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Threshold control of motor actions prevents destabilizing effects of proprioceptive delays

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Abstract

It is usually assumed that proprioceptive feedback comes to motoneurons too late to contribute to the initial activity of agonist muscles during fast arm movements, leading to the suggestion that this feedback is only efficient in slow movements and postural control. The argument does not take into account that the changes in the motoneuronal membrane potentials and the associated changes in the state of spinal neurons preceding the initial activity of muscles deeply affect, in a forward way, the state of reflex systems by shifting their thresholds, as suggested in the λ model for motor control. As a result, the initial muscle activity emerges with full contribution of these systems so that the effects of reflex delays become negligible. We tested the hypothesis that threshold control of muscle activation may be instrumental in preventing destabilizing effects of proprioceptive delays in spinal and trans-cortical pathways to motoneurons. The analysis was made by recording fast elbow movements (peak velocity ∼300–500°/s) and simulating them in a dynamic model that incorporates the notion of threshold control of intrinsic and reflex muscle properties. The model was robust in reproducing experimental movement patterns (R 2>0.95). It generated stable output despite substantial proprioceptive (up to 100 ms) and electromechanical (40 ms) delays. Stability was thus ensured for delays not only in segmental (about 25–50 ms) but also in trans-cortical loops (50–70 ms). Our study illustrates that a natural physiological process—threshold control—may manifest feed-forward properties hitherto attributed to hypothetical internal neural models.

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Acknowledgments

Supported by NSERC, CIHR, FQRNT, and IGB (University of Montreal), Canada. We thank Mindy Levin for improving the text.

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Authors and Affiliations

  1. Institute of Biomedical Engineering, University of Montreal and Rehabilitation Institute of Montreal (CRIR), 6300 Darlington Avenue, Montreal, QC, Canada, H3S 2J4

    Jean-François Pilon & Anatol G. Feldman

  2. Department of Physiology, Neurological Science Research Center, University of Montreal, Montreal, QC, Canada

    Anatol G. Feldman

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  1. Jean-François Pilon
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  2. Anatol G. Feldman
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Correspondence to Anatol G. Feldman.

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Pilon, JF., Feldman, A.G. Threshold control of motor actions prevents destabilizing effects of proprioceptive delays. Exp Brain Res 174, 229–239 (2006). https://doi.org/10.1007/s00221-006-0445-3

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