Journal of comparative physiology

, Volume 83, Issue 2, pp 187–222 | Cite as

Retinal and extraretinal photoreceptors mediate entrainment of the circadian locomotor rhythm in lizards

  • Herbert Underwood


The circadian locomotor activity rhythms of 7 species of lizards can readily be entrained (synchronized) toLD12: 12 (30–50 lux: 0) fluorescent light cycles after complete surgical removal of both eyes. Removal of the parietal eye and pineal organ does not prevent entrainment of blinded lizards. Appropriate control experiments established that lightper se, and not low amplitude temperature cycles or other obvious environmental variables, was the entraining stimulus for blinded lizards. In some cases, blocking the penetration of light to the brains of blinded lizards caused them to free-run (express their endogenous circadian rhythm) in the presence of a dim green light cycle, to which they had previously entrained, suggesting that the brain is the site of the extraretinal photoreceptor(s) mediating entrainment. The extraretinal photoreceptor(s) is capable of intensity discrimination since changing the intensity of aLD 12: 12 fluorescent light cycle caused a change in the phase-relationship between the entrained activity rhythm and the light cycle in a blinded gekko. The lateral eyes are also involved in mediating entrainment since removal of the lateral eyes of thoseSceloporus olivaceus which previously entrained to a dim green light cycle [LD 12: 12 (0.05 lux: 0)] caused them to free-run. Also, blinding had noticeable effects on the entrained activity patterns of some species of lizards.


Locomotor Activity Circadian Rhythm Light Cycle Activity Rhythm Temperature Cycle 
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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  1. Adler, K.: Extraoptic phase shifting of circadian locomotor rhythm in salamanders. Science164, 1290–1292 (1969).Google Scholar
  2. Adler, K.: Pineal end organ: Role in extraoptic entrainment of circadian locomotor rhythm in frogs. In: Biochronometry, ed. M. Menaker. Washington, D.C.: National Academy of Sciences 1971.Google Scholar
  3. Ariëns-Kappers, J.: Survey of the innervation of the epiphysis cerebri and the accessory pineal organs in vertebrates. Progr. Brain Res.10, 87–153 (1965).Google Scholar
  4. Ariëns-Kappers, J.: The sensory innervation of the pineal organ in the lizard,Lacerta viridis, with remarks on its position in the trend of pineal phylogenetic structural and functional evolution. Z. Zellforsch.81, 581–618 (1967).Google Scholar
  5. Aschoff, J.: Response curves in circadian periodicity. In: Circadian clocks, ed. J. Aschoff. Amsterdam: North-Holland Pub. Co. 1965.Google Scholar
  6. Bagnara, J. T., Hadley, M. E.: Endocrinology of the amphibian pineal. Amer. Zoologist10, 201–216 (1970).Google Scholar
  7. Benoit, J.: The role of the eye and of the hypothalamus in the photostimulation of gonads in the duck. Ann. N.Y. Acad. Sci.117, 204–217 (1964).Google Scholar
  8. Binkley, S., Kluth, E., Menaker, M.: Pineal function in sparrows: Circadian rhythms and body temperature. Science174, 311–314 (1971).Google Scholar
  9. Binkley, S., Kluth, E., Menaker, M.: Pineal and locomotor activity. J. comp. Physiol.77, 163–169 (1972).Google Scholar
  10. Browman, L. G.: The effect of bilateral optic enucleation upon the activity rhythms of the albino rat. J. comp. Psychol.36, 33–46 (1943).Google Scholar
  11. Bruss, R. T., Jacobson, E., Halberg, F., Zander, H. A., Bittner, J. J.: Effects of lighting regimen and blinding upon gross motor activity of mice. Fed. Proc.17, 21 (1958).Google Scholar
  12. Camp, C. L.: Classification of the lizards. Bull. Amer. Mus. Nat. Hist.48, 289–481 (1923).Google Scholar
  13. Conant, R.: A field guide to reptiles and amphibians. Boston: Houghton Mifflin Co. 1958.Google Scholar
  14. Dodt, E., Scherer, E.: The electroretinogram of the third eye. In: Advances in electrophysiology and -pathology of the visual system. 6th ISCERG Symposium. Leipzig: VEB G. Thieme 1968.Google Scholar
  15. Eakin, R. M., Stebbins, R. C.: Parietal eye nerve in the fence lizard. Science130, 1573–1574 (1959).Google Scholar
  16. Eakin, R. M., Westfall, J. A.: Further observations on the fine structure of the parietal eye of lizards. J. biophys. biochem. Cytol.8, 483–499 (1960).Google Scholar
  17. Enright, J. T.: Synchronization and ranges of entrainment. In: Crcadian clocks (ed. J. Aschoff). Amsterdam: North-Holland Publ. Co. 1965.Google Scholar
  18. Erikson, L. O.: Tagesperiodik geblendeter Bachsaiblinge. Naturwissenschaften59, 219–220 (1972).Google Scholar
  19. Gaston, S., Menaker, M.: Pineal function: The biological clock in the sparrow? Science160, 1125–1127 (1968).Google Scholar
  20. Gaston, S.: The influence of the pineal organ on the circadian activity rhythm in birds. In: Biochronometry (ed. M. Menaker). Washington, D.C.: National Academy of Sciences 1971.Google Scholar
  21. Glaser, R. Increase in locomotor activity following shielding of the parietal eye in night lizards. Science128, 1577–1578 (1958).Google Scholar
  22. Halberg, P., Visscher, M. B., Bittner, J. J.: Relation of visual factors to eosinophil rhythm in mice. Amer. J. Physiol.179, 229–235 (1954).Google Scholar
  23. Hamasaki, D. I.: Spectral sensitivity of the parietal eye of the green iguana. Vision Res.9, 515–523 (1969).Google Scholar
  24. Hamasaki, D. I., Dodt, E.: Light sensitivity of the lizard'sepiphysis cerebri. Pflügers Arch.313, 19–29 (1969).Google Scholar
  25. Heckrotte, C.: The effect of environmental factors on the locomotor activity of the plains garter snake. Anim. Behav.10, 193–207 (1962).Google Scholar
  26. Hoffmann, K.: Synchronisation der circadianen Aktivitätsperiodik von Eidechsen durch Temperaturcyclen verschiedener Amplitude. Z. vergl. Physiol.58, 225–228 (1968).Google Scholar
  27. Hoffmann, K.: Zur Synchronisation biologischer Rhythmen. Verh. d. Dtsch. Zool. Ges. 1970: 266–273.Google Scholar
  28. Homma, K., Sakakibara, Y.: Encephalic photoreceptors and their significance in photoperiodic control of sexual activity in Japanese quail. In: Biochronometry (ed. M. Menaker). Washington, D.C.: National Academy of Sciences 1971.Google Scholar
  29. Hunt, J. M., Schlosberg, H.: The influence of illumination upon general activity in normal, blinded, and castrated male white rats. J. comp. Psychol.28, 285–298 (1939).Google Scholar
  30. Kincl, F. A., Chang, C. C., Zbuzkova, V.: Observations on the influence of changing photoperiod on spontaneous wheel-running activity of neonatally pinealectomized rats. Endocrinology87, 38–42 (1970).Google Scholar
  31. Kleinholz, L. H.: Studies in reptilian colour changes II. The pituitary and adrenal glands in the regulation of the melanophores ofAnolis carolinensis. J. exp. Biol.15, 474–491 (1938).Google Scholar
  32. LaPointe, J. L.: Investigations of the function of the parietal eye in relation to locomotor activity cycles in the lizard,Xantusia vigilis. Ph. D. Thesis, Univ. of Calif., Berkeley 1966.Google Scholar
  33. Lauber, J. K., Body, J. E., Axelrod, J.: Enzymatic synthesis of melatonin in avian pineal body: Extraretinal response to light. Science161, 489–490 (1968).Google Scholar
  34. Machado, C. R. S., Machado, A. B. M., Wragg, L. E.: Circadian serotonin rhythm control: Sympathetic and nonsympathetic pathways in rat pineals of different ages. Endocrinology85, 846–848 (1969b).Google Scholar
  35. Machado, C. R. S., Wragg, L. E., Machado, A. B. M.: Circadian rhythm of serotonin in the pineal body of immunosympathectomized immature rats. Science164, 442–443 (1969a).Google Scholar
  36. McMillan, J. P.: Pinealectomy abolishes the circadian rhythm of migratory restlessness. J. comp. Physiol.79, 105–112 (1972).Google Scholar
  37. Menaker, M.: Extraretinal light perception in the sparrow, I. Entrainment of the biological clock. Proc. nat. Acad. Sci. (Wash.)59, 414–421 (1968a).Google Scholar
  38. Menaker, M.: Light perception by extraretinal receptors in the brain of the sparrow. Proc. Amer. Psychol. Ass. 76th, 299–300 (1968b).Google Scholar
  39. Menaker, M., Roberts, R., Elliott, J., Underwood, H.: Extraretmal light perception in the sparrow, III: The eyes do not participate in photoperiodic photoreception. Proc. nat. Acad. Sci. (Wash.)67, 320–325 (1970).Google Scholar
  40. Oksche, A., Kirschstein, H.: Unterschiedlicher elektronenmikroskopischer Feinbau der Sinneszellen im Parietalauge und im Pinealorgan (Epiphysis cerebri) von Lacertilia. Z. Zellforsch.87, 159–192 (1968).Google Scholar
  41. Parker, G. H.: Animal colour changes and their neurohumours. Cambridge, England: Cambridge Univ. Press 1948.Google Scholar
  42. Pearse, A. S.: The reactions of amphibians to light. Proc. Amer. Acad. Arts Sci.45, 161–208 (1910).Google Scholar
  43. Pittendrigh, C. S.: Circadian rhythms and the circadian organization of living systems. Cold Spr. Harb. Symp. quant. Biol.25, 159–184 (1960).Google Scholar
  44. Pittendrigh, C. S.: On the mechanism of the entrainment of a circadian rhythm by light cycles. In: Circadian clocks (ed. J. Aschoff). Amsterdam: North-Holland Publ. Co. 1965.Google Scholar
  45. Quay, W. B.: Individuation and lack of pineal effect in the rat's circadian locomotor rhythm. Physiol. Behav.3, 109–118 (1968).Google Scholar
  46. Quay, W. B.: Physiological significance of the pineal during adaptation to shifts in photoperiod. Physiol. Behav.5, 353–360 (1970a).Google Scholar
  47. Quay, W. B.: Precocious entrainment and associated characteristics of activity patterns following pinealectomy and reversal of photoperiod. Physiol. Behav.5, 1281–1290 (1970b).Google Scholar
  48. Quay, W. B.: Dissimilar functional effects of pineal stalk and cerebral meningeal interruptions on phase shifts of circadian activity rhythms. Physiol. Behav.7, 557–567 (1971).Google Scholar
  49. Quay, W. B.: Pineal homeostatic regulation of shifts in the circadian activity rhythm during maturation and aging. Trans. N.Y. Acad. Sci.34, 239–254 (1972).Google Scholar
  50. Reed, B. L.: The control of circadian pigment changes in the pencil fish: A proposed role for melatonin. Life Sci.7, 961–973 (1968).Google Scholar
  51. Richter, C. P.: Biological clocks in medicine and psychiatry. Springfield, III.: C. C. Thomas 1965.Google Scholar
  52. Richter, C. P.: Inherent twenty-four hour and lunar clocks of a primate—the squirrel monkey. Communications in Behavioral Biology1, 305–332 (1968).Google Scholar
  53. Scharrer, E.: Die Lichtempfindlichkeit blinder Elritzen (Untersuchungen über das Zwischenhirn der Fische I). Z. vergl. Physiol.7, 1–38 (1928).Google Scholar
  54. Snyder, S. H., Zweig, M., Axelrod, J., Fischer, J. E.: Control of the circadian rhythm in serotonin content of the rat pineal gland. Proc. nat. Acad. Sci. (Wash.)53, 301–305 (1965).Google Scholar
  55. Stebbins, R. C., Eakin, R. M.: The role of the “third eye” in reptilian behavior. Amer. Mus. Novitates1870, 1–40 (1958).Google Scholar
  56. Stebbins, R. C.: Effects of pinealectomy in the western fence lizardSceloporus occidentalis. Copeia1960, 276–283 (1960).Google Scholar
  57. Stebbins, R. C.: Activity changes in the striped plateau lizard with evidence on influence of the parietal eye. Copeia1963, 681–691 (1963).Google Scholar
  58. Stebbins, R. C.: A field guide to western reptiles and amphibians. Boston: Houghton Mifflin Co. 1966.Google Scholar
  59. Stebbins, R. C., Wilhoft, D. C.: Influence of the parietal eye on activity in lizards. In: The Galápagos: Proceedings of the symposia of the Galápagos international scientific project (ed. R. I. Bowman). Univ. of Calif. Press 1966.Google Scholar
  60. Stebbins, R. C.: The effect of parietalectomy on testicular activity and exposure to light in the desert night lizard (Xantusia vigilis). Copeia1970, 261–270 (1970).Google Scholar
  61. Steyn, W.: Electron microscopic observations on the epiphysial sensory cells in lizards and the pineal sensory cell problem. Z. Zellforsch.51, 735–747 (1960).Google Scholar
  62. Taylor, D. H., Ferguson, D. E.: Extraoptic celestial orientation in the southern cricket frogAcris gryllus. Science168, 390–392 (1970).Google Scholar
  63. Underwood, H.: Extraretinal light perception in lizards: Entrainment of the biological clock controlling locomotor activity. Ph. D. Thesis. Univ. of Texas, Austin 1972.Google Scholar
  64. Underwood, H., Menaker, M.: Extraretinal light perception: Entrainment of the biological clock controlling lizard locomotor activity. Science170, 190–193 (1970).Google Scholar
  65. Wetterberg, L., Geller, E., Yuwiler, A.: Harderian gland: An extraretinal photoreceptor influencing the pineal gland in neonatal rats? Science167, 884–885 (1970a).Google Scholar
  66. Wetterberg, L., Yuwiler, A., Ulrich, R., Geller, E., Wallace, R.: Harderian gland: Influence on pineal hydroxyindole-o-methyltransferase activity in neonatal rats. Science170, 194–196 (1970b).Google Scholar
  67. Wever, R.: A mathematical model for circadian rhythms. In: Circadian clocks (ed. J. Aschoff). Amsterdam: North-Holland Publ. Co. 1965.Google Scholar
  68. Wurtman, R. J., Axelrod, J., Kelly, D. E.: The pineal. New York: Academic Press 1968.Google Scholar
  69. Zweig, M., Snyder, S. H., Axelrod, J.: Evidence for a nonretinal pathway of light to the pineal gland of newborn rats. Proc. nat. Acad. Sci. (Wash.)56, 515–520 (1966).Google Scholar

Copyright information

© Springer-Verlag 1973

Authors and Affiliations

  • Herbert Underwood
    • 1
    • 2
  1. 1.Department of ZoologyThe University of TexasAustin
  2. 2.Max-Planck-Institut für VerhaltensphysiologieErling-AndechsFederal Republic of Germany

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