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. 1997 Nov 15;505(Pt 1):205–215. doi: 10.1111/j.1469-7793.1997.205bc.x

Energetics of lengthening in mouse and toad skeletal muscles.

J K Constable 1, C J Barclay 1, C L Gibbs 1
PMCID: PMC1160105  PMID: 9409483

Abstract

1. The energetics of lengthening were studied in amphibian and mammalian skeletal muscle. The aims were to determine whether energy absorption during stretch is a general property of skeletal muscle and to investigate the influence of lengthening velocity on energy absorption. 2. Experiments were performed in vitro (21 degrees C) using bundles of muscle fibres from fast-twitch extensor digitorum longus and slow-twitch soleus muscles of the mouse and tibialis anterior muscles of a toad, Bufo marinus. Initial heat production and mechanical work done on muscles were measured during isovelocity lengthening. Enthalpy output during lengthening was calculated as the difference between the amount of heat produced and the work done. 3. For all three muscle types, more energy was put into muscles as work than was produced as heat. Thus, part of the energy put into muscles to stretch them must have been absorbed. 4. For all three muscle types, the amount of energy absorbed was constant at velocities exceeding approximately 0.5 Vmax (Vmax is the maximum shortening velocity), but was significantly lower at slow velocities of lengthening. The same amount of energy was absorbed by all three muscles when lengthened at > or = 0.5 Vmax. 5. It was concluded that absorption of energy during lengthening occurs in mammalian as well as amphibian muscle and that lengthening velocity has only a small effect on the amount of energy absorbed.

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Selected References

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  1. ABBOTT B. C., AUBERT X. M. Changes of energy in a muscle during very slow stretches. Proc R Soc Lond B Biol Sci. 1951 Dec 31;139(894):104–117. doi: 10.1098/rspb.1951.0049. [DOI] [PubMed] [Google Scholar]
  2. 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]
  3. 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]
  4. Curtin N. A., Woledge R. C. A comparison of the energy balance in two successive isometric tetani of frog muscle. J Physiol. 1977 Sep;270(2):455–471. doi: 10.1113/jphysiol.1977.sp011962. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Ebashi S., Endo M., Otsuki I. Control of muscle contraction. Q Rev Biophys. 1969 Nov;2(4):351–384. doi: 10.1017/s0033583500001190. [DOI] [PubMed] [Google Scholar]
  6. 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]
  7. Edman K. A., Elzinga G., Noble M. I. Residual force enhancement after stretch of contracting frog single muscle fibers. J Gen Physiol. 1982 Nov;80(5):769–784. doi: 10.1085/jgp.80.5.769. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Edman K. A. The velocity of unloaded shortening and its relation to sarcomere length and isometric force in vertebrate muscle fibres. J Physiol. 1979 Jun;291:143–159. doi: 10.1113/jphysiol.1979.sp012804. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Edman K. A., Tsuchiya T. Strain of passive elements during force enhancement by stretch in frog muscle fibres. J Physiol. 1996 Jan 1;490(Pt 1):191–205. doi: 10.1113/jphysiol.1996.sp021135. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Flitney F. W., Hirst D. G. Filament sliding and energy absorbed by the cross-bridge in active muscle subjected to cycical length changes. J Physiol. 1978 Mar;276:467–479. doi: 10.1113/jphysiol.1978.sp012247. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Gilbert S. H., Matsumoto Y. A reexamination of the thermoelastic effect in active striated muscle. J Gen Physiol. 1976 Jul;68(1):81–94. doi: 10.1085/jgp.68.1.81. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Homsher E., Mommaerts W. F., Ricchiuti N. V., Wallner A. Activation heat, activation metabolism and tension-related heat in frog semitendinosus muscles. J Physiol. 1972 Feb;220(3):601–625. doi: 10.1113/jphysiol.1972.sp009725. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Homsher E. Muscle enthalpy production and its relationship to actomyosin ATPase. Annu Rev Physiol. 1987;49:673–690. doi: 10.1146/annurev.ph.49.030187.003325. [DOI] [PubMed] [Google Scholar]
  14. Huxley A. F. Muscular contraction. J Physiol. 1974 Nov;243(1):1–43. [PMC free article] [PubMed] [Google Scholar]
  15. Huxley H. E., Stewart A., Sosa H., Irving T. X-ray diffraction measurements of the extensibility of actin and myosin filaments in contracting muscle. Biophys J. 1994 Dec;67(6):2411–2421. doi: 10.1016/S0006-3495(94)80728-3. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. INFANTE A. A., KLAUPIKS D., DAVIES R. E. ADENOSINE TRIPHOSPHATE: CHANGES IN MUSCLES DOING NEGATIVE WORK. Science. 1964 Jun 26;144(3626):1577–1578. doi: 10.1126/science.144.3626.1577. [DOI] [PubMed] [Google Scholar]
  17. James R, Young I, I, Altringham J. The effect of tendon compliance on in vitro/in vivo estimations of sarcomere length. J Exp Biol. 1995;198(Pt 2):503–506. doi: 10.1242/jeb.198.2.503. [DOI] [PubMed] [Google Scholar]
  18. Johnston I. A. Muscle action during locomotion: a comparative perspective. J Exp Biol. 1991 Oct;160:167–185. doi: 10.1242/jeb.160.1.167. [DOI] [PubMed] [Google Scholar]
  19. Kretzschmar K. M., Wilkie D. R. A new method for absolute heat measurement, utilizing the Peltier effect. J Physiol. 1972 Jul;224(1):18P–21P. [PubMed] [Google Scholar]
  20. 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]
  21. Leijendekker W. J., van Hardeveld C., Elzinga G. Heat production during contraction in skeletal muscle of hypothyroid mice. Am J Physiol. 1987 Aug;253(2 Pt 1):E214–E220. doi: 10.1152/ajpendo.1987.253.2.E214. [DOI] [PubMed] [Google Scholar]
  22. 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]
  23. WOLEDGE R. C. The thermoelastic effect of change of tension in active muscle. J Physiol. 1961 Jan;155:187–208. doi: 10.1113/jphysiol.1961.sp006622. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Wakabayashi K., Sugimoto Y., Tanaka H., Ueno Y., Takezawa Y., Amemiya Y. X-ray diffraction evidence for the extensibility of actin and myosin filaments during muscle contraction. Biophys J. 1994 Dec;67(6):2422–2435. doi: 10.1016/S0006-3495(94)80729-5. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Wilkie D. R. Heat work and phosphorylcreatine break-down in muscle. J Physiol. 1968 Mar;195(1):157–183. doi: 10.1113/jphysiol.1968.sp008453. [DOI] [PMC free article] [PubMed] [Google Scholar]

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