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The pineal and melatonin: Regulators of circadian function in lower vertebrates

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Summary

The pineal has been identified as a major circadian pacemaker within the circadian system of a number of lower vertebrates although other pacemaking sites have been implicated as well. The rhythmic synthesis and secretion of the pineal hormone, melatonin, is suggested as the mechanism by which the pineal controls circadian oscillators located elsewhere. Both light and temperature cycles can entrain the pineal melatonin rhythm. The pineal, therefore, acts as a photo and thermoendocrine transducer which functions to synchronize internal cycle with cycles in the environment. A model is presented which portrays the pineal as a major component of a ‘multioscillator’ circadian system and which suggests how these multiple circadian clocks are coupled to each other and to cycles of light and temperature in the external world.

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Literature

  1. Adler, K., Extraoptic phase shifting of circadian locomotor rhythm in salamanders. Science164 (1969) 1290–1292.

    Article  CAS  PubMed  Google Scholar 

  2. Adler, K., Pineal end organ: role in extraoptic entrainment of circadian locomotor rhythm in frogs, in: Biochronometry, p. 342–350. Ed. M. Menaker. National Academy of Sciences, Washington, D.C. 1971.

    Google Scholar 

  3. Adler, K., and Taylor, D. H., Melatonin and thyroxine: influence on compass orientation in salamanders. J. comp. Physiol.136 (1980) 235–241.

    Article  CAS  Google Scholar 

  4. Anderson, K., and Turek, F., The influence of blinding and removal of the frontal organ on the activity ofXenopus laevis. Am. Zool.23 (1983) 884.

    Google Scholar 

  5. Bassi, C. J., and Powers, M. K., Circadian rhythm in goldfish visual sensitivity. Invest. Ophthalm. vis. Sci.28 (1987) 1811–1815.

    CAS  Google Scholar 

  6. Bernstein, S. A., Breding, D. J., and Fisher, S. K., The influence of light on cone disk shedding in the lizard,Sceloporus occidentalis. J. Cell Biol.99 (1984) 379–389.

    Article  CAS  PubMed  Google Scholar 

  7. Besharse, J. C., and Iuvone, P. M., Circadian clock inXenopus eye controlling retinal serotonin N-acetyltransferase. Nature305 (1983) 133–135.

    Article  CAS  PubMed  Google Scholar 

  8. Birks, E. K., and Ewing, R. D., Photoperiod effects on hydroxyindole-O-methyltransferase activity in the pineal gland of chinook salmon (Oncorhynchus tshawytscha). Gen. comp. Endocr.43 (1981) 277–283.

    Article  CAS  PubMed  Google Scholar 

  9. Birks, E. K., and Ewing, R. D., Seasonal changes in pineal melatonin content and hydroxyindole-O-methyltransferase activity in juvenile chinook salmon,Oncorhynchus tshawytscha. Gen. comp. Endocr.64 (1986) 91–98.

    Article  CAS  PubMed  Google Scholar 

  10. Dearry, A., and Barlow, R. B. Jr, Circadian rhythms in the green sunfish retina. J. gen. Physiol.89 (1987) 745–770.

    Article  CAS  PubMed  Google Scholar 

  11. Deguchi, T., A circadian oscillator in cultured cells of chicken pineal gland. Nature282 (1979) 94–96.

    Article  CAS  PubMed  Google Scholar 

  12. Demian, J. J., and Taylor, D. H., Photoreception and locomotor rhythm entrainment by the pineal body of the newt,Notophthalmus viridescens (Amphibia, Urodela, Salamandridae). J. Herpet.11 (1977) 131–139.

    Article  Google Scholar 

  13. Eriksson, L. O., Tagesperiodik geblendeter Bachsaiblinge. Naturwissenschaften59 (1972) 219–220.

    Article  Google Scholar 

  14. Eriksson, L. O., Die Jahresperiodik augen- und pinealorganloser BachsaiblingeSalvelinus fontinalis Mitchell. Aquilo Ser. Zool.13 (1972) 8–12.

    Google Scholar 

  15. Falcón, J., and Collin, J.-P., In vitro uptake and metabolism of [3H] indole compounds in the pineal organ of the pike. II. A radioautographic study. J. Pineal Res.2 (1985) 357–373.

    Article  PubMed  Google Scholar 

  16. Falcón, J., Guerlotté, J. F., Voisin, P., and Collin, J.-P., Rhythmic melatonin biosynthesis in a photoreceptive pineal organ: a study in the pike. Neuroendocrinology45 (1987) 479–486.

    Article  PubMed  Google Scholar 

  17. Firth, B. T., and Kennaway, D. J., Melatonin content of the pineal, parietal eye and blood plasma of the lizard,Trachydosaurus rugosus: effect of constant and fluctuating temperature. Brain Res.404 (1987) 313–318.

    Article  CAS  PubMed  Google Scholar 

  18. Firth, B. T., Kennaway, D. J., and Rozenbilds, M. A. M., Plasma melatonin in the scincid lizard,Trachydosaurus rugosus: diel rhythm, seasonality, and the effect of constant light and constant darkness. Gen. comp. Endocr.37 (1979) 493–500.

    Article  CAS  PubMed  Google Scholar 

  19. Garg, S. K., and Sundararaj, B. I., Role of pineal in the regulation of some aspects of circadian rhythmicity in the catfish,Heteropneustes fossilis (Bloch). Chronobiologia13 (1986) 1–11.

    CAS  PubMed  Google Scholar 

  20. Gern, W. A., and Greenhouse, S. S., Examination of in vitro melatonin secretion from superfused trout (Salmo gairdneri) pineal organs maintained under diel illumination or continuous darkness. Gen. comp. Endocr.71 (1988) 163–174.

    Article  CAS  PubMed  Google Scholar 

  21. Gern, W. A., and Norris, D. O., Plasma melatonin in the neotenic tiger salamander (Ambystoma tigrinum): effects of photoperiod and pinealectomy. Gen. comp. Endocr.38 (1979) 393–398.

    Article  CAS  PubMed  Google Scholar 

  22. Gern, W. A., Norris, D. O., and Duvall, D., The effect of light and temperature on plasma melatonin in neotenic tiger salamanders (Ambystoma tigrinum). J. Herpet.17 (1983) 228–234.

    Article  CAS  Google Scholar 

  23. Gern, W. A., Owens, D. W., and Ralph, C. L., Persistence of the nyctohemeral rhythm of melatonin secretion in pinealectomized or optic tract-sectioned trout (Salmo gairdneri). J. exp. Zool.205 (1978) 371–376.

    Article  CAS  Google Scholar 

  24. Goudie, C. A., Davis, K. B. and Simco, B. A., Influence of the eyes and pineal gland on locomotor activity patterns of channel catfishIctalurus punctatus. Physiol. Zool.56 (1983) 10–17.

    Article  Google Scholar 

  25. Guerlotté, J., Falcón, J., Voisin, P., and Collin, J.-P., Indoles in the photoreceptor cells of the lamprey pineal complex. Annls, Endocr., Paris47 (1986) 62–64.

    Google Scholar 

  26. Hamasaki, D. I., and Eder, D. J., Adaptive radiation of the pineal system, in: Handbook of Sensory Physiology, p. 497–548. Ed. F. Crescitelli. Springer, New York 1977.

    Google Scholar 

  27. Illnerová, H., and Vanuuek, J., Circadian rhythm in inducibility of rat pineal N-acetyltransferase after brief light pulses at night: control by a morning oscillator. J. comp. Physiol. A154 (1984) 739–744.

    Article  Google Scholar 

  28. Janik, D. S., Circadian organization in the desert iguana. Ph.D. dissertation. University of Oregon, Eugene 1987.

    Google Scholar 

  29. Joss, J. M. P., A rhythm in hydroxyindole-O-methyltransferase (HIOMT) activity in the scincid lizard,Lampropholas guichenoti. Gen. comp. Endocr.36 (1978) 521–525.

    Article  CAS  PubMed  Google Scholar 

  30. Kavaliers, M., The pineal organ and circadian organization of teleost fish. Rev. Can. Biol.38 (1979) 281–292.

    Google Scholar 

  31. Kavaliers, M., Pineal involvement in the control of circadian rhythmicity in the lake chub,Couesius plumbeus. J. exp. Zool.209 (1979) 33–40.

    Article  Google Scholar 

  32. Kavaliers, M., Circadian locomotor activity rhythms of the Turbot,Lota lota: seasonal differences in period length and the effect of pinealectomy. J. comp. Physiol.136 (1980) 215–218.

    Article  Google Scholar 

  33. Kavaliers, M., Retinal and extraretinal entrainment action spectra for the activity rhythms of the lake chub,Couesius plumbeus. Behav. neural Biol.30 (1980) 56–67.

    Article  CAS  PubMed  Google Scholar 

  34. Kavaliers, M., Circadian organization in white suckersCatostomus commersoni: the role of the pineal organ. Comp. Biochem. Physiol.68A (1981) 127–129.

    Article  Google Scholar 

  35. Lythgoe, J. N., and Shand, J., Endogenous circadian retinomotor movements in the neon tetra (Paracheirodon innesi). Invest. Ophthalm. vis. Sci.24 (1983) 1203–1210.

    CAS  Google Scholar 

  36. McNulty, J. A., Functional morphology of the pineal complex in cyclostomes, elasmobranchs, and bony fishes, in: Pineal Research Reviews, vol. 2, p. 1–40. Ed. R. J. Reiter. Alan R. Liss, Inc., New York 1984.

    Google Scholar 

  37. Menaker, M., Eyes — the second (and third) pineal glands?, in: Photoperiodism, Melatonin and the Pineal, p. 78–87. Eds D. Evered and S. Clark. Pitman, London 1985.

    Google Scholar 

  38. Menaker, M., and Wisner, S., Temperature-compensated circadian clock in the pineal ofAnolis. Proc. natl Acad. Sci. USA80 (1983) 6119–6121.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  39. Moore, R. Y., and Card, J. P., Visual pathways and the entrainment of circadian rhythms, in: The Medical and Biological Effects of Light. p. 123–133. Eds R. J. Wurtman, M. J. Baum and J. T. Potts, Jr. New York Academy of Sciences, New York 1985.

    Google Scholar 

  40. Ooka-Souda, S., and Kabasawa, H., Circadian rhythms in locomotor activity of the hagfish,Eptatretus burgeri III. Hypothalamus: a locus of the circadian pacemaker? Zool. Sci.5 (1988) 437–442.

    Google Scholar 

  41. Pang, S. F., Shiu, S. Y. W., and Tse, S. F., Effect of photic manipulation on the level of melatonin in the retinas of frogs (Rana tigrina regulosa). Gen. comp. Endocr.58 (1985) 464–470.

    Article  CAS  PubMed  Google Scholar 

  42. Pierce, M. E., and Besharse, J. C., Melatonin and dopamine interactions in the regulation of rhythmic photoreceptor metabolism, in: Pineal and Retinal Relationships, p. 219–237. Eds P. J. O'Brien and D. C. Klein, Academic Press, New York 1986.

    Google Scholar 

  43. Pittendrigh, C. S., On the mechanism of the entrainment of a circadian rhythm by light cycles, in: Circadian Clocks, p. 277–297. Ed. J. Aschoff, North-Holland, Amsterdam 1965.

    Google Scholar 

  44. Prasada Rao, P. D., and Sharma, S. C., Retinofugal pathways in juvenile and adult channel catfishIctalurus (Ameiurus) punctatus: an HRP and autoradiographic study. J. comp. Neurol.210 (1982) 37–48.

    Article  CAS  PubMed  Google Scholar 

  45. Quay, W. B., The parietal eye-pineal complex, in: Biology of the Reptilia, vol. 9, p. 245–406. Ed. C. Gans. Academic Press, New York 1979.

    Google Scholar 

  46. Ralph, C. L., Melatonin production by extrapineal tissues, in: Melatonin: Current Status and Perspectives, p. 35–46. Eds N. Birau and W. Schloot. Pergamon Press, New York 1981.

    Chapter  Google Scholar 

  47. Reiter, R. J., Action spectra, dose-response relationships, and temporal aspects of light's effects on the pineal gland, in: The Medical and Biological Effects of Light, p. 215–230. Eds R. J. Wurtman, M. J. Baum and J. T. Potts, Jr. New York Academy of Sciences, New York 1985.

    Google Scholar 

  48. Repérant, J., Rio, J. P., Miceli, D., and Lemire, M., A radioautographic study of retinal projections in type I and type II lizards. Brain Res.142 (1978) 401–411.

    Article  PubMed  Google Scholar 

  49. Takahashi, J. S., and Menaker, M., Role of the suprachiasmatic nuclei in the circadian system of the house sparrow,Passer domesticus. J. Neurosci.2 (1982) 815–828.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  50. Underwood, H., Circadian organization in lizards: the role of the pineal organ. Science195 (1977) 587–589.

    Article  CAS  PubMed  Google Scholar 

  51. Underwood, H., Circadian organization in the lizardSceloporus occidentalis: the effects of pinealectomy, blinding, and melatonin. J. comp. Physiol.141 (1981) 537–547.

    Article  CAS  Google Scholar 

  52. Underwood, H., Circadian pacemakers in lizards: phase-response curves and effects of pinealectomy. Am. J. Physiol.244 (1983) R857-R864.

    CAS  PubMed  Google Scholar 

  53. Underwood, H., Circadian organization in the lizardAnolis carolinensis: a multioscillator system. J. comp. Physiol. A152 (1983) 265–274.

    Article  Google Scholar 

  54. Underwood, H., Pineal melatonin rhythms in the lizardAnolis carolinensis; effects of light and temperature cycles. J. comp. Physiol. A157 (1985) 57–65.

    Article  CAS  PubMed  Google Scholar 

  55. Underwood, H., Extraretinal photoreception in the lizardSceloporus occidentalis: phase response curve. Am. J. Physiol.248 (1985) R407-R414.

    CAS  PubMed  Google Scholar 

  56. Underwood, H., Circadian rhythms in lizards: phase response curve for melatonin. J. Pineal Res.3 (1986) 187–196.

    Article  CAS  PubMed  Google Scholar 

  57. Underwood, H., Light at night cannot suppress pineal melatonin levels in the lizardAnolis carolinensis. Comp. Biochem. Physiol.84A (1986) 661–663.

    Article  CAS  Google Scholar 

  58. Underwood, H., and Calaban, M., Pineal melatonin rhythms in the lizardAnolls carolinensis: I. Response to light and temperature cycles. J. biol. Rhythms2 (1987) 179–193.

    Article  CAS  PubMed  Google Scholar 

  59. Underwood, H., and Gross, G., Vertebrate circadian rhythms: retinal and extraretinal photoreception. Experientia38 (1982) 1013–1021.

    Article  CAS  PubMed  Google Scholar 

  60. Underwood, H., and Harless, M., Entrainment of the circadian activity rhythm of a lizard to melatonin injections. Physiol. Behav.35 (1985) 267–270.

    Article  CAS  PubMed  Google Scholar 

  61. Underwood, H., and Menaker, M., Extraretinal photoreceptionin lizards. Photochem. Photobiol.23 (1976) 227–243.

    Article  CAS  Google Scholar 

  62. van Veen, T., Hartwig, H.G., and Muller, K., Light-dependent motor activity and photonegative behavior in the eel (Anguilla anguilla L.). Evidence for extraretinal and extrapineal photoreception. J. comp. Physiol.111 (1976) 209–219.

    Article  Google Scholar 

  63. Vivien-Roels, B., Arendt, J., and Bradtke, J., Circadian and circannual fluctuations of pineal indoleamines (serotonin and melatonin) inTestudo hermanni Gmelin (Reptilia, Chelonia) 1. Under natural conditions of photoperiod and temperature. Gen. comp. Endocr.37 (1979) 197–210.

    Article  CAS  PubMed  Google Scholar 

  64. Vivien-Roels, B., and Pévet, P., The pineal gland and the synchronization of reproductive cycles with variations of the environmental climatic conditions, with special reference to temperature, in: Pineal Research Reviews, vol. 1, p. 91–143. Ed. R. J. Reiter. Alan R. Liss, Inc., New York 1983.

    Google Scholar 

  65. Vivien-Roels, B., Pévet, P., and Claustrat, B., Pineal and circulating melatonin rhythms in the box turtleTerrapene carolina triunguis: effect of photoperiod, light pulse, and environmental temperature. Gen. comp. Endocr.69 (1988) 163–173.

    Article  CAS  PubMed  Google Scholar 

  66. Vivien-Roels, B., Pévet, P., Dubois, M.P., Arendt, J., and Brown, G.M., Immunohistochemical evidence for the presence of melatonin in the pineal gland, the retinal and the Harderian gland. Cell Tissue Res.217 (1981) 105–115.

    Article  CAS  PubMed  Google Scholar 

  67. Wiechmann, A.F., Melatonin: parallels in pineal gland and retina. Exp. Eye Res.42 (1986) 507–527.

    Article  CAS  PubMed  Google Scholar 

  68. Wiechmann, A.F., Bok, D., and Horwitz, J., Melatonin binding in the frog retina: autoradiographic and biochemical analysis. Invest. Opthalm. vis. Sci.27 (1986) 153–163.

    CAS  Google Scholar 

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Underwood, H. The pineal and melatonin: Regulators of circadian function in lower vertebrates. Experientia 45, 914–922 (1989). https://doi.org/10.1007/BF01953048

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