Summary
A detailed investigation of sarcomere lengthening and shortening during fixed-end tetani has been made along frog muscle fibres stretched over a large range of sarcomere lengths. A variety of sources of error common in such measurements are quantitated and give an uncertainty in sarcomere length of about 53–62 nm. The difference in sarcomere length calculated from the left and right first orders at rest was 21 nm ±16 nm and this is suggested to be a measure of ‘Bragg artefact’. The laser diffraction measurements showed that the shortening end regions decrease in size during contraction and that the magnitude of shortening is increased at greater fibre extensions. The average length change and sarcomere length of the central and end regions was 0.10 μm (2.85 μm) and −0.37 μm (2.66 μm), respectively. The sarcomere length of the end regions at the end of creep was regularly observed to be <2.1 μm. An unexpected finding was the occasional observation of striations in the transition zone between lengthening and shortening regions which remained nearly isometric during a period of tension rise during creep. Measurements of diffraction order linewidth do not suggest increased sarcomere length dispersion in these areas. A smooth transition from shortening to lengthening was always observed. Although our data are in general agreement with the models proposed by Morgan, Mochon and Julian (Biophys. J. 39 (1982) 189–96) and Edman and Reggiani(J. Physiol. (Lond.) 351 (1984) 169–98), specific differences which do exist are discussed.
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References
Altringham, J. D. &Bottinelli, R. (1985) The descending limb of the sarcomere length-force relation in single muscle fibres of the frog.J. Musc. Res. Cell Motility 6, 585–600.
Altringham, J. D., Bottinelli, R. &Lacktis, J. W. (1984) Is stepwise sarcomere shortening an artefact?Nature 307, 653–5.
Altringham, J. D. &Pollack, G. H. (1984) Sarcomere length changes in single frog muscle fibres during tetani at long sarcomere lengths. InContractile Mechanisms in Muscle. Adv. Exp. Med. Biol. 170, 473–85.
Baskin, R. J., Zagotta, W. &Burton, K. (1984) Intersarcomere dynamics of isometric single fibers following a rapid release.Biophys. J. 45, 345a.
Borejdo, J. &Mason, P. (1976) Sarcomere length changes during stimulation of frog semitendinosus muscle.J. Mechanochem. Cell Motility 3, 155–61.
Burton, K. &Baskin, R. J. (1986) Light diffraction studies ofLimulus single fibres.Pflügers Arch. ges Physiol. 406, 409–18.
Carlsen, F., Knappeis, G. G. &Buchthal, F. (1961) Ultrastructure of the resting and contracted striated muscle fiber at different degrees of stretch.J. Biophys. Biochem. Cytol. 11, 95–118.
Cleworth, D. R. &Edman, K. A. P. (1972) Changes in sarcomere length during isometric tension development in frog skeletal muscle.J. Physiol. (Lond.) 227, 1–17.
Edman, K. A. P. (1966) The relation between sarcomere length and active tension in isolated semiten-dinosus fibres of the frog.J. Physiol. (Lond.) 183, 407–17.
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. (Lond.) 351, 169–98.
Edman, K. A. P. &Reggiani, C. (1987) The sarcomere length-tension relation determined in short segments of intact muscle fibres of the frog.J. Physiol. (Lond.) 385, 709–32.
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.
Goldman, Y. E. (1987) Measurement of sarcomere shortening in skinned fibers from frog muscle by white light diffraction.Biophys. J. 52, 57–68.
Goldman, Y. E. &Simmons, R. M. (1984) Control of sarcomere length in skinned muscle fibres ofRana temporaria during mechanical transients.J. Physiol. (Lond.) 350, 497–518.
Gordon, A. M., Huxley, A. F. &Julian, F. J. (1966a) Tension development in highly stretched vertebrate muscle fibres.J. Physiol. (Lond.) 184, 143–69.
Gordon, A. M., Huxley, A. F. &Julian, F. J. (1966b) The variation in isometric tension with sarcomere length in vertebrate muscle fibres.J. Physiol. (Lond.) 184, 170–92.
Huxley, A. F. (1980)Reflections on Muscle. Princeton, New Jersey: Princeton Univ. Press.
Huxley, A. F. &Peachey, L. D. (1961) The maximum length for contraction in vertebrate striated muscle.J. Physiol. (Lond.) 56, 150–65.
Julian, F. J. &Morgan, D. L. (1979a) Intersarcomere dynamics during fixed-end tetanic contractions of frog muscle fibres.J. Physiol. (Lond.) 293, 365–78.
Julian, F. J. &Morgan, D. L. (1979b) The effect on tension of non-uniform distribution of length changes applied to frog muscle fibres.J. Physiol. (Lond.) 293, 379–92.
Julian, F. J. &Moss, R. L. (1980) Sarcomere length-tension relations of frog skinned muscle fibres at lengths above the optimum.J. Physiol. (Lond.) 304, 529–39.
Julian, F. J., Sollins, M. R. &Moss, R. L. (1978) Sarcomere length non-uniformity in relation to tetanic responses of stretched skeletal muscle fibres.Proc. R. Soc. Lond. B200, 109–16.
Kawai, M. &Kuntz, I. D. (1973) Optical diffraction studies of muscle fibers.Biophys. J. 13, 857–75.
Klimov, A. A. &Andreyev, O. A. (1982) Accuracy of measuring the length of the sarcomeres of contracted muscle by laser diffraction.Biophysics 27, 111–3.
Lieber, R. L. &Baskin, R. J. (1983) Intersarcomere dynamics of single muscle fibers during fixed-end tetani.J. gen. Physiol. 82, 347–64.
Lieber, R. L., Roos, K. P., Lubell, B. A., Cline, J. W. &Baskin, R. J. (1983) High-speed digital data acquisition of sarcomere length from isolated skeletal and cardiac muscle cells.IEEE Trans. Biomed. Engng 30, 50–7.
Lieber, R. L., Yeh, Y. &Baskin, R. J. (1984) Sarcomere length determination using laser diffraction. Effect of beam and fiber diameter.Biophys. J. 45, 1007–16.
Leung, A. F. (1983) Light diffractometry for determining the sarcomere length of striated muscle: An evaluation.J. Musc. Res. Cell Motility 4, 473–84.
Morgan, D. L., Mochon, S. &Julian, F. J. (1982) A quantitative model of intersarcomere dynamics during fixed-end contractions of single frog muscle fibers.Biophys. J. 39, 189–96.
Paolini, P. J., Sabbadini, R., Roos, K. P. &Baskin, R. J. (1976) Sarcomere length dispersion in single skeletal muscle fibers and fiber bundles.Biophys. J. 16, 919–30.
Rudel, R. &Zite-Ferenczy, F. (1979a) Do laser diffraction studies on striated muscle indicate stepwise sarcomere shortening?Nature 278, 573–5.
Rudel, R. &Zite-Ferenczy, F. (1979b) Interpretation of light diffraction by cross-striated muscle as Bragg reflexion of light by the lattice of contractile proteins.J. Physiol. (Lond.) 290, 317–30.
Tameyasu, T., Ishide, N. &Pollack, G. H. (1982) Discrete sarcomere length distribution in skeletal muscle.Biophys. J. 37, 489–92.
Ter Keurs, H. E. K. J., Iwazumi, T. &Pollack, G. H. (1978) The sarcomere length-tension relation in skeletal muscle.J. gen. Physiol. 72, 565–92.
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Burton, K., Zagotta, W.N. & Baskin, R.J. Sarcomere length behaviour along single frog muscle fibres at different lengths during isometric tetani. J Muscle Res Cell Motil 10, 67–84 (1989). https://doi.org/10.1007/BF01739857
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DOI: https://doi.org/10.1007/BF01739857