Skip to main content
Log in

A functional analysis of circadian pacemakers in nocturnal rodents

I. The stability and lability of spontaneous frequency

  • Published:
Journal of comparative physiology Aims and scope Submit manuscript

Summary

  1. 1.

    The circadian pacemakers controlling activity rhythms in four species of rodents are compared, as freerunning systems in constant darkness. In analyzing their stability the distinction is made between (1) spontaneous day-to-day instability of frequency, and (2) a longer-term lability, some of which is traceable to identified causes.

  2. 2.

    Serial correlation analysis indicates that the precision (day-to-day stability) of the pacemaker's period is ca. twice as good (estimated s.d.=0.6% of\(\bar \tau \) inMus musculus) as the already remarkable precision of the activity rhythm it drives (average s.d.=1.2% of\(\bar \tau \)).

  3. 3.

    Identifiable causes of long-term lability include age and several features of prior entrainment by light. The period and photoperiod of a light cycle have a predictable influence on the subsequent freerunning period (τ) of the pacemaker; they cause “after-effects”. So do single light pulses causing a phase-shift in the freerunning system. Constant light also has an after-effect opposite in sign from the after-effect of long photoperiods.

  4. 4.

    After-effects of “skeleton” photoperiods support the hypothesis that the transitions of light to darkness vv. are involved in the entrainment process which leads to changes in τ.

  5. 5.

    Both day-to-day instability and long term lability are most pronounced in species (Peromyscus maniculatus, Mus musculus) whose\(\mathop \tau \limits^ = \) is considerably shorter than 24 h; they are least pronounced in hamsters whose\(\mathop \tau \limits^ = \) is indistinguishably close to 24 h.

  6. 6.

    The differences between the species in τ and its lability are paralleled by differences in pacemaker lability as measured in light-induced after-effects and in the extent of changes with age. The species evidently differ in the “tightness” with which τ is homeostatically conserved.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  • Aschoff, J.: Die 24-Stundenperiodik der Maus unter konstanten Umgebungsbedingungen. Naturwissenschaften38, 506–507 (1951)

    Google Scholar 

  • Aschoff, J.: Exogenous and endogenous components in circadian rhythms. Cold Spr. Harb. Symp. quant. Biol.25, 11–28 (1960)

    Google Scholar 

  • Aschoff, J.: Spontane lokomotorische Aktivität. Handb. Zool.8, 11, 1–74 (1962)

    Google Scholar 

  • Aschoff, J.: Die Tagesperiodik licht- und dunkelaktiver Tiere. Rev. suisse Zool.71, 528–558 (1964)

    Google Scholar 

  • 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), pp. 3–29. Washington: Nat. Acad. Sci. 1971

    Google Scholar 

  • Aschoff, J., Wever, R.: Beginn und Ende der täglichen Aktivität freilebender Vögel. J. Ornithol.103, 1–27 (1962)

    Google Scholar 

  • Burchard, J.E.: Re-setting a biological clock. Ph. D. Thesis, Princeton University, 1–16 (1958)

  • 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 

  • Daan, S., Damassa, D., Pittendrigh, C. S., Smith, E.: An effect of castration and testosterone replacement on a circadian pacemaker in mice (Mus musculus). Proc. nat. Acad. Sci. (Wash.)72, 3744–3747 (1975)

    Google Scholar 

  • 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 (1976a)

    Google Scholar 

  • 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 (1976b)

    Google Scholar 

  • DeCoursey, P.J.: Effect of light on the circadian activity rhythm of the flying squirrel,Glaucomys volans. Z. vergl. Physiol.44, 331–354 (1961)

    Google Scholar 

  • DeCoursey, P.J.: Function of a light response rhythm in hamsters. J. cell. comp. Physiol.63, 189–196 (1964)

    Google Scholar 

  • Eskin, A.: Some properties of the system controlling the circadian activity rhythm of sparrows. In: Biochronometry (Ed. M. Menaker), pp. 55–80. Washington, D.C.: Nat. Acad. Sci. 1971

    Google Scholar 

  • Gwinner, E.: Circadian and circannual rhythms in birds. In: Avian biology (eds. D. S. Farner, J. R. King) vol. V, pp. 221–285. New York and London: Acad. Press 1975

    Google Scholar 

  • Guyton, A.C.: Textbook of medical physiology. 4th ed., 1032pp. Philadelphia-London-Toronto: Saunders 1971

    Google Scholar 

  • Hudson, J.W., Kimzey, S.L.: Temperature regulation and metabolic rhythms in populations of the house sparrow,Passer domesticus. Comp. Biochem. Physiol.17, 203–217 (1966)

    PubMed  Google Scholar 

  • Johnson, M.: Effect of continuous light on periodic spontaneous activity of white-footed mice (Peromyscus). J. exp. Zool.82, 315–318 (1939)

    Google Scholar 

  • Jones, D.C., Kimeldorf, D.J., Rubadeau, D.O., Castanera, T.: Relationships between volitional activity and age in the male rat. Amer. J. Physiol.172, 109 (1953)

    PubMed  Google Scholar 

  • Konopka, R., Benzer, S.: Clock mutants ofDrosophila melanogaster. Proc. nat. Acad. Sci. (Wash.)68, 2112–2116 (1971)

    Google Scholar 

  • Kramm, K. R.: Circadian activity in the antelope ground squirrel,Ammospermophilus leucurus. Ph. D. Thesis, U. C. Irvine, i–xviii, 1–267 (1971)

  • Lohmann, M.: Zur Bedeutung der lokomotorischen Aktivität in circadianen Systemen. Z. vergl. Physiol.55, 307–332 (1967)

    Google Scholar 

  • Menaker, M.: The freerunning period of the bat clock; seasonal variations at low body temperature. J. cell. comp. Physiol.57, 81–86 (1961)

    PubMed  Google Scholar 

  • Pittendrigh, C. S.: Perspectives in the study of biological clocks. In: Symp. on perspectives in marine biology. (ed. A. A. Buzzati-Traverso), pp. 239–268. Berkeley: Univ. of Calif. Press 1958

    Google Scholar 

  • Pittendrigh, C. S.: Circadian rhythms and the circadian organization of living systems. Cold. Spr. Harb. Symp. quant. Biol.25, 159–184 (1960)

    Google Scholar 

  • Pittendrigh, C. S.: Circadian rhythms, space research and manned space flight. In: Life sciences and space research V, pp. 122–134. Amsterdam: North-Holland 1967

    Google Scholar 

  • 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, G.O. Worden), pp. 437–458. Cambridge, Mass.: MIT Press 1974

    Google Scholar 

  • Pittendrigh, C. S., Bruce, V. G., Kaus, P.: On the significance of transients in daily rhythms. Proc. nat. Acad. Sci. (Wash.)44, 965–973 (1958)

    Google Scholar 

  • Pittendrigh, D. S., Caldarola, P. C.: General homeostasis of the frequency of circadian oscillations. Proc. nat. Acad. Sci. (Wash.)70, 2697–2701 (1973)

    Google Scholar 

  • Pittendrigh, C. S., Daan, S.: Circadian oscillations in rodents: a systematic increase of their frequency with age. Science186, 548–550 (1974)

    PubMed  Google Scholar 

  • Pittendrigh, C. S., Daan, S.: A functional analysis of circadian pacemakers in nocturnal rodents. IV. Entrainment: pacemaker as clock. J. comp. Physiol.106, 291–331 (1976a)

    Google Scholar 

  • 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 

  • Pittendrigh, C. S., Minis, D. H.: The entrainment of circadian oscillations by light and their role as photoperiodic clocks. Amer. Nat.98, 261–294 (1964)

    Google Scholar 

  • Pohl, H.: Seasonal change in light sensitivity inCarduelis flammea. Naturwissenschaften59, 518 (1972)

    Google Scholar 

  • Richter, C. P.: A behaviouristic study of the activity of the rat. Comp. Physiol. Monogr.1, 1–55 (1922)

    Google Scholar 

  • Semon, R.: Das Problem der Vererbung „Erworbener Eigenschaften.“ Leipzig: Verlag Engelmann (1912)

    Google Scholar 

  • Thorpe, W. H.: Learning and instinct in animals, 2nd ed., pp. i-x, 1–558. Cambridge, Mass.: Harvard Univ. Press 1966

    Google Scholar 

  • Wever, R.: Ein mathematisches Modell für biologische Schwingungen. Z. Tierpsychol.21, 359–372 (1964)

    Google Scholar 

  • Wever, R.: A mathematical model for circadian rhythms. In: Circadian clocks (ed. J. Aschoff), pp. 49–63. Amsterdam: North Holland 1965

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Pittendrigh, C.S., Daan, S. A functional analysis of circadian pacemakers in nocturnal rodents. J. Comp. Physiol. 106, 223–252 (1976). https://doi.org/10.1007/BF01417856

Download citation

  • Received:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF01417856

Keywords

Navigation