Literature DB >> 32267198

When 90% of the variance is not enough: residual EMG from muscle synergy extraction influences task performance.

Victor R Barradas1, Jason J Kutch2, Toshihiro Kawase3, Yasuharu Koike3, Nicolas Schweighofer2.   

Abstract

Muscle synergies are usually identified via dimensionality reduction techniques, such that the identified synergies reconstruct the muscle activity to an accuracy level defined heuristically, often set to 90% of the variance. Here, we question the assumption that the residual muscle activity not explained by the synergies is due to noise. We hypothesize instead that the residual activity is not entirely random and can influence the execution of motor tasks. Young healthy subjects performed an isometric reaching task in which the surface electromyography of 10 arm muscles was mapped onto a two-dimensional force used to control a cursor. Three to five synergies explained 90% of the variance in muscle activity. We altered the muscle-force mapping via "hard" and "easy" virtual surgeries. Whereas in both surgeries the forces associated with synergies spanned the same dimension of the virtual environment, the muscle-force mapping was as close as possible to the initial mapping in the easy surgery; in contrast, it was as far as possible in the hard surgery. This design maximized potential differences in reaching errors attributable to residual activity. Results show that the easy surgery produced smaller directional errors than the hard surgery. Additionally, simulations of surgeries constructed with 1 to 10 synergies show that the errors in the easy and hard surgeries differ significantly for up to 8 synergies, which explains 98% of the variance on average. Our study thus indicates the need for cautious interpretations of results derived from synergy extraction techniques based on heuristics with lenient accuracy levels.NEW & NOTEWORTHY The muscle synergy hypothesis posits that the central nervous system simplifies motor control by grouping muscles into modules. Current techniques use dimensionality reduction, such that the identified synergies reconstruct 90% of the muscle activity. We show that residual muscle activity following such identification can have a large systematic effect on movements, even when the number of synergies approaches the number of muscles. Current synergy extraction techniques must therefore be updated to identify true physiological synergies.

Keywords:  muscle synergies; residuals; virtual surgeries

Year:  2020        PMID: 32267198      PMCID: PMC7311728          DOI: 10.1152/jn.00472.2019

Source DB:  PubMed          Journal:  J Neurophysiol        ISSN: 0022-3077            Impact factor:   2.714


  43 in total

1.  Learning the parts of objects by non-negative matrix factorization.

Authors:  D D Lee; H S Seung
Journal:  Nature       Date:  1999-10-21       Impact factor: 49.962

2.  Neuromotor synergies as a basis for coordinated intentional action.

Authors:  W A Lee
Journal:  J Mot Behav       Date:  1984-06       Impact factor: 1.328

3.  Muscle coordination is habitual rather than optimal.

Authors:  Aymar de Rugy; Gerald E Loeb; Timothy J Carroll
Journal:  J Neurosci       Date:  2012-05-23       Impact factor: 6.167

4.  Central and sensory contributions to the activation and organization of muscle synergies during natural motor behaviors.

Authors:  Vincent C K Cheung; Andrea d'Avella; Matthew C Tresch; Emilio Bizzi
Journal:  J Neurosci       Date:  2005-07-06       Impact factor: 6.167

5.  Subject-specific muscle synergies in human balance control are consistent across different biomechanical contexts.

Authors:  Gelsy Torres-Oviedo; Lena H Ting
Journal:  J Neurophysiol       Date:  2010-04-14       Impact factor: 2.714

6.  A mathematical approach to the mechanical capabilities of limbs and fingers.

Authors:  Francisco J Valero-Cuevas
Journal:  Adv Exp Med Biol       Date:  2009       Impact factor: 2.622

7.  Practical limits on muscle synergy identification by non-negative matrix factorization in systems with mechanical constraints.

Authors:  Thomas J Burkholder; Keith W van Antwerp
Journal:  Med Biol Eng Comput       Date:  2012-11-03       Impact factor: 2.602

8.  Muscle synergies in neuroscience and robotics: from input-space to task-space perspectives.

Authors:  Cristiano Alessandro; Ioannis Delis; Francesco Nori; Stefano Panzeri; Bastien Berret
Journal:  Front Comput Neurosci       Date:  2013-04-19       Impact factor: 2.380

9.  Quantitative evaluation of muscle synergy models: a single-trial task decoding approach.

Authors:  Ioannis Delis; Bastien Berret; Thierry Pozzo; Stefano Panzeri
Journal:  Front Comput Neurosci       Date:  2013-02-26       Impact factor: 2.380

10.  Challenges and new approaches to proving the existence of muscle synergies of neural origin.

Authors:  Jason J Kutch; Francisco J Valero-Cuevas
Journal:  PLoS Comput Biol       Date:  2012-05-03       Impact factor: 4.475

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  7 in total

Review 1.  How to improve the muscle synergy analysis methodology?

Authors:  Nicolas A Turpin; Stéphane Uriac; Georges Dalleau
Journal:  Eur J Appl Physiol       Date:  2021-01-26       Impact factor: 3.078

2.  Evidence for shared neural information between muscle synergies and corticospinal efficacy.

Authors:  David R Young; Caitlin L Banks; Theresa E McGuirk; Carolynn Patten
Journal:  Sci Rep       Date:  2022-05-27       Impact factor: 4.996

3.  Myoelectric interface training enables targeted reduction in abnormal muscle co-activation.

Authors:  Marc W Slutzky; Jinsook Roh; Gang Seo; Ameen Kishta; Emily Mugler
Journal:  J Neuroeng Rehabil       Date:  2022-07-01       Impact factor: 5.208

4.  Design of an Isometric End-Point Force Control Task for Electromyography Normalization and Muscle Synergy Extraction From the Upper Limb Without Maximum Voluntary Contraction.

Authors:  Woorim Cho; Victor R Barradas; Nicolas Schweighofer; Yasuharu Koike
Journal:  Front Hum Neurosci       Date:  2022-05-27       Impact factor: 3.473

5.  Dissociation between abnormal motor synergies and impaired reaching dexterity after stroke.

Authors:  Alkis M Hadjiosif; Meret Branscheidt; Manuel A Anaya; Keith D Runnalls; Jennifer Keller; Amy J Bastian; Pablo A Celnik; John W Krakauer
Journal:  J Neurophysiol       Date:  2022-02-02       Impact factor: 2.714

6.  Learning to use Muscles.

Authors:  Gerald E Loeb
Journal:  J Hum Kinet       Date:  2021-01-29       Impact factor: 2.193

7.  Variability of Muscle Synergies in Hand Grasps: Analysis of Intra- and Inter-Session Data.

Authors:  Una Pale; Manfredo Atzori; Henning Müller; Alessandro Scano
Journal:  Sensors (Basel)       Date:  2020-08-01       Impact factor: 3.576

  7 in total

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