Skip to main content
Log in

Modelling diffusive O2 supply to isolated preparations of mammalian skeletal and cardiac muscle

  • Published:
Journal of Muscle Research & Cell Motility Aims and scope Submit manuscript

Abstract

The purpose of this study was to use A. V. Hill’s equation describing diffusion of O2 into cylindrical muscles to assess the adequacy of O2 supply for commonly used isolated preparations of mammalian cardiac and skeletal muscles. The diffusion equation was solved numerically to give the maximum, steady state O2 diffusion distances (i.e. the distance from the surface of the muscle to the radial location where \({P}_{{\rm O}_{2}}\) is 0) for both resting and contracting muscles and for a range of temperatures. Non-steady state solutions for the rest-to-work transition were also determined to estimate how long contractile activity could be continued before anoxia develops at the muscle centre. The influence on muscle oxygenation of myoglobin-facilitated O2 diffusion was also assessed. The analysis was performed for typical sized, whole muscles from adult rats and mice, for frog sartorius muscle and for a range of temperatures. Muscle O2 consumption rates were taken from the literature. The results indicated that (1) diffusive O2 supply would be adequate to support resting metabolism of soleus and EDL muscles of rat and mouse but may not be adequate to support the transient high resting metabolic rate of papillary muscles shortly after dissection, (2) during steady contractile activity of soleus and EDL muscles, particularly those from the rat, over a reasonable range of duty cycles, adequate O2 supply could only be ensured if the radii of preparations was substantially smaller than those of whole muscles and (3) for cardiac muscles, diffusive O2 supply could only support steady-state metabolism at twitch frequencies <1 Hz for whole papillary muscles from rat and <3 Hz for those from mouse. Reducing experimental temperature markedly enhances O2 supply to skeletal, but not cardiac, muscle. O2 supply from myoglobin had only minimal effects on oxygenation under typical isolated muscle conditions.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References

  • Barclay CJ, (1992) Effect of fatigue on rate of isometric force development in mouse fast- and slow-twitch muscles Am J Physiol 263: C1065–1072

    PubMed  CAS  Google Scholar 

  • Barclay CJ, (1996) Mechanical efficiency and fatigue of fast and slow muscles of the mouse J Physiol 497: 781–794

    PubMed  CAS  Google Scholar 

  • Barclay CJ, Arnold PD, Gibbs CL, (1995) Fatigue and heat production in repeated contractions of mouse skeletal muscle J Physiol 488: 741–752

    PubMed  CAS  Google Scholar 

  • Barclay CJ, Constable JK, Gibbs CL, (1993) Energetics of fast- and slow-twitch muscles of the mouse J Physiol 472: 61–80

    PubMed  CAS  Google Scholar 

  • Barclay CJ, Curtin NA, Woledge RC, (1993) Changes in crossbridge and non-crossbridge energetics during moderate fatigue of frog muscle fibres J Physiol 468: 543–555

    PubMed  CAS  Google Scholar 

  • Barclay CJ, Loiselle DS, (1992) Dependence of muscle fatigue on stimulation protocol: effect of hypocaloric diet J Appl Physiol 72: 2278–2284

    PubMed  CAS  Google Scholar 

  • Barclay CJ, Weber CL, (2004) Slow skeletal muscles of the mouse have greater initial efficiency than fast muscles but the same net efficiency J Physiol 559: 519–533

    Article  PubMed  CAS  Google Scholar 

  • Barclay CJ, Widén C, Mellors LJ, (2003) Initial mechanical efficiency of isolated cardiac muscle J Exp Biol 206: 2725–2732

    Article  PubMed  CAS  Google Scholar 

  • Baxi J, Barclay CJ, Gibbs CL, (2000) Energetics of rat papillary muscle during contractions with sinusoidal length changes Am J Physiol 278: H1545–1554

    CAS  Google Scholar 

  • Bluhm WF, Kranias EG, Dillmann WH, Meyer M, (2000) Phospholamban: a major determinant of the cardiac force-frequency relationship Am J Physiol 278: H249–255

    CAS  Google Scholar 

  • Buckberg GD, Brazier JR, Nelson RL, Goldstein SM, McConnell DH, Cooper N, (1977) Studies of the effects of hypothermia on regional myocardial blood flow and metabolism during cardiopulmonary bypass. I. The adequately perfused beating, fibrillating and arrested heart J Thorac Cardio Surg 73: 87–94

    CAS  Google Scholar 

  • Chin ER, Balnave CD, Allen DG, (1997) Role of intracellular calcium and metabolites in low-frequency fatigue of mouse skeletal muscle Am J Physiol 272: C550–559

    PubMed  CAS  Google Scholar 

  • Cox JP, Gibbs CL, (1997) Skeletal muscle resting metabolism in cold-acclimated rats: effect of age, noradrenaline and hyperosmolarity Clin Exp Pharmacol Physiol 24: 403–407

    Article  PubMed  CAS  Google Scholar 

  • Crow MT, Kushmerick MJ, (1982) Chemical energetics of slow- and fast-twitch muscles of the mouse J Gen Physiol 79: 147–166

    Article  PubMed  CAS  Google Scholar 

  • Cummins ME, Soomal RS, Curtin NA, (1989) Fatigue of isolated mouse muscle due to isometric tetani and tetani with high power output Q J Exp Physiol 74: 951–953

    PubMed  CAS  Google Scholar 

  • Dahlstedt AJ, Katz A, Wieringa B, Westerblad H, (2000) Is creatine kinase responsible for fatigue? Studies of isolated skeletal muscle deficient in creatine kinase FASEB J 14: 982–990

    PubMed  CAS  Google Scholar 

  • Dawson MJ, Gadian DG, Wilkie DR, (1978) Muscular fatigue investigated by phosphorus nuclear magnetic resonance Nature 274: 861–866

    Article  PubMed  CAS  Google Scholar 

  • Ford LE, Huxley AF, Simmons RM, (1977) Tension responses to sudden length change in stimulated frog muscle fibres near slack length J Physiol 269: 441–515

    PubMed  CAS  Google Scholar 

  • Gibbs CL, Gibson WR, (1972) Energy production of rat soleus muscle Am J Physiol 223: 864–871

    PubMed  CAS  Google Scholar 

  • Gibbs CL, Loiselle DS, (2001) Cardiac basal metabolism Jap J Physiol 51: 399–426

    Article  PubMed  CAS  Google Scholar 

  • Gillis GB, Biewener AA, (2001) Hindlimb muscle function in relation to speed and gait: in vivo patterns of strain and activation in a hip and knee extensor of the rat, (Rattus norvegicus) J Exp Biol 204: 2717–2731

    PubMed  CAS  Google Scholar 

  • Hill AV, (1928) The diffusion of oxygen and lactic acid through tissue Proc R Soc Lond B 104: 39–96

    Article  CAS  Google Scholar 

  • Hill AV, (1964) The effect of load on the heat of shortening of muscle Proc R Soc Lond B 159: 297–318

    PubMed  CAS  Google Scholar 

  • Hill AV, (1965) Trails and Trials in Physiology Edward Arnold Ltd., London

    Google Scholar 

  • Hill AV, Woledge RC, (1962) An examination of absolute values in myothermic measurements J Physiol 162: 311–333

    PubMed  CAS  Google Scholar 

  • Hill DK, (1940) The time course of oxygen consumption of stimulated frog’s muscle J Physiol 98: 207–227

    PubMed  CAS  Google Scholar 

  • Holubarsch C, Alpert NR, Goulette R, Mulieri LA, (1982) Heat production during hypoxic contracture of rat myocardium Circ Res 51: 777–786

    PubMed  CAS  Google Scholar 

  • Jurgens KD, Papadopoulos S, Peters T, Gros G, (2000) Myoglobin: Just an oxygen store or also an oxygen transporter? NIPS 15: 269–274

    PubMed  CAS  Google Scholar 

  • Kristensen M, Albertsen J, Rentsch M, Juel C, (2005) Lactate and force production in skeletal muscle J Physiol 562: 521–526

    Article  PubMed  CAS  Google Scholar 

  • Kushmerick MJ, Meyer RA, (1985) Chemical changes in rat leg muscle by phosphorus nuclear magnetic resonance Am J Physiol 248: C542–549

    PubMed  CAS  Google Scholar 

  • Lodder MA, de Haan A, (1992) Muscle fatigue and efficiency in relation to interval duration of successive contractions Eur J Appl Physiol Occupat Physiol 64: 42–46

    Article  CAS  Google Scholar 

  • Loiselle DS, (1985a) The effect of temperature on the basal metabolism of cardiac muscle Pflugers Arch 405: 163–169

    Article  CAS  Google Scholar 

  • Loiselle DS, (1985b) The rate of resting heat production of rat papillary muscle. Pflugers Arch 405: 155–162

    Article  CAS  Google Scholar 

  • Loiselle DS, (1987) The effect of myoglobin-facilitated oxygen transport on the basal metabolism of papillary muscle Biophys J 51: 905–913

    PubMed  CAS  Google Scholar 

  • Loiselle DS, Gibbs CL, (1979) Species differences in cardiac energetics Am J Physiol 237: H90–98

    PubMed  CAS  Google Scholar 

  • Lombardi V, Piazzesi G, (1990) The contractile response during steady lengthening of stimulated frog muscle fibres J Physiol 431: 141–171

    PubMed  CAS  Google Scholar 

  • Lou F, Sun YB, (1994) Moderate fatigue studied at great sarcomere lengths in frog single muscle fibres Acta Physiol Scand 152: 163–172

    PubMed  CAS  Google Scholar 

  • Mahler M, (1978a) Diffusion and consumption of oxygen in the resting frog sartorius muscle J Gen Physiol 71: 533–557

    Article  CAS  Google Scholar 

  • Mahler M, (1978b) Kinetics of oxygen consumption after a single isometric tetanus of frog sartorius muscle at 20°C J Gen Physiol 71: 559–580

    Article  CAS  Google Scholar 

  • Mahler M, (1985) First-order kinetics of muscle oxygen consumption, and an equivalent proportionality between QO2 and phosphorylcreatine level. Implications for the control of respirationJ Gen Physiol 86: 135–165

    Article  PubMed  CAS  Google Scholar 

  • Mahler M, Louy C, Homsher E, Peskoff A, (1985) Reappraisal of diffusion, solubility, and consumption of oxygen in frog skeletal muscle, with applications to muscle energy balance J Gen Physiol 86: 105–134

    Article  PubMed  CAS  Google Scholar 

  • Mast F, Woledge RC, Elzinga G, (1990) Analysis of thermopile records from contracting isolated cardiac muscle Am J Physiol 259: H1601–H1605

    PubMed  CAS  Google Scholar 

  • Paradise NF, Schmitter JL, Surmitis JM, (1981) Criteria for adequate oxygenation of isometric kitten papillary muscle Am J Physiol 241: H348–H353

    PubMed  CAS  Google Scholar 

  • Paul RJ, (1983) Physical and biochemical energy balance during an isometric tetanus and steady state recovery in frog sartorius at 0° C J Gen Physiol 81: 337–354

    Article  PubMed  CAS  Google Scholar 

  • Pedersen TH, Clausen T, Nielsen OB, (2003) Loss of force induced by high extracellular [K+] in rat muscle: effect of temperature, lactic acid and beta2-agonist J Physiol 551: 277–286

    Article  PubMed  CAS  Google Scholar 

  • Press WH, Flannery BP, Teukolsky SA, Vetterling WT, (1998) Numerical Recipes in C Cambridge University Press, Cambridge

    Google Scholar 

  • Reggiani C, Potma EJ, Bottinelli R, Canepari M, Pellegrino MA, Stienen GJM, (1997) Chemo-mechanical energy transduction in relation to myosin isoform composition in skeletal muscle fibres of the rat J Physiol 502: 449–460

    Article  PubMed  CAS  Google Scholar 

  • Schenkman KA, (2001) Cardiac performance as a function of intracellular oxygen tension in buffer-perfused hearts Am J Physiol 281: H2463–2472

    CAS  Google Scholar 

  • Segal SS, Faulkner JA, (1985) Temperature-dependent physiological stability of rat skeletal muscle in vitro Am J Physiol 248: C265–C270

    PubMed  CAS  Google Scholar 

  • Segal SS, Faulkner JA, White TP, (1986) Skeletal muscle fatigue in vitro is temperature dependent J Appl Physiol 61: 660–665

    PubMed  CAS  Google Scholar 

  • Spande JI, Schottelius BA, (1970) Chemical basis of fatigue in isolated mouse soleus muscle Am J Physiol 219: 1490–1495

    PubMed  CAS  Google Scholar 

  • Wendt IR, Gibbs CL, (1973) Energy production of rat extensor digitorum longus muscle Am J Physiol 224: 1081–1086

    PubMed  CAS  Google Scholar 

  • Wendt IR, Gibbs CL, (1976) Recovery heat production of mammalian fast- and slow-twitch muscles Am J Physiol 230: 637–643

    PubMed  CAS  Google Scholar 

  • Westerblad H, Duty S, Allen DG, (1993) Intracellular calcium concentration during low-frequency fatigue in isolated single fibers of mouse skeletal muscle J Appl Physiol 75: 382–388

    PubMed  CAS  Google Scholar 

  • Widén C, Barclay CJ, (2005) Resting metabolism of mouse papillary muscle Pflugers Arch 450: 209–216

    Article  PubMed  CAS  Google Scholar 

  • Wittenberg BA, Wittenberg JB, (1985) Oxygen pressure gradients in isolated cardiac myocytes J Biol Chem 260: 6548–6554

    PubMed  CAS  Google Scholar 

  • Wittenberg JB, Wittenberg BA, (2003) Myoglobin function reassessed J Exp Biol 206: 2011–2020

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgements

The author thanks D. Loiselle for assistance with modelling effects of myoglobin and C. Widén for critical reading of the manuscript. This work was supported by a Griffith University Encouragement Grant.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to C. J. Barclay.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Barclay, C.J. Modelling diffusive O2 supply to isolated preparations of mammalian skeletal and cardiac muscle. J Muscle Res Cell Motil 26, 225–235 (2005). https://doi.org/10.1007/s10974-005-9013-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10974-005-9013-x

Keywords

Navigation