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Journal of comparative physiology

, Volume 106, Issue 3, pp 291–331 | Cite as

A functional analysis of circadian pacemakers in nocturnal rodents

IV. Entrainment: Pacemaker as clock
  • Colin S. Pittendrigh
  • Serge Daan
Article

Summary

  1. 1.

    In thefirst part of the paper, the model of non-parametric entrainment of circadian pacemakers is tested for the case of nocturnal rodents. The model makes use of the available data on freerunning period (τ) in constant darkness (Pittendrigh and Daan, 1976a) and on phase response curves (PRC) for short light pulses (Daan and Pittendrigh, 1976a). It is tested in experiments using 1 or 2 light pulses per cycle.

     
  2. 2.

    Mesocricetus auratus andPeromyscus leucopus entrain to Zeitgebers involving 1 pulse (15′ or 60′) per cycle. The phase angle differences between rhythm and light cycle depends on the periods (τ andT) as predicted by the model. Entrainment ofP. leucopus is unstable due to the after effects on τ created by the light pulse.

     
  3. 3.

    The limiting values of zeitgeber period to which the animals entrain are much closer to 24 h than inDrosophila pseudoobscura, as the model predicts. However, frequent failures to entrain toT=23 andT=25 h are only explained if we take considerable interindividual variation in both τ and PRC into account.

     
  4. 4.

    With 2 pulses per cycle, the model predicts that entrainment will be more stable when activity is in the longer interval between the pulses than when it is in the shorter interval. This is true in the experimental data, where the phase relationships match predictions for skeleton photoperiods up to ca. 14 h. Increasing asymmetry forces animals into a “phase jump”, so that activity shifts from the shorter to the longer interval. Theseψ-jumps are accurately predicted in the hamster, but they occur at much longer photoperiods than predicted inP. leucopus.

     
  5. 5.

    Thus, the unqualified model, using a rigidly fixed species τ and PRC, is surely inadequate to explain entrainment. The extent to which variations in τ and PRC-shape, both “spontaneous” and induced by the entrainment process, can be known or inferred restricts the validity of the predictions. Yet we conclude, from a good deal of agreement between experiment and prediction (i), from the close correspondence between complete and skeleton photoperiods (ii), and on behavioural grounds (iii), that non-parametric entrainment by short light signals has a major share in the entrainment of nocturnal rodent rhythms in nature.

     
  6. 6.

    With these restrictions in mind, we analyse in thesecond part of the paper how the empirical regularities concerning τ and PRC, and reported earlier (Pittendrigh and Daan, 1976; Daan and Pittendrigh, 1976a, b), contribute to the stabilization of the phase angle difference (ψ) between the pacemaker and the external world. Use is made of computer simulations of artificial pacemakers with variable τ and PRC.

     
  7. 7.

    ψ is most sensitive to instabilities in τ when\(\bar \tau \) is close to 24 h. Thus the verycircadian nature of these pacemakers helps to conserveψ. Selection pressure for homeostasis ofτ has been large in a species (M. auratus) where\(\bar \tau \)=24 h. The effect ofψ-instability is further reduced by entrainment with 2 pulses (dawn and dusk), made possible by the PRC's having both an advance and a delay section.

     
  8. 8.

    To analyze the contributions toψ-conservation with seasonally changing photoperiod, we have assumed that it is of functional significance to conserve the phase of activity with respect to dusk (nocturnal animals) or to dawn (diurnal animals). We distinguish three contributions of nocturnal pacemaker behaviour to this type ofψ-conservation: increased amplitude of the PRC (i), asymmetry in the PRC, such that the slope of the delay-part is steeper than the slope of the advance-part (ii), and a short freerunning period in DD (iii).

     
  9. 9.

    A further contribution must derive from parametric effects of light, which are not traceable by the model, but certainly effective in preventing in complete photoperiods theψ-jump which is seen in skeleton photoperiods. The existence of parametric effects is further demonstrated by the change of τ with light intensity in LL, described by Aschoff's Rule, which presumably reflects differences in PRC-shape between nocturnal and diurnal animals (Daan and Pittendrigh, 1976b).

     
  10. 10.

    The paper concludes with an attempt to distinguish the features of circadian clocks that are analytically necessary for entrainment to occur (i), or have functional meaning, either in the measurement of the lapse of time (ii) or in the identification of local time (iii).

     

Keywords

Light Pulse Circadian Clock Phase Response Curve Phase Jump Circadian Pacemaker 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

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References

  1. Aschoff, J.: Tierische Periodik unter dem Einfluß von Zeitgebern. Z. Tierpsychol.15, 1–30 (1958)Google Scholar
  2. Aschoff, J.: Exogenous and endogenous components in circadian rhythms. Cold Spr. Harb. Symp. quant. Biol.25, 11–28 (1960)Google Scholar
  3. Aschoff, J., Gerecke, U., Kureck, A., Pohl, H., Rieger, P., von Saint Paul, U., Wever, R.: Interdependent parameters of circadian activity rhythms in birds and man. In: Biochronometry (ed. M. Menaker).Google Scholar
  4. Bruce, V., Weight, F., Pittendrigh, C.S.: Resetting the sporulation rhythm inPilobolus with short light flashes of high intensity. Science131, 728–730 (1961)Google Scholar
  5. Daan, S., Aschoff, J.: Circadian rhythms of locomotor activity in captive birds and mammals: their variations with season and latitude. Oecologia18, 269–316 (1975)Google Scholar
  6. Daan, S., Pittendrigh, C.S.: A functional analysis of circadian pacemakers in nocturnal rodents. II. The variability of phase response curves. J. comp. Physiol.106, 253–266 (1967a)Google Scholar
  7. Daan, S., Pittendrigh, C.S.: A functional analysis of circadian pacemakers in nocturnal rodents. III. Heavy water and constant light: homeostasis of frequency? J. comp. Physiol.106, 267–290 (1967b)Google Scholar
  8. DeCoursey, P.J.: Daily activity rhythms in the flying squirrel,Glaucomys volans. Ph. D. Thesis, University of Wisconsin 162 pp. (1959)Google Scholar
  9. DeCoursey, P.J.: LD ratios and the entrainment of circadian activity in a nocturnal and a diurnal rodent. J. comp. Physiol.78, 221–235 (1972)Google Scholar
  10. Elliott, J.A.: Photoperiodic regulation of testis function in the golden hamster: relation to the circadian system. Ph. D. Thesis, University of Texas, Austin 1974Google Scholar
  11. Enright, J.T.: Ecological aspects of endogenous rhythmicity. Ann. Rev. Ecol. Syst.1, 221–238 (1970)Google Scholar
  12. Eriksson, L.O.: Spring inversion of the diel rhythm of locomotor activity in young sea-going trout (Salmo trutta trutta L.) and Atlantic salmon (Salmo salar L.) Aquilo, Ser. Zool.14, 68–79 (1973)Google Scholar
  13. Erkinaro, E.: The seasonal change of the activity ofMicrotus agrestis. Acta. oecol. scand.12, 157–163 (1961)Google Scholar
  14. Erkinaro, E.: Der Phasenwechsel der lokomotorischen Aktivität beiMicrotus agrestis (L.),M. arvalis (Pall.) undM. oeconomus (Pall.). Aquilo, Ser. Zool.8, 1–31 (1969)Google Scholar
  15. Frisch, K. von: Die Sonne als Kompaß im Leben der Bienen. Experientia (Basel)6, 210–221 (1950)Google Scholar
  16. Hoffmann, K.: Zur Beziehung zwischen Phasenlage und Spontanfrequenz bei der endogenen Tagesperiodik. Z. Naturforsch.18b, 154–157 (1963)Google Scholar
  17. Hoffmann, K.: Die relative Wirksamkeit von Zeitgebern. Oecologia (Berl.)3, 184–206 (1969)Google Scholar
  18. Holst, E. von: Die relative Koordination als Phenomen und als Methode zentralvervöser Funktionsanalyse. Ergebn. Physiol.42, 228–306 (1939)Google Scholar
  19. Kalleberg, H.: Observations in a stream tank of territoriality and competition in juvenile salmon and trout (Salmo salar L. andSalmo trutta L.) Rep. Inst. Freshwater Res. Drottningholm39, 55–98 (1958)Google Scholar
  20. Kramer, G.: Orientierte Zugaktivität gekäfigter Singvögel. Naturwissenschaften37, 188 (1950)Google Scholar
  21. Lohmann, M.: Zur Bedeutung der lokomotorischen Aktivität in circadianen Systemen. Z. vergl. Physiol.55, 307–332 (1967)Google Scholar
  22. Pittendrigh, C.S.: On temperature independence in the clock system controlling emergence time inDrosophila. Proc. nat. Acad. Sci. (Wash.)40, 1018–1029 (1954)Google Scholar
  23. Pittendrigh, C.S.: Circadian rhythms and the circadian organization of living systems. Cold Spr. Harb. Symp. quant. Biol.25, 159–184 (1960)Google Scholar
  24. Pittendrigh, C.S.: The circadian oscillation inDrosophila pseudoobscura pupae: A model for the photoperiodic clock. Z. Pflanzenphysiol.54, 275–307 (1966)Google Scholar
  25. Pittendrigh, C.S.: Circadian oscillations in cells and the circadian organization of multicellular systems. In: The neurosciences: Third study program, Vol. 38 (eds. F.O. Schmitt, F.G. Worden), pp. 437–458, Cambridge, Mass.: MIT Press 1974Google Scholar
  26. Pittendrigh, C.S., Bruce, V.C.: An oscillator model for biological clocks. In: Rhythmic and synthetic processes in growth. p. 75–109. Princeton, N.J.: Princeton University Press 1957Google Scholar
  27. Pittendrigh, C.S., Caldarola, P. C.: General homeostasis of the frequency of circadian oscillations. Proc. nat. Acad. Sci. (Wash.)70, 2697–2701 (1973)Google Scholar
  28. Pittendrigh, C.S., Daan, S.: A functional analysis of circadian pacemakers in nocturnal rodents. I. The stability and lability of spontaneous frequency. J. comp. Physiol.106, 223–252 (1976a)Google Scholar
  29. Pittendrigh, C.S., Daan, S.: A functional analysis of circadian pacemakers in nocturnal rodents. V. Pacemaker structure: A clock for all seasons. J. comp. Physiol.106, 333–355 (1976b)Google Scholar
  30. Rensing, L., Brunken, W.: Zur Frage der Allgemeingültigkeit circadianer Gesetzmäßigkeiten. Biol. Zbl.86, 545–565 (1967)Google Scholar
  31. Swade, R.H., Pittendrigh, C.S.: Circadian locomotor rhythms of rodents in the Arctic. Amer. Nat.101, 431–466 (1967)Google Scholar
  32. Wever, R.: Zum Mechanismus der biologischen 24-Stunden-Periodik. Kybernetik1, 139–154 (1962)PubMedGoogle Scholar
  33. Winfree, A.: An integrated view of the resetting of a circadian clock. J. theor. Biol.27, 327–374 (1970)Google Scholar

Copyright information

© Springer-Verlag 1976

Authors and Affiliations

  • Colin S. Pittendrigh
    • 1
  • Serge Daan
    • 1
  1. 1.Department of Biological SciencesStanford UniversityStanfordUSA

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