Perception of Natural Zeitgeber Signals

  • G. Fleissner
  • G. Fleissner

Abstract

Biological clocks detect timing cues in their natural environment from the daily twilight transitions during dusk and dawn. Compared to lab conditions (lights on/off programs) these natural zeitgeber signals guarantee better external and internal synchronisation with respect to precision (onset of activity), threshold (of effective stimuli) and range of entrainment. This has been shown in humans, various rodent species, birds and arthropods. It is a so far unsolved problem, which sensory and neuronal mechanisms allow for twilight recognition, as image forming eyes extinguish timing cues via their light/dark adaptation. Neurobiological studies on the photoreceptor system of scorpions have lead to a preliminary network model which is mainly based on the re-afference principle. Scorpion eyes are controlled by the circadian clock and have a strong circadian sensitivity rhythm compensating for the external day/night changes. Furthermore, within these eyes there is a second afferent non-visual channel receiving a copy of the efferent circadian signal to correct the impact of the circadian adaptation on the perceived light program and to compare external and internal timing of dusk. This information flow may provide a clear signal to the pacemaker concerning its correct phase angle to the natural light dark program. Sensory models have been proposed in lower vertebrates and insects, where extraretinal and retinal photoreceptor systems may interact to recognise the spectral and intensity changes of twilight. The results and models discussed provide a basis for changing the experimental paradigms for the analysis of entrainment mechanisms in circadian systems.

Keywords

Migration Retina Arena Reme Zucker 

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References

  1. Aggelopoulos, N.C., Meissl, H. (2000) Responses of neurones of the rat suprachiasmatic nucleus (SCN) to retinal illumination under photopic and scotopic conditions. J. Physiol. (in press).Google Scholar
  2. Aschoff, J. (1969) Phasenlage der Tagesperiodik in Abhängigkeit von Jahreszeit und Breitengrad. Oecologia (Berlin) 3: 125–165.CrossRefGoogle Scholar
  3. Aschoff, J., Meyer-Lohmann, J. (1954) Die Aktivität gekäfigter Grünfinken im 24-Stunden-Tag bei unterschiedlich langer Lichtzeit mit und ohne Dämmerung. Z. Tierpsychol. 12: 254–265.CrossRefGoogle Scholar
  4. Aschoff, J., Weyer, R. (1965) Circadian rhythms of finches in light-dark cycles with interposed twilights. Comp. Biochem. Physiol. 16: 307–314.Google Scholar
  5. Beersma, D.G., Spoelstra, K., Daan, S. (1999) Accuracy of human circadian entrainment under natural light conditions: Model simulations. J. Biol. Rhythms 14: 524–531.PubMedGoogle Scholar
  6. Boulos, Z., Macchi, M., Houpt, T.A., Terman, M. (1996a) Photic entrainment in hamsters: effects of simulated twilights and nest box availability. J. Biol. Rhythms 11: 216–233.CrossRefGoogle Scholar
  7. Boulos, Z., Macchi, M., Terman, M. (1996b) Effects of twilights on circadian entrainment patterns and reentrainment rates in squirrel monkeys. J. Comp. Physiol. A 179: 687–694.CrossRefGoogle Scholar
  8. Boulos, Z., Macchi, M., Terman, M. (1996c) Twilight transitions promote circadian entrainment to lengthening light-dark cycles. Am. J. Physiol. 271: R813–818.Google Scholar
  9. Boulos, Z., Terman, J.S., Terman, M. (1996d) Circadian phase-response curves for simulated dawn and dusk twilights in hamsters. Physiol. Behay. 60: 1269–1275.CrossRefGoogle Scholar
  10. Cooper, H.M., Dkhissi, O., Sicard, B., Groscarret, H. (1998) Light evoked C-Fos expression in the SCN is different under on/off and twilight conditions. In: Touitou, Y. (ed.) Biological clocks. Mechanisms and Applications. Elsevier Science B.V., Paris Amsterdam. pp. 181–188.Google Scholar
  11. Cymborowski, B., Korf, H.W. (1995) Immunocytochemical demonstration of S-antigen (arrestin) in the brain of the blowfly Calliphora vicina. Cell Tiss. Res. 279: 109–114.CrossRefGoogle Scholar
  12. Daan, S. (1981) Adaptive daily strategies in behavior. In: Aschoff, J. (ed.) Biological Rhythms. Hb Behay. Neurbiol. Vol. 4. Plenum Press, New York. pp. 275–298.CrossRefGoogle Scholar
  13. DeCoursey, P.J. (1986) Light-sampling behaviour in photo-entrainment of a rodent circadian rhythm. J. Comp. Physiol. A 159: 161–169.PubMedCrossRefGoogle Scholar
  14. DeCoursey, P.J. (1989) Photoentrainment of circadian rhythm. An ecologist’s viewpoint. In: Hiroshige, T., Honma, K. (eds.) Circadian Clocks and Ecology. 3rd Sapporo Symposium on Biological Clocks. Hokkaido University Press, Sapporo. pp. 187–206.Google Scholar
  15. Dubey, C. (1989). Die circadiane.Google Scholar
  16. Erkert, H.G. (1974) Der Einfluß des Mondlichts auf die Aktivitätsperiodik nachtaktiver Säugetiere. Oecologia 14: 269–287.CrossRefGoogle Scholar
  17. Fleissner, G. (1968) Untersuchungen zur Sehphysiologie der Skorpione. Verh Deutsche Zool. Ges. Innsbruck. pp. 375–380.Google Scholar
  18. Fleissner, G. (1972) Circadian sensitivity changes in the median eyes of the North African scorpion, Androctonus australis. In: Wehner, R. (ed.) Information processing in the visual system of arthropods. Springer, Berlin Heidelberg New York. pp. 133–139.CrossRefGoogle Scholar
  19. Fleissner, G. (1977a) The absolute sensitivity of the median and lateral eyes of the scorpion, Androctonus australis L. (Buthidae, Scorpiones). J. Comp. Physiol. 108: 109–120.CrossRefGoogle Scholar
  20. Fleissner, G. (1977b) Differences in the physiological properties of the median and the lateral eyes and their possible meaning for the entrainment of the scorpion’s circadian rhythm. J. Interdiscipl. Cycle Res. 8: 15–26.CrossRefGoogle Scholar
  21. Fleissner, G. (1983) Efferent neurosecretory fibres as pathways for the circadian clock signals in the scorpion. Naturwissenschaften 70: 366.CrossRefGoogle Scholar
  22. Fleissner, G. (1985) Intracellular recordings of light responses from spiking and nonspiking cells in the median and lateral eyes of the scorpion. Naturwissenschaften 72: 46–48.CrossRefGoogle Scholar
  23. Fleissner, G., Fleissner, G. (1978) The optic nerve mediates the circadian pigment migration in the median eyes of the scorpion. Comp. Biochem. Physiol. A 61: 69–71.CrossRefGoogle Scholar
  24. Fleissner, G., Fleissner, G. (1993) Seeing time. In: Wiese, K., Gribakin, F., Popov, A.V., Renninger, G. (eds.) Sensory systems of invertebrates. Birkhäuser Verlag, Basel, Boston, Berlin. pp. 288–306.Google Scholar
  25. Fleissner, G., Fleissner, G. (1998) Natural photic Zeitgeber signals and underlying neuronal mechanisms in scorpions. In: Touitou, Y. (ed.) Biological Clocks. Mechanisms and Applications. Elsevier, Paris. pp. 171–180.Google Scholar
  26. Fleissner, G., Fleissner, G., Frisch, B. (1993) A new type of putative non-visual photoreceptors in the optic lobe of beetles. Cell Tiss. Res. 273: 435–445.CrossRefGoogle Scholar
  27. Fleissner, G., Heinrichs, S. (1982) Neurosecretory cells in the circadian-clock system of the scorpion, Androctonus australis. Cell Tiss. Res. 224: 233–238.CrossRefGoogle Scholar
  28. Fleissner, G., Schliwa, M. (1977) Neurosecretory fibres in the median eyes of the scorpion, Androctonus australis L. Cell Tiss. Res. 178: 189–198.Google Scholar
  29. Fleissner, G., Siegler, W. (1978) Arhabdomeric cells in the retina of the median eyes of the scorpion. Naturwissenschaften. 65: 210–211.PubMedCrossRefGoogle Scholar
  30. Gao, N., Schantz, M.V., Foster, R.G., Hardie, J. (1999) The putative brain photoperiodic photoreceptors in the vetch aphid, Megoura viciae. J. Insect Physiol. 45: 1011–1019.PubMedCrossRefGoogle Scholar
  31. Gorman, M.R., Zucker, I. (1998) Mammalian seasonal rhythms: New perspectives gained from the use of simulated natural photoperiods. In: Touitou, Y. (ed.) Biological Clocks. Mechanisms and Applications. Elsevier Science B.V. pp. 195–204.Google Scholar
  32. Hebert, M., Dumont, M., Paquet, J. (1998) Seasonal and diurnal patterns of human illumination under natural conditions. Chronobiol. Int. 15: 59–70.PubMedCrossRefGoogle Scholar
  33. Helfrich-Förster, C., Stengl, M., Homberg, U. (1998) Organization of the circadian system in insects. Chronobiol. Int. 15: 567–594.PubMedCrossRefGoogle Scholar
  34. Ichikawa, T. (1990) Spectral sensitivities of elementary color-coded neurons in butterfly larva. J. Neurophysiol. 64: 1861–1872.PubMedGoogle Scholar
  35. Kavaliers, M., Ross, D.M. (1981) Twilight and day length affect the seasonality of entrainment and endogenous circadian rhythms in a fish, Couesius plumbeus. Can. J. Zool. 59: 1326–1334.CrossRefGoogle Scholar
  36. Kenagy, G.J. (1976) The periodicity of daily activity and its seasonal changes in free-ranging and captive kangaroo rats. Oecologia 24: 105–140.CrossRefGoogle Scholar
  37. Krüll, F., Demmelmeyer, H., Remmert, H. (1985) On the circadian rhythm of animals in high polar latitudes. Naturwissenschaften 72: 197–203.CrossRefGoogle Scholar
  38. Ltittgen, M.A. (1993) Entrainment der circadianen Laufrhythmik durch Lichtzeitgeber: Untersuchung biologisch relevanter Lichtparameter am Beispiel der Lokomotionsrhythmik von Androctonus australis L. ( Scorpiones, Buthidae). PhD-Thesis University Frankfurt am Main.Google Scholar
  39. McMahon, D.G., Block, G.D. (1987) The Bulla ocular circadian pacemaker. II. Chronic changes in membrane potential lengthen free running period. J. Comp. Physiol. A 161: 347–354.PubMedCrossRefGoogle Scholar
  40. Meissl, H., Brandstätter, R. (1992) Photoreceptive functions of the teleost pineal organ and their implications in biological rhythms. In: Ali, M.A. (ed.) Rhythms in Fishes. Plenum Press, New York. pp. 235–254.CrossRefGoogle Scholar
  41. Meissl, H., Ekström, P. (1993) Extraretinal photoreception by pineal systems: A tool for photoperiodic time measurements? Trends Comp. Biochem. Physiol. pp. 1223–1240.Google Scholar
  42. Okudaira, N., Kripke, D.F., Webster, J.B. (1983) Naturalistic studies of human light exposure. Am. J. Physiol. 245: R613 — R615.PubMedGoogle Scholar
  43. Page, T.L. (1982) Extraretinal photoreception in entrainment and photoperiodism in invertebrates. Experientia 38: 1007–1013.CrossRefGoogle Scholar
  44. Pittendrigh, C.S. (1965) On the mechanism of entrainment of a circadian rhythm by light cycles. In: Aschoff, J. (ed.) Circadian clocks. North Holland Publ. Co. pp. 277–297.Google Scholar
  45. Pittendrigh, C.S. (1981) Circadian systems: entrainment. In: Aschoff, J. (ed.) Biological rhythms. Hb Behav Neurobiol Vol. 4. Plenum Press, New York. pp. 95–124.CrossRefGoogle Scholar
  46. Pittendrigh, C.S., Daan, S. (1976) A functional analysis of circadian pacemakers in nocturnal rodents. IV. Entrainment: pacemaker as a clock. J. Comp. Physiol. A. 106: 291–331.CrossRefGoogle Scholar
  47. Remmert, H. (1978) Ökologie. Springer-Verlag, Berlin-Heidelberg-New York.CrossRefGoogle Scholar
  48. Terman, M., Schlager, D., Fairhurst, S., Perlman, B. (1989) Dawn and dusk simulation as a therapeutic intervention. Biol. Psychiatry 25: 966–970.PubMedCrossRefGoogle Scholar
  49. Truman, J.W. (1976) Extraretinal photoreception in insects. Photophysiology 23: 215–225.PubMedGoogle Scholar
  50. Von Holst, E., Mittelstaedt, H. (1950) Das Reafferenzprinzip. Naturwissenschaften 37: 464–476.CrossRefGoogle Scholar
  51. Waterkamp, M., Fleissner, G., Fleissner, G. (1998) Information processing in the extraretinal photoreceptor systems of beetles. Proc. SRBR 6: 135.Google Scholar
  52. Wirz-Justice, A., Terman, M., Terman, J.S., Boulos, Z., Remé, C.E., Danilenko, K.V. (1998) Circadian functions and clinical applications of dawn simulation. In: Y., Touitou (eds.) Biological Clocks. Mechanisms and Applications. Elsevier Science B.V. 189–194.Google Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2002

Authors and Affiliations

  • G. Fleissner
    • 1
  • G. Fleissner
    • 1
  1. 1.Zoologisches InstitutJ.W. Goethe-UniversitätFrankfurt a. M.Germany

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