Skip to main content
The Journal of Physiology logoLink to The Journal of Physiology
. 1988 Jan;395:115–130. doi: 10.1113/jphysiol.1988.sp016911

Activation heat in rabbit cardiac muscle.

C L Gibbs 1, D S Loiselle 1, I R Wendt 1
PMCID: PMC1191986  PMID: 3411477

Abstract

1. Activation heat was estimated myothermically in right ventricular papillary muscles of rabbits using several different methods. 2. Gradual pre-shortening of muscles to a length (lmin) where no active force development took place upon stimulation led to relatively low estimates of activation heat (1.59 +/- 0.26-2.06 +/- 0.57 mJ g-1 blotted wet weight, mean +/- S.E.M., n = 10). 3. Quick releases applied during the latency period, before force development, from lmax to various muscle lengths allowed a heat-stress relation to be established. The zero-stress intercept of this relation estimated the activation heat to be 3.27 +/- 0.40 mJ g-1; this was close to the experimentally measured value of 3.46 +/- 0.39 mJ g-1 (mean +/- S.E.M., n = 23) found by quick release from lmax to lmin. 4. The magnitude of the activation heat measured by the quick-release technique is dependent upon the extracellular Ca2+ concentration and there is good correlation between activation heat magnitude and peak developed stress. 5. In agreement with expectations based on the aequorin data of Allen & Kurihara (1982) a prolonged period of time spent at a short length is shown to depress the subsequently determined activation heat. 6. Hyperosmotic solutions (2.5 x normal) only abolished active stress development at low stimulus rates (0.2 Hz) and the activation heat measured at lmax under these conditions was 2.03 +/- 0.12 mJ g-1 (mean +/- S.E.M., n = 6). This value was significantly lower than the latency release estimate of activation heat in the same preparations (2.93 +/- 0.39 mJ g-1). 7. The latency release method of estimating activation heat results in activation heat values that account for approximately 30% of total active energy flux per contraction; a fraction comparable to that found in skeletal muscle. Calculations based on the data suggest that, under our experimental conditions, total Ca2+ release per beat lies between 50 and 100 nmol g-1 wet weight which would produce less than half-maximal myofibrillar ATPase activity when allowance is made for the passive Ca2+-buffering capacity of the myocardial cell.

Full text

PDF

Selected References

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

  1. Allen D. G., Jewell B. R., Murray J. W. The contribution of activation processes to the length-tension relation of cardiac muscle. Nature. 1974 Apr 12;248(449):606–607. doi: 10.1038/248606a0. [DOI] [PubMed] [Google Scholar]
  2. Allen D. G., Kurihara S. The effects of muscle length on intracellular calcium transients in mammalian cardiac muscle. J Physiol. 1982 Jun;327:79–94. doi: 10.1113/jphysiol.1982.sp014221. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Alpert N. R., Mulieri L. A. Increased myothermal economy of isometric force generation in compensated cardiac hypertrophy induced by pulmonary artery constriction in the rabbit. A characterization of heat liberation in normal and hypertrophied right ventricular papillary muscles. Circ Res. 1982 Apr;50(4):491–500. doi: 10.1161/01.res.50.4.491. [DOI] [PubMed] [Google Scholar]
  4. Bremel R. D., Weber A. Cooperation within actin filament in vertebrate skeletal muscle. Nat New Biol. 1972 Jul 26;238(82):97–101. doi: 10.1038/newbio238097a0. [DOI] [PubMed] [Google Scholar]
  5. Chapman J. B., Gibbs C. L. An energetic model of muscle contraction. Biophys J. 1972 Mar;12(3):227–236. doi: 10.1016/S0006-3495(72)86082-X. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Chapman J. B., Gibbs C. L., Gibson W. R. Effects of calcium and sodium on cardiac contractility and heat production in rabbit papillary muscle. Circ Res. 1970 Oct;27(4):601–610. doi: 10.1161/01.res.27.4.601. [DOI] [PubMed] [Google Scholar]
  7. Chapman R. A. Control of cardiac contractility at the cellular level. Am J Physiol. 1983 Oct;245(4):H535–H552. doi: 10.1152/ajpheart.1983.245.4.H535. [DOI] [PubMed] [Google Scholar]
  8. Cooper G., 4th Myocardial energetics during isometric twitch contractions of cat papillary muscle. Am J Physiol. 1979 Feb;236(2):H244–H253. doi: 10.1152/ajpheart.1979.236.2.H244. [DOI] [PubMed] [Google Scholar]
  9. Fabiato A. Calcium-induced release of calcium from the cardiac sarcoplasmic reticulum. Am J Physiol. 1983 Jul;245(1):C1–14. doi: 10.1152/ajpcell.1983.245.1.C1. [DOI] [PubMed] [Google Scholar]
  10. Fabiato A., Fabiato F. Dependence of the contractile activation of skinned cardiac cells on the sarcomere length. Nature. 1975 Jul 3;256(5512):54–56. doi: 10.1038/256054a0. [DOI] [PubMed] [Google Scholar]
  11. Fabiato A. Myoplasmic free calcium concentration reached during the twitch of an intact isolated cardiac cell and during calcium-induced release of calcium from the sarcoplasmic reticulum of a skinned cardiac cell from the adult rat or rabbit ventricle. J Gen Physiol. 1981 Nov;78(5):457–497. doi: 10.1085/jgp.78.5.457. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Gibbs C. L. Cardiac energetics. Physiol Rev. 1978 Jan;58(1):174–254. doi: 10.1152/physrev.1978.58.1.174. [DOI] [PubMed] [Google Scholar]
  13. Gibbs C. L., Gibson W. R. Effect of ouabain on the energy output of rabbit cardiac muscle. Circ Res. 1969 Jun;24(6):951–967. doi: 10.1161/01.res.24.6.951. [DOI] [PubMed] [Google Scholar]
  14. Gibbs C. L., Gibson W. R. Energy production in cardiac isotonic contractions. J Gen Physiol. 1970 Dec;56(6):732–750. doi: 10.1085/jgp.56.6.732. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Gibbs C. L. Modification of the physiological determinants of cardiac energy expenditure by pharmacological agents. Pharmacol Ther. 1982;18(2):133–157. doi: 10.1016/0163-7258(82)90065-1. [DOI] [PubMed] [Google Scholar]
  16. Gibbs C. L., Mommaerts W. F., Ricchiuti N. V. Energetics of cardiac contractions. J Physiol. 1967 Jul;191(1):25–46. doi: 10.1113/jphysiol.1967.sp008235. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Gibbs C. L., Ricchiuti N. V., Mommaerts W. F. Activation heat in frog sartorius muscle. J Gen Physiol. 1966 Jan;49(3):517–535. doi: 10.1085/jgp.49.3.517. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Gibbs C. L., Vaughan P. The effect of calcium depletion upon the tension-independent component of cardiac heat production. J Gen Physiol. 1968 Sep;52(3):532–549. doi: 10.1085/jgp.52.3.532. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Gordon A. M., Huxley A. F., Julian F. J. The variation in isometric tension with sarcomere length in vertebrate muscle fibres. J Physiol. 1966 May;184(1):170–192. doi: 10.1113/jphysiol.1966.sp007909. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. HILL A. V. The heat of activation and the heat of shortening in a muscle twitch. Proc R Soc Lond B Biol Sci. 1949 Jun 23;136(883):195–211. doi: 10.1098/rspb.1949.0019. [DOI] [PubMed] [Google Scholar]
  21. HILL A. V. The priority of the heat production in a muscle twitch. Proc R Soc Lond B Biol Sci. 1958 Mar 18;148(932):397–402. doi: 10.1098/rspb.1958.0033. [DOI] [PubMed] [Google Scholar]
  22. HOWARTH J. V. The behaviour of frog muscle in hypertonic solutions. J Physiol. 1958 Nov 10;144(1):167–175. doi: 10.1113/jphysiol.1958.sp006093. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Hasselbach W., Oetliker H. Energetics and electrogenicity of the sarcoplasmic reticulum calcium pump. Annu Rev Physiol. 1983;45:325–339. doi: 10.1146/annurev.ph.45.030183.001545. [DOI] [PubMed] [Google Scholar]
  24. 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]
  25. Jewell B. R. A reexamination of the influence of muscle length on myocardial performance. Circ Res. 1977 Mar;40(3):221–230. doi: 10.1161/01.res.40.3.221. [DOI] [PubMed] [Google Scholar]
  26. Loiselle D. S., Gibbs C. L. Species differences in cardiac energetics. Am J Physiol. 1979 Jul;237(1):H90–H98. doi: 10.1152/ajpheart.1979.237.1.H90. [DOI] [PubMed] [Google Scholar]
  27. Loiselle D. S. The rate of resting heat production of rat papillary muscle. Pflugers Arch. 1985 Sep;405(2):155–162. doi: 10.1007/BF00584537. [DOI] [PubMed] [Google Scholar]
  28. Mulieri L. A., Alpert N. R. Activation heat and latency relaxation in relation to calcium movement in skeletal and cardiac muscle. Can J Physiol Pharmacol. 1982 Apr;60(4):529–541. doi: 10.1139/y82-073. [DOI] [PubMed] [Google Scholar]
  29. 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]
  30. Pierce G. N., Philipson K. D., Langer G. A. Passive calcium-buffering capacity of a rabbit ventricular homogenate preparation. Am J Physiol. 1985 Sep;249(3 Pt 1):C248–C255. doi: 10.1152/ajpcell.1985.249.3.C248. [DOI] [PubMed] [Google Scholar]
  31. Rall J. A. Dependence of energy output on force generation during muscle contraction. Am J Physiol. 1978 Jul;235(1):C20–C24. doi: 10.1152/ajpcell.1978.235.1.C20. [DOI] [PubMed] [Google Scholar]
  32. Rall J. A. Effects of previous activity on the energetics of activation in frog skeletal muscle. J Gen Physiol. 1980 Jun;75(6):617–631. doi: 10.1085/jgp.75.6.617. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Rall J. A. Effects of temperature on tension, tension-dependent heat, and activation heat in twitches of frog skeletal muscle. J Physiol. 1979 Jun;291:265–275. doi: 10.1113/jphysiol.1979.sp012811. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Rall J. A. Energetics of Ca2+ cycling during skeletal muscle contraction. Fed Proc. 1982 Feb;41(2):155–160. [PubMed] [Google Scholar]
  35. Smith I. C. Energetics of activation in frog and toad muscle. J Physiol. 1972 Feb;220(3):583–599. doi: 10.1113/jphysiol.1972.sp009724. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Solaro R. J., Wise R. M., Shiner J. S., Briggs F. N. Calcium requirements for cardiac myofibrillar activation. Circ Res. 1974 Apr;34(4):525–530. doi: 10.1161/01.res.34.4.525. [DOI] [PubMed] [Google Scholar]
  37. Suga H., Hayashi T., Shirahata M. Ventricular systolic pressure-volume area as predictor of cardiac oxygen consumption. Am J Physiol. 1981 Jan;240(1):H39–H44. doi: 10.1152/ajpheart.1981.240.1.H39. [DOI] [PubMed] [Google Scholar]
  38. Weber K. T., Janicki J. S. Myocardial oxygen consumption: the role of wall force and shortening. Am J Physiol. 1977 Oct;233(4):H421–H430. doi: 10.1152/ajpheart.1977.233.4.H421. [DOI] [PubMed] [Google Scholar]
  39. 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]
  40. ter Keurs H. E., Rijnsburger W. H., van Heuningen R., Nagelsmit M. J. Tension development and sarcomere length in rat cardiac trabeculae. Evidence of length-dependent activation. Circ Res. 1980 May;46(5):703–714. doi: 10.1161/01.res.46.5.703. [DOI] [PubMed] [Google Scholar]

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

RESOURCES