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.

Conflict of interest statement

The authors declare no conflict of interest.

Figures

Fig. 1.

Model of muscle pattern generation by a combination of muscle synergies. This is a schematic illustrating how the recorded electromyograms (EMGs) can be reconstructed by linearly combining several time-invariant muscle synergies, each activated by a distinct time-dependent coefficient waveform. Each of the two synergies (red and green bars) has activation components across three model muscles identified as M1, M2, and M3. These components specify an invariant muscle activation balance profile that is scaled, across time, by the synergy's coefficient waveform shown below the synergies (its color matching that of its corresponding synergy). The muscle waveforms produced by scaling synergies with their coefficients then are summed across synergies to explain the recorded EMGs (thick blue lines).

Fig. 2.

Comparison of muscle synergies for the unaffected and stroke-affected arms of a stroke patient. (A) Five muscle synergies extracted from the electromyograms (EMGs) collected from the unaffected arm of patient 2 (Pt2). (B) Five muscle synergies extracted from the EMGs collected from the stroke-affected arm of patient 2. Each normal-arm synergy was matched to an affected-arm synergy giving the highest scalar product between the pair after all synergy vectors were normalized to the Euclidean norm. These scalar product values are shown between their corresponding normal–affected synergy pairs. (C) Cosines of the five principal angles between the vector spaces spanned by the synergy sets shown in A and B. A threshold for dimensionality determination (dotted horizontal line) was specified through a randomization procedure (see Materials and Methods). TrLat, lateral head of triceps brachii; TrMed, medial head of triceps brachii; BicShort, short head of biceps brachii; BicLong, long head of biceps brachii; DeltA, anterior part of deltoid; DeltP, posterior part of deltoid; RhombMaj, rhomboid major; BrRad, brachioradialis; Supin, supinator; Brac, brachialis; PectClav, calvicular head of pectoralis major; Infrasp, infraspinatus.

Fig. 3.

Consistency of muscle synergies across subjects. (A) Averages of the seven synergy clusters (mean ± SD) for the group of healthy subjects (n = 6). (B) Averages of the seven synergy clusters (mean ± SD) for the group of stroke patients (n = 8). Each of the seven synergies for the healthy subjects was matched to a synergy for the stroke patients giving the highest scalar product. (Values are shown above between their corresponding synergy pairs.) TrLat, lateral head of triceps brachii; TrMed, medial head of triceps brachii; BicShort, short head of biceps brachii; BicLong, long head of biceps brachii; DeltA, anterior part of deltoid; DeltM, medial part of deltoid; DeltP, posterior part of deltoid; TrapSup, superior trapezius; RhombMaj, rhomboid major; BrRad, brachioradialis; Supin, supinator; Brac, brachialis; PronTer, pronator teres; PectClav, calvicular head of pectoralis major; Infrasp, infraspinatus; TeresMaj, teres major.

Fig. 4.

Reconstruction of electromyogram (EMG) episodes using the extracted synergies and their coefficients. Shown here are examples of EMGs collected from the unaffected (U) and affected (A) arms of patient 5 during three different tasks: (Upper) reconstructed EMGs; (Lower) time-varying coefficients of the extracted synergies. The colors composing the EMG reconstruction match the colors of coefficients such that the colors reflect the respective contribution of each synergy to the reconstruction of each muscle at each time point. (A) Reconstruction of EMG episodes collected during the task of reaching across a single spatial constraint. (B) Reconstruction of EMG episodes collected during the task of reaching across two spatial constraints. (C) Reconstruction of EMG episodes collected during the task of shoulder circumduction. The symbols ▾, →, and ↓ indicate how complex interarm EMG differences may be more compactly described by differences in the recruitment pattern of several motor synergies (see Results). TrLat, lateral head of triceps brachii; TrMed, medial head of triceps brachii; BicShort, short head of biceps brachii; BicLong, long head of biceps brachii; DeltA, anterior part of deltoid; DeltM, medial part of deltoid; DeltP, posterior part of deltoid; TrapSup, superior trapezius; RhombMaj, rhomboid major; BrRad, brachioradialis; Supin, supinator; Brac, brachialis; PronTer, pronator teres; PectClav, calvicular head of pectoralis major; Infrasp, infraspinatus; TeresMaj, teres major.