European Journal of Applied Physiology

, Volume 114, Issue 11, pp 2309–2319 | Cite as

Influence of thigh activation on the \(\dot{V}\)O2 slow component in boys and men

  • Brynmor C. Breese
  • Alan R. Barker
  • Neil Armstrong
  • Jonathan Fulford
  • Craig A. WilliamsEmail author
Original Articles



During constant work rate exercise above the lactate threshold (LT), the initial rapid phase of pulmonary oxygen uptake (\(\dot{V}\)O2) kinetics is supplemented by an additional \(\dot{V}\)O2 slow component (\(\dot{V}\)O2Sc) which reduces the efficiency of muscular work. The \(\dot{V}\)O2Sc amplitude has been shown to increase with maturation but the mechanisms are poorly understood. We utilized the transverse relaxation time (T 2) of muscle protons from magnetic resonance imaging (MRI) to test the hypothesis that a lower \(\dot{V}\)O2 slow component (\(\dot{V}\)O2Sc) amplitude in children would be associated with a reduced muscle recruitment compared to adults.


Eight boys (mean age 11.4 ± 0.4) and eight men (mean age 25.3 ± 3.3 years) completed repeated step transitions of unloaded-to-very heavy-intensity (U → VH) exercise on a cycle ergometer. MRI scans of the thigh region were acquired at rest and after VH exercise up to the \(\dot{V}\)O2Sc time delay (ScTD) and after 6 min. T 2 for each of eight muscles was adjusted in relation to cross-sectional area and then summed to provide the area-weighted ΣT 2 as an index of thigh recruitment.


There were no child/adult differences in the relative \(\dot{V}\)O2Sc amplitude [Boys 14 ± 7 vs. Men 18 ± 3 %, P = 0.15, effect size (ES) = 0.8] during which the change (∆) in area-weighted ΣT 2 between the ScTD and 6 min was not different between groups (Boys 1.6 ± 1.2 vs. Men 2.3 ± 1.1 ms, P = 0.27, ES = 0.6). A positive and strong correlation was found between the relative \(\dot{V}\)O2Sc amplitude and the magnitude of the area-weighted ∆ΣT 2 in men (r = 0.92, P = 0.001) but not in boys (r = 0.09, P = 0.84).


This study provides evidence to show that progressive muscle recruitment (as inferred from T 2 changes) contributes to the development of the \(\dot{V}\)O2Sc during intense submaximal exercise independent of age.


Oxidative metabolism Magnetic resonance imaging Transverse relaxation time Children 



Adductor magnus


Analysis of variance


Gas exchange threshold




Integrated electromyogram


Magnetic resonance imaging


Rectus femoris




Slow component time delay


Standard deviation




Transverse relaxation time


Echo time


Carbon dioxide output


Minute ventilation


Oxygen uptake


Slow component of oxygen uptake


Vastus intermedius


Vastus lateralis


Vastus medialis


Time constant



The authors have no conflicts of interest. We would like to thank the pupils and staff from Wynstream Primary School for their participation in this research project. Jonathan Fulford’s salary was supported via the NIHR Clinical Research Facility.

Conflict of interest

The authors declare no conflict of interest and that no companies or manufacturers will benefit from the results of this study.


  1. Adams GR, Duvoisin MR, Dudley GA (1992) Magnetic resonance imaging and electromyography as indexes of muscle function. J Appl Physiol 73:1578–1583PubMedGoogle Scholar
  2. Armon Y, Cooper DM, Flores R, Zanconato S, Barstow TJ (1991) Oxygen uptake dynamics during high-intensity exercise in children and adults. J Appl Physiol 70:841–848PubMedCrossRefGoogle Scholar
  3. Armstrong N, Barker AR (2009) Oxygen uptake kinetics in children and adolescents: a review. Pediatr Exerc Sci 21:130–147PubMedGoogle Scholar
  4. Barker AR, Welsman JR, Fulford J, Welford D, Armstrong N (2010) Quadriceps muscle energetics during incremental exercise in children and adults. Med Sci Sports Exerc 42:1303–1313PubMedCrossRefGoogle Scholar
  5. Barker AR, Williams CA, Jones AM, Armstrong N (2011) Establishing maximal oxygen uptake in young people during a ramp cycle test to exhaustion. Br J Sports Med 45:498–503PubMedCrossRefGoogle Scholar
  6. Barker AR, Trebilcock E, Breese B, Jones AM, Armstrong N (2014) The effect of priming exercise on O2 uptake kinetics, muscle O2 delivery and utilization, muscle activity, and exercise tolerance in boys. Appl Physiol Nutr Metabol 39:308–317CrossRefGoogle Scholar
  7. 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 81:1642–1650PubMedGoogle Scholar
  8. Beaver WL, Wasserman K, Whipp BJ (1986) A new method for detecting anaerobic threshold by gas exchange. J Appl Physiol 60:2020–2027PubMedGoogle Scholar
  9. Bell RD, MacDougall JD, Billeter R, Howald H (1980) Muscle fiber types and morphometric analysis of skeletal msucle in six-year-old children. Med Sci Sports Exerc 12:28–31PubMedCrossRefGoogle Scholar
  10. Benson AP, Grassi B, Rossiter HB (2013) A validated model of oxygen uptake and circulatory dynamic interactions at exercise onset in humans. J Appl Physiol 115:743–755PubMedCrossRefGoogle Scholar
  11. Breese BC, Williams CA, Barker AR, Welsman JR, Fawkner SG, Armstrong N (2010) Longitudinal changes in the oxygen uptake kinetic response to heavy-intensity exercise in 14- to 16-year-old boys. Pediatr Exerc Sci 22:69–80PubMedGoogle Scholar
  12. Breese BC, Barker AR, Armstrong N, Jones AM, Williams CA (2012) The effect of baseline metabolic rate on pulmonary O2 uptake kinetics during very heavy intensity exercise in boys and men. Respir Physiol Neurobiol 180:223–229PubMedCrossRefGoogle Scholar
  13. Burnley M, Doust JH, Ball D, Jones AM (2002) Effects of prior heavy exercise on \(\dot{V}\)O2 kinetics during heavy exercise are related to changes in muscle activity. J Appl Physiol 93: 167–174Google Scholar
  14. Burnley M, Doust JH, Jones AM (2006) Time required for the restoration of normal heavy exercise \(\dot{V}\)O2 kinetics following prior heavy exercise. J Appl Physiol 101: 1320–1327Google Scholar
  15. Cohen J (1988) Statistical power analysis for the behavioural sciences. Lawrence Erlbaum Associates, MahwahGoogle Scholar
  16. Crow MT, Kushmerick MJ (1982) Chemical energetics of slow- and fast-twitch muscles of the mouse. J Gen Physiol 79:147–166PubMedCrossRefGoogle Scholar
  17. Edgerton VR, Smith JL, Simpson DR (1975) Muscle fibre type populations of human leg muscles. Histochem J 7:259–266PubMedCrossRefGoogle Scholar
  18. Endo MY, Kobayakawa M, Kinugasa R, Kuno S, Akima H, Rossiter HB, Miura A, Fukuba Y (2007) Thigh muscle activation distribution and pulmonary \(\dot{V}\)O2 kinetics during moderate, heavy and very heavy intensity cycling exercise in humans. Am J Physiol Reg Integr Comp Physiol 293: R812–820Google Scholar
  19. Ericson MO, Nisell R, Arborelius UP, Ekholm J (1985) Muscular activity during ergometer cycling. Scand J Rehab Med 17:53–61Google Scholar
  20. Fawkner SG, Armstrong N (2004) Longitudinal changes in the kinetic response to heavy-intensity exercise in children. J Appl Physiol 97:460–466PubMedCrossRefGoogle Scholar
  21. Garland SW, Wang W, Ward SA (2006) Indices of electromyographic activity and the “slow” component of oxygen uptake kinetics during high-intensity knee-extension exercise in humans. Eur J Appl Physiol 97:413–423PubMedCrossRefGoogle Scholar
  22. Grassi B, Poole DC, Richardson RS, Knight DR, Erickson BK, Wagner PD (1996) Muscle O2 uptake kinetics in humans: implications for metabolic control. J Appl Physiol 80:988–998PubMedGoogle Scholar
  23. Hepple RT, Howlett RA, Kindig CA, Stary CM, Hogan MC (2010) The O2 cost of the tension-time integral in isolated single myocytes during fatigue. Am J Physiol Reg Integr Comp Physiol 298:R983–R988CrossRefGoogle Scholar
  24. Jenner G, Foley JM, Cooper TG, Potchen EJ, Meyer RA (1994) Changes in magnetic resonance images of muscle depend on exercise intensity and duration, not work. J Appl Physiol 76:2119–2124PubMedGoogle Scholar
  25. Johnson MA, Polgar J, Weightman D, Appleton D (1973) Data on the distribution of fibre types in thirty-six human muscles. An autopsy study. J Neurol Sci 18:111–129PubMedCrossRefGoogle Scholar
  26. Jones AM, Grassi B, Christensen PM, Krustrup P, Bangsbo J, Poole DC (2011) Slow component of \(\dot{V}\)O2 kinetics: mechanistic bases and practical applications. Med Sci Sports Exerc 43: 2046–2062Google Scholar
  27. Krustrup P, Soderlund K, Mohr M, Bangsbo J (2004) The slow component of oxygen uptake during intense, sub-maximal exercise in man is associated with additional fibre recruitment. Pflugers Arch 447:855–866PubMedCrossRefGoogle Scholar
  28. Krustrup P, Jones AM, Wilkerson DP, Calbet JA, Bangsbo J (2009) Muscular and pulmonary O2 uptake kinetics during moderate- and high-intensity sub-maximal knee-extensor exercise in humans. J Physiol 587:1843–1856PubMedCrossRefPubMedCentralGoogle Scholar
  29. Layec G, Bringard A, Le Fur Y, Vilmen C, Micallef JP, Perrey S, Cozzone PJ, Bendahan D (2009) Effects of a prior high-intensity knee-extension exercise on muscle recruitment and energy cost: a combined local and global investigation in humans. Exp Physiol 94:704–719PubMedCrossRefGoogle Scholar
  30. Lexell J, Sjostrom M, Nordlund AS, Taylor CC (1992) Growth and development of human muscle: a quantitative morphological study of whole vastus lateralis from childhood to adult age. Muscle Nerve 15:404–409PubMedCrossRefGoogle Scholar
  31. Meyer RA, Prior BM (2000) Functional magnetic resonance imaging of muscle. Exerc Sport Sci Rev 28:89–92PubMedGoogle Scholar
  32. Poole DC, Ward SA, Gardner GW, Whipp BJ (1988) Metabolic and respiratory profile of the upper limit for prolonged exercise in man. Ergonomics 31:1265–1279PubMedCrossRefGoogle Scholar
  33. 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
  34. Pringle JS, Doust JH, Carter H, Tolfrey K, Campbell IT, Sakkas GK, Jones AM (2003) Oxygen uptake kinetics during moderate, heavy and severe intensity “submaximal” exercise in humans: the influence of muscle fibre type and capillarisation. Eur J Appl Physiol 89:289–300PubMedCrossRefGoogle Scholar
  35. Prior BM, Ploutz-Snyder LL, Cooper TG, Meyer RA (2001) Fiber type and metabolic dependence of T 2 increases in stimulated rat muscles. J Appl Physiol 90:615–623PubMedGoogle Scholar
  36. Reid RW, Foley JM, Jayaraman RC, Prior BM, Meyer RA (2001) Effect of aerobic capacity on the T 2 increase in exercised skeletal muscle. J Appl Physiol 90:897–902PubMedGoogle Scholar
  37. Richardson RS, Frank LR, Haseler LJ (1998) Dynamic knee-extensor and cycle exercise: functional MRI of muscular activity. Int J Sports Med 19:182–187PubMedCrossRefGoogle Scholar
  38. Rossiter HB, Ward SA, Kowalchuk JM, Howe FA, Griffiths JR, Whipp BJ (2001) Effects of prior exercise on oxygen uptake and phosphocreatine kinetics during high-intensity knee-extension exercise in humans. J Physiol 537:291–303PubMedCrossRefPubMedCentralGoogle Scholar
  39. Rossiter HB, Ward SA, Howe FA, Kowalchuk JM, Griffiths JR, Whipp BJ (2002) Dynamics of intramuscular 31P-MRS Pi peak splitting and the slow components of PCr and O2 uptake during exercise. J Appl Physiol 93:2059–2069PubMedGoogle Scholar
  40. 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 32:2040–2045PubMedCrossRefGoogle Scholar
  41. Scheuermann BW, Hoelting BD, Noble ML, Barstow TJ (2001) The slow component of O2 uptake is not accompanied by changes in muscle EMG during repeated bouts of heavy exercise in humans. J Physiol 531:245–256PubMedCrossRefPubMedCentralGoogle Scholar
  42. Shinohara M, Moritani T (1992) Increase in neuromuscular activity and oxygen uptake during heavy exercise. Ann Physiol Anthropol 11:257–262PubMedCrossRefGoogle Scholar
  43. Tonson A, Ratel S, Le Fur Y, Vilmen C, Cozzone PJ, Bendahan D (2010) Muscle energetics changes throughout maturation: a quantitative 31P-MRS analysis. J Appl Physiol 109:1769–1778PubMedCrossRefPubMedCentralGoogle Scholar
  44. Vanhatalo A, Poole DC, Dimenna FJ, Bailey SJ, Jones AM (2011) Muscle fiber recruitment and the slow component of O2 uptake: constant work rate vs all-out sprint exercise. Am J Physiol Reg Integr Comp Physiol 300:R700–R707CrossRefGoogle Scholar
  45. Whipp BJ (1994) The slow component of O2 uptake kinetics during heavy exercise. Med Sci Sports Exerc 26:1319–1326PubMedGoogle Scholar
  46. Whipp BJ, Wasserman K (1972) Oxygen uptake kinetics for various intensities of constant-load work. J Appl Physiol 33:351–356PubMedGoogle Scholar
  47. Whipp BJ, Davis JA, Torres F, Wasserman K (1981) A test to determine parameters of aerobic function during exercise. J Appl Physiol 50:217–221PubMedGoogle Scholar
  48. Wilkerson DP, Koppo K, Barstow TJ, Jones AM (2004) Effect of work rate on the functional ‘gain’ of phase II pulmonary O2 uptake response to exercise. Respir Physiol Neurobiol 142:211–223PubMedCrossRefGoogle Scholar
  49. Williams CA, Carter H, Jones AM, Doust JH (2001) Oxygen uptake kinetics during treadmill running in boys and men. J Appl Physiol 90:1700–1706PubMedGoogle Scholar
  50. Zoladz JA, Gladden LB, Hogan MC, Nieckarz Z, Grassi B (2008) Progressive recruitment of muscle fibers is not necessary for the slow component of \(\dot{V}\)O2 kinetics. J Appl Physiol 105: 575–580Google Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2014

Authors and Affiliations

  • Brynmor C. Breese
    • 1
    • 3
  • Alan R. Barker
    • 1
  • Neil Armstrong
    • 1
  • Jonathan Fulford
    • 2
  • Craig A. Williams
    • 1
    Email author
  1. 1.Children’s Health and Exercise Research Centre, Sport and Health Sciences, College of Life and Environmental SciencesUniversity of ExeterExeterUK
  2. 2.Peninsula NIRH Clinical Research FacilityUniversity of Exeter Medical School, University of ExeterExeterUK
  3. 3.Centre for Research in Translational Biomedicine, School of Biomedical and Healthcare SciencesPlymouth UniversityPlymouthUK

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