conclusion also suggests an approach to stroke rehabilitation by focusing on those synergies with altered activations after stroke.