Literature DB >> 19369362

Structured variability of muscle activations supports the minimal intervention principle of motor control.

Francisco J Valero-Cuevas1, Madhusudhan Venkadesan, Emanuel Todorov.   

Abstract

Numerous observations of structured motor variability indicate that the sensorimotor system preferentially controls task-relevant parameters while allowing task-irrelevant ones to fluctuate. Optimality models show that controlling a redundant musculo-skeletal system in this manner meets task demands while minimizing control effort. Although this line of inquiry has been very productive, the data are mostly behavioral with no direct physiological evidence on the level of muscle or neural activity. Furthermore, biomechanical coupling, signal-dependent noise, and alternative causes of trial-to-trial variability confound behavioral studies. Here we address those confounds and present evidence that the nervous system preferentially controls task-relevant parameters on the muscle level. We asked subjects to produce vertical fingertip force vectors of prescribed constant or time-varying magnitudes while maintaining a constant finger posture. We recorded intramuscular electromyograms (EMGs) simultaneously from all seven index finger muscles during this task. The experiment design and selective fine-wire muscle recordings allowed us to account for a median of 91% of the variance of fingertip forces given the EMG signals. By analyzing muscle coordination in the seven-dimensional EMG signal space, we find that variance-per-dimension is consistently smaller in the task-relevant subspace than in the task-irrelevant subspace. This first direct physiological evidence on the muscle level for preferential control of task-relevant parameters strongly suggest the use of a neural control strategy compatible with the principle of minimal intervention. Additionally, variance is nonnegligible in all seven dimensions, which is at odds with the view that muscle activation patterns are composed from a small number of synergies.

Mesh:

Year:  2009        PMID: 19369362      PMCID: PMC2712269          DOI: 10.1152/jn.90324.2008

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


  28 in total

1.  Predictive modulation of muscle coordination pattern magnitude scales fingertip force magnitude over the voluntary range.

Authors:  F J Valero-Cuevas
Journal:  J Neurophysiol       Date:  2000-03       Impact factor: 2.714

2.  Structure of motor variability in marginally redundant multifinger force production tasks.

Authors:  M L Latash; J F Scholz; F Danion; G Schöner
Journal:  Exp Brain Res       Date:  2001-11       Impact factor: 1.972

3.  Optimal feedback control as a theory of motor coordination.

Authors:  Emanuel Todorov; Michael I Jordan
Journal:  Nat Neurosci       Date:  2002-11       Impact factor: 24.884

4.  Finger coordination during discrete and oscillatory force production tasks.

Authors:  Mark L Latash; John F Scholz; Frederic Danion; Gregor Schöner
Journal:  Exp Brain Res       Date:  2002-09-06       Impact factor: 1.972

Review 5.  Hand function: peripheral and central constraints on performance.

Authors:  Marc H Schieber; Marco Santello
Journal:  J Appl Physiol (1985)       Date:  2004-06

Review 6.  Optimality principles in sensorimotor control.

Authors:  Emanuel Todorov
Journal:  Nat Neurosci       Date:  2004-09       Impact factor: 24.884

7.  Neural control of motion-to-force transitions with the fingertip.

Authors:  Madhusudhan Venkadesan; Francisco J Valero-Cuevas
Journal:  J Neurosci       Date:  2008-02-06       Impact factor: 6.167

8.  Estimating effective degrees of freedom in motor systems.

Authors:  Robert H Clewley; John M Guckenheimer; Francisco J Valero-Cuevas
Journal:  IEEE Trans Biomed Eng       Date:  2008-02       Impact factor: 4.538

9.  Quantification of fingertip force reduction in the forefinger following simulated paralysis of extensor and intrinsic muscles.

Authors:  F J Valero-Cuevas; J D Towles; V R Hentz
Journal:  J Biomech       Date:  2000-12       Impact factor: 2.712

10.  Muscle synergies during shifts of the center of pressure by standing persons.

Authors:  Vijaya Krishnamoorthy; Mark L Latash; John P Scholz; Vladimir M Zatsiorsky
Journal:  Exp Brain Res       Date:  2003-08-07       Impact factor: 1.972

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  92 in total

Review 1.  Principles of sensorimotor learning.

Authors:  Daniel M Wolpert; Jörn Diedrichsen; J Randall Flanagan
Journal:  Nat Rev Neurosci       Date:  2011-10-27       Impact factor: 34.870

2.  Extracting synergies in gait: using EMG variability to evaluate control strategies.

Authors:  Rajiv Ranganathan; Chandramouli Krishnan
Journal:  J Neurophysiol       Date:  2012-06-20       Impact factor: 2.714

Review 3.  Motor control is decision-making.

Authors:  Daniel M Wolpert; Michael S Landy
Journal:  Curr Opin Neurobiol       Date:  2012-05-29       Impact factor: 6.627

4.  Long-term training modifies the modular structure and organization of walking balance control.

Authors:  Andrew Sawers; Jessica L Allen; Lena H Ting
Journal:  J Neurophysiol       Date:  2015-10-14       Impact factor: 2.714

5.  Proximal arm kinematics affect grip force-load force coordination.

Authors:  Billy C Vermillion; Peter S Lum; Sang Wook Lee
Journal:  J Neurophysiol       Date:  2015-08-19       Impact factor: 2.714

6.  Effect of visual and tactile feedback on kinematic synergies in the grasping hand.

Authors:  Vrajeshri Patel; Martin Burns; Ramana Vinjamuri
Journal:  Med Biol Eng Comput       Date:  2015-12-11       Impact factor: 2.602

7.  Robustness of muscle synergies underlying three-dimensional force generation at the hand in healthy humans.

Authors:  Jinsook Roh; William Z Rymer; Randall F Beer
Journal:  J Neurophysiol       Date:  2012-01-25       Impact factor: 2.714

8.  Children With and Without Dystonia Share Common Muscle Synergies While Performing Writing Tasks.

Authors:  Francesca Lunardini; Claudia Casellato; Matteo Bertucco; Terence D Sanger; Alessandra Pedrocchi
Journal:  Ann Biomed Eng       Date:  2017-05-30       Impact factor: 3.934

Review 9.  The coordination of movement: optimal feedback control and beyond.

Authors:  Jörn Diedrichsen; Reza Shadmehr; Richard B Ivry
Journal:  Trends Cogn Sci       Date:  2009-12-11       Impact factor: 20.229

Review 10.  Movement variability near goal equivalent manifolds: fluctuations, control, and model-based analysis.

Authors:  Joseph P Cusumano; Jonathan B Dingwell
Journal:  Hum Mov Sci       Date:  2013-11-07       Impact factor: 2.161

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