Skip to main content
NCBI home page
The Journal of Physiology logoLink to The Journal of Physiology
. 1992 Jan;445:659–711. doi: 10.1113/jphysiol.1992.sp018945

Tension transients during steady lengthening of tetanized muscle fibres of the frog.

G Piazzesi 1, F Francini 1, M Linari 1, V Lombardi 1
PMCID: PMC1180003  PMID: 1501149

Abstract

1. Steady lengthenings at different velocities (0.02-1.6 microns/s per half-sarcomere, temperature 2.5-5.5 degrees C) were imposed on isolated frog muscle fibres at the plateau of the isometric tetanus (tension T0). When tension during lengthening had attained a steady value (Ti), which varied from about 1.5 to about 2 times T0 depending on lengthening velocity, tension transients were elicited by applying step length changes of different amplitudes. The change in length of a selected segment, close to the end of the fibre connected to the force transducer, was controlled by means of a striation follower. 2. The instantaneous plots of tension versus the length change during the step itself showed that at the high forces developed during steady lengthening, as at the plateau of isometric tetanus, the elasticity of the fibre was almost undamped in the whole range of lengthening velocities used. 3. The tension transient elicited by step length changes imposed in isometric conditions exhibited the characteristic four phases described previously: following the tension change simultaneous with the step (phase 1), there was a quick partial recovery (phase 2, the speed of which increased going from the largest step stretch to the largest step release), a subsequent pause or inversion in recovery (phase 3) and finally a slower approach to the tension before the step (phase 4). 4. In the region of small steps the plot of the extreme tension attained during the step (T1) versus step amplitude appeared more linear during steady lengthening than in isometric conditions and deviated progressively from linearity with increase in the size of step releases. The amount of instantaneous shortening necessary to drop tension to zero (Y0), measured by the abscissa intercept of the straight line drawn through T1 points for small steps, was about 4.1 nm per half-sarcomere in isometric conditions and 5.4 nm per half-sarcomere during lengthening at low speed (0.09 microns/s per half-sarcomere, Ti about 1.6 T0). Taken altogether this indicates, in agreement with previous work, that force enhancement during steady lengthening is due to increase in both number and extension of attached cross-bridges. During lengthening at high speed (0.8 microns/s per half-sarcomere), further enhancement in steady force (Ti about 1.9 T0) was accompanied by increase of Y0 to 6.3 nm per half-sarcomere, indicating that increase in lengthening velocity exclusively produces increase in cross-bridge extension.(ABSTRACT TRUNCATED AT 400 WORDS)

Full text

PDF
659

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. ABBOTT B. C., AUBERT X. M., HILL A. V. The absorption of work by a muscle stretched during a single twitch or a short tetanus. Proc R Soc Lond B Biol Sci. 1951 Dec 31;139(894):86–104. doi: 10.1098/rspb.1951.0048. [DOI] [PubMed] [Google Scholar]
  2. Ambrogi-Lorenzini C., Colomo F., Lombardi V. Development of force-velocity relation, stiffness and isometric tension in frog single muscle fibres. J Muscle Res Cell Motil. 1983 Apr;4(2):177–189. doi: 10.1007/BF00712029. [DOI] [PubMed] [Google Scholar]
  3. Cecchi G., Colomo F., Lombardi V. A loudspeaker servo system for determination of mechanical characteristics of isolated muscle fibres. Boll Soc Ital Biol Sper. 1976 May 30;52(10):733–736. [PubMed] [Google Scholar]
  4. Cecchi G., Colomo F., Lombardi V., Piazzesi G. Stiffness of frog muscle fibres during rise of tension and relaxation in fixed-end or length-clamped tetani. Pflugers Arch. 1987 Jun;409(1-2):39–46. doi: 10.1007/BF00584747. [DOI] [PubMed] [Google Scholar]
  5. Cecchi G., Griffiths P. J., Taylor S. Stiffness and force in activated frog skeletal muscle fibers. Biophys J. 1986 Feb;49(2):437–451. doi: 10.1016/S0006-3495(86)83653-0. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Colomo F., Lombardi V., Piazzesi G. The recovery of tension in transients during steady lengthening of frog muscle fibres. Pflugers Arch. 1989 Jun;414(2):245–247. doi: 10.1007/BF00580970. [DOI] [PubMed] [Google Scholar]
  7. Curtin N. A., Gilbert C., Kretzschmar K. M., Wilkie D. R. The effect of the performance of work on total energy output and metabolism during muscular contraction. J Physiol. 1974 May;238(3):455–472. doi: 10.1113/jphysiol.1974.sp010537. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Edman K. A., Elzinga G., Noble M. I. Enhancement of mechanical performance by stretch during tetanic contractions of vertebrate skeletal muscle fibres. J Physiol. 1978 Aug;281:139–155. doi: 10.1113/jphysiol.1978.sp012413. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Eisenberg E., Hill T. L., Chen Y. Cross-bridge model of muscle contraction. Quantitative analysis. Biophys J. 1980 Feb;29(2):195–227. doi: 10.1016/S0006-3495(80)85126-5. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Ferenczi M. A., Homsher E., Trentham D. R. The kinetics of magnesium adenosine triphosphate cleavage in skinned muscle fibres of the rabbit. J Physiol. 1984 Jul;352:575–599. doi: 10.1113/jphysiol.1984.sp015311. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Ford L. E., Huxley A. F., Simmons R. M. Proceedings: Mechanism of early tension recovery after a quick release in tetanized muscle fibres. J Physiol. 1974 Jul;240(2):42P–43P. [PubMed] [Google Scholar]
  12. Ford L. E., Huxley A. F., Simmons R. M. Tension responses to sudden length change in stimulated frog muscle fibres near slack length. J Physiol. 1977 Jul;269(2):441–515. doi: 10.1113/jphysiol.1977.sp011911. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Ford L. E., Huxley A. F., Simmons R. M. Tension transients during steady shortening of frog muscle fibres. J Physiol. 1985 Apr;361:131–150. doi: 10.1113/jphysiol.1985.sp015637. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Ford L. E., Huxley A. F., Simmons R. M. The relation between stiffness and filament overlap in stimulated frog muscle fibres. J Physiol. 1981 Feb;311:219–249. doi: 10.1113/jphysiol.1981.sp013582. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. HILL A. V. THE EFFECT OF LOAD ON THE HEAT OF SHORTENING OF MUSCLE. Proc R Soc Lond B Biol Sci. 1964 Jan 14;159:297–318. doi: 10.1098/rspb.1964.0004. [DOI] [PubMed] [Google Scholar]
  16. HUXLEY A. F. Muscle structure and theories of contraction. Prog Biophys Biophys Chem. 1957;7:255–318. [PubMed] [Google Scholar]
  17. HUXLEY A. F., PEACHEY L. D. The maximum length for contraction in vertebrate straiated muscle. J Physiol. 1961 Apr;156:150–165. doi: 10.1113/jphysiol.1961.sp006665. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Huxley A. F. A note suggesting that the cross-bridge attachment during muscle contraction may take place in two stages. Proc R Soc Lond B Biol Sci. 1973 Feb 27;183(1070):83–86. doi: 10.1098/rspb.1973.0006. [DOI] [PubMed] [Google Scholar]
  19. Huxley A. F. Muscular contraction. J Physiol. 1974 Nov;243(1):1–43. [PMC free article] [PubMed] [Google Scholar]
  20. Huxley A. F., Simmons R. M. Proposed mechanism of force generation in striated muscle. Nature. 1971 Oct 22;233(5321):533–538. doi: 10.1038/233533a0. [DOI] [PubMed] [Google Scholar]
  21. Huxley H. E., Brown W. The low-angle x-ray diagram of vertebrate striated muscle and its behaviour during contraction and rigor. J Mol Biol. 1967 Dec 14;30(2):383–434. doi: 10.1016/s0022-2836(67)80046-9. [DOI] [PubMed] [Google Scholar]
  22. Huxley H. E., Simmons R. M., Faruqi A. R., Kress M., Bordas J., Koch M. H. Changes in the X-ray reflections from contracting muscle during rapid mechanical transients and their structural implications. J Mol Biol. 1983 Sep 15;169(2):469–506. doi: 10.1016/s0022-2836(83)80062-x. [DOI] [PubMed] [Google Scholar]
  23. Katz B. The relation between force and speed in muscular contraction. J Physiol. 1939 Jun 14;96(1):45–64. doi: 10.1113/jphysiol.1939.sp003756. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Kushmerick M. J., Davies R. E. The chemical energetics of muscle contraction. II. The chemistry, efficiency and power of maximally working sartorius muscles. Appendix. Free energy and enthalpy of atp hydrolysis in the sarcoplasm. Proc R Soc Lond B Biol Sci. 1969 Dec 23;174(1036):315–353. doi: 10.1098/rspb.1969.0096. [DOI] [PubMed] [Google Scholar]
  25. Lombardi V., Menchetti G. The maximum velocity of shortening during the early phases of the contraction in frog single muscle fibres. J Muscle Res Cell Motil. 1984 Oct;5(5):503–513. doi: 10.1007/BF00713257. [DOI] [PubMed] [Google Scholar]
  26. Lombardi V., Piazzesi G. The contractile response during steady lengthening of stimulated frog muscle fibres. J Physiol. 1990 Dec;431:141–171. doi: 10.1113/jphysiol.1990.sp018324. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Schoenberg M., Brenner B., Chalovich J. M., Greene L. E., Eisenberg E. Cross-bridge attachment in relaxed muscle. Adv Exp Med Biol. 1984;170:269–284. doi: 10.1007/978-1-4684-4703-3_24. [DOI] [PubMed] [Google Scholar]

Articles from The Journal of Physiology are provided here courtesy of The Physiological Society

RESOURCES