Fatigue Influences the Recruitment, but Not Structure, of Muscle Synergies

Abstract

The development of fatigue elicits multiple adaptations from the neuromuscular system. Muscle synergies are common patterns of neuromuscular activation that have been proposed as the building blocks of human movement. We wanted to identify possible adaptations of muscle synergies to the development of fatigue in the upper limb. Recent studies have reported that synergy structure remains invariant during the development of fatigue, but these studies did not examine isolated synergies. We propose a novel approach to characterise synergy adaptations to fatigue by taking advantage of the spatial tuning of synergies. This approach allows improved identification of changes to individual synergies that might otherwise be confounded by changing contributions of overlapping synergies. To analyse upper limb synergies, we applied non-negative matrix factorization to 14 EMG signals from muscles of 11 participants performing isometric contractions. A preliminary multidirectional task was used to identify synergy directional tuning. A subsequent fatiguing task was designed to fatigue the participants in their synergies’ preferred directions. Both tasks provided virtual reality feedback of the applied force direction and magnitude, and were performed at 40% of each participant’s maximal voluntary force. Five epochs were analysed throughout the fatiguing task to identify progressive changes of EMG amplitude, median frequency, synergy structure, and activation coefficients. Three to four synergies were sufficient to account for the variability contained in the original data. Synergy structure was conserved with fatigue, but interestingly synergy activation coefficients decreased on average by 24.5% with fatigue development. EMG amplitude did not change systematically with fatigue, whereas EMG median frequency consistently decreased across all muscles. These results support the notion of a neuromuscular modular organisation as the building blocks of human movement, with adaptations to synergy recruitment occurring with fatigue. When synergy tuning properties are considered, the reduction of activation of muscle synergies may be a reliable marker to identify fatigue.

Muscle synergies are associated with intermuscular coherence in an isometric upper limb task

“…Animal (Tresch and Bizzi 1999;Bizzi et al 2008;Hart and Giszter 2013) and computational (Neptune et al 2009) models using electrical stimulation support a neural origin for muscle synergies. Similarly, human experiments are consistent with a neural origin of muscle synergies during natural movements (d'Avella and Bizzi 2005;Safavynia and Ting 2012), affecting learning rates (Berger et al 2013;Sawers et al 2015), for postural control (Weiss and Flanders 2004), when extracted from the frequency domain (Frere 2017), irrespective of muscle fatigue (Ortega-Auriol et al 2018), and in the presence of CNS damage after stroke (Cheung et al 2009;Berger et al 2013). Conversely, evidence for muscle synergies as a result of purely mechanical constraints arise from computer simulations of the upper arm movement on a single plane (Inouye and Valero-Cuevas 2016) and cadaveric studies (Kutch and Valero-Cuevas 2012).…”

“…EMG processing: The processing of multidirectional trials for synergy extraction is described in detail in our previous research (Ortega-Auriol et al 2018). Briefly, EMG signals were: trimmed for the intermediate two seconds of the target match period, band-pass filtered (bidirectional Butterworth, 2 nd order, 5-400 Hz.…”

“…The experiment took place on a single session, where participants performed three tasks: maximal voluntary force (MVF), multidirectional trials, and synergy tuned trials. Part of the experimental protocol has been described previously (Ortega-Auriol et al 2018). While seated the participants exerted 40% of the MVF over a handle instrumented with a force transducer ( Figure 1a) located at 40% of the arm length (acromion -3 rd metacarpal head) in front of the shoulder.…”

Muscle Synergy Analysis of a Hand-Grasp Dataset: A Limited Subset of Motor Modules May Underlie a Large Variety of Grasps

“…Consequently, pre-processing could be a source of data misinterpretation. Furthermore, the insurgence of fatigue was not inspected in this study, while it was demonstrated in the literature that fatigue may influence the recruitment of synergies, even if their spatial composition is preserved (Ortega-Auriol et al, 2018 ). As described in the section Introduction, several factors may have an effect on sEMG signal and make synergies tough to be generalized.…”

“…Few studies addressed these effects until now, and the effect on the resulting muscle synergies. Considering upper limb synergies, Ortega et al observed that synergy structure was conserved with fatigue, but interestingly synergy activation coefficients decreased on average by 24.5% with fatigue development (Ortega-Auriol et al, 2018 ). In Tagliabue et al ( 2015 ) two-digit grasping is analyzed.…”