Summary
Single skeletal muscle fibres from the frog were stimulated to produce isometric twitches and released after a delay to shorten isotonically unloaded or against a finite load (P). When varying the delay, the velocity of the initial shortening (V) against a given non-zero load reached its maximum value earlier than the peak of the isometric tension. The velocity of unloaded shortening (V 0, slack test, range: 3.7–5.6 nm ms−1 per half-sarcomere) was independent of the delay of the release. For any given delay,V was hyperbolically related toP, except for the high-load end of theP-V curve at which the velocity took lower values than extrapolated from the hyperbolic relation. The relation betweenV and the load in units ofP 1 (corresponding toV=1 nm ms−1 per half-sarcomere) coincided in the hyperbolic range with the relations obtained at other delays of the release.P 1 was basically proportional to the maximum power which also had its peak value during the rising phase of the twitch. The quick releases required to reach the non-hyperbolic range of theP-V curves were estimated to be <9 nm per half-sarcomere irrespective of the delay of the release. At load levels in the non-hyperbolic rangeV could be increased if the quick release was followed by a brief (2 ms) extra reduction in the load preceding the shortening at isotonic load. The results can be explained if the kinetic properties of the individual strongly bound crossbridges are unaffected by the changing level of activation during the course of the contraction. The time-dependence of the non-hyperbolic range of theP-V relation can be accounted for if crossbridges attached before the release remain attached after the release thus constituting an internal load. The difference in time course of isometric tension as compared to velocity of initial shortening against a given load,P 1, and maximum power may arise as the result of a reduction in the level of activation caused by the release to the isotonic load level.
Similar content being viewed by others
References
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.
Aubert, X. (1956) La relation entre la force et la vitesse d'alongement et de racourcissement du muscle strié.Arch. Int. Physiol. Biochim. 64, 121–2.
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.
Cecchi, G., Colomo, F. &Lombardi, V. (1978) Force-velocity relation in normal and nitrate-treated frog single muscle fibres during rise of tension in an isometric tetanus.J. Physiol., Lond. 285, 257–73.
Civan, M. M. &Podolsky, R. J. (1966) Contractile kinetics of striated muscle fibres following quick changes in load.J. Physiol., Lond. 84, 511–34.
Close, R. I. &Lännergren, J. I. (1984) Arsenazo III calcium transients and latency relaxation in skeletal muscle fibres at different sarcomere lengths.J. Physiol., Lond. 355, 323–44.
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.,Lond. 291, 143–59.
Edman, K. A. P., Mulieri, L. A. &Scubon-Mulieri, B. (1976) Nonhyperbolic force-velocity relationship in single muscle fibres. Actaphysiol. Scand. 98, 143–56.
Edman, K. A. P. &Reggiani, C. (1982) Differences in maximum velocity of shortening along muscle fibres.J. Physiol, Lond. 329, 47–48P.
Edman, K. A. P. &Reggiani, C. (1985) Differences in maximum velocity of shortening along single muscle fibres of the frog.J. Physiol, Lond. 365, 147–63.
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., Lond. 269, 441–515.
Gulati, J. &Babu, A. (1985) Contraction kinetics of intact and skinned frog muscle fibers and the degree of activation. Effects of intracellular Ca2+ on unloaded shortening.J. gen. Physiol. 86, 479–500.
Gulati, J. &Podolsky, R. J. (1981) Isotonic contraction of skinned muscle fibers on a slow time base.J. gen. Physiol. 78, 233–57.
Haselgrove, J. C. (1973) X-ray evidence for a conformational change in the actin-containing filaments of vertebrate striated muscle.Cold Spring Harb. Symp. quant. Biol. 37, 341–52.
Haugen, P. (1984a) The force-velocity relation of a frog muscle fibre as a function of time after stimulation.Acta physiol. Scand. 120, 9A.
Haugen, P. (1984b) Is the velocity of unloaded shortening of a skeletal muscle fibre dependent on the level of activation?Acta physiol. Scand. 121, 24A.
Haugen, P. (1985) Evidence that the kinetic properties of the individual cross-bridges remain unchanged during the course of a muscle contraction.Acta physiol. Scand. 124, Suppl.542, 205.
Haugen, P. &Sten-Knudsen, P. (1976) Sarcomere lengthening and tension drop in the latent period of isolated frog skeletal muscle fibres.J. gen. Physiol. 68, 247–65.
Haugen, P. &Sten-Knudsen, O. (1987) The time course of the contractile force measured during a twitch at constant sarcomere length.J. Musc. Res. Cell Motility 8, 173–87.
Hill, A. V. (1938) The heat of shortening and the dynamic constants of muscle.Proc. R. Soc. Ser. B 126, 136–95.
Hill, A. V. (1970)First and Last Experiments in Muscle Mechanics, pp. 1–141. Cambridge: University Press.
Huxley, A. F. (1957) Muscle structure and theories of contraction.Prog. Biophys. molec. Biol. 7, 255–318.
Huxley, A. F. &Simmons, R. M. (1971) Proposed mechanism of force generation in striated muscle.Nature, Lond. 233, 533–8.
Huxley, A. F. &Simmons, R. M. (1973) Mechanical transients and the origin of muscular force.Cold Spring Harb. Symp. quant. Biol. 37, 669–80.
Huxley, H. E. (1973) Structural changes in actin- and myosin-containing filaments during contraction.Cold Spring Harb. Symp. quant. Biol. 37, 361–76.
Jewell, B. R. &Wilkie, D. R. (1958) Ananalysis of the mechanical components in frog's striated muscle.J. Physiol., Lond. 143, 515–40.
Jewell, B. R. &Wilkie, D. R. (1960) The mechanical properties of relaxing muscle.J. Physiol., Lond. 152, 30–47.
Julian, F. J. &Moss, R. L. (1981) Effects of calcium and ionic strength on shortening velocity and tension development in frog skinned muscle fibres.J. Physiol., Lond. 311, 179–99.
Julian, F. J., Rome, L. C., Stephenson, D. G. &Stritz, S. (1986) The maximum speed of shortening in living and skinned frog muscle fibres.J. Physiol., Lond. 370, 181–99.
Julian, F. J. &Sollins, M. R. (1973) Regulation of force and speed of shortening in muscle contraction.Cold Spring Harb. Symp. quant. Biol. 37, 635–46.
Lombardi, V. &Menchetti, G. (1984) The maximum velocity of shortening during the early phases of the contraction in frog single muscle fibres.J. Musc. Res. Cell Motility 5, 503–13.
Millman, B. M. (1964) Contraction in the opaque part of the adductor muscle of the oyster (Crassostrea angulata).J. Physiol., Lond. 173, 238–62.
Moss, R. L. (1982) The effect of calcium on the maximum velocity of shortening in a skinned skeletal muscle fibre of the rabbit.J. Musc. Res. Cell Motility 3, 295–311.
Moss, R. L. (1986) Effects on shortening velocity of rabbit skeletal muscle due to variation in the level of thin-filament activation.J. Physiol., Lond. 377, 487–505.
Parry, D. A. D. &Squire, J. M. (1973) Structural role of tropomyosin in muscular regulation: analysis of the X-ray diffraction patterns from relaxed and contracting muscles.J. molec. Biol. 75, 33–55.
Petit, J.-L. (1931) Les propriétés visco-élastiques du muscle à l'état de repos et à l'état d'excitation.Arch. Int. Physiol. 34, 113–38.
Phillips Jr,G. N., Fillers, J. P. &Cohen, C. (1986) Tropomyosin crystal structure and muscle regulation.J. molec. Biol. 192, 111–31.
Podolin, R. A. &Ford, L. E. (1983) The influence of calcium on shortening velocity of skinned frog muscle cells.J. Musc. Res. Cell Motility 4, 263–82.
Podolin, R. A. &Ford, L. E. (1986) Influence of partial activation on force-velocity properties of frog skinned muscle fibers in millimolar magnesium ion.J. gen. Physiol. 87, 607–31.
Podolsky, R. J. (1960) Kinetics of muscular contraction: the approach to the steady state.Nature, Lond. 188, 666–8.
Podolsky, R. J. &Teichholz, L. E. (1970) The relation between calcium and contraction kinetics in skinned muscle fibres.J. Physiol., Lond. 211, 19–35.
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.), pp. 223–41. New York: Raven Press.
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Haugen, P. Changes in contractile dynamics during the course of a twitch of a frog muscle fibre. J Muscle Res Cell Motil 8, 448–460 (1987). https://doi.org/10.1007/BF01578434
Received:
Revised:
Issue Date:
DOI: https://doi.org/10.1007/BF01578434