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Do cross-bridges contribute to the tension during stretch of passive muscle?

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Abstract

The tension rise during stretch of passive skeletal muscle is biphasic, with an initial steep rise, followed by a subsequent more gradual change. The initial rise has been interpreted as being due to the presence of numbers of long-term, stable cross-bridges in resting muscle fibres. A point of weakness with the cross-bridge interpretation is that the initial stiffness reaches its peak value at muscle lengths beyond the optimum for myofilament overlap. To explain this result it has been suggested that despite the reduced overlap at longer lengths, the closer interfilament spacing and a higher sensitivity of the myofilaments to Ca2+ allows more stable cross-bridges to form. Recently the stretch responses of passive muscle have been re-examined and it has been suggested that it is not necessary to invoke cross-bridge mechanisms at all. Explanations based on a viscous resistance to interfilament sliding and mechanical properties of the elastic filaments, the gap filaments, were thought to adequately account for the observed tension changes. However, an important property of passive muscle, the dependence of stretch responses on the immediate history of contraction and length changes, thixotropy, cannot be explained simply in terms of viscous and viscoelastic properties. The review discusses the cross-bridge interpretation of muscle thixotropy and the relationship of passive stiffness to filament resting tension and latency relaxation. It is proposed that cross-bridges can exist in three states; one, responsible for the resting stiffness, requires resting levels of calcium. When, during activation, calcium levels rise, cross-bridges enter a low-force, high-stiffness state, signalled by latency relaxation, before they move to the third, force-generating state. It is concluded that, compared with viscoelastic models, a cross-bridge-based explanation of passive muscle properties is better able to accommodate the currently known facts although, as new information becomes available, this view may need to be revised.

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Authors and Affiliations

  1. Department of Physiology, Monash University, Clayton, Victoria, 3168, Australia

    U. Proske

  2. Department of Electrical and Computer Systems Engineering, Monash University, Clayton, Victoria, 3168, Australia

    D. L. Morgan

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  1. U. Proske
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  2. D. L. Morgan
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Proske, U., Morgan, D.L. Do cross-bridges contribute to the tension during stretch of passive muscle?. J Muscle Res Cell Motil 20, 433–442 (1999). https://doi.org/10.1023/A:1005573625675

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