Skip to main content
Log in

The tension response to stretch of intact skeletal muscle fibres of the frog at varied tonicity of the extracellular medium

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

Summary

Ramp stretches (2–3% of the fibre length; velocity <0.3 fibre lengths per s) were imposed on tetanically stimulated skeletal muscle fibres from the frog (1.4–3.0°C; sarcomere length 2.1–2.2 μm). The fibre was immersed in normal Ringer solution (osmotic strength 1.00 R) or in solutions made hypotonic by reduction of the sodium concentration (0.81 R) or hypertonic by addition of different amounts of sucrose (1.22 R and 1.44 R). The shape of the force response to stretch was similar at the different tonicity levels but the force enhancement (E) during stretch was significantly increased by raised tonicity and reduced by lowered tonicity. Since the steady state isometric force (T0), in contrast to E, is markedly reduced by raised tonicity and increased by lowerd tonicity the total force during stretch (T0+E) was little affected by changes in tonicity. After the end of stretch tension decayed towards the isometric level with a time course that could be approximated by a double exponential function. The rate constant of both the fast (t1/2≈10 ms) and the slow (t1/2≈300 ms) exponential process was reduced by increased tonicity suggesting reduced rate of crossbridge detachment. The different effects of varied tonicity on T0 and on E would be consistent with the idea that varied tonicity affects the distribution between high-force and low-force crossbridge states during isometric contraction but not during stretch. The effect may be simulated by assuming that increased tonicity reduces the difference in the strength of binding (energy of binding) between the two attached crossbridge states in the model of Huxley and Simmons.

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

  • APRIL, E. W. & MAUGHAN, D. W. (1986) Active force as a function of filament spacing in crayfish skinned muscle fibers. Pflügers Arch. 407, 456–60.

    Google Scholar 

  • BLINKS, J. R. (1965) Influence of osmotic strength on crosssection and volume of isolated single muscle fibers. J. Physiol. 177, 42–57.

    Google Scholar 

  • BOYLE, P. J. & CONWAY, E. J. (1941) Potassium accumulation in muscle and associated changes. J. Physiol. 100, 1–63.

    Google Scholar 

  • 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. Natl. Acad. Sci. USA 79, 7288–91.

    Google Scholar 

  • CURTIN, N. A. & DAVIES, R. E. (1973) Chemical and mechanical changes during stretching of activated frog skeletal muscle. Cold Spring Harbor Symp. Quant. Biol. 37, 619–26.

    Google Scholar 

  • CURTIN, N. A., GILBERT, C., KRETZSCHMAR, K. M. & WILKIE, D. R. (1974) The effect of the performance of work on total energy output and metabolism during muscular contraction. J. Physiol. 238, 455–72.

    Google Scholar 

  • EDMAN, K. A. P. (1979) The velocity of unloaded shortening and its relation to sarcomere length and isometric force in vertebrate muscle fibres. J. Physiol. 291, 143–59.

    Google Scholar 

  • EDMAN, K. A. P. & ANDERSON, K.-E. (1968) The variation in active tension with sarcomere length in vertebrate skeletal muscle and its relation to fibre width. Experientia. 24, 134–6.

    Google Scholar 

  • EDMAN, K. A. P., ELZINGA, G. & NNOBLE, M. I. M. (1979) The effect of stretch on contracting skeletal muscle fibers. In: Cross-bridge mechanism in Muscle Contraction (edited by SUGI, H. & POLLACK, G. H.) pp. 297–310. Tokyo: University of Tokyo Press.

    Google Scholar 

  • EDMAN, K. A. P., ELZINGA, G. & NOBLE, M. I. M. (1981) Critical sarcomere extension required to recruit a decaying component of extra force during stretch in tetanic contractions of frog skeletal muscle fibers. J. Gen. Physiol. 78, 365–82.

    Google Scholar 

  • EDMAN, K. A. P., ELZINGA, G. & NOBLE, M. I. M. (1982) Residual force enhancement after stretch of contracting frog single muscle fibers. J. Gen. Physiol. 80, 769–84.

    Google Scholar 

  • EDMAN, K. A. P. & HWANG, J. C. (1977) The force-velocity relationship in vertebrate muscle fibres at varied tonicity of the extracellular medium. J. Physiol. 269, 255–72.

    Google Scholar 

  • EDMAN, K. A. P. & REGGIANI, C. (1984) Redistribution of sarcomere length during isometric contraction of frog muscle fibres and its relation to tension creep. J. Physiol. 351, 169–98.

    Google Scholar 

  • FORD, L. E., HUXLEY, A. F. & SIMMONS, R. M. (1977) Tension responses to sudden length change in stimulated frog muscle fibres near slack length. J. Physiol. 269, 441–515.

    Google Scholar 

  • GOLDMAN, Y. E. & SIMMONS, R. M. (1986) The stiffness of frog skinned muscle fibres at altered lateral filament spacing. J. Physiol. 378, 175–94.

    Google Scholar 

  • GORDON, A. M. & GODT, R. E. (1970) Some effects of hypertonic solutions on contraction and excitation-contraction coupling in frog skeletal muscles. J. Gen. Physiol. 55, 254–75.

    Google Scholar 

  • GORDON, A. M., GODT, R. E., DONALDSON, S. K. B. & HARRIS, C. E. (1973) Tension in skinned frog muscle fibers in solutions of varying ionic strength and neutral salt composition. J. Gen. Physiol. 62, 550–74.

    Google Scholar 

  • GULATI, J. & BABU, A. (1986) Kinetics of force redevelopment in isolated intact frog fibers in solutions of varied osmolarity Biophys. J. 49, 949–55.

    Google Scholar 

  • HOMSHER, E. (1987) Muscle enthalpy production and its relationship to actomyosin ATPase. Ann. Rev. Physiol. 49, 673–90.

    Google Scholar 

  • HOWARTH, J. V. (1958) The behaviour of frog muscle in hypertonic solutions. J. Physiol. 144, 167–75.

    Google Scholar 

  • HUXLEY, A. F. (1957) Muscle structure and theories of contraction. Prog. Biophys. Biophys. Chem. P 7, 255–318.

    Google Scholar 

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

    Google Scholar 

  • IRVING, T. C. & MILLMAN, B. M. (1992) Z-line/I-band and A-band lattices of intact frog sartorius muscle at altered interfilament spacing. J. Muscle Res. Cell Motil. 13, 100–5.

    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.

    Google Scholar 

  • LOMBARDI, V. & PIAZZESI, G. (1990) The contractile response during steady lengthening of stimulated frog muscle fibres. J. Physiol. 431, 141–71.

    Google Scholar 

  • MÅNSSON, A. (1989a) The effects of tonicity on tension and stiffness of tetanized skeletal muscle fibres of the frog. Acta Physiol. Scand. 136, 205–16.

    Google Scholar 

  • MÅNSSON, A. (1989b) Changes in force and stiffness during stretch of skeletal muscle fibers, effects of hypertonicity. Biophys. J. 56, 429–33.

    Google Scholar 

  • MÅNSSON, A. (1990) The tension-response to stretch of skeletal muscle fibres at varied tonicity of the bathing solution. Acta Physiol. Scand. 140, 23A.

    Google Scholar 

  • MÅNSSON, A. (1991) Effects of hypertonic solution on force and stiffness at rest and during the rise of a tetanus. J. Muscle Res. Cell Motil. 12, 99.

    Google Scholar 

  • MÅNSSON, A. (1993) Tension transients in skeletal muscle fibres of the frog at varied tonicity of the extracellular medium. J. Muscle Res. Cell Motil. 14, 15–25.

    Google Scholar 

  • MÅNSSON, A. & EDMAN, K. A. P. (1985) Effects of amrinone on the contractile behaviour of frog striated muscle fibres. Acta Physiol. Scand. 125, 481–93.

    Google Scholar 

  • ROME, E. (1968) X-ray diffraction studies of the filament lattice of striated muscle in various bathing media. J. Mol. Biol. 37, 331–44.

    Google Scholar 

  • SEOW, C. Y. & FORD, L. E. (1993) High ionic strength and low pH detain activated skinned rabbit skeletal muscle cross-bridges in a low force state. J. Gen. Physiol. 101, 487–511.

    Google Scholar 

  • THAMES, M. D., TEICHHOLZ, L. E. & PODOLSKY, R. J. (1974) Ionic strength and the contraction kinetics of skinned muscle fibres. J. Gen. Physiol. 63, 509–30.

    Google Scholar 

  • TSUCHIYA, T. (1988) Passive interaction between sliding filaments in the osmotically compressed skinned muscle fibers of the frog. Biophys. J. 53, 415–23.

    Google Scholar 

  • TSUCHIYA, T. & EDMAN, K. A. P. (1990) Mechanism of force enhancement after stretch in intact single muscle fibres of the frog. Acta Physiol. Scand. 140, 23A.

    Google Scholar 

  • WOLEDGE, R. C., CURTIN, N. A. & HOMSHER, E. (1985) Energetic aspects of muscle contraction. Monographs of the Physiological Society 41.

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Månsson, A. The tension response to stretch of intact skeletal muscle fibres of the frog at varied tonicity of the extracellular medium. J Muscle Res Cell Motil 15, 145–157 (1994). https://doi.org/10.1007/BF00130425

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00130425

Keywords

Navigation