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. 1990 May;424:133–149. doi: 10.1113/jphysiol.1990.sp018059

Changes in force and stiffness induced by fatigue and intracellular acidification in frog muscle fibres.

K A Edman 1, F Lou 1
PMCID: PMC1189805  PMID: 2391650

Abstract

1. Changes in force and stiffness were recorded simultaneously during 1 s isometric (fixed ends) tetani of single fibres isolated from the anterior tibialis muscle of Rana temporaria (temperature 1-3 degrees C; sarcomere length, 2.10 micron). Stiffness was measured as the change in force that occurred in response to a 4 kHz sinusoidal length oscillation of the fibre. Some experiments were performed in which stiffness was determined from a fast (0.2 ms) length step that was applied to a 'tendon-free' segment of the muscle fibre during the tetanus plateau. 2. A moderate degree of fatigue was produced by decreasing the time between tetani from 300 s (control) to 15 s. By this treatment the maximum tetanic force (Ftet) was reversibly reduced to 70-75% of the control value. Maximum tetanic stiffness (Stet) was related to Ftet according to the following regression (both variables expressed as percentage of their control values): Stet = 0.369 Ftet + 62.91 (correlation coefficient, 0.95; P less than 0.001). A 25% decrease in isometric force during fatigue was thus associated with merely 9% reduction of fibre stiffness. 3. Whereas the rate of rise of force during tetanus was markedly reduced by fatiguing stimulation, the rate of rise of stiffness was only slightly affected. 4. Intracellular acidification (produced by raised extracellular CO2 concentration) largely reproduced the contractile changes observed during fatigue. However, for a given decrease in tetanic force there was a smaller reduction in fibre stiffness during acidosis than during fatigue. 5. Caffeine (0.5 mM) added to the fibre after development of fatigue and intracellular acidosis greatly potentiated the isometric twitch but did not affect maximum tetanic force. This finding provides evidence that the contractile system was fully activated during the tetanus plateau both in the fatigued state and during acidosis. 6. The results suggest that the decrease in contractile strength after frequent tetanization (intervals between tetani, 15 s) is attributable to altered kinetics of cross-bridge function leading to reduced number of active cross-bridges and, most significantly, to reduced force output of the individual bridge. The possible role of increased intracellular H+ concentration in the development of muscle fatigue is discussed.

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Selected References

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  1. Allen D. G., Lee J. A., Westerblad H. Intracellular calcium and tension during fatigue in isolated single muscle fibres from Xenopus laevis. J Physiol. 1989 Aug;415:433–458. doi: 10.1113/jphysiol.1989.sp017730. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Ashley C. C., Moisescu D. G. Effect of changing the composition of the bathing solutions upon the isometric tension-pCa relationship in bundles of crustacean myofibrils. J Physiol. 1977 Sep;270(3):627–652. doi: 10.1113/jphysiol.1977.sp011972. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Bagni M. A., Cecchi G., Schoenberg M. A model of force production that explains the lag between crossbridge attachment and force after electrical stimulation of striated muscle fibers. Biophys J. 1988 Dec;54(6):1105–1114. doi: 10.1016/S0006-3495(88)83046-7. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Bosma M. M. Anion channels with multiple conductance levels in a mouse B lymphocyte cell line. J Physiol. 1989 Mar;410:67–90. doi: 10.1113/jphysiol.1989.sp017521. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Bressler B. H., Clinch N. F. The compliance of contracting skeletal muscle. J Physiol. 1974 Mar;237(3):477–493. doi: 10.1113/jphysiol.1974.sp010493. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. 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]
  7. Chase P. B., Kushmerick M. J. Effects of pH on contraction of rabbit fast and slow skeletal muscle fibers. Biophys J. 1988 Jun;53(6):935–946. doi: 10.1016/S0006-3495(88)83174-6. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Cooke R., Franks K., Luciani G. B., Pate E. The inhibition of rabbit skeletal muscle contraction by hydrogen ions and phosphate. J Physiol. 1988 Jan;395:77–97. doi: 10.1113/jphysiol.1988.sp016909. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Curtin N. A. Buffer power and intracellular pH of frog sartorius muscle. Biophys J. 1986 Nov;50(5):837–841. doi: 10.1016/S0006-3495(86)83524-X. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Curtin N. A., Edman K. A. Effects of fatigue and reduced intracellular pH on segment dynamics in 'isometric' relaxation of frog muscle fibres. J Physiol. 1989 Jun;413:159–174. doi: 10.1113/jphysiol.1989.sp017647. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Dawson M. J., Gadian D. G., Wilkie D. R. Mechanical relaxation rate and metabolism studied in fatiguing muscle by phosphorus nuclear magnetic resonance. J Physiol. 1980 Feb;299:465–484. doi: 10.1113/jphysiol.1980.sp013137. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Dawson M. J., Gadian D. G., Wilkie D. R. Muscular fatigue investigated by phosphorus nuclear magnetic resonance. Nature. 1978 Aug 31;274(5674):861–866. doi: 10.1038/274861a0. [DOI] [PubMed] [Google Scholar]
  13. Edman K. A., Mattiazzi A. R. Effects of fatigue and altered pH on isometric force and velocity of shortening at zero load in frog muscle fibres. J Muscle Res Cell Motil. 1981 Sep;2(3):321–334. doi: 10.1007/BF00713270. [DOI] [PubMed] [Google Scholar]
  14. Edman K. A. Mechanical deactivation induced by active shortening in isolated muscle fibres of the frog. J Physiol. 1975 Mar;246(1):255–275. doi: 10.1113/jphysiol.1975.sp010889. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Edman K. A., Reggiani C. Redistribution of sarcomere length during isometric contraction of frog muscle fibres and its relation to tension creep. J Physiol. 1984 Jun;351:169–198. doi: 10.1113/jphysiol.1984.sp015240. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Edwards R. H., Hill D. K., Jones D. A. Metabolic changes associated with the slowing of relaxation in fatigued mouse muscle. J Physiol. 1975 Oct;251(2):287–301. doi: 10.1113/jphysiol.1975.sp011093. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Fabiato A., Fabiato F. Effects of pH on the myofilaments and the sarcoplasmic reticulum of skinned cells from cardiace and skeletal muscles. J Physiol. 1978 Mar;276:233–255. doi: 10.1113/jphysiol.1978.sp012231. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. 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]
  19. Ford L. E., Huxley A. F., Simmons R. M. Tension transients during the rise of tetanic tension in frog muscle fibres. J Physiol. 1986 Mar;372:595–609. doi: 10.1113/jphysiol.1986.sp016027. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Godt R. E., Nosek T. M. Changes of intracellular milieu with fatigue or hypoxia depress contraction of skinned rabbit skeletal and cardiac muscle. J Physiol. 1989 May;412:155–180. doi: 10.1113/jphysiol.1989.sp017609. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Gonzalez-Serratos H., Somlyo A. V., McClellan G., Shuman H., Borrero L. M., Somlyo A. P. Composition of vacuoles and sarcoplasmic reticulum in fatigued muscle: electron probe analysis. Proc Natl Acad Sci U S A. 1978 Mar;75(3):1329–1333. doi: 10.1073/pnas.75.3.1329. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Grabowski W., Lobsiger E. A., Lüttgau H. C. The effect of repetitive stimulation at low frequencies upon the electrical and mechanical activity of single muscle fibres. Pflugers Arch. 1972;334(3):222–239. doi: 10.1007/BF00626225. [DOI] [PubMed] [Google Scholar]
  23. Hatta I., Sugi H., Tamura Y. Stiffness changes in frog skeletal muscle during contraction recorded using ultrasonic waves. J Physiol. 1988 Sep;403:193–209. doi: 10.1113/jphysiol.1988.sp017245. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. 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]
  25. Julian F. J., Morgan D. L. Variation of muscle stiffness with tension during tension transients and constant velocity shortening in the frog. J Physiol. 1981;319:193–203. doi: 10.1113/jphysiol.1981.sp013901. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Kanaya H., Takauji M., Nagai T. Properties of caffeine- and potassium-contractures in fatigued frog single twitch muscle fibers. Jpn J Physiol. 1983;33(6):945–954. doi: 10.2170/jjphysiol.33.945. [DOI] [PubMed] [Google Scholar]
  27. Kentish J. C. The effects of inorganic phosphate and creatine phosphate on force production in skinned muscles from rat ventricle. J Physiol. 1986 Jan;370:585–604. doi: 10.1113/jphysiol.1986.sp015952. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Lännergren J., Westerblad H. Force and membrane potential during and after fatiguing, continuous high-frequency stimulation of single Xenopus muscle fibres. Acta Physiol Scand. 1986 Nov;128(3):359–368. doi: 10.1111/j.1748-1716.1986.tb07989.x. [DOI] [PubMed] [Google Scholar]
  29. Lännergren J., Westerblad H. Maximum tension and force-velocity properties of fatigued, single Xenopus muscle fibres studied by caffeine and high K+. J Physiol. 1989 Feb;409:473–490. doi: 10.1113/jphysiol.1989.sp017508. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Mason P. Dynamic stiffness and crossbridge action in muscle. Biophys Struct Mech. 1977 Dec 27;4(1):15–25. doi: 10.1007/BF00538837. [DOI] [PubMed] [Google Scholar]
  31. Nassar-Gentina V., Passonneau J. V., Vergara J. L., Rapoport S. I. Metabolic correlates of fatigue and of recovery from fatigue in single frog muscle fibers. J Gen Physiol. 1978 Nov;72(5):593–606. doi: 10.1085/jgp.72.5.593. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Schoenberg M., Wells J. B. Stiffness, force, and sarcomere shortening during a twitch in frog semitendinosus muscle bundles. Biophys J. 1984 Feb;45(2):389–397. doi: 10.1016/S0006-3495(84)84163-6. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Spande J. I., Schottelius B. A. Chemical basis of fatigue in isolated mouse soleus muscle. Am J Physiol. 1970 Nov;219(5):1490–1495. doi: 10.1152/ajplegacy.1970.219.5.1490. [DOI] [PubMed] [Google Scholar]

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