Pflügers Archiv

, Volume 447, Issue 6, pp 855–866 | Cite as

The slow component of oxygen uptake during intense, sub-maximal exercise in man is associated with additional fibre recruitment

  • Peter Krustrup
  • Karin Söderlund
  • Magni Mohr
  • Jens BangsboEmail author
Exercise, Temperature Regulation


Single muscle fibre metabolites and pulmonary oxygen uptake (O2) were measured during moderate and intense, sub-maximal exercise to test the hypothesis that additional fibre recruitment is associated with the slow component of O2. Seven healthy, male subjects performed 20 min moderate (MOD, ~50% ofO2,max) and intense (INT, ~80%O2,max) cycling at 70 rpm. Glycogen content decreased significantly in type I and IIa fibres during INT, but only in type I fibres during MOD. During INT, creatine phosphate (CP) content decreased significantly both in types I and II fibres in the first 3 min (ΔCP: 16.0±2.7 and 16.8±4.7 mmol kg−1 d.w., respectively) and in the next 3 min (ΔCP: 16.2±4.9 and 25.7±6.7 mmol kg−1 d.w., respectively) with no further change from 6–20 min. CP content was below the pre-exercise level (mean−1 SD) in 11, 37, 70 and 74% of the type I fibres after 0, 3, 6 and 20 min of INT, respectively, and in 13, 45, 83 and 74% of the type II fibres. During INT,O2 increased significantly by 6±1 and 4±1% in the periods 3–6 and 6–20 min, respectively (ΔO2,(6−3min): 0.14±0.02 l min−1), whereasO2 was unchanged from 3 to 20 min of MOD. Exponential fitting revealed a slow component of O2 during INT that appeared after ~2.6 min and amounted to 0.24 l min−1. The present study demonstrates that additional type I and II fibres are recruited with time during intense sub-maximal exercise in temporal association with a significant slow component of O2.


Single fibres CP and glycogen breakdown Aerobic and anaerobic metabolism 



We thank the enthusiastic volunteers participating in the study. We also thank Ingelise Kring, Merete Vannby, Winnie Taagerup and Berit Sjöberg for excellent technical assistance. Furthermore, the valuable work with mathematical modelling ofO2 curves by Dr. Ansgar Sørensen is appreciated. The study was supported by a grant from The Danish National Research Foundation (504-14). In addition, support was obtained from The Sports Research Council (Idraettens Forskningsråd).


  1. 1.
    Aaron EA, Seow KC, Johnson BD, Dempsey JA (1992) Oxygen cost of exercise hyperpnea: implications for performance. J Appl Physiol 72:1818–1825Google Scholar
  2. 2.
    Bangsbo J (1998) Quantification of anaerobic energy production during intense exercise. Med Sci Sports Exerc 30:47–52PubMedGoogle Scholar
  3. 3.
    Bangsbo J (2000) Muscle oxygen uptake in humans at onset of and during intense exercise. Acta Physiol Scand 168:457–464CrossRefPubMedGoogle Scholar
  4. 4.
    Bangsbo J, Graham T, Johansen L, Strange S, Christensen C, Saltin B (1992) Elevated muscle acidity and energy production during exhaustive exercise in humans. Am J Physiol 263:R891–R899PubMedGoogle Scholar
  5. 5.
    Bangsbo J, Krustrup P, González-Alonso J, Saltin B (2001) ATP production and efficiency of human skeletal muscle during intense exercise: effect of previous exercise. Am J Physiol 280:E956–E964Google Scholar
  6. 6.
    Bangsbo J, Madsen K, Kiens B, Richter EA (1996) Effect of muscle acidity on muscle metabolism and fatigue during intense exercise in man. J Physiol (Lond) 495:587–596Google Scholar
  7. 7.
    Barclay CJ (1996) Mechanical efficiency and fatigue of fast and slow muscles of the mouse. J Physiol (Lond) 497:781–794Google Scholar
  8. 8.
    Barstow TJ, Molé P (1991) Linear and non-linear characteristics of oxygen uptake kinetics during heavy exercise. J Appl Physiol 71:2099–2106PubMedGoogle Scholar
  9. 9.
    Barstow TJ, Casaburi R, Wasserman K (1993) O2 uptake kinetics and the O2 deficit as related to exercise intensity and blood lactate. J Appl Physiol 75:755–762Google Scholar
  10. 10.
    Barstow TJ, Jones AM, Nguyen PH, Casaburi R (1996) Influence of muscle fiber type and pedal frequency on oxygen uptake kinetics of heavy exercise. J Appl Physiol 81:1624–1650Google Scholar
  11. 11.
    Bergström J (1962) Muscle electrolytes in man. Scand J Clin Lab Invest (Suppl) 68:1–101Google Scholar
  12. 12.
    Bigland-Ritchie B, Donovan EF, Roussos CS (1981) Conduction velocity and EMG power spectrum changes in fatigue of sustained maximal efforts. J Appl Physiol 51:1300–1305PubMedGoogle Scholar
  13. 13.
    Brooke MH, Kaiser KK (1970) Three myosine adenosine triphosphatase” systems: the nature of their pH lability and sulfhydryl dependence. J Histochem Cytochem 18:670–672PubMedGoogle Scholar
  14. 14.
    Burnley M, Doust JH, Ball D, Jones AM (2002) Effects of prior exercise onO2 kinetics during heavy exercise are related to changes in muscle activity. J Appl Physiol 93:167–174PubMedGoogle Scholar
  15. 15.
    Cooke R, Franks K, Luciani GB, Pate E (1988) The inhibition of rabbit skeletal muscle contraction by hydrogen ions and phosphate. J Physiol (Lond) 395:77–97Google Scholar
  16. 16.
    Coyle EF, Sidossis LS, Horowitz JF, Beltz JD (1992) Cycling efficiency is related to percentage of Type I muscle fibres. Med Sci Sports Exerc 24:782–788PubMedGoogle Scholar
  17. 17.
    Crow MT, Kushmerick MJ (1982) Chemical energetics of slow- and fast-twitch muscles of the mouse. J Gen Physiol 79:147–166PubMedGoogle Scholar
  18. 18.
    Di Prampero PE, Boutellier U, Marguerat A (1988) Efficiency of work performance and contraction velocity in isotonic tetani of frog sartorius. Pflugers Arch 412:455–461PubMedGoogle Scholar
  19. 19.
    Ericson MO, Nisell R, Arborelius UP, Ekholm J (1985) Muscular activity during ergometer cycling. Scand J Rehabil Med 17:53–61PubMedGoogle Scholar
  20. 20.
    Gaesser GA, Poole DC (1996) The slow component of oxygen uptake kinetics in humans. Exerc Sport Sci Rev 24:35–71PubMedGoogle Scholar
  21. 21.
    Gaesser GA, Ward SA, Baum VC, Whipp BJ (1994) Effects of infused epinephrine on slow phase O2 uptake kinetics during heavy exercise in humans. J Appl Physiol 77:2413–2419PubMedGoogle Scholar
  22. 22.
    Gollnick PD, Piehl K, Saltin B (1974) Selective glycogen depletion pattern in human skeletal muscle fibres after exercise of varying intensity and at varying pedalling rates. J Physiol (Lond) 241:45–57Google Scholar
  23. 23.
    He Z-H, Bottinelli R, Pellegrino MA, Ferenczi MA, Reggiani C (2000) ATP consumption and efficiency of human single muscle fibers with different myosin isoform composition. Biophys J 79:945–961PubMedGoogle Scholar
  24. 24.
    Horowitz JF, Sidossis LS, Coyle EF (1994) High efficiency of type I muscle fibers improves performance. Int J Sports Med 15:152–157PubMedGoogle Scholar
  25. 25.
    Houtman CJ, Stegeman DF, Van Dijk JP, Zwarts MJ (2003) Changes in muscle fiber conduction velocity indicate recruitment of distinct motor unit populations. J Appl Physiol 95:1045–1054Google Scholar
  26. 26.
    Jones AM, Carter H, Doust JH (1999) A disproportionate increase inO2 coincident with lactate threshold during treadmill exercise. Med Sci Sports Exerc 31:1299–1306PubMedGoogle Scholar
  27. 27.
    Kitamura K, Jorgensen CR, Gobel FL, Taylor HL, Wang Y (1972) Hemodynamic correlates of myocardial oxygen consumption during upright exercise. J Appl Physiol 32:516–522Google Scholar
  28. 28.
    Koga S, Shiojiri T, Kondo N, Barstow TJ (1997) Effect of increased muscle temperature on oxygen uptake kinetics during exercise. J Appl Physiol 83:1333–1338Google Scholar
  29. 29.
    Koppo K, Jones AM, Vanden Bossche L, Bouckaert J (2002) Effect of prior exercise onO2 slow component is not related to muscle temperature. Med Sci Sports Exerc 34:1600–1604PubMedGoogle Scholar
  30. 30.
    Krustrup P, González-Alonso J, Quistorff B, Bangsbo J (2001) Muscle heat production and anaerobic energy turnover during repeated intense dynamic exercise in humans. J Physiol (Lond) 536:947–956Google Scholar
  31. 31.
    Krustrup P, Ferguson RA, Kjaer M, Bangsbo J (2003) ATP and heat production in human skeletal muscle during dynamic exercise: higher efficiency of anaerobic than aerobic ATP resynthesis. J Physiol (Lond) 549:255–269Google Scholar
  32. 32.
    Kuznetsov AV, Tiivel T, Sikk P, Kaambre T, Kay L, Daneshrad Z, Rossi A, Kadaja L, Peet N, Seppet E, Saks VA (1996) Striking differences between the kinetics of regulation of respiration by ADP in slow-twitch and fast-twitch muscles in vivo. Eur J Biochem 241:909–915PubMedGoogle Scholar
  33. 33.
    Lowry OH, Passonneau JV (1972) A flexible system of enzymatic analysis. Academic Press, New YorkGoogle Scholar
  34. 34.
    Medbø JI, Tabata I (1989) Relative importance of aerobic and anaerobic energy release during short-lasting exhausting bicycle exercise. J Appl Physiol 67:1881–1886PubMedGoogle Scholar
  35. 35.
    Moritani T, Sherman WM, Shibata M, Matsumoto T, Shinohara M (1992) Oxygen availability and motor unit activity in humans. Eur J Appl Physiol 64:552–556Google Scholar
  36. 36.
    Poole DC, Schaffartzik W, Knight DR, Derion T, Kennedy B, Guy HJ, Prediletto R, Wagner PD (1991) Contribution of exercising legs to the slow component of oxygen uptake kinetics in humans. J Appl Physiol 71:1245–1260PubMedGoogle Scholar
  37. 37.
    Poole DC, Gladden LB, Kurdak S, Hogan MC (1994) l-(+)-Lactate infusion into working dog gastrocnemius: no evidence lactate per se mediatesO2 slow component. J Appl Physiol 76:787–792PubMedGoogle Scholar
  38. 38.
    Pringle JS, Doust JH, Carter H, Tolfrey K, Jones AM (2003) Effect of pedal rate on primary and slow-component oxygen uptake responses during heavy-cycle exercise. J Appl Physiol. 94:1501–1507Google Scholar
  39. 39.
    Pringle JS, Doust JH, Carter H, Tolfrey K, Campbell IT, Jones AM (2003) Oxygen uptake kinetics during moderate, heavy and severe intensity ‘sub-maximal’ exercise in humans: the influence of muscle fiber type and capillarisation. Eur J Appl Physiol 89:289–300PubMedGoogle Scholar
  40. 40.
    Rasmussen UF, Krustrup P, Bangsbo J, Rasmussen HN (2001) Effect of exhaustive bicycle exercise upon the metabolism of isolated human skeletal muscle mitochondria. Pflugers Arch 443:180–187CrossRefPubMedGoogle Scholar
  41. 41.
    Rossiter HB, Ward SA, Kowalchuk JM, Howe FA, Griffiths JR, Whipp BJ (2002) Dynamic asymmetry of phosphocreatine concentration and O2 uptake between the on- and off-transients of moderate and high-intensity exercise in humans. J Physiol (Lond) 541:991–1002Google Scholar
  42. 42.
    Roston WL, Whipp BJ, Davis JA, Cunningham DA, Effros RM, Wasserman K (1987) Oxygen uptake kinetics and lactate concentration during exercise in humans. Am Rev Respir Dis 135:1080–1084PubMedGoogle Scholar
  43. 43.
    Sahlin K, Söderlund K, Tonkonogi M, Hirakoba K (1997) Phosphocreatine content in single fibres of human muscle after sustained submaximal exercise. Am J Physiol 273:C172–C178PubMedGoogle Scholar
  44. 44.
    Sargeant AJ (1987) Effect of muscle temperature on leg extension force and short-term power output in humans. Eur J Appl Physiol 56:693–698Google Scholar
  45. 45.
    Saunders MJ, Evans EM, Arngrimsson SA, Allison JD, Warren GL, Cureton KJ (2000) Muscle activation and the slow component rise in oxygen uptake during cycling. Med Sci Sports Exerc 32:2040–2045PubMedGoogle Scholar
  46. 46.
    Scheuermann BW, Hoelting BD, Noble ML, Barstow TJ (2001) The slow component O2 uptake is not accompanied by changes in muscle EMG during repeated bouts of heavy exercise in humans. J Physiol (Lond) 531:245–256Google Scholar
  47. 47.
    Söderlund K, Hultman E (1991) ATP and phosphocreatine changes in single human muscle fibres following intense electrical stimulation. Am J Physiol 261:E737–E741PubMedGoogle Scholar
  48. 48.
    Tonkonogi M, Harris B, Sahlin K (1998) Mitochondrial oxidative function in human saponin-skinned muscle fibres: effects of prolonged exercise. J Physiol (Lond) 510:279–286Google Scholar
  49. 49.
    Tordi N, Perrey S, Harvey A, Hughson RL (2003) Oxygen uptake kinetics during two bouts of heavy cycling separated by fatiguing sprint exercise in humans. J Appl Physiol 94:533–541Google Scholar
  50. 50.
    Viitasalo JT, Luhtanen P, Rahkila P, Rusko H (1985) Electromyographic activity related to aerobic and anaerobic threshold in ergometer bicycling. Acta Physiol Scand 124:287–293PubMedGoogle Scholar
  51. 51.
    Völlestad NK, Blom PC (1985) Effect of varying exercise intensity on glycogen depletion in human muscle fibres. Acta Physiol Scand 125:395–405PubMedGoogle Scholar
  52. 52.
    Westerblad H, Bruton JD, Lannergren J (1997) The effect of intracellular pH on contractile function of intact, single fibres of mouse muscle declines with increasing temperature. J Physiol (Lond) 500:193–204Google Scholar
  53. 53.
    Whipp BJ, Wasserman K (1972) Oxygen uptake for various intensities of constant-load exercise. J Appl Physiol 33:351–356PubMedGoogle Scholar
  54. 54.
    Whipp BJ, Wasserman K (1986) Effect of anaerobiosis on the kinetics of O2 uptake during exercise. Fed Proc 45:2942–2947PubMedGoogle Scholar
  55. 55.
    Wibom R, Söderlund K, Lundin A, Hultman E (1991) A luminometric method for determination of ATP and phosphocreatine in single human skeletal muscle fibres. J Biolumin Chemilumin 6:123–129PubMedGoogle Scholar
  56. 56.
    Willis WT, Jackman MR (1994) Mitochondrial function during heavy exercise. Med Sci Sports Exerc 26:1347–1354PubMedGoogle Scholar
  57. 57.
    Womack CJ, Davis SE, Blumer JL, Barrett E, Weltman AL, Gaesser GA (1995) Slow component of O2 uptake during heavy exercise: adaptations to endurance training. J Appl Physiol 79:838–845Google Scholar
  58. 58.
    Zoladz JA, Rademaker AC, Sargeant AJ (1995) Non-linear relationship between O2 uptake and power output at high intensities of exercise in humans. J Physiol (Lond) 488:211–217Google Scholar

Copyright information

© Springer-Verlag  2004

Authors and Affiliations

  • Peter Krustrup
    • 1
  • Karin Söderlund
    • 2
  • Magni Mohr
    • 1
  • Jens Bangsbo
    • 1
    Email author
  1. 1.Institute of Exercise and Sport Sciences, Department of Human PhysiologyAugust Krogh Institute, University of CopenhagenCopenhagen ØDenmark
  2. 2.University College of Physical Education and Sports and the Department of Physiology and PharmacologyKarolinska InstituteStockholmSweden

Personalised recommendations