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Sleep and Biological Rhythms

, Volume 4, Issue 3, pp 199–206 | Cite as

Effects of physical exercise on human circadian rhythms

  • Yujiro YamanakaEmail author
  • Ken-ichi Honma
  • Satoko Hashimoto
  • Nana Takasu
  • Toshihiko Miyazaki
  • Sato Honma
Review Article

Abstract

Bright light is the principal zeitgeber for the biological clock in mammals, including humans. But there is a line of evidence that non-photic stimuli such as physical activity play an important role in entrainment. Scheduled physical activity, such as wheel and forced treadmill running, has been reported to phase-shift and entrain the circadian rhythm in rodent species. In humans, several studies have reported the phase-shifting effects of physical exercise. A single bout of physical exercise at night was demonstrated to phase-delay the circadian rhythm in plasma melatonin. However, for the entrainment of human circadian rhythm, a phase-advance shift is needed. Previously, we demonstrated that scheduled physical exercise in the waking period facilitated the entrainment of plasma melatonin rhythm to the sleep/wake schedule of 23 h 40 min. This result suggested that timed physical exercise produced phase-advance shifts. A regular physical exercise also facilitated entrainment of the circadian rhythms associated with acute phase-delay shifts of the sleep/wake and light/dark schedule. These findings suggest that physical exercise is useful to adjust the circadian rhythm to external time cues, especially for totally blind people and elderly people.

Key words

circadian rhythm entrainment human phase shift physical exercise 

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References

  1. 1.
    Atkinson G, Reilly T. Circadian variation in sports performance. Sports Med. 1996; 21: 292–312.CrossRefPubMedGoogle Scholar
  2. 2.
    Drust B, Waterhouse J, Atkinson G, Edwards B, Reilly T. Circadian rhythms in sports performance — an update. Chronobiol. Int. 2005; 22: 21–44.CrossRefPubMedGoogle Scholar
  3. 3.
    Welsh DK, Logothetis DE, Meiste M, Reppert SM. Individual neurons dissociated from rat suprachiasmatic nucleus express independently phased circadian firing rhythms. Neuron 1995; 14: 697–706.CrossRefPubMedGoogle Scholar
  4. 4.
    Honma S, Shirakawa T, Honma K. Circadian periods of single suprachiasmatic neurons in rats. Neurosci. Lett. 1998; 250: 157–60.CrossRefPubMedGoogle Scholar
  5. 5.
    Honma K, Honma S. A human phase response curve for bright light pulses. Jap. J. Psychiatr. Neurol. 1988; 42: 167–8.Google Scholar
  6. 6.
    Minor D, Waterhouse J, Wirz-Justice A. A human phase-response curve to light. Neurosci. Lett. 1991; 133: 36–40.CrossRefGoogle Scholar
  7. 7.
    Beersma DGM, Daan S. Strong or weak phase resetting by lights pulse in human? J. Biol. Rhythms 1993; 8: 340–7.CrossRefPubMedGoogle Scholar
  8. 8.
    Lockley SW, Skene DJ, Arendt J, Tabandeh H, Bird AC, Defrance R. Relationship between melatonin rhythms and visual loss in the blind. J. Clin. Endocrinol. Metab. 1997; 82: 3763–70.PubMedGoogle Scholar
  9. 9.
    Klerman EB, Rimmer DW, Dijk DJ, Kronauer RE, Rizzo JF III, Czeisler CA. Nonphotic entrainment of the human circadian pacemaker. Am. J. Physiol. 1998; 274: R991–R996.PubMedGoogle Scholar
  10. 10.
    Van Reeth O, Sturis J, Byrne MM et al. Nocturnal exercise phase delays circadian rhythms of melatonin and thyrotropin secretion in normal men. Am. J. Physiol. 1994; 266: E964–E974.PubMedGoogle Scholar
  11. 11.
    Buxton OM, Frank SA, L’Hermite-Baleriaux M, Leproult R, Turek FW, Van Cauter E. Roles of intensity and duration of nocturnal exercise in causing phase delays of human circadian rhythms. Am. J. Physiol. 1997; 273: E536–E542.PubMedGoogle Scholar
  12. 12.
    Aschoff J. Exogenous and endogenous components in circadian rhythms. Cold Spring Harb. Symp. Quant. Biol. 1960; 25: 11–28.CrossRefPubMedGoogle Scholar
  13. 13.
    Mrosovsky N. Locomotor activity and non-photic influences on circadian clocks. Biol. Rev. 1996; 71: 343–72.CrossRefPubMedGoogle Scholar
  14. 14.
    Mistlberger RE, Skene DJ. Social influence on mammalian circadian rhythms: animal and human studies. Biol. Rev. 2004; 79: 533–56.CrossRefPubMedGoogle Scholar
  15. 15.
    Mrosovsky N. Phase response curves for social entrainment. J. Comp. Physiol. 1988; 162: 35–46.CrossRefGoogle Scholar
  16. 16.
    Van Reeth O, Turek FW. Stimulated activity mediates phase shifts in the hamster circadian clock induced by dark pulses or benzodiazepines. Nature 1989; 339: 49–51.CrossRefPubMedGoogle Scholar
  17. 17.
    Edgar DM, Dement WC. Regularly scheduled voluntary exercise synchronizes the mouse circadian clock. Am. J. Physiol. Regul. Integr. Comp. Physiol. 1991; 261: R928–R933.Google Scholar
  18. 18.
    Mistlberger RE. Effects of daily schedules of forced activity on free-running circadian rhythms in the rat. J. Biol. Rhythms 1991; 6: 71–80.CrossRefPubMedGoogle Scholar
  19. 19.
    Hastings MH, Mead SM, Vindlacheruvu RR, Ebling FJP, Maywood ES, Grosse J. Non-photic phase shifting of the circadian activity rhythm of Syrian hamsters: the relative potency of arousal and melatonin. Brain Res. 1992; 591: 20–6.CrossRefPubMedGoogle Scholar
  20. 20.
    Marchant EG, Mistlberger RE. Entrainment and shifting of circadian rhythms in mice by forced treadmill running. Physiol. Behav. 1996; 60: 657–63.CrossRefPubMedGoogle Scholar
  21. 21.
    Mistlberger RE, Marchant EG, Sinclair SV. Nonphotic phase shifting and the motivation to run: cold exposure reexamined. J. Biol. Rhythms 1996; 11: 208–15.CrossRefPubMedGoogle Scholar
  22. 22.
    Yamada N, Shimoda K, Takahashi K, Takahashi S. Change in period of freerunning rhythms determined by two different tools in blinded rats. Physiol. Behav. 1986; 36: 357–62.CrossRefPubMedGoogle Scholar
  23. 23.
    Yamada N, Shimoda K, Ohi K, Takahashi S, Takahashi K. Free-access to a running wheel shortens the period of free-running rhythm in blinded rat. Physiol. Behav. 1988; 42: 87–91.CrossRefPubMedGoogle Scholar
  24. 24.
    Johnson RF, Smale L, Moore RY, Morin LP. Lateral geniculate lesions block circadian phase-shift responses to benzodiazepine. Proc. Natl. Acad. Sci. USA 1988; 83: 5301–4.CrossRefGoogle Scholar
  25. 25.
    Janik D, Mikkelsen JD, Mrosovsky N. Cellular colocalization of Fos and neuropeptide Y in the intergeniculate leaflet after nonphotic phase-shifting events. Brain Res. 1995; 698: 137–45.CrossRefPubMedGoogle Scholar
  26. 26.
    Dudley TE, DiNardo LA, Glass JD. Endogenous regulation of serotonin release in the hamster suprachiasmatic nucleus. J. Neurosci. 1998; 18: 5045–52.PubMedGoogle Scholar
  27. 27.
    Grossman GH, Mistlberger RE, Antle MC, Ehlen JC, Glass JD. Sleep deprivation stimulates serotonin release in the suprachiasmatic nucleus. Neuroreport 2000; 11: 1929–32.CrossRefPubMedGoogle Scholar
  28. 28.
    Hastings MH, Best JD, Ebling FJ et al. Entrainment of the circadian clock. Prog. Brain Res. 1996; 111: 147–74.CrossRefPubMedGoogle Scholar
  29. 29.
    Weinert D, Waterhouse J. Daily activity and body temperature rhythms do not change simultaneously with age in laboratory mice. Physiol. Behav. 1999; 66: 605–12.CrossRefPubMedGoogle Scholar
  30. 30.
    Waterhouse J, Edwards B, Bedford P, Hughes A, Robinson K, Nevill A, Weinert D, Reilly T. Thermoregulation during mild exercise at different circadian times. Chronobiol. Int. 2004; 21: 253–75.CrossRefPubMedGoogle Scholar
  31. 31.
    Turek FW. Effects of stimulated physical activity on the circadian pacemaker of vertebrates. J. Biol. Rhythms 1989; 4: 135–47.CrossRefPubMedGoogle Scholar
  32. 32.
    Wickland C, Turek FW. Phase-shifting effect of triazolam on the hamster’s circadian rhythm of activity is not mediated by a change in body temperature. Brain Res. 1991; 560: 12–16.CrossRefPubMedGoogle Scholar
  33. 33.
    Mrosovsky N, Biello SM. Nonphotic phase shifting in the old and the cold. Chronobiol. Int. 1994; 11: 232–52.CrossRefPubMedGoogle Scholar
  34. 34.
    Buxton OM, Lee CW, L’Hermite-Baleriaux M, Turek FW, Van Cauter E. Exercise elicits phase shifts and acute alterations of melatonin that vary with circadian phase. Am. J. Physiol. Regul. Integr. Comp. Physiol. 2003; 284: R714–R724.CrossRefPubMedGoogle Scholar
  35. 35.
    Miyazaki T, Hashimoto S, Masubuchi S, Honma S, Honma K. Phase-advance shifts of human circadian pacemaker are accelerated by daytime physical exercise. Am. J. Physiol. Regul. Integr. Comp. Physiol. 2001; 281: R197–R205.PubMedGoogle Scholar
  36. 36.
    Beersma DG, Hiddinga AE. No impact of physical activity on the period of the circadian pacemaker in humans. Chronobiol. Int. 1998; 15: 49–57.CrossRefPubMedGoogle Scholar
  37. 37.
    Aldemir H, Atkinson G, Cable T, Edwards B, Waterhouse J, Reilly T. A comparison of the immediate effects of moderate exercise in the early morning and late afternoon on core temperature and cutaneous thermoregulatory mechanisms. Chronobiol. Int. 2000; 17: 197–207.CrossRefPubMedGoogle Scholar
  38. 38.
    Aoki K, Kondo N, Shibasaki M, Takano S, Tominaga H, Katsuura T. Circadian variation of sweating response to passive heat stress. Acta Physiol. Scand. 1997; 161: 397–402.CrossRefPubMedGoogle Scholar
  39. 39.
    Torii M, Nakayama H, Sasaki T. Thermoregulation of exercising men in the morning rise and evening fall phase of internal temperature. Br. J. Sports Med. 1995; 29: 113–20.CrossRefPubMedPubMedCentralGoogle Scholar
  40. 40.
    Kobayashi T, Ishikawa T, Tomita S, Yoshida H, Arakawa K. Exercise for a good night time sleep. Effects of timing of 1 h exercise upon the night sleep. Sleep Biol. Rhythms 2005; 3: A23.Google Scholar
  41. 41.
    Tanaka H, Taira K, Arakawa M et al. Effects of short nap and exercise on elderly people having difficulty in sleeping. Psychiatry Clin. Neurosci. 2001; 55: 173–4.CrossRefPubMedGoogle Scholar
  42. 42.
    Vitiello MV, Prinz PN, Schwartz RS. The subjective sleep quality of healthy older men and women is enhanced by participation in two fitness training programs. Sleep. Res. 1994; 23: 148.Google Scholar
  43. 43.
    King AC, Oman RE, Brassington GS, Bliwise DL, Haskell WL. Moderate-intensity exercise and self-rated quality of sleep in older adults. A randomized controlled trial. JAMA 1997; 277: 32–7.CrossRefPubMedGoogle Scholar
  44. 44.
    Singh NA, Clements KM, Eiatarone MA. A randomized controlled trial of the effect of exercise on sleep. Sleep 1997; 20: 95–101.PubMedGoogle Scholar
  45. 45.
    Vitiello MV, Larsen LH, Prinz PN, Schwartz RS. Sleep quality and circadian temperature rhythm of healthy older adults improve following successful aerobic training. Sleep Res. 1996; 25: 115.Google Scholar
  46. 46.
    Reilly T, Atkinson G, Budgett R. Effects of temazepam on physiological and performance variables following a westerly flight across five time zones. J. Sports Sci. 1997; 15: 62.Google Scholar
  47. 47.
    Mrosovsky N, Salmon PA. A behavioral method for accelerating re-entrainment of rhythms to new light-dark cycles. Nature 1987; 330: 372–3.CrossRefPubMedGoogle Scholar
  48. 48.
    Klein KE, Wegman HM. The resynchronization of human circadian rhythms after transmeridian flights as a result of flight direction and mode of activity. In: Scheving LE, Halberg E, Pauly JE, eds. Chronobiology. Igaku Shoin LTD: Tokyo, 1974; 564–70.Google Scholar
  49. 49.
    Shiota M, Sudo M, Ohshima M. Using outdoor exercise to decrease jet lag in airline crewmember. Aviat. Space Environ. Med. 1996; 67: 1150–60.Google Scholar
  50. 50.
    Barger LK, Wright KP Jr, Hughes RJ, Czeisler CA. Daily exercise facilitates phase delay of circadian melatonin rhythm in very dim light. Am. J. Physiol. Regul. Integr. Comp. Physiol. 2004; 286: R1077–R1084.CrossRefPubMedGoogle Scholar
  51. 51.
    Eastman CI, Hoese EK, Youngstedt SD, Liu L. Phaseshifting human circadian rhythms with exercise during the night shift. Physiol. Behav. 1995; 58: 1287–91.CrossRefPubMedGoogle Scholar
  52. 52.
    Baehr EK, Eogg LE, Eastman CI. Intermittent bright light and exercise to entrain human circadian rhythms to night work. Am. J. Physiol. 1999; 284: R1542–R1550.Google Scholar
  53. 53.
    Youngstedt SD, Kripke DE, Elliott JA. Circadian phase-delaying effects of bright light alone and combined with exercise in human. Am. J. Physiol. 2002; 282: R259–R266.Google Scholar
  54. 54.
    Weitzman ED, Moline ML, Czeisler CA, Zimmerman JC. Chronobiology of aging: temperature, sleep-wake rhythms and entrainment. Neurobiol. Aging 1982; 3: 299–309.CrossRefPubMedGoogle Scholar
  55. 55.
    Czeisler CA, Dumont M, Duffy JE et al. Association of sleep-wake habits in older people with changes in output of circadian pacemaker. Lancet 1992; 340: 933–6.CrossRefPubMedGoogle Scholar
  56. 56.
    Monk TH, Buysse DJ, Reynolds CE, Kupfer DJ, Houck PR. Circadian temperature rhythms of older people. Exp. Gerontol. 1995; 30: 455–74.CrossRefPubMedGoogle Scholar
  57. 57.
    Duffy JE, Dijk DJ, Hall EE, Czeisler CA. Later endogenous circadian temperature nadir relative to an earlier wake time in older people. Am. J. Physiol. Endocrinol. Metab. 1998; 275: R1478–R1487.Google Scholar
  58. 58.
    Carrier J, Monk TH, Reynolds CE, Buysse BJ, Kupfer DJ. Are age differences in sleep due to phase difference in the output of the circadian timing system? Chronobiol. Int. 1999; 16: 79–91.CrossRefPubMedGoogle Scholar
  59. 59.
    Vitiello MV, Smallwood RG, Avery DH, Pascualy RA, Martin DC, Prinz PN. Circadian temperature rhythms in young adult and aged men. Neurobiol. Aging 1986; 7: 97–100.CrossRefPubMedGoogle Scholar
  60. 60.
    Baehr EK, Revelle W, Eastman CI. Individual differences in the phase and amplitude of the human circadian temperature rhythm: with an emphasis on morning-eveningness. J. Sleep Res. 2000; 9: 117–27.CrossRefPubMedGoogle Scholar
  61. 61.
    Baehr EK, Eastman CI, Revelle W, Olson SH, Wolfe LE, Zee PC. Circadian phase-shifting effects of nocturnal exercise in older compared with young adults. Am. J. Physiol. Regul. Integr. Comp. Physiol. 2003; 284: R1542–50.CrossRefPubMedGoogle Scholar

Copyright information

© Japanese Society of Sleep Research 2006

Authors and Affiliations

  • Yujiro Yamanaka
    • 1
    Email author
  • Ken-ichi Honma
    • 1
  • Satoko Hashimoto
    • 1
  • Nana Takasu
    • 1
  • Toshihiko Miyazaki
    • 1
  • Sato Honma
    • 1
  1. 1.Department of PhysiologyHokkaido University Graduate School of MedicineSapporoJapan

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