Springer Nature is making SARS-CoV-2 and COVID-19 research free. View research | View latest news | Sign up for updates

The time course of the contractile force measured during a twitch under fixed sarcomere length

  • 48 Accesses

  • 11 Citations

Summary

A sarcomere length-controlled feedback system was constructed utilizing the laser diffraction technique of Haugen & Sten-Knudsen (1976) to detect sarcomere length changes. The system allowed the sarcomere length to be kept constant within 0.02% during an isometric twitch. The contractile force developed approximates closely to the force exerted by the crossbridges when their translatory movements are prevented. Thus, the force developed under this condition should correspond to the intensity of the active state as defined by A. V. Hill (1949). The time course of the twitch under constant sarcomere length differs substantially from that of the active state curves obtained using quick stretches and quick releases. Thus, (1) the force does not rise quickly to its maximum but rather resembles the fixed-end twitch curve by leading it only slightly (5 ms at 5°C). (2) Its peak value does not reach the level of the tetanic plateau, but is only 9% higher than the maximum fixed-end twitch tension. (3) The force remains above the curve of the fixed-end twitch during its entire course. It is shown that the quick-stretch procedure which results in active state curves as those obtained by A. V. Hill (1949) led to a considerable elongation of the sarcomeres.

It is concluded that the slow rise of the contractile force under ordinary isometric conditions is due to properties inherent in the contractile machinery other than those resulting from the extension of series elastic components.

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

References

  1. Ambrogi-Lorenzini, C., Colomo, F. &Lombardi, V. (1983) Development of force-velocity relation, stiffness and isometric tension in frog single muscle fibres.J. Musc. Res. Cell Motility 4, 177–89.

  2. Baskin, R. J., Roos, K. P. &Yeh, Y. (1979) Light diffraction study of single skeletal muscle fibers.Biophys. J. 28, 45–64.

  3. Brenner, B., Schoenberg, M., Chalovich, J. M., Greene, L. E. &Eisenberg, E. (1982) Evidence for cross-bridge attachment in relaxed muscle at low ionic strength.Proc. natn. Acad Sci, U. S. A. 79, 7288–91.

  4. Briden, K. J. &Alpert, N. R. (1972) The effect of shortening on the time-course of active state decay.J. gen. Physiol. 60, 202–20.

  5. Buchthal, F. &Kaiser, E. (1944) Factors determining tension development in skeletal muscle.Acta physiol. Scand. 8, 38–74.

  6. Cecchi, G., Colomo, F., Lombardi, V. &Piazzesi, G. (1984) Stiffness and isometric tension during tetanus rise in frog muscle fibre segments under length-clamp conditions.J. Physiol., Lond. 357, 104P.

  7. Cecchi, G., Colomo, F., Lombardi, V. &Piazzesi, G. (1985) Rise of stiffness and of isometric tension during a tetanus in frog muscle fibre segments under length clamp conditions.J. Musc. Res. Cell Motility 6, 103.

  8. Cecchi, G., Griffiths, P. J. &Taylor, S. R. (1982) Muscular contraction: Kinetics of crossbridges attachment studied by high-frequency stiffness measurements.Science, N. Y. 217, 70–2.

  9. Cecchi, G., Griffiths, P. J. &Taylor, S. R. (1986) Stiffness and force in activated frog skeletal muscle fibres.Biophys. J. 49, 437–51.

  10. Close, R. I. &LÄnnergren, J. I. (1984) Arsenazo III calcium transients and latency relaxation in frog skeletal muscle fibres at different sarcomere lengths.J. Physiol, Lond. 355, 323–44.

  11. Edman, K. a. p. (1970) The rising phase of the active state in single skeletal muscle fibres of the frog.Acta physiol. Scand. 79, 167–73.

  12. Edman, K. A. P. &Kiessling, A. (1971) The time course of the active state in relation to sarcomere length and movement studied in single skeletal muscle fibres of the frog.Acta physiol. Scand. 81, 182–96.

  13. Ford, L. E., Huxley, A. F. &Simmons, R. M. (1977) Tension responses to sudden length changes in stimulated frog muscle fibres near slack length.J. Physiol, Lond. 269, 441–515.

  14. Ford, L. E., Huxley, A. F. &Simmons, R. M. (1981) The relation between stiffness and filamentary overlap in stimulated frog muscle fibres.J. Physiol, Lond. 311, 219–49.

  15. Ford, L. E., Huxley, A. F. &Simmons, R. M. (1986) Tension transients during the rise of tetanic tension in frog muscle fibres.J. Physiol, Lond. 372, 595–609.

  16. Haugen, P. (1982a) Increase in resistance to stretch during the latent period in single muscle fibres of the frog.Acta physiol. Scand. 114, 187–92.

  17. Haugen, P. (1982b) Short-range elasticity after tetanic stimulation in single muscle fibres of the frog.Acta physiol. Scand. 114, 487–95.

  18. Haugen, P. (1983) The stiffness of isolated frog muscle fibres during single contraction after a quick stretch as compared with isometric conditions.Acta physiol. Scand. 118, 11A.

  19. Haugen, P. (1987) The stiffness under isotonic releases during a twitch of a frog muscle fibre. InCurrent Problems of the Sliding Filament Model and Mechanics (edited bySugi, H. andPollack, G. h.), Plenum Publishing Corporation (in press).

  20. Haugen, P. &Sten-Knudsen, O. (1976) Sarcomere lengthening and tension drop in the latent period of isolated frog skeletal muscle fibers.J. gen. Physiol. 68, 247–65.

  21. Haugen, P. &Csten-Knudsen, O. (1981) The dependence of the short-range elasticity on sarcomere length in resting isolated frog muscle fibres.Ada physiol Scand. 112, 113–20.

  22. Haugen, P. &Sten-Knudsen, O. (1982) The intensity of the active state measured during a single contraction of an isolated muscle fibre of the frog.Acta physiol. Scand. 114, 12A.

  23. Herbst, M. &Piontek, P. (1974) Changes of stiffness of skeletal muscle during latency relaxation.Biochem. Biophys. Res. Commun. 57, 120–5.

  24. Hill, A. V. (1938) The heat of shortening and the dynamic constants of muscle.Proc. R. Soc. Ser. B 126, 136–95.

  25. Hill, A. V. (1949) The abrupt transition from rest to activity in muscle.Proc. R. Soc. Ser. B 136, 399–420.

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

  27. Huxley, H. E., Faruqi, A. R., Kress, M., Bordas, J. &Koch, M. H. J. (1982) Time-resolved X-ray diffraction studies of the myosin layer-line reflections during muscle contraction.J. molec. Biol. 158, 637–84.

  28. Jewell, B. R. &Wilkie, D. R. (1960) The mechanical properties of relaxing muscle.J. Physiol., Lond. 152, 30–47.

  29. Julian, F. J. &Morgan, D. L. (1979) The effect of nonuniform distribution of length changes applied to frog muscle fibres.J. Physiol, Lond. 293, 379–92.

  30. Lieber, R. L., Yin, Y. &Baskin, R. J. (1984) Sarcomere length determination using laser diffraction: the effect of beam and fiber diameter.Biophys.J. 45, 1007–16.

  31. Mason, P. &Hasan, H. (1980) Muscle crossbridge action in excitation and relaxation.Experientia 36, 949–50.

  32. Matsubara, I. &Yagi, N. (1978) A time-resolved X-ray diffraction study of muscle during twitch.J. Physiol., Lond. 278, 297–307.

  33. Oba, T., Baskin, R. J. &Lieber, R. L. (1981) Light diffraction studies of active muscle fibres as a function of sarcomere length.J. Musc. Res. Cell Motility 2, 215–24.

  34. Ritchie, J. M. (1954) The effect of nitrate on the active state of muscle.J. Physiol. Lond. 126, 155–68.

  35. Rudel, R. &Zite-Ferenczy, F. (1979a) Interpretation of light diffraction by cross-striated muscle as Bragg reflection of light by the lattice of contractile proteins.J. Physiol, Lond. 290, 317–30.

  36. RÜdel, R. &Zite-Ferenczy, F. (1979b) Do laser diffraction studies on striated muscle indicate stepwise shortening?Nature, Lond. 278, 573–5.

  37. RÜdel, R. &Zite-Ferenczy, F. (1980) Efficiency of light diffraction by cross-striated muscle fibres under stretch and during isometric contraction.Biophys. J. 30, 507–16.

  38. Simmons, R. M. &Jewell, B. R. (1974) Mechanics and models of muscular contraction. InRecent Advances in Physiology (edited byLinden, R. J.) Vol. 9, pp. 87–147. London: Churchill.

  39. Schoenberg, M. &Wells, J. B. (1984) Stiffness, force, and sarcomere shortening during a twitch in frog semitendinosus muscle bundles.Biophys. J. 45, 389–97.

  40. Sten-Knudsen, O. (1953) Torsional elasticity of the isolated cross striated muscle fibre.Acta. physiol. Scand. 28, suppl. 104, 1–240.

  41. Tamura, Y., Hatta, I., Matsuda, T., Sugi, H. &Tsuchiya, T. (1982) Changes in muscle stiffness during contraction using ultrasonic waves.Nature, Lond. 299, 631–3.

  42. Trueblood, C. E., Walsh, T. P. &Weber, A. (1982) Is the steric model of tropomyosin action valid? InBasic Biology of Muscles: A Comparative Approach, (edited byTwarog, B. M., Levine, R. J. C. andDewey, M. M. J., pp. 223–41. New York: Raven Press.

  43. Wakabayashi, K., Tanaka, H., Amemiya, Y., Fujishima, A., Kobayashi, T., Hamanaka, T., Sugi, H. &Mitsui, T. (1985) Time-resolved X-ray diffraction studies on the intensity changes of the 5.9 and 5.1 nm actin layer lines from frog skeletal muscle during an isometric tetanus using synchrotron radiation.Biophys. J. 47, 847–50.

  44. Wells, J. B. (1976) Onset of mechanical change following stimulation in frog striated muscle.Biophys. J. 116, 122a.

  45. Yagi, N. &Matsubara, I. (1977) Equatorial X-ray reflexions from contracting muscle after an applied stretch.Pflügers Arch. 372, 113–4.

Download references

Author information

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Haugen, P., Sten-Knudsen, O. The time course of the contractile force measured during a twitch under fixed sarcomere length. J Muscle Res Cell Motil 8, 173–187 (1987). https://doi.org/10.1007/BF01753993

Download citation

Keywords

  • Active State
  • Feedback System
  • Translatory Movement
  • Length Change
  • Laser Diffraction