European Journal of Applied Physiology

, Volume 99, Issue 4, pp 331–341 | Cite as

Exercise as a synchroniser of human circadian rhythms: an update and discussion of the methodological problems

  • Greg Atkinson
  • Ben Edwards
  • Thomas Reilly
  • Jim Waterhouse
Review Article

Abstract

We review the literature on whether exercise is a synchroniser of human circadian rhythms, and highlight the specific methodological problems that are associated with this topic. In applied research, exercise has been investigated as a treatment for jet lag and shift-work problems. In these studies, there have been difficulties in controlling the characteristics of the exercise bout, the athletic status of research participants and exposure to other confounding synchronisers. Therefore, it is unclear at present whether exercise can help mitigate the problems associated with transmeridian travel and shift-work. In laboratory-based experiments, participants have exercised at various times of the day and the change in phase of various circadian rhythms has been measured. Although it is difficult to control for the considerable masking effects of exercise on these estimates of circadian timing, it is clear that nocturnal exercise can induce phase delays in the onset of melatonin. Reports of exercise-induced phase advances of the melatonin rhythm are rarer, as are any phase-shifting effects at all on the body temperature rhythm. In practical terms, the substantial levels of activity needed to obtain phase shifts may not be attainable by the majority of people. In mechanistic terms, the lack of agreement with the phase-shifting effects of bright light suggests that exercise is not exerting its effects via photic entrainment pathways. An alternative explanation may involve exercise-induced hyperthermia. Moreover, it is perplexing why exercise should have a different phase response curve to light, given that humans are diurnally active.

Keywords

Masking Rhythm entrainment Exercise intensity and duration Fitness Phase shift Melatonin Body temperature 

References

  1. Aoki K, Kondo N, Shimomura Y, Iwanaga K, Harada H, Katsuura T (2002) Time-of-day effect on non-thermal control of sweating response to maintained static exercise in humans European. J Appl Physiol 86:388–393CrossRefGoogle Scholar
  2. Arendt J (1994) The pineal. In: Touitou Y, Haus E (eds) Biologic rhythms in Clinical Medicine. Springer, Berlin Heidelberg New York, pp 348–362Google Scholar
  3. Aschoff J, Wever J (1980) The circadian system of man. In: Aschoff J (eds) The Handbook of behavioural neurobiology vol 4. Biological rhythms 17:311–331Google Scholar
  4. Atkinson G, Coldwells A, Reilly T, Waterhouse J (1993) A comparison of circadian rhythms in work performance between physically active and inactive subjects. Ergonomics 36:273–281PubMedGoogle Scholar
  5. Atkinson G, Drust B, Reilly T, Waterhouse J (2003) Relevance of melatonin to sports medicine and science. Sports Med 33:809–831PubMedCrossRefGoogle Scholar
  6. Atkinson G, Todd C, Reilly T, Waterhouse JM (2005) Diurnal variation in cycling performance: influence of warm-up. J Sports Sci 23:321–329PubMedCrossRefGoogle Scholar
  7. Baehr EK, Eastman CI, Revelle W, Losee Olson SH, Wolfe LF, Zee PC (2003) Circadian phase-shifting effects of nocturnal exercise in older compared to young adults. Am J Physiol Regul Integr Comp Physiol 284:R1542–R1550PubMedGoogle Scholar
  8. Barger LK, Wright KP, Hughes RJ, Czeisler CA (2004) Daily exercise facilitates phase delays of circadian rhythm in dim light. Am J Physiol Regul Integr Comp Physiol 286:R1077–R1084PubMedGoogle Scholar
  9. Biddle SJH, Mutrie N (2001) Psychology of physical activity: determinants, well-being and interventions. Routledge, LondonGoogle Scholar
  10. Boivin DB, Duffy JF, Kronauer RA, Czeisler CA (1994) Sensitivity of the human circadian pacemaker to moderately bright light. J Biol Rhyth 9:315–331Google Scholar
  11. Boivin D, Duffy J, Kronauer R, Czeisler C (1996) Dose-response relationships for resetting of human circadian clock by light. Nature 379:540–542PubMedCrossRefGoogle Scholar
  12. Buxton OM, Frank SA, L’Hermite-Baleriaux M, Leproult R, Turek FW, van Cauter E (1997) Roles of intensity and duration of nocturnal exercise in phase delaying human circadian rhythms. Am J Physiol 273:E536–E542PubMedGoogle Scholar
  13. Buxton O, Frank S, L’Hermite-Baleriaux M, Leproult R, Turek F, van Cauter E (2003) Exercise elicits phase shifts and acute alterations of melatonin that vary with circadian phase. Am J Physiol Regul Integr Comp Physiol 284:R714–R724PubMedGoogle Scholar
  14. Cagnacci A (1997) Influences of melatonin on human circadian rhythms. Chronobiol Int 14:205–220PubMedGoogle Scholar
  15. Callard D, Davenne D, Lagarde D, Meney I, Gentil C, van Hoecke J (2001) Nychthemeral variations in core temperature and heart rate: continuous cycling exercise versus continuous rest. Int J Sports Med 22:553–557PubMedCrossRefGoogle Scholar
  16. Canal-Corretger MM, Cambras T, Diez-Noguera A (2003) Tau and phase response curves for non-photic stimuli in blinded rats. Biol Rhythm Res 34:91–99CrossRefGoogle Scholar
  17. Carr DB, Reppert SM, Bullen B, Skirinar G, Beitins I, Arnold M, Rosenblatt M, Martin JB, McArthur JB (1981) Plasma melatonin increases during exercise in women. J Clin Endocrin Metab 53:224–225Google Scholar
  18. Czeisler C, Brown E, Ronda J, Kronauer R, Richardson G, Freitag W (1985) A clinical method to assess the endogenous circadian phase (ECP) of the deep circadian oscillator in man. Sleep Res 14:295Google Scholar
  19. Czeisler C, Kronauer R, Allan J, Duffy J, Jewett M, Brown E, Ronda J (1989) Bright light induction of strong (type 0) resetting of the human circadian pacemaker. Science 244:1328–1333PubMedCrossRefGoogle Scholar
  20. Eastman CI, Hoese EK, Youngstedt SD, Liu L (1995) Phase-shifting human circadian rhythms with exercise during the night shift. Physiol Behav 58:1287–1291PubMedCrossRefGoogle Scholar
  21. Edwards B, Waterhouse J, Atkinson G, Reilly T (2002) Exercise does not necessarily influence the phase of circadian rhythm in temperature in healthy humans. J Sport Sci 20:725–732CrossRefGoogle Scholar
  22. Friedenreich CM (2001) Physical activity and cancer prevention: from observational to intervention research. Cancer Epidemiol Biomarkers Prev 10:287–301PubMedGoogle Scholar
  23. Ftaiti F, Duflot JC, Nicol C, Grelot L (2001) Tympanic temperature and heart rate changes in firefighters during treadmill runs performed with different fireproof jackets. Ergonomics 44:502–512PubMedGoogle Scholar
  24. Gaddy JR, Rollag MD, Brainard GC (1993) Pupil size reulation of threshold of light-induced melatonin suppression. J Clin Endocrinol Metab 77:1398–1401PubMedCrossRefGoogle Scholar
  25. Harbin G, Durst L, Harbin D (1989) Evaluation of oculomotor response in relationship to sports performance. Med Sci Sports Exerc 12:258–262Google Scholar
  26. Hardman AE, Stensel DJ (2003) Physical activity and health. the evidence explained. Routledge, LondonGoogle Scholar
  27. Harma MI, Ilmarinen J, Yletyinen I (1982) Circadian variation of physiological functions in physically average and very fit dayworkers. J Hum Ergol 11(Supp l):33–46Google Scholar
  28. Harma MI, llmarinen J, Knauth P, Rutenfranz J, Hanninen P (1988a) Physical training intervention in shift-workers. 1 The effects of intervention on fitness, fatigue, sleep, and psychomotor symptoms. Ergonomics 31:39–50Google Scholar
  29. Harma Mi, Ilmarinen J, Knauth P, Rutenfranz J, Hanninen O (1988b) Physical-training intervention in female shift workers. 2 The effects of intervention on the circadian-rhythms of alertness, short-term memory, and body-temperature. Ergonomics 31:51–63Google Scholar
  30. Honma K, Honma S (1988) A human phase response curve for bright light pulses. Jpn J Psychiatry Neurol 42:167–168Google Scholar
  31. Horne JA, Moore VJ (1984) Sleep EEG effects with and without additional body cooling. Electroencephalogr Clin Neurophysiol 60:33–38Google Scholar
  32. Hu FB, Stampfer MJ, Colditz GA, Ascherio A et al (2000) Physical activity and risk of stroke in women. J Am Med Assoc 283:2961–2967CrossRefGoogle Scholar
  33. Ishigaki T, Fujishiro H, Tsujita J, En Y, Yamato M, Nakano S, Hori S (2001) Relationship between helmet temperature and tympanic temperature during American football practice. Jpn J Phys Fitness Sports Med 50:333–338Google Scholar
  34. Ishigaki H, Miyao M, Ishihara S (1991) Change in pupil size as a function of exercise. J Hum Ergol (Tokyo) 20:61–66Google Scholar
  35. Ivy JL, Zderic TW, Fogt DL (1999) Prevention and treatment of non-insulin dependent diabetes mellitus. Ex Sport Sci Rev 27:1–35CrossRefGoogle Scholar
  36. Klein KE, Wegmann HM (1974) The resynchronisation of human circadian rhythms after transmeridian flights as a result of flight direction and mode of activity. In: Scheving LE, Halberg F, Pauly JE (eds) Chronobiology. Igku Shoin, Tokyo, pp 564–570Google Scholar
  37. Klerman EB, Lee Y, Czeisler CA, Kronauer RE (1999) Linear demasking techniques are unreliable for estimating the circadian phase of ambulatory temperature data. J Biol Rhythm 14:260–274CrossRefGoogle Scholar
  38. Koteja P, Swallow JG, Carter PA, Garland T (2003) Different effects of intensity and duration of locomotor activity on circadian period. J Biol Rhythm 18:491–501CrossRefGoogle Scholar
  39. Mermin J, Czeisler C (1987) Comparison of ambulatory temperature recordings at varying levels of physical exertion: average amplitude is unchanged by strenuous exercise. Sleep Res 16:253Google Scholar
  40. Minors DS, Waterhouse JM (1992) Investigating the endogenous component of human circadian rhythms: a review of some simple alternatives to constant routines. Chronobiol Int 9:55–78PubMedGoogle Scholar
  41. Minors D, Waterhouse JM, Wirz-Justice A (1991) A human phase-response curve to light. Neurosci Let 133:36–40CrossRefGoogle Scholar
  42. Mistlberger RE, Antle MC, Webb IC, Jones M, Weinberg J, Pollock MS (2003) Circadian clock resetting by arousal in Syrian hamsters: the role of stress and activity. J Physiol Regul Integr Comp Physiol 285:R917–R925Google Scholar
  43. Mistlberger R, Skene DJ (2005) Nonphotic entrainment in humans? J Biol Rhyth 20:339–352CrossRefGoogle Scholar
  44. Monteleone P, Maj M, Fusco M, Orazzo C, Kernali D (1990) Physical exercise at night blunts the nocturnal increase of plasma melatonin levels in healthy humans. Life Sci 47:1989–1995PubMedCrossRefGoogle Scholar
  45. Moog R, Hildebrant G (1987) Comparison of different causes of masking effects. In: Haider M, Koller M, Cerinka R (eds) Night and shift-work: long-term effects and their prevention. Peter Lang, New York, pp 131–140Google Scholar
  46. Mrosovsky N, Salmon P (1987) A behavioural method for accelerating re-entrainment of rhythms to new light-dark cycles. Nature 330:372–373PubMedCrossRefGoogle Scholar
  47. Piercy J, Lack L (1988) Daily exercise can shift the endogenous circadian phase. J Sleep Res 17:393Google Scholar
  48. Powell KE, Thompson PD, Caspersen CJ, Kendrick JS (1987) Physical-activity and the incidence of coronary heart-disease. Annu Rev Public Health 8:253–287PubMedCrossRefGoogle Scholar
  49. Redlin U, Mrosovsky N (1997) Exercise and human circadian rhythms: what we know and what we need to know. Chronobiol Int 14:221–229PubMedCrossRefGoogle Scholar
  50. Refinetti R, Menaker M (1992) The circadian rhythm of body temperature. Physiol Behav 51:613–637PubMedCrossRefGoogle Scholar
  51. Reilly T, Bambaeichi E (2003) Methodological issues in studies of rhythms in human performance. Biol Rhythm Res 34:321–336CrossRefGoogle Scholar
  52. Reilly T, Atkinson G, Budgett R (2001) Effect of low-dose temazepam on physiological variables and performance tests following a westerly flight across five time zones. Int J Sports Med 22:166–174PubMedCrossRefGoogle Scholar
  53. Sato KT, Kane NL, Soos G, Gisolfi CV, Kondo M, Sato K (1996) Re-examination of tympanic membrane as a core temperature. J Appl Physiol 80:1233–1239PubMedCrossRefGoogle Scholar
  54. Schmidt KP, Koehler WK, Fleissner G, Pflug B (1992) Locomotor activity accelerates the adjustment of the temperature rhythm in shift work. In: Diez-Noguera A, Cambras T (eds) Chronobiology and Chronomedicine. Peter Lang, New York, pp 389–395Google Scholar
  55. Shiota M, Sudou M, Ohshima M (1996) Using outdoor exercise to decrease jet-lag in air crew-members. Aviat Space Env Med 67:1155–1560Google Scholar
  56. Strassman RJ, Appenzellar O, Lewy AJ, Qualls CR, Peake GT (1989) Increase in plasma melatonin, β-endorphin, and cortisol after a 28.5-mile mountain race: relationship to performance and lack of effect of naltrex-one. J Clin Endocrin Metab 69:540–545CrossRefGoogle Scholar
  57. Suvanto S, Härma M (1993) The prediction of the adaptation of circadian rhythms to rapid time-zone changes. Ergonomics 36:111–116PubMedGoogle Scholar
  58. Thientz G, Lang U, Deriaz O, Ceretelli P, Sizonenko P (1984) Day-time plasma melatonin response to physical exercise in humans. J Steroid Biochem 20:1470CrossRefGoogle Scholar
  59. Tipton CM (2001) A perspective: animals, exercise research, and medicine and science in sports and exercise. Med Sci Sports Exerc 33:1981–1982PubMedCrossRefGoogle Scholar
  60. Tremblay MS, Chu SY, Mureika R (1995) Methodological and statistical considerations for exercise-related hormone evaluations. Sports Med 20:90–108PubMedGoogle Scholar
  61. Van Reeth O, Sturis J, Byrne MM, Blackman JD, L’Hermite-Balèriaux M, Leproult R, Oliner C, Refetoff S, Turek FW, Van Cauter E (1994) Nocturnal exercise delays circadian rhythms of melatonin and thyrotrophin secretion in normal men. Am J Physiol 266:E964–E974PubMedGoogle Scholar
  62. Van Someren EJW, Lijzenga C, Mirmiran M, Swaab DF (1997) Long-term fitness training improves the circadian rest-activity rhythm in healthy elderly males. J Biol Rhythms 12:146–156PubMedGoogle Scholar
  63. Van Someren EJW (2003) Thermosensitivity of the circadian timing system. Sleep Biol Rhythms 1:55–64CrossRefGoogle Scholar
  64. Vaughan GM, McDonald S, Jordan R, Allen J, Bell R, Stevens E (1979) Melatonin, pituitary function and stress in humans. Psychoneuroendocrinology 4:351–362PubMedCrossRefGoogle Scholar
  65. Waterhouse J, Drust B, Weinert D, Edwards B, Gregson W, Atkinson G, Kao S, Aizawa S, Reilly T (2005) The circadian rhythm of core temperature: origin and some implications for exercise performance. Chronobiol Int 22:205–223Google Scholar
  66. Waterhouse J, Edwards B, Nevill A, Atkinson G, Reilly T, Davies P, Godfrey R (2000a) Do subjective symptoms predict our perception of jet-lag? Ergonomics 43:1514–1527CrossRefGoogle Scholar
  67. Waterhouse J, Kao S, Weinert D, Edwards B, Atkinson G, Reilly T (2005) Measuring phase shifts in humans following a simulated time-zone transition: agreement between constant routine and purification methods. Chronobiol Int 22:829–858PubMedCrossRefGoogle Scholar
  68. Waterhouse J, Minors D, Folkard S, Owens D, Atkinson G, Macdonald I, Reilly T, Sytnik N, Tucker P (1998) Light of domestic intensity produces phase shifts of the circadian oscillator in humans. Neurosci Lett 245:97–100PubMedCrossRefGoogle Scholar
  69. Waterhouse J, Weinert D, Minors D, Folkard S, Owens D, Atkinson G, Macdonald I, Sytnik N, Tucker P, Reilly T (2000b) A comparison of some different methods for purifying core temperature data from humans. Chronobiol Int 17:539–566CrossRefGoogle Scholar
  70. Woods RL, Thomson WD (1995) Effects of exercise on aspects of visual function. Ophthalmic Physiol Opt 15:5–12PubMedCrossRefGoogle Scholar
  71. Yeo S, Scarborough M (1996) Exercise-induced hyperthermia may prevent accurate core temperature measurement by tympanic membrane thermometer. J Nur Meas 4:143–151Google Scholar
  72. Youngstedt SD, Kripke DF, Elliott JA (2002) Circadian phase-delay effects of bright light alone and combined with exercise in humans. Am J Physiol Regul Integr Comp Physiol 273:E536–E542Google Scholar

Copyright information

© Springer-Verlag 2006

Authors and Affiliations

  • Greg Atkinson
    • 1
  • Ben Edwards
    • 1
  • Thomas Reilly
    • 1
  • Jim Waterhouse
    • 1
  1. 1.Research Institute for Sport and Exercise Sciences, Henry Cotton CampusLiverpool John Moores UniversityLiverpoolUK

Personalised recommendations