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The Journal of Neuroscience, February 6, 2008, 28(6):1366-1373; doi:10.1523/JNEUROSCI.4993-07.2008
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Behavioral/Systems/Cognitive
Neural Control of Motion-to-Force Transitions with the Fingertip
Madhusudhan Venkadesan1,2 andFrancisco J. Valero-Cuevas2,3,4 1Department of Mathematics and 2Sibley School of Mechanical and Aerospace Engineering, Cornell University, Ithaca, New York 14853, and 3Department of Biomedical Engineering and 4Division of Biokinesiology and Physical Therapy, University of Southern California, Los Angeles, California 90089-2905
Correspondence should be addressed to Francisco J. Valero-Cuevas, Department of Biomedical Engineering, University of Southern California, Ronald Tutor Hall 404, 3710 McClintock Avenue, Los Angeles, CA 90089-2905. Email: valero{at}usc.edu
The neural control of tasks such as rapid acquisition of precision pinch remains unknown. Therefore, we investigated the neural control of finger musculature when the index fingertip abruptly transitions from motion to static force production. Nine subjects produced a downward tapping motion followed by vertical fingertip force against a rigid surface. We simultaneously recorded three-dimensional fingertip force, plus the complete muscle coordination pattern using intramuscular electromyograms from all seven index finger muscles. We found that the muscle coordination pattern clearly switched from that for motion to that for isometric force
65 ms before contact (p = 0.0004). Mathematical modeling and analysis revealed that the underlying neural control also switched between mutually incompatible strategies in a time-critical manner. Importantly, this abrupt switch in underlying neural control polluted fingertip force vector direction beyond what is explained by muscle activation-contraction dynamics and neuromuscular noise (p
0.003). We further ruled out an impedance control strategy in a separate test showing no systematic change in initial force magnitude for catch trials where the tapping surface was surreptitiously lowered and raised (p = 0.93). We conclude that the nervous system predictively switches between mutually incompatible neural control strategies to bridge the abrupt transition in mechanical constraints between motion and static force. Moreover because the nervous system cannot switch between control strategies instantaneously or exactly, there arise physical limits to the accuracy of force production on contact. The need for such a neurally demanding and time-critical strategy for routine motion-to-force transitions with the fingertip may explain the existence of specialized neural circuits for the human hand.
Key words: motor control; neural control; finger; hand; contact transition; force
Received May 18, 2007; revised Dec. 7, 2007; accepted Dec. 10, 2007.
Correspondence should be addressed to Francisco J. Valero-Cuevas, Department of Biomedical Engineering, University of Southern California, Ronald Tutor Hall 404, 3710 McClintock Avenue, Los Angeles, CA 90089-2905. Email: valero{at}usc.edu
This article has been cited by other articles:
K. G. Keenan, V. J. Santos, M. Venkadesan, and F. J. Valero-Cuevas
Maximal Voluntary Fingertip Force Production Is Not Limited by Movement Speed in Combined Motion and Force Tasks
J. Neurosci., July 8, 2009; 29(27): 8784 - 8789.
[Abstract] [Full Text] [PDF]
F. J. Valero-Cuevas, M. Venkadesan, and E. Todorov
Structured Variability of Muscle Activations Supports the Minimal Intervention Principle of Motor Control
J Neurophysiol, July 1, 2009; 102(1): 59 - 68.
[Abstract] [Full Text] [PDF]
M. Venkadesan and F. J Valero-Cuevas
Effects of neuromuscular lags on controlling contact transitions
Phil Trans R Soc A, March 28, 2009; 367(1891): 1163 - 1179.
[Abstract] [Full Text] [PDF]
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