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

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.motor control ͉ motor modules ͉ neurorehabilitation ͉ motor primitives ͉ electromyography

Synergy temporal sequences and topography in the spinal cord: evidence for a traveling wave in frog locomotion

“…With respect to activations of specific groups of muscles, synergies have been proposed as building blocks of motor control (Grillner 1981;Ting and Macpherson 2004;Cheung et al 2005Cheung et al , 2009d'Avella et al 2006;Krouchev et al 2006;Yakovenko et al 2011;Overduin et al 2012;Berger et al 2013;Bizzi and Cheung 2013;Krouchev and Drew 2013). There is also evidence that encoding of muscle synergies already takes place in the spinal cord (Saltiel et al 2001;Stein 2008;Hart and Giszter 2010;Roh et al 2011).…”

Modular control during incline and level walking in humans

“…For this so-called 'degrees of freedom problem' Bernsteın (1967) developed a well-accepted theory of motor control simplification, in which the complexity of the high movement diversity is reduced by combining a lower number of basic muscle activation patterns to accomplish a specific motor task (Chhabra and Jacobs, 2006). There is some evidence that the selection, activation and flexible combination of these basic patterns, called muscle synergies, are of a neural origin and follow a modular organization (Bizzi and Cheung, 2013;Bizzi et al, 2008;Cheung et al, 2009b;d'Avella et al, 2003;Roh et al, 2011). These basic muscular activation patterns are proposed to be adjusted in their specific timing and force generation (Latash et al, 2010;Martin et al, 2009).…”

Neuro-Muscular Control of Coordinated and Effective Movements: Revisiting Modular Concepts in the CNS

“…In this regard it exhibited a lot of 'plasticity' in recruiting additional neurons, devoting them to executing newer learnt tasks (with readjustment of topographic cortical maps), increasing the number of synapses concerned with the newly learnt movement 20 and in physical addition of the number of dendritic spines in cortical neurons recruited to learn and practice a skilled movement 21 . Not only induction of activity in the cortical M1 cells was involved with integration of information inputs from other areas of the nervous system, but also the activation of specific descending commands via the M1 neurons appeared to extract different muscle synergies at the spinal cord (normal vs. stroke patients) to accomplish a certain task as reported by Cheung et al 22 . Instrumented activation of M1 neurons have also been seen to activate muscle synergies as a response (in the form of postural adjustment) to sudden perturbation to the physical plant 23 .…”