Mechanisms of Non-photic Entrainment

  • Emma J. Wams
  • Sjaak J. Riede
  • Ivor van der Laan
  • Tim ten Bulte
  • Roelof A. HutEmail author


This chapter reviews how non-photic cues like temperature, food, anxiety and induced activity lead to circadian rhythm entrainment in mammals. Generally speaking, when dealing with entrainment by different photic and non-photic zeitgebers, we are only able to show that a certain type of stimulus can or cannot entrain the circadian system, therefore, the comparison is difficult to be quantified for the purpose of interpretation. For example, the effect of temperature as a zeitgeber could be different when used alone or when used in anti-phase with the light-dark cycle. Timed feeding and anxiety can also cause non-photic entrainment of circadian rhythms, with a potentially strong selective benefits for prey species like mice and rats.

Although significant work has been done on non-photic entrainment, there are still many open questions to date. Here we will describe different aspects of non-photic entrainment of the circadian system in mammals, with focus on certain open questions especially when nocturnal and diurnal animals are compared.


Non-photic PRC Non-photic entrainment Social entrainment Induced activity entrainment Diurnal Nocturnal Non-photic paradox Scheduled exercise 


  1. 1.
    Refinetti R (2015) Comparison of light, food, and temperature as environmental synchronizers of the circadian rhythm of activity in mice. J Physiol Sci 65:359–366CrossRefPubMedGoogle Scholar
  2. 2.
    Van der Vinne V, Riede SJ, Gorter JA, Eijer WG, Sellix MT, Menaker M, Daan S, Pilorz V, Hut RA (2014) Cold and hunger induce diurnality in a nocturnal mammal. Proc Natl Acad Sci U S A 111:15256–15260CrossRefPubMedPubMedCentralGoogle Scholar
  3. 3.
    Buhr ED, Yoo SH, Takahashi JS (2010) Temperature as a universal resetting cue for mammalian circadian oscillators. Science 330:379–385CrossRefPubMedPubMedCentralGoogle Scholar
  4. 4.
    Stephan FK, Swann JM, Sisk CL (1979) Anticipation of 24-hr feeding schedules in rats with lesions of the suprachiasmatic nucleus. Behav Neural Biol 25:346–363CrossRefPubMedGoogle Scholar
  5. 5.
    Pellman BA, Kim E, Reilly M, Kashima J, Motch O, de la Iglesia HO, Kim JJ (2015) Time-specific fear acts as a non-photic entraining stimulus of circadian rhythms in rats. Sci Rep 5:14916CrossRefPubMedPubMedCentralGoogle Scholar
  6. 6.
    Daan S (1981) Adaptive daily strategies in behavior. In: Aschoff J (ed) Handbook of behavioral neurobiology. Plenum Publishing Cooperation, New York, pp 275–297Google Scholar
  7. 7.
    Daan S, Koene P (1981) On the timing of foraging flights by Oystercatchers, Haematopus ostralegus, on tidal mudflats. Neth J Sea Res 15:1–22CrossRefGoogle Scholar
  8. 8.
    Rijnsdorp A, Daan S, Dijkstra C (1981) Hunting in the Kestrel, Falco tinnunculus, and the adaptive significance of daily habits. Oecologia 50:391–406CrossRefGoogle Scholar
  9. 9.
    Mrosovsky N (1988) Phase response curves for social entrainment. J Comp Physiol A 162:35–46CrossRefPubMedGoogle Scholar
  10. 10.
    Mrosovsky N (1995) A non-photic gateway to the circadian clock of hamsters. CIBA Found Symp 183:154–167PubMedGoogle Scholar
  11. 11.
    Marimuthu G, Rajan S, Chandrashekaran MK (1981) Social entrainment of the circadian rhythm in the flight activity of the Microchiropteran bat Hipposideros speoris. Behav Ecol Sociobiol 8:147–150CrossRefGoogle Scholar
  12. 12.
    Rusak B, Mistlberger RE, Losier B, Jones CH (1988) Daily hoarding opportunity entrains the pacemaker for hamster activity rhythms. J Comp Physiol A 164:165–171CrossRefPubMedGoogle Scholar
  13. 13.
    Reebs SG, Mrosovsky N (1989) Effects of induced wheel running on the circadian activity rhythms of Syrian hamsters: entrainment and phase response curve. J Biol Rhythms 4:39–48CrossRefPubMedGoogle Scholar
  14. 14.
    Edgar DM, Dement WC (1991) Regularly scheduled voluntary exercise synchronizes the mouse circadian clock. Am J Physiol 261:R928–R933PubMedGoogle Scholar
  15. 15.
    Hastings MH, Duffield GE, Smith EJD, Maywood ES, Ebling FJP (1998) Entrainment of the circadian system of mammals by nonphotic cues. Chronobiol Int 15:425–445CrossRefPubMedGoogle Scholar
  16. 16.
    Kas MJ, Edgar DM (1999) A nonphotic stimulus inverts the diurnal-nocturnal phase preference in Octodon degus. J Neurosci 19:328–333PubMedGoogle Scholar
  17. 17.
    Kas MJ, Edgar DM (1999) Scheduled voluntary wheel running activity modulates free-running circadian body temperature rhythms in Octodon degus. in prepGoogle Scholar
  18. 18.
    Edgar DM, Martin CE, Dement WC (1991) Activity feedback to the mammalian circadian pacemaker: influence on the observed measures of rhythm period length. J Biol Rhythms 6:185–199CrossRefPubMedGoogle Scholar
  19. 19.
    Johnson CH (1999) Forty years of PRCs-what have we learned ? Chronobiol Int 16:711–743CrossRefPubMedGoogle Scholar
  20. 20.
    Van Oosterhout F, Lucassen EA, Houben T, Vanderleest HT, Antle MC, Meijer JH (2012) Amplitude of the SCN clock enhanced by the behavioral activity rhythm. PLoS ONE 7:e39693CrossRefPubMedPubMedCentralGoogle Scholar
  21. 21.
    Melancon MO, Lorrain D, Dionne IJ (2014) Exercise and sleep in aging: emphasis on serotonin. Pathol Biol 62:276–283CrossRefPubMedGoogle Scholar
  22. 22.
    Reebs SG (1989) Acoustical entrainment of circadian activity rhythms in house sparrows: constant light is not necessary. Ethology 80:172–181CrossRefGoogle Scholar
  23. 23.
    Menaker M, Eskin A (1966) Entrainment of circadian rhythms by sound in Passer domesticus. Science 154:1579–1581CrossRefPubMedGoogle Scholar
  24. 24.
    Erkert HG, Schardt U (1991) Social entrainment of circadian activity rhythms in common marmosets, Callithrix j. jacchus (Primates). Ethology 87:189–202CrossRefGoogle Scholar
  25. 25.
    Hut RA, Mrosovsky N, Daan S (1999) Nonphotic entrainment in a diurnal mammal, the European ground squirrel (Spermophilus citellus). J Biol Rhythms 14:409–419CrossRefPubMedGoogle Scholar
  26. 26.
    Glass JD, Tardif SD, Clements R, Mrosovsky N (2001) Photic and nonphotic circadian phase resetting in a diurnal primate, the common marmoset. Am J Physiol Regul Integr Comp Physiol 280:R191–R197PubMedGoogle Scholar
  27. 27.
    Klerman EB, Rimmer DW, Dijk D-J, Kronauer RE, Rizzo JF III, Czeisler CA (1998) Nonphotic entrainment of the human circadian pacemaker. Am J Physiol 274:R991–R996PubMedGoogle Scholar
  28. 28.
    Mistlberger RE, Skene DJ (2005) Nonphotic entrainment in humans? J Biol Rhythms 20:339–352CrossRefPubMedGoogle Scholar
  29. 29.
    Gerkema MP, Davies WI, Foster RG, Menaker M, Hut RA (2013) The nocturnal bottleneck and the evolution of activity patterns in mammals. Proc Biol Sci 280:20130508CrossRefPubMedPubMedCentralGoogle Scholar
  30. 30.
    Roenneberg T, Kuehnle T, Juda M, Kantermann T, Allebrandt K, Gordijn M, Merrow M (2007) Epidemiology of the human circadian clock. Sleep Med Rev 11:429–438CrossRefPubMedGoogle Scholar
  31. 31.
    Wittmann M, Dinich J, Merrow M, Roenneberg T (2006) Social jetlag: misalignment of biological and social time. Chronobiol Int 23:497–509CrossRefPubMedGoogle Scholar
  32. 32.
    Roenneberg T, Vetter C, Allebrandt KV, Merrow M (2012) Linking sleep timing and obesity Current Biology 22:939–943Google Scholar
  33. 33.
    Roenneberg T, Kuehnle T, Pramstaller PP, Ricken J, Havel M, Guth A, Merrow M (2004) A marker for the end of adolescence. Curr Biol 14:R1038–R1039CrossRefPubMedGoogle Scholar
  34. 34.
    Van der Vinne V, Zerbini G, Siersema A, Pieper A, Merrow M, Hut RA, Roenneberg T, Kantermann T (2015) Timing of examinations affects school performance differently in early and late chronotypes. J Biol Rhythms 30:53–60CrossRefPubMedGoogle Scholar

Copyright information

© Springer (India) Pvt. Ltd. 2017

Authors and Affiliations

  • Emma J. Wams
    • 1
  • Sjaak J. Riede
    • 1
  • Ivor van der Laan
    • 1
  • Tim ten Bulte
    • 1
  • Roelof A. Hut
    • 1
    Email author
  1. 1.Chronobiology Unit, Groningen Institute for Evolutionary Life SciencesUniversity of GroningenGroningenThe Netherlands

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