Skip to main content
Log in

A three-state model for oscillation in muscle: Sinusoidal analysis

  • Published:
Journal of Muscle Research & Cell Motility Aims and scope Submit manuscript

Summary

The crossbridge mechanism leading to oscillation in insect flight muscle is studied theoretically based on a three-state model proposed by Nishiyamaet al. [Biochim. biophys. Acta 460, 523–36 (1977)]. Skeletal muscle as well as insect flight muscle shows oscillatory contraction. We demonstrate this oscillatory contraction in muscle by choosing proper rate constants among the three states of the model. It is established that our model gives out not only Hill's force-velocity relation but also other mechanical properties of skeletal muscle. The model is then compared with two types of experiment by Kawai & Brandt [J. Musc. Res. Cell Motility 1, 279–303 (1980)] and by Steiger & Rüegg [Pflügers Arch. 307, 1–21 (1969)]. Kawai & Brandt obtained the Nyquist plot showing the relation between the phase shift and the amplitude of tension change in response to sinusoidal length changes at various frequencies. Steiger & Rüegg studied the power output and ATPase activity at various frequencies of the length change. Our theoretical results are in good agreement with the results of these two experiments. To determine the crossbridge mechanism which produces the positive power output, spatio-temporal crossbridge distributions in the three states are calculated. It is shown that, after the stretching phase of sinusoidal change in muscle length, the delayed rise of tension is caused by attachment of crossbridges to the active state via the preactive state while the delayed fall is caused by detachment from the active state after release. To obtain the oscillatory property it is not necessary to assume that stretch in muscle length increases the attaching rate as originally proposed by Thorson & White [Biophys. J. 9, 360–90 (1969)].

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References

  • Abbott, R. H. (1973) An interpretation of the effects of fiber length and calcium on the mechanical properties of insect flight muscle.Cold Spring Harbor Symp. quant. Biol. 37, 647–54.

    Google Scholar 

  • Abbott, R. H. &Steiger, G. J. (1977) Temperature and amplitude dependence of tension transients in glycerinated skeletal and insect fibrillar muscle.J. Physiol., Lond. 266, 13–42.

    Google Scholar 

  • Brokaw, C. J. (1975) Molecular mechanism for oscillation in flagella and muscle.Proc. natn. Acad. Sci. U.S.A. 72, 3102–6.

    Google Scholar 

  • Brokaw, C. J. (1976) Computer simulation of flagellar movement. IV. Properties of an oscillatory two-state cross-bridge model.Biophys. J. 16, 1029–41.

    PubMed  Google Scholar 

  • Cheung, A. S. &Gray, B. F. (1983) Muscle tension response to sinusoidal length perturbation: a theoretical study.J. Musc. Res. Cell Motility 4, 615–23.

    Google Scholar 

  • Ford, L. E., Huxley, A. F. &Simmons, R. M. (1974) Mechanism of early tension recovery after a quick release in tetanized muscle fibres.J. Physiol., Lond. 240, 42–3P.

    Google Scholar 

  • Goodall, M. C. (1956) Auto-oscillations in extracted muscle fibre systems.Nature, Lond. 177, 1238–9.

    Google Scholar 

  • Gray, B. F. &Gonda, I. (1977a) The sliding filament model of muscle contraction. I. Quantum mechanical formalism.J. theoret. Biol. 69, 167–85.

    Google Scholar 

  • Gray, B. F. &Gonda, I. (1977b) The sliding filament model of muscle contraction. II. The energetic and dynamical predictions of a quantum mechanical transducer model.J. theoret. Biol. 69, 187–230.

    Google Scholar 

  • Güth, K., Kuhn, H. J., Brexler, B., Berberich, W. &Rüegg, J. C. (1979) Stiffness and tension during and after sudden length changes of glycerinated single insect fibrillar muscle fibres.Biophys. Struct. Mechanism. 5, 255–76.

    Google Scholar 

  • Herzig, J. w. (1977) A model of stretch activation based on stiffness measurements in glycerol extracted insect fibrillar flight muscle. InInsect Flight Muscle (edited byTregear, R. T.), pp. 209–19. Amsterdam: North Holland.

    Google Scholar 

  • Hill, T. L. (1974) Theoretical formalism for the sliding filament model of contraction of striated muscle.Progr. Biophys. molec. Biol. 28, 267–340.

    Google Scholar 

  • Hill, T. L., Eisenberg, E., Chen, Y. &Podolsky, R. J. (1975) Some self-consistent two-state sliding filament models of muscle contraction.Biophys. J. 15, 335–72.

    PubMed  Google Scholar 

  • Huxley, A. F. &Simmons, R. M. (1971) Proposed mechanism of force generation in striated muscle.Nature, Lond. 233, 533–8.

    Google Scholar 

  • Huxley, A. F. (1974) Muscular contraction.J. Physiol., Lond. 243, 1–43.

    Google Scholar 

  • Jewell, B. R. &Rüegg, J. C. (1966) Oscillatory contraction of insect fibrillar muscle after glycerol extraction.Proc. R. Soc. Ser. B. 164, 428–59.

    Google Scholar 

  • Julian, F. J., Sollins, K. R. &Sollins, M. R. (1974) A model for the transient and steady-state mechanical behavior of contracting muscle.Biophys. J. 14, 546–62.

    PubMed  Google Scholar 

  • Kawai, M. &Brandt, P. W. (1980) Sinusoidal analysis: a high resolution method for correlating biochemical reactions with physiological processes in activated skeletal muscles of rabbit, frog and crayfish.J. Musc. Res. Cell Motility 1, 279–303.

    Google Scholar 

  • Lorand, L. &Moos, C. (1956) Auto-oscillations in extracted muscle fibre systems.Nature, Lond. 177, 1239.

    Google Scholar 

  • Machin, K. E. &Pringle, J. W. S. (1960) The physiology of insect fibrillar muscle. III. The effect of sinusoidal changes of length on a beetle flight muscle.Proc. R. Soc. Ser. B. 152, 311–30.

    Google Scholar 

  • Murase, M., Tanaka, H., Nishiyama, K. &Shimizu, H. (1984) A three-state model for oscillation in muscle.J. Musc. Res. Cell Motility 5, 466–7.

    Google Scholar 

  • Pringle, J. W. S. (1949) The excitation and contraction of the flight muscles of insects.J. Physiol., Lond. 108, 226–32.

    Google Scholar 

  • Pringle, J. W. S. (1978) Stretch activation of muscle: function and mechanism.Proc. R. Soc. Ser. B. 201, 107–30.

    Google Scholar 

  • Nishiyama, K. &Shimizu, H. (1979) Dynamic analysis of the structure and function of sarcomeres.Biochim. biophys. Acta. 587, 540–55.

    PubMed  Google Scholar 

  • Nishiyama, K. &Shimizu, H. (1981) A Monte Carlo study of stochastic phenomena in biological systems. I. Mathematical treatment of the geometrical structure of muscle.Math. Biosci. 54, 115–35.

    Google Scholar 

  • Nishiyama, K., Shimizu, H., Kometani, K. &Chaen, S. (1977) The three-state model for the elementary process of energy conversion in muscle.Biochim. biophys. Acta 460, 523–36.

    PubMed  Google Scholar 

  • Steiger, G. J. &Rüegg, J. C. (1969) Energetics and ‘efficiency’ in the isolated contractile machinery of an insect fibrillar muscle at various frequencies of oscillation.Pflügers Arch. 307, 1–21.

    Google Scholar 

  • Steiger, G. J. &Abbott, R. H. (1981) Biochemical interpretation of tension transients produced by a four-state mechanical model.J. Musc. Res. Cell Motility 2, 245–60.

    Google Scholar 

  • Thorson, J. &White, D. C. S. (1969) Distributed representations for actin-myosin interaction in the oscillatory contraction of muscle.Biophys. J. 9, 360–90.

    PubMed  Google Scholar 

  • Thorson, J. &White, D. C. S. (1983) Role of cross-bridge distortion in the small-signal mechanical dynamics of insect and rabbit striated muscle.J. Physiol., Lond. 343, 59–84.

    Google Scholar 

  • White, D. C. S. &Thorson, J. (1972) Phosphate starvation and the nonlinear dynamics of insect fibrillar flight muscle.J. gen. Physiol. 60, 307–36.

    PubMed  Google Scholar 

  • White, D. C. S. &Thorson, J. (1973) The kinetics of muscle contraction.Progr. Biophys. molec. Biol. 27, 173–255.

    Google Scholar 

  • White, D. C. S. (1973) Links between mechanical and biochemical kinetics of muscle.Cold Spring Harbor Symp. quant. Biol. 37, 201–13.

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Murase, M., Tanaka, H., Nishiyama, K. et al. A three-state model for oscillation in muscle: Sinusoidal analysis. J Muscle Res Cell Motil 7, 2–10 (1986). https://doi.org/10.1007/BF01756196

Download citation

  • Received:

  • Revised:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF01756196

Keywords

Navigation