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Comparison of the tension responses to ramp shortening and lengthening in intact mammalian muscle fibres: crossbridge and non-crossbridge contributions

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Abstract

We examined the tension responses to ramp shortening and lengthening over a range of velocities (0.1–5 L 0/s) and at 20°C and 30°C in tetanized intact fibre bundles from a rat fast (flexor hallucis brevis) muscle; fibre length (L 0) was 2.2 mm and sarcomere length ∼2.5 μm. The tension change during ramp releases as well as ramp stretches showed an early transition (often appearing as an inflection) at 1–4 ms; the tension change at this transition and the length change at which it occurred increased with velocity. A second transition, indicated by a more gradual reduction in slope, occurred when the length had changed by 14–28 nm per half-sarcomere; the tension at this transition increased with lengthening velocity towards a plateau and it decreased with shortening velocity towards zero tension. The velocity dependence of the time to the transitions and the length change at the transitions showed some asymmetries between shortening and lengthening. Based on analyses of the velocity dependence of the tension and modelling, we propose that the first transition reflects the tension change associated with the crossbridge power stroke in shortening, or with the reversal of the power stroke in lengthening. Modelling shows that the reduction in slope at the second transition occurs when most of the crossbridges (myosin heads) that were attached at the start of the ramp become detached. After the second transition, the tension reaches a steady level in the model whereas the tension continues to increase during lengthening and continues to decrease during shortening in the experiments; this continuous tension change is seen at a wide range of initial sarcomere lengths and when active force is reduced by the myosin inhibitor, BTS. The continuous tension decline during shortening is not abolished by caffeine, but the rate of decline is reduced when the active force is depressed by BTS. We propose that stiffening of non-crossbridge visco-elastic elements upon activation contributes to the continuous tension rise during lengthening and the release of such tension and Ca-insensitive deactivation contribute to the tension decline during shortening in muscle fibres.

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Acknowledgements

We thank The Wellcome Trust for the support of our research and Professor Paul Edman (University of Lund, Sweden) for helpful suggestions on the work and comments on the manuscript.

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  1. Muscle Contraction Group, Department of Physiology, School of Medical Sciences, University of Bristol, Bristol, BS8 1TD, UK

    H. Roots, G. W. Offer & K. W. Ranatunga

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  1. H. Roots
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  2. G. W. Offer
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  3. K. W. Ranatunga
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Correspondence to K. W. Ranatunga.

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Roots, H., Offer, G.W. & Ranatunga, K.W. Comparison of the tension responses to ramp shortening and lengthening in intact mammalian muscle fibres: crossbridge and non-crossbridge contributions. J Muscle Res Cell Motil 28, 123–139 (2007). https://doi.org/10.1007/s10974-007-9110-0

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