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J Neurophysiol 102: 59-68, 2009. First published April 15, 2009; doi:10.1152/jn.90324.2008
0022-3077/09 $8.00
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Structured Variability of Muscle Activations Supports the Minimal Intervention Principle of Motor Control

Francisco J. Valero-Cuevas13,*, Madhusudhan Venkadesan3,4,* and Emanuel Todorov5,6,*

1Department of Biomedical Engineering, University of Southern California and 2Division of Biokinesiology and Physical Therapy, University of Southern California, Los Angeles, California; 3Sibley School of Mechanical and Aerospace Engineering and 4Department of Mathematics, Cornell University, Ithaca, New York; 5Departments of Applied Mathematics and Computer Science and Engineering, University of Washington, Seattle, Washington; and 6Department of Cognitive Science, University of California San Diego, La Jolla, California

Submitted 1 March 2008; accepted in final form 8 April 2009

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.


Address for reprint requests and other correspondence: F. J. Valero-Cuevas, The University of Southern California, 3710 McClintock Ave, RTH 404, Los Angeles, California 90089-2905 (E-mail: valero{at}usc.edu)







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