Circadian Organization in Fish and Amphibians

  • G. M. Cahill


Circadian systems in fish and amphibians share several characteristics with other non-mammalian vertebrates. The most salient of these characteristics at the physiological level is the presence in multiple tissues of independently photosensitive and self-sustaining circadian oscillators. The circadian oscillators that regulate melatonin synthesis in the pineal and retina have been the most extensively investigated. In particular, studies of teleost pineals and of the retina of Xenopus laevis have contributed to our understanding of the cellular and molecular bases of rhythm generation, entrainment and output pathways in these organs. However, our understanding of how these and other oscillatory structures interact to drive rhythmicity in intact fish and amphibians has lagged behind progress in other vertebrates, primarily because convenient and reliable measures of behavioral rhythmicity were lacking. Recent technical advances have made it possible to record robust swimming activity rhythms from larval zebrafish. These methods may also be applicable to measurement of behavioral rhythms in other fish and amphibians. Recent studies of the zebrafish and Xenopus homologs of mammalian clock-related genes indicates that molecular clock mechanisms in fish and amphibians are similar, but not identical to those in other vertebrates. In particular, these studies have revealed new complexities in molecular mechanisms of vertebrate circadian rhythmicity, and they have also contributed to our understanding of system organization in these animals.


Circadian Clock Circadian System Circadian Oscillator Melatonin Secretion Larval Zebrafish 
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  1. Ali, M.A. (1992) Rhythms in Fishes. Plenum Press, New York.CrossRefGoogle Scholar
  2. Anderson, K.D. (1987) Role of the eyes, frontal organ and pineal organ in the generation of the circadian activity rhythm and its entrainment by light in the South African clawed frog, Xenopus laevis. Ph.D. Dissertation, Northwestern University.Google Scholar
  3. Bégay, V., Falcon, J., Cahill, G.M., Klein, D.C., Coon, S.L. (1998) Transcripts encoding two melatonin synthesis enzymes in the teleost pineal organ: circadian regulation in pike and zebrafish, but not in trout. Endocrinol. 139: 905–912.CrossRefGoogle Scholar
  4. Besharse, J.C., Iuvone, P.M. (1983) Circadian clock in Xenopus eye controlling retinal serotonin N-acetyltransferase. Nature 305: 133–135.PubMedCrossRefGoogle Scholar
  5. Bolliet, V., Ali, M.A., Lapointe, F.J., Falcon, J. (1996) Rhythmic melatonin secretion in different teleost species: an in vitro study. J. Comp. Physiol. B 165: 677–683.Google Scholar
  6. Bolliet, V., Bégay; V., Taragnat, C., Ravault, J.P., Collin, J.P., Falcon, J. (1997) Photoreceptor cells of the pike pineal organ as cellular circadian oscillators. Eur. J. Neurosci 9: 643–653.Google Scholar
  7. Burrill, J.D., Easter, S.S. Jr. (1991) Development of the retinofugal projections in the embryonic and larval zebrafish (Brachydanio rerio), J. Comp. Neurol. 346: 583–600.Google Scholar
  8. Cahill, G.M. (1996) Circadian regulation of melatonin production in cultured zebrafish pineal and retina. Brain Res. 708: 177–181.PubMedCrossRefGoogle Scholar
  9. Cahill, G.M. (1997) Circadian melatonin rhythms in cultured zebrafish pineals are not affected by catecholamine agonists. Gen. Comp. Endocrinol. 105: 270–275.Google Scholar
  10. Cahill, G.M., Besharse, J.C. (1991) Resetting the circadian clock in cultured Xenopus eyecups: regulation of retinal melatonin rhythms by light and D2 dopamine receptors. J. Neurosci. 11: 2959–71.PubMedGoogle Scholar
  11. Cahill, G.M., Besharse, J.C. (1993) Circadian clock functions localized in Xenopus retinal photoreceptors. Neuron 10: 573–577.Google Scholar
  12. Cahill, G.M., Besharse, J.C. (1995) Circadian rhythmicity in vertebrate retinas: Regulation by a photoreceptor oscillator. Prog. Retinal Eye Res. 14: 267–291.Google Scholar
  13. Cahill, G.M., Hurd, M.W., Batchelor, M.M. (1998) Circadian rhythmicity in the locomotor activity of larval zebrafish. Neuroreport 9: 3445–3449.PubMedCrossRefGoogle Scholar
  14. Cermakian, N., Whitmore, D., Foulkes, N.S., Sassone-Corsi, P. (2000) Asynchronous oscillations of two zebrafish CLOCK partners reveal differential clock control and function. Proc. Natl. Acad. Sci. USA 97: 4339–4344.Google Scholar
  15. Coon, S.L., Bégay, V., Falcon, J., Klein, D.C. (1998) Expression of melatonin synthesis genes is controlled by a circadian clock in the pike pineal organ but not in the trout. Biol. Cell. 90: 399–405.Google Scholar
  16. Coon, S.L., Bégay, V., Deurloo, D., Falcon, J., Klein, D.C. (1999) Two arylalkylamine N-acetyltransferase genes mediate melatonin synthesis in fish. J. Biol. Chem. 274: 9076–9082.Google Scholar
  17. Falcon, J., Marmillon, J.B., Claustrat, B., Collin, J.P. (1989) Regulation of melatonin secretion in a photoreceptive pineal organ: an in vitro study in the pike. J. Neurosci. 9: 1943–1950.PubMedGoogle Scholar
  18. Falcon, J., Thibault, C., Martin, C., Brun-Marmillon, J., Claustrat, B., Collin, J.P. (1991) Regulation of melatonin production by catecholamines and adenosine in a photoreceptive pineal organ. An in vitro study in the pike and the trout. J. Pineal Res. 11: 123–134.PubMedCrossRefGoogle Scholar
  19. Gern, W.A., Greenhouse, S.S. (1988) Examination of in vitro melatonin secretion from superfused trout (Salmo gairdneri) pineal organs maintained under diel illumination of continuous darkness, Gen. Comp. Endocrinol. 71: 163–174.Google Scholar
  20. Green, C.B., Besharse, J.C. (1996a) Use of a high stringency differential display screen for identification of retinal mRNAs that are regulated by a circadian clock. Mol. Brain Res. 37: 157–165.Google Scholar
  21. Green, C.B., Besharse, J.C. (1996b) Identification of a novel vertebrate circadian clock-regulated gene encoding the protein nocturnin. Proc. Natl. Acad. Sci. USA 93: 14884–1488.PubMedCrossRefGoogle Scholar
  22. Green, C.B., Cahill, G.M., Besharse, J.C. (1995) Regulation of tryptophan hydroxylase expression by a retinal circadian oscillator in vitro. Brain Res. 677: 283–290.PubMedCrossRefGoogle Scholar
  23. Green, C.B., Liang, M.Y., Steenhard, B.M., Besharse, J.C. (1999) Ontogeny of circadian and light regulation of melatonin release in Xenopus laevis embryos. Dev. Brain Res. 117: 109–116.Google Scholar
  24. Harada, Y., Goto, M., Ebihara, S., Fujisawa, H., Kasegawa, k, Oishi, T. (1998) Circadian locomotor activity rhythms in the African clawed frog, Xenopus laevis: The role of the eye and the hypothalamus. Biol. Rhythm Res. 29: 30–48.Google Scholar
  25. Hasegawa, M., Cahill, G.M. (1999a) A role for cyclic AMP in entrainment of the circadian oscillator in Xenopus retinal photoreceptors by dopamine but not by light. J. Neurochem. 72: 1812–1820.PubMedCrossRefGoogle Scholar
  26. Hasegawa, M., Cahill, G.M. (1999b) Modulation of rhythmic melatonin synthesis in Xenopus retinal photoreceptors by cyclic AMP. Brain Res. 824: 161–167.PubMedCrossRefGoogle Scholar
  27. Hurd, M.W., Debruyne, J., Straume, M., Cahill, G.M. (1998) Circadian rhythms of locomotor activity in zebrafish. Physiol. Behay. 65: 465–472.Google Scholar
  28. Holmqvist, B.I., Östholm, T., Ekström, P. (1992) Retinohypothalamic projections and the suprachiasmatic nucleus of the teleost brain. In Ali, M.A. (ed.) Rhythms in Fishes, Plenum Press, New York, pp. 293–318.CrossRefGoogle Scholar
  29. Iigo, M., Tabata, M. (1996) Circadian rhythms of locomotor activity in the goldfish Carassius auratus. Physiol. Behay. 60: 775–781.Google Scholar
  30. Iigo, M., Kezuka, H., Aida, K., Hanyu, I. (1991) Circadian rhythms of melatonin secretion from superfused goldfish (Carassius auratus) pineal glands in vitro. Gen. Comp. Endocrinol. 83: 152–158.Google Scholar
  31. Jimenez, A.J., Fernandez-Llebrez, P., Perez-Figares, J.M. (1995) Central projections from the goldfish pineal organ traced by HRP-immunocytochemistry. Histol Histopathol. 10: 847–852.PubMedGoogle Scholar
  32. Kavaliers, M. (1978) Seasonal changes in the circadian period of the lake chub, Couesius plumbeus. Can. J. Zool. 56: 2591–2596.CrossRefGoogle Scholar
  33. Kavaliers, M. (1979) Pineal involvement in the control of circadian rhythmicity in the lake chub, Couesius plumbeus. J. Exp. Zool. 209: 33–40.Google Scholar
  34. Kavaliers, M. (1980) Circadian locomotor activity rhythms of the burbot, Lota iota: Seasonal differences in period length and the effect of pinealectomy. J. Comp. Physiol. 136: 215–218.Google Scholar
  35. Kavaliers, M., Ralph, C.L. (1980) Pineal involvement in the control of behavioral thermoregulation of the white sucker, Catostomus commersoni. J. Exp. Zool. 212: 301–303.Google Scholar
  36. Kezuka, H., Aida, K., Hanyu, I. (1989) Melatonin secretion from goldfish pineal gland in organ culture. Gen. Comp. Endocrinol. 75: 217–221.Google Scholar
  37. Knox, B.E., Schlueter, C., Sanger, B.M., Green, C.B., Besharse, J.C. (1998) Transgene expression in Xenopus rods. FEBS Lett. 423: 117–121.PubMedCrossRefGoogle Scholar
  38. Korf, H.W., Schomerus, C., Stehle, J.H. (1998) The pineal organ, its hormone melatonin, and the photoneuroendocrine system. Adv. Anat. Embryol. Cell Biol. 146: 1–100.CrossRefGoogle Scholar
  39. Kwok, C., Korn, R.M., Davis, M.E., Burt, D.W., Critcher, R., McCarthy L, Paw, B.H., Zon, L.I., Goodfellow, P.N., Schmitt, K. (1998) Characterization of whole genome radiation hybrid mapping resources for non-mammalian vertebrates. Nucleic Acids Res. 26: 3562–3566.PubMedCrossRefGoogle Scholar
  40. Li, L. Dowling, J.E. (1998) Zebrafish visual sensitivity is regulated by a circadian clock. Visual Neurosci. 15: 851–857.Google Scholar
  41. Max, M., Menaker, M. (1992) Regulation of melatonin production by light, darkness, and temperature in the trout pineal. J. Comp. Physiol. A 170: 479–489.Google Scholar
  42. Morita, Y., Tabata, M., Uchida, K., Samejima, M. (1992) Pineal-dependent locomotor activity of lamprey, Lampetra japonica, measured in relation to LD cycle and circadian rhythmicity. J. Comp. Physiol. A 171: 555–562.Google Scholar
  43. Ooka-Souda, S., Kadota, T., Kabasawa, H. (1993) The preoptic nucleus: the probable location of the circadian pacemaker of the hagfish, Eptatretus burgeri. Neurosci. Lett. 164: 33–36.Google Scholar
  44. Postlethwait, J.H., Yan Y-L, Gates, M.A., Home, S., Amores, A., Brownlie, A., Donovan, A., Egan, E.S., Force, A., Gong, Z., Goutel, C., Fritz, A., Kelsh, R., Knapik, E., Liao, E., Paw, B., Ransom, D., Singer, A., Thomson, M., Abduljabbar, T.S., Yelick, P., Beier, D., Joly J-S, Larhammar, D., Rosa, F., Westerfield, M., Zon, L.I., Johnson, S.L., Talbot, W.S. (1998) Vertebrate genome evolution and the zebrafish gene map. Nat. Genet. 18: 345–349.Google Scholar
  45. Samejima, M., Tamotsu, S., Uchida, K., Moriguchi, Y., Morita, Y. (1997) Melatonin excretion rhythms in the cultured pineal organ of the lamprey, Lampetra japonica. Biol. Signals 6: 241–246.Google Scholar
  46. Sanchez-Vazquez, F.J., Madrid, J.A., Zamora, S., Iigo, M., Tabata, M. (1996) Demand feeding and locomotor circadian rhythms in the goldfish, Carassius auratus: dual and independent phasing. Physiol. Behay. 60: 665–74.Google Scholar
  47. Shimoda, N., Knapik, E.W., Ziniti, J., Sim, C., Yamada, E., Kaplan, S., Jackson, D., de Sauvage, F., Jacob, H., Fishman, M.C. (1999) Zebrafish genetic map with 2000 microsatellite markers. Genomics 58: 219–232.PubMedCrossRefGoogle Scholar
  48. Tabata, M., Minh-Nyo, M., Oguri, M. (1988) Involvement of retinal and extraretinal photoreceptors in the mediation of nocturnal locomotor activity rhythms in the catfish, Silurus asotus. Exp. Biol. 47: 219–225.Google Scholar
  49. Valenciano, A.I., Alonso-Gomez, A.L., Iuvone, P.M. (1999) Diurnal rhythms of tryptophan hydroxylase activity in Xenopus laevis retina: opposing phases in photoreceptors and inner retinal neurons. Neuroreport. 10: 2131–5.PubMedCrossRefGoogle Scholar
  50. Wang, Y., Mangel, S.C. (1996) A circadian clock regulates rod and cone input to fish retinal cone horizontal cells. Proc. Natl. Acad. Sci. USA 93: 4655–4660.Google Scholar
  51. Weigle, C., Wicht, H., Korf, H.W. (1996) A possible homologue of the suprachiasmatic nucleus in the hypothalamus of lampreys (Lampetra fluviatilis L.). Neurosci. Lett. 217: 173–176.Google Scholar
  52. Whitmore, D., Foulkes, N.S., Sassone-Corsi, P. (2000) Light acts directly on organs and cells in culture to set the vertebrate circadian clock. Nature 404: 87–91.PubMedCrossRefGoogle Scholar
  53. Whitmore, D., Foulkes, N.S., Strahle, U., Sassone-Corsi, P. (1998) Zebrafish Clock rhythmic expression reveals independent peripheral circadian oscillators. Nature Neurosci. 1: 701–707.PubMedCrossRefGoogle Scholar
  54. Ydfiez, J., Anadon, R., Holmqvist, B.I., Ekstrom, P. (1993) Neural projections of the pineal organ in the larval lamprey (Petromyzon marinus L.) revealed by indocarbocyanine dye tracing, Neurosci. Lett. 164: 213–216.Google Scholar
  55. Young, M.W. (1999) Molecular control of circadian behavioral rhythms. Recent Prog. Horm. Res. 54: 87–94.Google Scholar
  56. Zachmann, A., Falcon, J., Knijff, S.C.M., Bolliet, V., Ali, M,A. (1992) Effects of photoperiod and temperature on rhythmic melatonin secretion from the pineal organ of the white sucker (Catostomus commersoni) in vitro. Gen. Comp. Endocrinol. 86: 26–33.PubMedCrossRefGoogle Scholar
  57. Zhu, H., LaRue, S., Whiteley, A., Steeves, T.D., Takahashi, J.S., Green, C.B. (2000) The Xenopus clock gene is constitutively expressed in retinal photoreceptors. Mol. Brain Res. 75: 303–308.PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2002

Authors and Affiliations

  • G. M. Cahill
    • 1
  1. 1.Department of Biology and BiochemistryUniversity of HoustonHoustonUSA

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