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. 1995 Nov 1;488(Pt 3):741–752. doi: 10.1113/jphysiol.1995.sp021005

Fatigue and heat production in repeated contractions of mouse skeletal muscle.

C J Barclay 1, P D Arnold 1, C L Gibbs 1
PMCID: PMC1156739  PMID: 8576863

Abstract

1. This study tested the hypothesis that moderate fatigue of skeletal muscle arises from a mismatch between energy demand and energy supply. Fatigue was defined as the decline in isometric force. Energy supply and demand were assessed from measurements of muscle heat production. 2. Experiments were performed in vitro (21 degrees C) with bundles of muscle fibres from mouse fast-twitch extensor digitorum longus muscle and slow-twitch soleus muscle. Fibre bundles were fatigued using a series of thirty isometric tetani. Cycle duration (time between successive tetani) was 5 s. The amount of fatigue that occurred during a series of tetani was varied by varying contraction duty cycle (tetanus duration/cycle duration) by varying tetanus duration. 3. Peak isometric force and total heat production in each cycle were measured. For each cycle, the amounts of initial heat (H(i)) and recovery heat (Hr) produced were calculated and used as indices of energy use and supply, respectively. H(i) and Hr were used to estimate the net initial chemical breakdown (in energy units) in each cycle (H(i,net)). 4. The magnitude of H(i,net) was greatest in the early stages of the contraction protocol when Hr was still increasing towards a steady value. The magnitude of decline in force between successive tetani was proportional to H(i,net) for both muscles. 5. The results are consistent with the idea that the development of moderate levels of fatigue at the start of a series of contractions is due to the rate of energy supply being inadequate to match the rate of energy use.

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Selected References

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  1. Barclay C. J., Constable J. K., Gibbs C. L. Energetics of fast- and slow-twitch muscles of the mouse. J Physiol. 1993 Dec;472:61–80. doi: 10.1113/jphysiol.1993.sp019937. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Barclay C. J., Curtin N. A., Woledge R. C. Changes in crossbridge and non-crossbridge energetics during moderate fatigue of frog muscle fibres. J Physiol. 1993 Aug;468:543–556. doi: 10.1113/jphysiol.1993.sp019787. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Barclay C. J. Effect of fatigue on rate of isometric force development in mouse fast- and slow-twitch muscles. Am J Physiol. 1992 Nov;263(5 Pt 1):C1065–C1072. doi: 10.1152/ajpcell.1992.263.5.C1065. [DOI] [PubMed] [Google Scholar]
  4. Brown G. C. Control of respiration and ATP synthesis in mammalian mitochondria and cells. Biochem J. 1992 May 15;284(Pt 1):1–13. doi: 10.1042/bj2840001. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Bugnard L. The relation between total and initial heat in single muscle twitches. J Physiol. 1934 Nov 12;82(4):509–519. doi: 10.1113/jphysiol.1934.sp003203. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. 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]
  7. Crow M. T., Kushmerick M. J. Chemical energetics of slow- and fast-twitch muscles of the mouse. J Gen Physiol. 1982 Jan;79(1):147–166. doi: 10.1085/jgp.79.1.147. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Cummins M. E., Soomal R. S., Curtin N. A. Fatigue of isolated mouse muscle due to isometric tetani and tetani with high power output. Q J Exp Physiol. 1989 Nov;74(6):951–953. doi: 10.1113/expphysiol.1989.sp003367. [DOI] [PubMed] [Google Scholar]
  9. Curtin N. A., Kometani K., Woledge R. C. Effect of intracellular pH on force and heat production in isometric contraction of frog muscle fibres. J Physiol. 1988 Feb;396:93–104. doi: 10.1113/jphysiol.1988.sp016952. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Curtin N. A., Woledge R. C. Energy changes and muscular contraction. Physiol Rev. 1978 Jul;58(3):690–761. doi: 10.1152/physrev.1978.58.3.690. [DOI] [PubMed] [Google Scholar]
  11. Edman K. A., Lou F. Changes in force and stiffness induced by fatigue and intracellular acidification in frog muscle fibres. J Physiol. 1990 May;424:133–149. doi: 10.1113/jphysiol.1990.sp018059. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Fitts R. H. Cellular mechanisms of muscle fatigue. Physiol Rev. 1994 Jan;74(1):49–94. doi: 10.1152/physrev.1994.74.1.49. [DOI] [PubMed] [Google Scholar]
  13. 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]
  14. Funk C. I., Clark A., Jr, Connett R. J. A simple model of aerobic metabolism: applications to work transitions in muscle. Am J Physiol. 1990 Jun;258(6 Pt 1):C995–1005. doi: 10.1152/ajpcell.1990.258.6.C995. [DOI] [PubMed] [Google Scholar]
  15. 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]
  16. Heizmann C. W., Berchtold M. W., Rowlerson A. M. Correlation of parvalbumin concentration with relaxation speed in mammalian muscles. Proc Natl Acad Sci U S A. 1982 Dec;79(23):7243–7247. doi: 10.1073/pnas.79.23.7243. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Homsher E., Lacktis J., Yamada T., Zohman G. Repriming and reversal of the isometric unexplained enthalpy in frog skeletal muscle. J Physiol. 1987 Dec;393:157–170. doi: 10.1113/jphysiol.1987.sp016817. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Idström J. P., Subramanian V. H., Chance B., Schersten T., Bylund-Fellenius A. C. Oxygen dependence of energy metabolism in contracting and recovering rat skeletal muscle. Am J Physiol. 1985 Jan;248(1 Pt 2):H40–H48. doi: 10.1152/ajpheart.1985.248.1.H40. [DOI] [PubMed] [Google Scholar]
  19. Kushmerick M. J., Meyer R. A. Chemical changes in rat leg muscle by phosphorus nuclear magnetic resonance. Am J Physiol. 1985 May;248(5 Pt 1):C542–C549. doi: 10.1152/ajpcell.1985.248.5.C542. [DOI] [PubMed] [Google Scholar]
  20. Leijendekker W. J., Elzinga G. Metabolic recovery of mouse extensor digitorum longus and soleus muscle. Pflugers Arch. 1990 Apr;416(1-2):22–27. doi: 10.1007/BF00370217. [DOI] [PubMed] [Google Scholar]
  21. Mahler M. First-order kinetics of muscle oxygen consumption, and an equivalent proportionality between QO2 and phosphorylcreatine level. Implications for the control of respiration. J Gen Physiol. 1985 Jul;86(1):135–165. doi: 10.1085/jgp.86.1.135. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Mast F., Elzinga G. Recovery heat production of isolated rabbit papillary muscle at 20 degrees C. Pflugers Arch. 1988 Jun;411(6):600–605. doi: 10.1007/BF00580854. [DOI] [PubMed] [Google Scholar]
  23. Meyer R. A. A linear model of muscle respiration explains monoexponential phosphocreatine changes. Am J Physiol. 1988 Apr;254(4 Pt 1):C548–C553. doi: 10.1152/ajpcell.1988.254.4.C548. [DOI] [PubMed] [Google Scholar]
  24. Meyer R. A., Brown T. R., Kushmerick M. J. Phosphorus nuclear magnetic resonance of fast- and slow-twitch muscle. Am J Physiol. 1985 Mar;248(3 Pt 1):C279–C287. doi: 10.1152/ajpcell.1985.248.3.C279. [DOI] [PubMed] [Google Scholar]
  25. Mulieri L. A., Luhr G., Trefry J., Alpert N. R. Metal-film thermopiles for use with rabbit right ventricular papillary muscles. Am J Physiol. 1977 Nov;233(5):C146–C156. doi: 10.1152/ajpcell.1977.233.5.C146. [DOI] [PubMed] [Google Scholar]
  26. Nassar-Gentina V., Passonneau J. V., Rapoport S. I. Fatigue and metabolism of frog muscle fibers during stimulation and in response to caffeine. Am J Physiol. 1981 Sep;241(3):C160–C166. doi: 10.1152/ajpcell.1981.241.3.C160. [DOI] [PubMed] [Google Scholar]
  27. Paul R. J. Physical and biochemical energy balance during an isometric tetanus and steady state recovery in frog sartorius at 0 degree C. J Gen Physiol. 1983 Mar;81(3):337–354. doi: 10.1085/jgp.81.3.337. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Rall J. A. Relationship of isometric unexplained energy production to parvalbumin content in frog skeletal muscle. Prog Clin Biol Res. 1989;315:117–126. [PubMed] [Google Scholar]
  29. Sahlin K., Edström L., Sjöholm H., Hultman E. Effects of lactic acid accumulation and ATP decrease on muscle tension and relaxation. Am J Physiol. 1981 Mar;240(3):C121–C126. doi: 10.1152/ajpcell.1981.240.3.C121. [DOI] [PubMed] [Google Scholar]
  30. Troup J. P., Metzger J. M., Fitts R. H. Effect of high-intensity exercise training on functional capacity of limb skeletal muscle. J Appl Physiol (1985) 1986 May;60(5):1743–1751. doi: 10.1152/jappl.1986.60.5.1743. [DOI] [PubMed] [Google Scholar]
  31. Westerblad H., Lee J. A., Lännergren J., Allen D. G. Cellular mechanisms of fatigue in skeletal muscle. Am J Physiol. 1991 Aug;261(2 Pt 1):C195–C209. doi: 10.1152/ajpcell.1991.261.2.C195. [DOI] [PubMed] [Google Scholar]
  32. Wilkie D. R. Generation of protons by metabolic processes other than glycolysis in muscle cells: a critical view. J Mol Cell Cardiol. 1979 Mar;11(3):325–330. doi: 10.1016/0022-2828(79)90446-2. [DOI] [PubMed] [Google Scholar]
  33. Woledge R. C., Reilly P. J. Molar enthalpy change for hydrolysis of phosphorylcreatine under conditions in muscle cells. Biophys J. 1988 Jul;54(1):97–104. doi: 10.1016/S0006-3495(88)82934-5. [DOI] [PMC free article] [PubMed] [Google Scholar]

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