Development of Mammalian Circadian Rhythms

  • Fred C. Davis
  • Steven M. Reppert
Part of the Handbook of Behavioral Neurobiology book series (HBNE, volume 12)

Abstract

The goal of developmental biology is to understand the origins of biological organization as it unfolds within each generation. Investigations of development often begin with describing how normal development proceeds, then ask how the observed processes or events are regulated. At the level of the whole organism, the most fundamental of such questions (even if oversimplified) is to ask whether the behavior, structure, or physiologic process of interest is inborn or is in some way shaped by the external environment under which the organism develops. This was one of the earliest questions to be asked about circadian rhythms. Charles Darwin contested the view he attributed to Wilhelm Pfeffer that the persistent rhythms of leaf movements in plants under constant conditions should be attributed to “ ‘Nachwirkung’ or the aftereffects of light and darkness.” Darwin concluded instead that “the periodicity of their movements is to a certain extent inherited” (Darwin, 1896). Seventy-five years later, as the modern field of circadian biology was being established, experiments with several different organisms investigated whether organisms needed to be exposed to 24-hour cycles in light and dark during development in order to express circadian rhythms when mature (Aschoff, 1960; Pittendrigh, 1954). The conclusion from these studies was that the expression of circadian rhythms is “independent of any ontogenetic learning process” (Pittendrigh, 1954). For the whole organism, this conclusion is still appropriate today, but as the regulation of circadian rhythmicity continues to be elucidated, the general question persists.Understanding the relative contributions of intrinsic programs and environmental effects in guiding the differentiation of specific features of circadian organization remains a goal of developmental studies.

Keywords

Dopamine Serotonin Histamine Prolactin Phenylalanine 

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References

  1. Altman, J., & Bayer, S. A. (1978a). Development of the diencephalon in the rat I. Autoradiographic study of the time of origin and settling patterns of neurons of the hypothalamus. Journal of Comparative Neurology, 182, 945–972.PubMedGoogle Scholar
  2. Altman, J., & Bayer, S. A. (1978b). Development of the diencephalon in the rat II. Correlation of the embryonic development of the hypothalamus with the time of origin of its neurons. Journal of Comparative Neurology, 182, 973–994.PubMedGoogle Scholar
  3. Altman, J., & Bayer, S. A. (1986). The development of the rat hypothalamus. Advances in Anatomy Embryology and Cell Biology, 100, 1–178.Google Scholar
  4. Altman, J., & Bayer, S. A. (1995). Atlas of prenatal rat brain development. Boca Raton, FL: CRC Press. Antoch, M. P., Song, E. J., Chang, A. M., Vitaterna, M. H., Zhao, Y. L., Wilsbacher, L. D., Sangoram, A.M.Google Scholar
  5. King, D. P., Pinto, L. H., & Takahashi, J. S. (1997). Functional identification of the mouse circadian clock gene by transgenic BAC rescue. Cell, 89, 655–667.PubMedGoogle Scholar
  6. Arduini, D., Rizzo, G., Parlad, E., Dell’Acqua, S., Romanini, C., & Mancuso, S. (1987). Loss of circadian rhythms of fetal behaviour in a totally adrenalectomized pregnant woman. Gynecological and Obstetrical Investigations, 23, 226–229.Google Scholar
  7. Armstrong, B. G., Nolin, A. D., & McDonald, A. D. (1989). Work in pregnancy and birth weight for gestational age. British Journal of Industrial Medicine, 46, 196–199.PubMedGoogle Scholar
  8. Armstrong, S. M. (1989). Melatonin and circadian control in mammals Experientia, 45, 933–938.Google Scholar
  9. Aschoff, J. (1960). Exogenous and endogenous components in circadian rhythms. Cold Spring Harbor Symposium on Quantitative Biology, 25, 11–28.Google Scholar
  10. Aschoff, J., Gerecke, U., & Weyer, R. (1967). Desynchronization of human circadian rhythms. Japanese Journal of Physiology, 17, 450–457.PubMedGoogle Scholar
  11. Axelsson, G., Rylander, R., & Man, I. (1989). Outcome of pregnancy in relation to irregular and inconvenient work schedules. British Journal of Industrial Medicine, 46, 393–398.PubMedGoogle Scholar
  12. Ban, Y., Shigeyoshi, Y., & Okamura, H. (1997). Development of vasoactive intestinal peptide mRNA rhythm in the rat suprchiasmatic nucleus. Journal of Neuroscience, 17, 3920–3931.PubMedGoogle Scholar
  13. Barr, M. J. (1973). Prenatal growth of wistar rats: Circadian periodicity of fetal growth late in gestation. Teratology, 7, 283–287.Google Scholar
  14. Botchkina, G. I. & Morin, L. P. (1993). Development of the hamster serotoninergic system: Cell groups and diencephalic projections. Journal of Comparative Neurology, 338, 405–431.PubMedGoogle Scholar
  15. Botchkina, G. I., & Morin, L. P. (1995a). Ontogeny of radial glia, astrocytes and vasoactive intestinal peptide immunoreactive neurons in hamster suprachiasmatic nucleus. Developmental Brain Research, 86, 48–56.PubMedGoogle Scholar
  16. Botchkina, G. I., & Morin, L. P. (1995b). Organization of permanent and transient neuropeptide Y-immunoreactive neuron groups and fiber systems in the developing hamster diencephalon.Journal of Comparative Neurology, 357, 573–602.PubMedGoogle Scholar
  17. Broekhuizen, S., & Maaskamp, F. (1980). Behaviour of does and leverets of the European hare (Lepus europaeus) whilst nursing. Journal of Zoology (London), 191, 487–501.Google Scholar
  18. Cambras, T., & Diez-Noguera, A. (1991). Evolution of rat motor activity circadian rhythm under three different light patterns. Physiology and Behavior, 49, 63–68.PubMedGoogle Scholar
  19. Card, J. P., & Moore, R. Y. (1984). The suprachiasmatic nucleus of the golden hamster: Immunohistochemical analysis of cell and fiber distribution. Neuroscience, 13, 415–431.PubMedGoogle Scholar
  20. Carlson, L. L., Weaver, D. R., & Reppert, S. M. (1991). Melatonin receptors and signal transduction during development in Siberian hamsters (Phodopus sungorus). Developmental Brain Research, 59, 83–88.PubMedGoogle Scholar
  21. Cassone, V. M., Speh, J. C., Card, J. P., & Moore, R. Y. (1988). Comparative anatomy of the mammalian hypothalmic suprachiasmatic nucleus. Journal of Biological Rhythms, 3, 71–91.PubMedGoogle Scholar
  22. Chamberlain, P. E, Manning, F. A., Morrison, I., & Lange, I. R. (1984). Circadian rhythm in bladder volumes in the term human fetus. Obstetrics and Gynecology, 64, 657–660.PubMedGoogle Scholar
  23. Clegg, D. A., O’Hara, B. E, Heller, H. C., & Kilduff, T. S. (1995). Nicotine administration differentially affects gene expression in the maternal and fetal circadian clock. Developmental Brain Research, 84, 46–54.PubMedGoogle Scholar
  24. Constandil, L., Parraguez, V. H., Torrealba, F., Valenzuela, G., & Serón-Ferré, M. (1995). Day-night changes in c fos expression in the fetal sheep suprachiasmatic nucleus at late gestation. Reproduction Fertility and Development, Z 411–413.Google Scholar
  25. Coons, S., & Guilleminault, C. (1984). Development of consolidated sleep and wakeful periods in relation to the day/night cycle in infancy. Developmental Medicine and Child Neurology, 26, 169–176.PubMedGoogle Scholar
  26. Cooper, Z. K. (1939). Mitotic rhythm in human epidermis. Journal oflnvestigativeDermatology, 2, 289–300.Google Scholar
  27. Cooper, H. M., Tessonneaud, A., Caldani, A., Locatelli, A., Richard, S., & Viguier-Martinez, M.-C. (1993).Morphology and distribution of retinal ganglion cells (RGC) projecting to the suprachiasmatic nucleus in the sheep. Society for Neuroscience Abstracts, 11, 1704.Google Scholar
  28. Darwin, C. (1896). The power of movement in plants. New York: Appleton.Google Scholar
  29. Davis, F, C. (1981). Ontogeny of circadian rhythms. In J. Aschoff (Ed.), Handbook of behavioral neurobiology, Vol. 4, Biological rhythms (pp. 257–274). New York: Plenum Press.Google Scholar
  30. Davis, F. C. (1982). Development of the suprachiasmatic nuclei and other circadian pacemakers. In D. C. Klein (Ed.), Melatonin rhythm generating system: Developmental aspects (pp. 1–19). Basel: KargerGoogle Scholar
  31. Davis, F. C. (1989). Daily variation in maternal and fetal weight gain in mice and hamsters. Journal of Experimental Zoology, 250, 273–282.PubMedGoogle Scholar
  32. Davis, F. C., & Gorski, R. A. (1984). Unilateral lesions of the hamster suprachiasmatic nuclei: Evidence for redundant control of circadian rhythms. Journal of Comparative Physiology A, 154, 221–232.Google Scholar
  33. Davis, F. C., & Gorski, R. A. (1986). Development of hamster circadian rhythms: Prenatal entrainment of the pacemaker. Journal of Biological Rhythms, 1, 77–89.Google Scholar
  34. Davis, E C., & Gorski, R. A. (1988). Development of hamster circadian rhythms: Role of the maternal suprachiasmatic nucleus. Journal of Comparative Physiology A, 162, 601–610.Google Scholar
  35. Davis, F. C., & Mannion, J. (1988). Entrainment of hamster pup circadian rhythms by prenatal melatonin injections to the mother. American Journal of Physiology, 255, R439–R448.PubMedGoogle Scholar
  36. Davis, F. C., & Menaker, M. (1981). Development of the mouse circadian pacemaker: Independence from environmental cycles. Journal of Comparative Physiology A, 143, 527–539.Google Scholar
  37. Davis, F. C., & Viswanathan, N. (1996). The effect of transplanting one or two suprachiasmatic nuclei on the period of the restored rhythm. Journal of Biological Rhythms, 11, 291–301.PubMedGoogle Scholar
  38. Davis, E C., Darrow, J. M., & Menaker, M. (1983). Sex difference in the circadian control of hamster wheel-running activity. American Journal of Physiology, 244, R93–R105.PubMedGoogle Scholar
  39. Davis, F. C., Boada, R., & LeDeaux, J. (1990). Neurogenesis of the hamster suprachiasmatic nucleus. Brain Research, 519, 192–199.PubMedGoogle Scholar
  40. Davis, F. C., Frank, M. G., & Heller, H. C. (1999). Ontogeny of sleep and circadian rhythms. In F. W. Turek & P. C. Zee (Eds.), Regulation of sleep and circadian rhythms, Vol. 133Lung biology in health and disease. New York: Marcel Dekker.Google Scholar
  41. Deacon, S., & Arendt, J. (1995). Melatonin-induced temperature suppression and its acute phase-shifting effects correlate in a dose-dependent manner in humans. Brain Research, 688, 77–85.PubMedGoogle Scholar
  42. Decavel, C., & Van den Pol, A. N. (1990). GABA: A dominant neurotransmitter in the hypothalamus. Journal of Comparative Neurology, 302, 1019–1037.PubMedGoogle Scholar
  43. Deguchi, T. (1975). Ontogenesis of a biological clock for serotonin: Acetyl coenzyme A N-acetyltransfer-ase in pineal gland of rat. Proceedings of the National Academy of Sciences of the USA, 72, 2814–2818.PubMedGoogle Scholar
  44. De Vries, G. J., Buijs, R. M., & Swaab, D. F. (1981). Ontogeny of the vasopressinergic neurons of the suprachiasmatic nucleus and their extrahypothalamic projections in the rat brain-Presence of a sex difference in the lateral septum. Brain Research, 218, 67–78.PubMedGoogle Scholar
  45. de Vries, J. I. P., Visser, G. H. A., Mulder, E. J. H., & Prechtl, H. F. R. (1987). Diurnal and other variations in fetal movement and heart rate patterns at 20–22 weeks. Early Human Development, 15, 333–348.PubMedGoogle Scholar
  46. Drucker-Colin, R., Aguilar-Roblero, R., Garcia-Hernandez, F., Fernandez-Cancino, F., & Rattoni, F. B.(1984). Fetal suprachiasmatic nucleus transplants: Diurnal rhythm recovery of lesioned rats. Brain Research, 311, 353–357.Google Scholar
  47. Duffield, G. E., Dickerson, J. M., Alexander, I. H. M., & Ebling, E J. P. (1995). Ontogeny of a photic response in the suprachiasmatic nucleus in the Siberian hamster (phodopus sungorus). European Journal of Neuroscience, 7, 1089–1096.PubMedGoogle Scholar
  48. Duncan, M. J., & Davis, F. C. (1993). Developmental appearance and age related changes in specific 2-[1251]iodomelatonin binding sites in the suprachiasmatic nuclei of female Syrian hamsters. Developmental Brain Research, 73, 205–212.PubMedGoogle Scholar
  49. Duncan, M. J., Banister, M. J., & Reppert, S. M. (1986). Developmental appearance of light-dark entrainment in the rat. Brain Research, 369, 326–330.PubMedGoogle Scholar
  50. Ehrstrom, C. (1984). Circadian rhythm of fetal movements. Acta Obstetrica et Gynecologica Scandinavica, 63, 539–541.Google Scholar
  51. Elliott, J. A., & Goldman, B. D. (1989). Reception of photoperiodic information by fetal Siberian hamsters: Role of the mother’s pineal gland. Journal of Experimental Zoology, 252, 237–244.PubMedGoogle Scholar
  52. Ellison, N., Weller, J. L., & Klein, D. C. (1972). Development of a circadian rhythm in the activity of pineal seritonin N-acetyltransferase. Journal of Neurochemistry, 19, 1335–1341.PubMedGoogle Scholar
  53. Fletcher, K. L., Leung, K., Myers, M. M., & Stark, R. I. (1996). Diurnal rhythms in cardiorespiratory function of the fetal baboon. Early Human Development, 46, 27–42.PubMedGoogle Scholar
  54. Fuchs, J. L., & Moore, R. Y. (1980). Development of circadian rhythmicity and light responsiveness in the rat suprachiasmatic nucleus: A study using the 2-deoxy[1–14C] glucose method. Proceedings of the National Academy of Sciences, 77, 1204–1208.Google Scholar
  55. Ganzhorn, J. U., & Wright, P. C. (1994). Temporal patterns in primate leaf eating: The possible role of leaf chemistry. Folia Primatologica, 63, 203–208.Google Scholar
  56. Gibson, A. A. M. (1992). Current epidemiology of SIDS. Journal of Clinical Pathology, 45 (Supplement), 7–10.PubMedGoogle Scholar
  57. Glotzbach, S. T., Sollars, P., Ariagno, R. L., & Pickard, G. E. (1992). Development of the human retinohypothalamic tract. Society for Neuroscience Abstracts, 18, 875.Google Scholar
  58. Glotzbach, S. F., Edgar, D. M., Boeddiker, M., & Ariagno, R. L. (1994). Biological rhythmicity in normal infants during the first 3 months of life. Pediatrics, 94, 482–488.PubMedGoogle Scholar
  59. Glotzbach, S. E, Edgar, D. M., & Ariagno, R. L. (1995). Biological rhythmicity in preterm infants prior to discharge from neonatal intensive care. Pediatrics, 95, 4231–237.Google Scholar
  60. Griffioen, H. A., Duindam, H., Van der Woude, T. P., Rietveld, W. J., & Boer, G. J. (1993). Functional development of fetal suprachiasmatic nucleus grafts in suprachiasmatic nucleus-lesioned rats. Brain Research Bulletin, 31, 145–160.PubMedGoogle Scholar
  61. Grosse, J., & Davis, F. C. (1998). Melatonin entrains restored circadian activity rhythms of Syrian hamsters bearing fetal SCN grafts. Journal of Neuroscience, 18, 8032–8037.PubMedGoogle Scholar
  62. Grosse, J., Velickovic, A., & Davis, E C. (1996). Entrainment of Syrian hamster circadian activity rhythms by neonatal melatonin injections. American Journal of Physiology, 270, R533–R540.PubMedGoogle Scholar
  63. Güldner, F.-H. (1978). Synapses of optic nerve afferents in the rat suprachiasmatic nucleus. I. Identifica-tion, qualitative description, development and distribution. Cell and Tissue Research, 194, 17–35.PubMedGoogle Scholar
  64. He, X., Treacy, M. N., Simmons, D. M., Ingraham, H. A., Swanson, L. W., & Rosenfeld, M. G. (1989).Expression of a large family of POU-domain regulatory genes in mammalian brain development.Nature, 340, 35–42.PubMedGoogle Scholar
  65. Hellbrugge, T., Lange, J. E., Rutenfranz, J., & Stehr, K. (1964). Circadian periodicity of physiological functions in different stages of infancy and childhood. Annals of the New York Academy of Sciences, 117, 361–373.Google Scholar
  66. Hiroshige, T., Honma, K., & Watanabe, K. (1982a). Possible zeitgebers for external entrainment of the circadain rhythm of plasma corticosterone in blind infantile rats. Journal of Physiology, 325, 507–519.PubMedGoogle Scholar
  67. Hiroshige, T., Honma, K., & Watanabe, K. (1982b). Prenatal onset and maternal modifications of the circadian rhythm of plasma corticosterone in blind infantile rats. Journal of Physiology, 325, 521–532.PubMedGoogle Scholar
  68. Hoffman, K. (1959). Die aktivitatsperiodik von im 18- und 36-stunden-tag erfruteten eidechsen. Zeitschriftfur vergleichende Physiologie, 42, 422–432.Google Scholar
  69. Holtzman, R. L., Malach, R., & Gozes, I. (1989). Disruption of the optic pathway during development affects vasoactive intestinal peptide mRNA expression. New Biologist, 1, 215–221.PubMedGoogle Scholar
  70. Honma, S., Honma, K, Shirakawa, T., & Hiroshige, T. (1984). Effects of elimination of maternal ceircadian rhythms during pregnancy on the postnatal development of circadian corticosterone rhythm in blinded infantile rats. Endocrinology, 114, 44–50.PubMedGoogle Scholar
  71. Honnebier, M. B. O. M., Swaab, D. F & Mirmiran, M. (1989). Diurnal rhythmicity during early human development. In S. M. Reppert (Ed.), Development of circadian rhythmicity and photoperiodism in mammals (pp. 221–244). Ithaca, NY: Perinatology PressGoogle Scholar
  72. Horton, T. H. (1983). Growth and maturation in Microtus montanus: Effects of photoperiods before and after weaning. Canadian Journal of Zoology, 62, 1741–1746.Google Scholar
  73. Hudson, R., & Distel, H. (1989). Temporal pattern of suckling in rabbit pups: A model of circadian synchrony between mother and young. In S. M. Reppert (Ed.), Development of rhythmicity and photoperiodism in mammals (pp. 83–102). Ithaca, NY: Perinatology PressGoogle Scholar
  74. Ibuka, N. (1987). Circadian rhythms in sleep-wakefullness and wheel-running activity in a congenitally anophthalmic rat mutant. Physiology and Behavior, 39, 321–326.PubMedGoogle Scholar
  75. Illnerovã, H., Buresovã, M., & Presl, J. (1993). Melatonin rhythm in human milk. Journal of Clinical Endocrinology and Metabolism, 77, 838–841.PubMedGoogle Scholar
  76. Inouye, I. T., & Kawamura, H. (1979). Persistence of circadian rhythmicity in a mammalian hypothalamic “island” containing the suprachiasmatic nucleus. Proceedings of the National Academy of Sciences of the USA, 76, 5962–5966.PubMedGoogle Scholar
  77. Iuvone, P. M. & Gan, J. (1995). Functional interaction of melatonin receptors and Dl dopamine receptors in cultured chick retinal neurons. Journal of Neuroscience, 15, 2179–2185.PubMedGoogle Scholar
  78. Jaldo-Alba, F., Munoz-Hoyos, A., Molina-Carballo, A., Molina-Font, J. A., & Acuna-Castroviejo, D. (1993). Light deprivation increases plasma levels of melatonin during the first 72 h of life in human infants. Acta Endocrinologica, 129, 442–445.PubMedGoogle Scholar
  79. Jilge, B. (1993). The ontogeny of circadian rhythms in the rabbit. Journal of Biological Rhythms, 8, 247–260.PubMedGoogle Scholar
  80. Jilge, B. (1995). Ontogeny of the rabbit’s circadian rhythms without an external zeitgeber. Physiology and Behavior, 58, 131–140.PubMedGoogle Scholar
  81. Johnson, R. F., Moore, R. Y., & Morin, L. P. (1988). Loss of entrainment and anatomical plasticity after lesions of the hamster retinohypothalamic tract. Brain Research, 460, 297–313.PubMedGoogle Scholar
  82. Johnson, R. F., Morin, L. P., & Moore, R. Y. (1988). Retinohypothalamic projections in the hamster and rat demonstrated using cholera toxin. Brain Research, 462, 301–312.PubMedGoogle Scholar
  83. Kagotani, Y., Hashimoto, T., Tsuruo, Y., Kawano, H., Daikoku, S., & Chihara, K. (1989). Development of the neuronal system containing neuropeptide Y in the rat hypothalamus. International Journal of Developmental Neuroscience, 7, 359–374.PubMedGoogle Scholar
  84. Kaufman, C. M., & Menaker, M. (1993). Effect of transplanting suprachiasmatic nuclei from donors of different ages into completely SCN lesioned hamsters. Journal of Neural Transplantation and Plasticity, 4, 257–265.PubMedGoogle Scholar
  85. Kaufman, C. M., & Menaker, M. (1994). Ontogeny of light-induced Fos-like immunoreactivity in the hamster suprachiasmatic nucleus. Brain Research, 633, 162–166.PubMedGoogle Scholar
  86. Kennaway, D. J., Stamp, G. E., & Goble, F. C. (1992). Development of melatonin production in infants and the impact of prematurity. Journal of Clinical Endocrinology and Metabolism, 75, 367–369.PubMedGoogle Scholar
  87. Kennaway, D. J., Goble, F. C., & Stamp, G. E. (1996). Factors influencing the development of melatonin rhythmicity in humans. Journal of Clinical Endocrinology and Metabolism, 81, 1525–1532.PubMedGoogle Scholar
  88. King, D. P., Zhao, Y. L., Sangoram, A. M., Wilsbacher, L. D., Tanaka, M., Antoch, M. P., Steeves, T. D. L., Vitaterna, M. H., Kornhauser, J. M., Lowrey, P. L., Turek, F. W., & Takahashi, J. S. (1997). Positional cloning of the mouse circadian clock gene. Cell, 89, 641–653.PubMedGoogle Scholar
  89. Klein, D. C. (1972). Evidence for placental transfer of 3H-acetyl-melatonin. Nature, 237, 117–119. Kleitman, N. & Engelmann, T. G. (1953). Sleep characteristics of infants. Journal of Applied Physiology, 6, 269–282.Google Scholar
  90. Koritsanszky, S. (1981). Fetal and early postnatal cyto-and synaptogenesis in the suprachiasmatic nucleus of the rat hypothalamus. Acta Morphologica Academiae Scientiarum Hungaricae, 29, 227–239.PubMedGoogle Scholar
  91. Krieger, D. T. (1972). Circadian corticosteroid periodicity: Critical period for abolition by neonatal injection of corticosteroid. Science, 178, 1205–1207.PubMedGoogle Scholar
  92. Krieger, D. T., & Hauser, H. (1977). Suprachiasmatic nuclear lesions do not abolish food-shifted circadian adrenal and temperature rhythmicity. Science, 197, 398–399.Google Scholar
  93. Kuhlman, S., Watts, A. G., Sanchez-Watts, G., & Davis, F. C. (1995). Developmental expression of preprovasoactive intestinal polypeptide (VIP) mRNA in the Syrian hamster suprachiasmatic nucleus. Society for Neuroscience Abstracts, 21, 452.Google Scholar
  94. Laemle, L. K., & Rusa, R. (1992). VIP-like immunoreactivity in the suprachiasmatic nuclei of a mutant anophthalmic mouse. Brain Research, 589, 124–128.PubMedGoogle Scholar
  95. Laemle, L. K., Repke, K B., Hawkes, R., & Rice, F. L. (1991). Synaptogenesis in the rat suprachiasmatic nucleus: A light microscopic immunocytochemical survey. Brain Research, 544, 108–117.PubMedGoogle Scholar
  96. Leard, L. E., Macdonald, E. S., Heller, H. C., & Kilduff, T. S. (1994). Ontogeny of photic-induced c fos mRNA expression in rat suprachiasmatic nuclei. Neuroreport, 5, 2683–2687.PubMedGoogle Scholar
  97. Lehman, M. N., Silver, R., Gladstone, W. R., Kahn, R. M., Gibson, M., & Bittman, E. L. (1987). Circadian rhythmicity restored by neural transplant. Immunocytochemical characterization of the graft and its integration with the host brain. Journal of Neuroscience, 7, 1626–1638.PubMedGoogle Scholar
  98. Lenn, N. J., Beebe, B., Sc Moore, R. Y. (1977). Postnatal development of the suprachiasmatic hypothalamic nucleus of the rat. Cell and Tissue Research, 178, 463–475.PubMedGoogle Scholar
  99. LeSauter, J., Lehman, M. N., & Silver, R. (1996). Restoration of circadian rhythmicity by transplants of SCN “micropunches.” Journal of Biological Rhythms, 11, 163–171.PubMedGoogle Scholar
  100. Lewy, A. J. (1992). Melatonin shifts human circadian rhythms according to a phase-response curve. Chronobiology International, 9, 380–392.PubMedGoogle Scholar
  101. Magnin, M., Cooper, H. M., & Mick, G. (1989). Retinohypothalamic pathway: A breach in the law of Newton-Muller-Gudden? Brain Research, 488, 390–397.PubMedGoogle Scholar
  102. Mai, J. K., Kedziora, O., Teckhaus, L., & Sofroniew, M. V. (1991). Evidence for subdivisions in the human suprachiasmatic nucleus. Journal of Comparative Neurology, 305, 508–525.PubMedGoogle Scholar
  103. Mann, N. P., Haddow, R., Stokes, L., Goodley, S. & Rutter, N. (1986). Effect of night and day on preterm infants in a newborn nursery: Randomised trial. British Journal of Medicine, 293 1265–1267.Google Scholar
  104. Martin du Pan, R. (1974). Some clinical applications of our knowledge of the evolution of the circadian rhythm in infants. In L. E. Scheving, F. Halberg, & J. E. Pauly (Eds.), Chronobiology (pp. 342–347). Tokyo: Iguku Shoin.Google Scholar
  105. McMillen, I. C., & Nowak, R. (1989). Maternal pinealectomy abolishes the diurnal rhythm in plasma melatonin concentrations in the fetal sheep and pregnant ewe during late gestation. Journal ofEndocrinology, 120, 459–464.Google Scholar
  106. McMillen, I. C., Kok, J. S. M., Adamson, T.M., Deayton, J. M., & Nowak, R. (1991). Development of circadian sleep-wake rhythms in preterm and full-term infants. Pediatric Research, 29, 381–384.PubMedGoogle Scholar
  107. Miller, J. D., Morin, L. P., Schwartz, F.J., & Moore, R. Y. (1996). New insights into the mammalian circadian clock. Sleep, 19, 641–667.PubMedGoogle Scholar
  108. Miller, M. W. (1992). Circadian rhythm of cell proliferation in the telencephalic ventricular zone: Effect of in utero exposure to ethanol. Brain Research, 595, 17–24.PubMedGoogle Scholar
  109. Mirmiran, M., & Kok, J. H. (1991). Circadian rhythms in early human development. Early Human Development, 26, 121–128.PubMedGoogle Scholar
  110. Moore, R. Y. (1973). Retinohypothalamic projection in mammals: A comparative study. Brain Research, 49, 403–409.PubMedGoogle Scholar
  111. Moore, R. Y., & Bernstein, M. E. (1989). Synaptogenesis in the rat suprachiasmatic nucleus demonstrated by electron microscopy and synapsin I immunoreactivity. Journal of Neuroscience, 9, 2151–2162.PubMedGoogle Scholar
  112. Moore, R. Y., & Lenn, N. J. (1972). A retinohypothalamic projection in the rat. Journal of Comparative Neurology, 146, 1–14.PubMedGoogle Scholar
  113. Moore, R. Y., Speh, J. C., & Card, J. P. (1995). The retinohypothalamic tract originates from a distinct subset of retinal ganglion cells. Journal of Comparative Neurology, 352, 351–366.PubMedGoogle Scholar
  114. Morin, L. P. (1994). The circadian visual system. Brain Research Reviews, 19, 102–127.PubMedGoogle Scholar
  115. Mosko, S., & Moore, R. Y. (1978). Neonatal suprachiasmatic nucleus ablation: Absence of functional and morphological plasticity. Proceedings of the National Academy of Sciences of the USA, 75, 6243–6246.PubMedGoogle Scholar
  116. Mosko, S., & Moore, R. Y. (1979). Retinohypothalamic tract development: Alteration by suprachiasmatic lesions in the neonatal rat. Brain Research, 164, 1–15.Google Scholar
  117. Niimi, K, Harada, I., Kusaka, Y., & Kishi, S. (1962). The ontogenetic development of the diencephalon of the mouse. Tokushima Journal of Experimental Medicine, 8, 203–238.Google Scholar
  118. Ninkina, N. N. (1995). Nerve growth factor-regulated properties of sensory neurones in Oct-2 null mutant mice. Molecular Brain Research, 33, 233–244.PubMedGoogle Scholar
  119. Noguchi, T., Sugisaki, T., Kudo, M., & Satoh, I. (1986). Retarded growth of the suprachiasmatic nucleus and pineal body in dw and lit dwarf mice. Developmental Brain Research, 26, 161–172.Google Scholar
  120. Nuesslein, B., & Schmidt, I. (1990). Development of circadian cycle of core temperature in juvenile rats. American Journal of Physiology, 259, R270–R276.PubMedGoogle Scholar
  121. Nuesslein-Hildesheim, B., & Schmidt, I. (1996). Manipulation of potential perinatal zeitgebers for the juvenile circadian temperature rhythm in rats. American Journal of Physiology, 271, R1388–R1395.PubMedGoogle Scholar
  122. Nurminen, T. (1989). Shift work, fetal development and course of pregnancy. Scandinavian Journal of Work and Environmental Health, 15, 395–403.Google Scholar
  123. Okamura, H., Fukui, K, Koyama, E., Tsutou, H. L. O., Tsutou, T., Terubayashi, H., Fujisawa, H., & Ibata, Y. (1983). Time of vasopressin neuron origin in the mouse hypothalamus: Examination by combined technique of immunocytochemistry and [3H]thymidine autoradiography. Developmental Brain Research, 9, 223–226.Google Scholar
  124. Parmelee, A. H., Wenner, W. H., & Schulz, H. R. (1964). Infant sleep patterns: From birth to 16 weeks of age. Journal of Pediatrics, 65, 576–582.PubMedGoogle Scholar
  125. Patrick, J., Campbell, K, Carmichael, L., Natale, R., & Richardson, B. (1981). Daily relationships between fetal and maternal heart rates at 38 to 40 weeks of pregnancy. CMA Journal, 124, 1177–1178.Google Scholar
  126. Patrick, J., Campbell, K., Carmichael, L., Natale, R., & Richardson, B. (1982a). Patterns of gross fetal bodymovements over 24-hour observation intervals during the last 10 weeks of pregnancy. American Journal of Obstetrics and Gynecology, 142, 363–371.PubMedGoogle Scholar
  127. Patrick, J., Campbell, K., Carmichael, L., & Probert, C. (1982b). Influence of maternal heart rate and gross fetal body movements on the daily pattern of fetal heart rate near term. American Journal of Obstetrics and Gynecology, 144, 533–538.PubMedGoogle Scholar
  128. Pickard, G. E. (1980). Morphological characteristics of retinal ganglion cells projecting to the supra-chiasmatic nucleus: A horseradish peroxidase study. Brain Research, 183, 458–465.PubMedGoogle Scholar
  129. Pittendrigh, C. S. (1954). On temperature independence in the clock system controlling emergence timein Drosophila. Proceedings of the National Academy of Sciences of the USA, 40, 1018–1029.PubMedGoogle Scholar
  130. Pollak, C. P. (1994). Regulation of sleep rate and circadian consolidation of sleep and wakefulness in aninfant. Sleep, 17, 567–575.PubMedGoogle Scholar
  131. Provencio, I., Wong, S., Lederman, A. B., Argamaso, S. M., & Foster, R. G. (1994). Visual and circadianresponses to light in aged retinally degenerate mice. Vision Research, 34, 1799–1806.PubMedGoogle Scholar
  132. Redman, J., Armstrong, S., & Ng, K. T. (1983). Free-running activity rhythms in the rat: Entrainment by melatonin. Science, 219, 1089–1091.PubMedGoogle Scholar
  133. Reh, T. A. (1992). Generation of neuronal diversity in the vertebrate retina. In Determinants of neural identity (pp. 433–467). New York: Academic Press.Google Scholar
  134. Reppert, S. M., & Klein, D. C. (1978). Transport of maternal [3H] melatonin to suckling rats and the fate of [3H]melatonin in the neonatal rat. Endocrinology, 102, 582–588.PubMedGoogle Scholar
  135. Reppert, S. M., & Schwartz, W. J. (1983). Maternal coordination of the fetal biological clock in utero. Science, 220, 969–971.PubMedGoogle Scholar
  136. Reppert, S. M., & Schwartz, W. J. (1984). Functional activity of the suprachiasmatic nuclei in the fetal primate. Neuroscience Letters, 46, 145–149.PubMedGoogle Scholar
  137. Reppert, S. M., & Schwartz, W. J. (1986). Maternal suprachiasmatic nuclei are necessary for maternal coordination of the developing circadian system. Journal of Neuroscience, 6, 2724–2729.PubMedGoogle Scholar
  138. Reppert, S. M. & Uhl, G. R. (1987). Vasopressin messenger ribonucleic acid in supraoptic and suprachiasmatic nuclei: Appearance and circadian regulation during development. Endocrinology, 120, 2483–2487.PubMedGoogle Scholar
  139. Reppert, S. M., Shea, R. A., Anderson, A., & Klein, D. C. (1979). Maternal-fetal transfer of melatonin in a non-human primate. Pediatric Research, 13, 788–791.PubMedGoogle Scholar
  140. Reppert, S. M., Coleman, R. J., Heath, H. W., & Swedlow, J. R. (1984). Pineal N-acetyltransferase activity in 10-day-old rats: A paradigm for studying the developing circadian system. Endocrinology, 115, 918–925.PubMedGoogle Scholar
  141. Reppert, S. M., Henshaw, D., Schwartz, W. J., & Weaver, D. R. (1987). The circadian-gated timing of birth in rats: Disruption by maternal SCN lesions or by removal of the fetal brain. Brain Research, 403, 398–402.PubMedGoogle Scholar
  142. Reppert, S. M., Weaver, D. R., Rivkees, S. A., & Stopa, E. G. (1988). Putative melatonin receptors in a human biological clock. Science, 242, 78–84.PubMedGoogle Scholar
  143. Rivkees, S. A., & Reppert, S. M. (1990). Entrainment of circadian phase in developing gray short-tailed opossums: Mother vs. environment. American Journal of Physiology, 259, E384–E388.PubMedGoogle Scholar
  144. Rivkees, S. A. & Reppert, S. M. (1991). Appearance of melatonin receptors during embryonic life in Siberian hamsters (Phodopus sungorous). Brain Research, 568, 345–349.PubMedGoogle Scholar
  145. Rivkees, S. A., Weaver, D. R., & Reppert, S. M. (1992). Circadian and developmental regulation of Oct-2 gene expression in the suprachiasmatic nuclei. Brain Research, 598, 332–336.PubMedGoogle Scholar
  146. Rivkees, S. A., Hofman, P. L., & Fortman, J. (1997). Newborn primate infants are entrained by low intensity lighting. Proceedings of National Academy of Sciences of the USA, 94, 292–297.Google Scholar
  147. Rivkees, S. A., Fox, C. A., Jacobsen, C. D., & Reppert, S. M. (1988). Anatomic and functional development of the suprachiasmatic nuclei in the gray short-tailed opposum. Journal of Neuroscience, 8, 4269–4276.PubMedGoogle Scholar
  148. Robinson, M. L. & Fuchs, J. L. (1993). [1251]Vasoactive intestinal peptide binding in rodent supra-chiasmatic nucleus: Developmental and circadian studies. Brain Research, 605, 271–279.PubMedGoogle Scholar
  149. Roca, A. L., Godson, C., Weaver, D. R., & Reppert, S. M. (1996). Structure, characterization, and expression of the gene encoding the mouse Mella melatonin receptor. Endocrinology, 137, 3469–3477.PubMedGoogle Scholar
  150. Romero, M.-T., & Silver, R. (1990). Time course of peptidergic expression in fetal suprachiasmatic nucleus transplanted into adult hamster. Developmental Brain Research, 57, 1–6.PubMedGoogle Scholar
  151. Salzarulo, P., Fagioli, I., & Ricour, C. (1985). Long term continuously fed infants do not develop heart rate circadian rhythm. Early Human Development, 12, 285–289.PubMedGoogle Scholar
  152. Sauerbier, I. (1986). Circadian variation in teratogenic response to dexamethasone in mice. Drug and Chemical Toxicology, 9, 25–31.PubMedGoogle Scholar
  153. Sauerbier, I. (1987). Circadian modification of ethanol damage in utero to mice. American Journal of Anatomy, 178, 170–174.PubMedGoogle Scholar
  154. Scheuch, G. C., & Silver, J. (1982). Ontogeny of the suprachiasmatic nuclei in genetically anopthalmic mice: Anatomical and behavioral studies. In D. C. Klein (Ed.), Melatonin rhythm generating system: Developmental aspects (pp. 20–41). Basel: Karger.Google Scholar
  155. Sengelaub, D. R., & Finlay, B. L. (1982). Cell death in the mammalian visual system during normal development: I. Retinal ganglion cells. Journal of Comparative Neurology, 204, 311–317.PubMedGoogle Scholar
  156. Serón-Ferré, M., Ducsay, C. A., Sc Valenzuela, G. J. (1993). Circadian rhythms during pregnancy. Endocrine Reviews, 14, 594–609.PubMedGoogle Scholar
  157. Shaw, D., & Goldman, B. D. (1995). Gender differences in influence of prenatal photoperiods on postnatal pineal melatonin rhythms and serum prolactin and follicle-stimulating hormone in the Siberian hamster (Phodopus sungorus). Endocrinology, 136, 4237–4246.PubMedGoogle Scholar
  158. Shibata, S., & Moore, R. Y. (1987). Development of neuronal activity in the rat suprachiasmatic nucleus. Developmental Brain Research, 34, 311–315.Google Scholar
  159. Shibata, S., & Moore, R. Y. (1988). Development of a fetal circadian rhythm after disruption of the maternal circadian system. Developmental Brain Research, 41, 313–317.Google Scholar
  160. Shimada, M., & Nakamura, T. (1973). Time of neuron origin in mouse hypothalamic nuclei. Experimental Neurology, 41, 163–173.PubMedGoogle Scholar
  161. Silver, J. (1977). Abnormal development of the suprachiasmatic nuclei of the hypothalamus in a strain of genetically anophthalmic mice. Journal of Comparative Neurology, 176, 589–606.PubMedGoogle Scholar
  162. Silver, R., Lehman, M. N., Gibson, M., Gladstone, W. R., & Bittman, E. L. (1990). Dispersed cell suspensions of fetal SCN restore circadian rhythmicity in SCN-lesioned adult hamsters. Brain Research, 525, 45–58.PubMedGoogle Scholar
  163. Silver, R., LeSauter, J., Tresco, P. A., & Lehman, M. N. (1996). A diffusible coupling signal from the transplanted suprachiasmatic nucleus controlling circadian locomotor rhythms. Nature, 382, 810–813.PubMedGoogle Scholar
  164. Sitka, U., Weinert, D., Berle, K., Rumler, W., & Schuh, J. (1994). Investigations of the rhythmic function of heart rate, blood pressure and temperature in neonates. European Journal of Pediatrics, 153, 117–122.PubMedGoogle Scholar
  165. Spangler, G. (1991). The emergence of adrenocortical circadian function in newborns and infants and its relationship to sleep, feeding and material adrenocortical activity. Early Human Development, 25, 197–208.PubMedGoogle Scholar
  166. Speh, J. C., & Moore, R. Y. (1993). Retinohypothalamic tract development in the hamster and rat. Developmental Brain Research, 76, 171–181.PubMedGoogle Scholar
  167. Stanfield, B., & Cowan, W. M. (1976). Evidence for a change in the retino-hypothalamic projection in the rat following early removal of one eye. Brain Research, 104, 129–136.PubMedGoogle Scholar
  168. Stark, R. I., & Daniel, S. S. (1989). Circadian rhythm of vasopressin levels in cerebrospinal fluid of the fetus: Effect of continuous light. Endocrinology, 124, 3095–3101.PubMedGoogle Scholar
  169. Stetson, M. H., Elliott, J. A., & Goldman, B. D. (1986). Maternal transfer of photoperiodic information influences the photoperiodic response of prepubertal djungarian hamsters. Biology of Reproduction, 34, 664–669.PubMedGoogle Scholar
  170. Swaab, D. F., Zhou, J. N., Ehlhart, T., & Hofman, M. A. (1994). Development of vasoactive intestinal polypeptide neurons in the human suprachiasmatic nucleus in relation to birth and sex. Developmental Brain Research, 79, 249–259.PubMedGoogle Scholar
  171. Swanson, L. W. (1987). The hypothalamus. In A. Björkland, T. Hökfelt, & L. W. Swanson (Eds.),Handbook of chemical neuroanatomy, Vol. 5: Integrated systems of the CNS, (Part I, pp. 1–124). Amsterdam: Elsevier.Google Scholar
  172. Takahashi, K., & Deguchi, T. (1983). Entrainment of the circadian rhythms of blinded infant rats by nursing mothers. Physiology and Behavior, 31, 373–378.PubMedGoogle Scholar
  173. Takahashi, K, Hayafuji, C., & Murakami, N. (1982). Foster mother rat entrains circadian adrenocortical rhythm in blinded pups. American Journal of Physiology, 243, 443–449.Google Scholar
  174. Takahashi, K., Ohi, K, Shimoda, K., Tamada, N., & Hayashi, S. (1989). Postnatal maternal entrainment of circadian rhythms. In S. M. Reppert (Ed.), Development of circadian rhythmicity and photoperiodism in mammals (pp. 67–82). Ithaca, NY: Perinatology Press.Google Scholar
  175. Tamarkin, L., Westrom, W. K., Hamill, A. I., & Goldman, B. D. (1976). Effect of melatonin on the reproductive systems of male and female Syrian hamsters: A diurnal rhythm in sensitivity to melatonin. Endocrinology, 99, 1534–1541.PubMedGoogle Scholar
  176. Tenreiro, S., Dowse, H. B., D’Souza, S., Minors, D., Chiswick, M., Simms, D., & Waterhouse, J. (1991). The development of ultradian and circadain rhythms in premature babies maintained in constant conditions. Early Human Development, 27, 33–52.PubMedGoogle Scholar
  177. Terman, J. S., Remé, C. E., & Terman, M. (1993). Rod outer segment disk shedding in rats with lesions of the suprachiasmatic nucleus. Brain Research, 605, 256–264.PubMedGoogle Scholar
  178. Tominaga, K, Inouye, S.-I. T., & Okamura, H. (1994). Organotypic slice culture of the rat suprachiasmatic nucleus: Sustenance of cellular architecture and circadian rhythm. Neuroscience, 59, 1025–1042.PubMedGoogle Scholar
  179. Tosini, G. & Menaker, M. (1996). Circadian rhythms in cultured mammalian retina. Science, 272, 419–421.PubMedGoogle Scholar
  180. Treep, J. A., Abe, H., Rusak, B., & Goguen, D. M. (1995). Two distinct retinal projections to the hamster suprachiasmatic nucleus. Journal of Biological Rhythms, 10, 299–307.PubMedGoogle Scholar
  181. Ugrumov, M. V., Popov, A. P., Vladimirov, S. V., Kasmambetova, S., Novodjilova, A. P., & Tramu, G. (1994a). Development of the suprachiasmatic nucleus in rats during ontogenesis: Serotoninimmunopositive fibers. Neuroscience, 58, 161–165.PubMedGoogle Scholar
  182. Ugrumov, M. V., Popov, A. P., Vladimirov, S. V., Kasmambetova, S., & Thibault, J. (1994b). Development of the suprachiasmatic nucleus in rats during ontogenesis: Tyrosine hydroxylase immunopositive cell bodies and fibers. Neuroscience, 58, 151–160.PubMedGoogle Scholar
  183. Ugrumov, M. V., Trembleau, A., & Calas, A. (1994c). Altered vasoactive intestinal polypeptide gene expression in the fetal rat suprachiasmatic nucleus following prenatal serotonin deficiency. International Journal of Developmental Neuroscience, 12, 143–149.PubMedGoogle Scholar
  184. Updike, P. A., Accurso, F. J., & Jones, R. H. (1985). Physiologic ciradian rhythmicity in preterm infants. Nursing Research, 34, 160–163.PubMedGoogle Scholar
  185. Van den Pol, A. N. & Tsujimoto, K. L. (1985). Neurotransmitters of the hypothalamic suprachiasmatic nucleus: immunocytochemical analysis of 25 neuronal antigens. Neuroscience, 15, 1049–1086.PubMedGoogle Scholar
  186. Visser, G. H. A., Goodman, J. D. S., Levine, D. H., & Dawes, G. S. (1982). Diurnal and other cyclic varia-tions in human fetal heart rate near term. American Journal of Obstetrics and Gynecology, 142, 535–544.PubMedGoogle Scholar
  187. Viswanathan, N. (1989). Presence—absence cycles of the mother and not light—darkness are the zeitgeber for the circadian rhythm of newborn mice. Experientia, 45, 383–385.Google Scholar
  188. Viswanathan, N. (1990). Role of relative durations of presence/absence of mother mouse (Mus booduga) in circadian rhythm of pups. Current Science, 59, 409–411.Google Scholar
  189. Viswanathan, N., & Chandrashekaran, M. K. (1985). Cycles of presence and absence of mother mouse entrain the circadian clock of pups. Nature, 317, 530–531.PubMedGoogle Scholar
  190. Viswanathan, N., & Davis, F. C. (1993). The fetal circadian pacemaker is not involved in the timing of birth in hamsters. Biology of Reproduction, 48, 530–537.PubMedGoogle Scholar
  191. Viswanathan, N., & Davis, F. C. (1995). Suprachiasmatic nucleus grafts restore circadian function in aged hamsters. Brain Research, 686, 10–16.PubMedGoogle Scholar
  192. Viswanathan, N., & Davis, F. C. (1997). Single prenatal injections of melatonin or the Dl-dopamine receptor agonist SKF 38393 to pregnant hamsters sets the offsprings’ circadian rhythms to phases 180§ apart. Journal of Comparative Physiology A, 180, 339–346.Google Scholar
  193. Viswanathan, N., Weaver, D. R., Reppert, S. M., & Davis, F. C. (1994). Entrainment of the fetal hamster circadian pacemaker by prenatal injections of the dopamine agonist, SKF 38393. Journal of Neuroscience, 14, 5393–5398.PubMedGoogle Scholar
  194. Vitaterna, M. H., King, D. P., Chang, A.M., Kornhauser, J. M., Lowrey, P. L., McDonald, J. D., Dove, W. F., Pinto, L. H., Turek, E W., & Takahashi, J. S. (1994). Mutagenesis and mapping of a mouse gene, clock, essential for circadian behavior. Science, 264, 719–725.PubMedGoogle Scholar
  195. Weaver, D. R., & Reppert, S. M. (1995). Definition of the developmental transition from dopaminergic to photic regulation of c-fos gene expression in the rat suprachiasmatic nucleus. Molecular Brain Research, 33, 136–148.PubMedGoogle Scholar
  196. Weaver, D. R., & Reppert, S. M. (1986). Maternal melatonin communicates daylength to the fetus in djungarian hamsters. Endocrinology, 119, 2861–2863.PubMedGoogle Scholar
  197. Weaver, D. R., & Reppert, S. M. (1987). Maternal—fetal communication of circadian phase in a precocious rodent, the spiny mouse. American Journal of Physiology, 253, E401—E409.PubMedGoogle Scholar
  198. Weaver, D. R. & Reppert, S. M. (1989a). Periodic feeding of SCN-lesioned pregnant rats entrains the fetal biological clock. Developmental Brain Research, 46, 291–296.PubMedGoogle Scholar
  199. Weaver, D. R. & Reppert, S. M. (1989b). Direct in utero perception of light by the mammalian fetus. Developmental Brain Research, 47, 151–155.PubMedGoogle Scholar
  200. Weaver, D. R., Keohan, J. T., & Reppert, S. M. (1987). Definition of a prenatal sensitive period for maternal—fetal communication of day length. American Journal of Physiology, 253, E701—E704.PubMedGoogle Scholar
  201. Weaver, D. R., Rivkees, S. A., & Reppert, S. M. (1989). Localization and characterization of melatonin receptors in rodent brain by in vitro autoradiography. Journal of Neuroscience, 9, 2581–2590.PubMedGoogle Scholar
  202. Weaver, D. R., Rivkees, S. A., & Reppert, S. M. (1992). Dl-dopamine receptors activate c-fos expression in the fetal suprachiasmatic nuclei. Proceedings of National Academy of Sciences of the USA, 89, 9201–9204.Google Scholar
  203. Weaver, D. R., Roca, A. L., & Reppert, S. M. (1995). c-fos and jun-B mRNAs are transiently expressed infetal rodent suprachiasmatic nucleus following dopaminergic stimulation. Developmental Brain Re-search, 85, 293–297.Google Scholar
  204. Weinert, D., Sitka, U., Minors, D. S., & Waterhouse, J. M. (1994). The development of circadian rhythmicity in neonates. Early Human Development, 36, 117–126.PubMedGoogle Scholar
  205. Welsh, D. K., Logothetis, D. E., Meister, M., & Reppert, S. M. (1995). Individual neurons dissociated from rat suprachiasmatic nucleus express independently phased circadian firing rhythms. Neuron, 14, 697–706.PubMedGoogle Scholar
  206. Weyer, R. A. (1984). Sex differences in human circadian rhythms: Intrinsic periods and sleep fractions. Experientia, 40, 1226–1234.Google Scholar
  207. Whitnall, M. H., Key, S., Ben-Barak, Y., Ozato, K., & Gainer, H. (1985). Neurophysin in the hypothalamoneurohypophysial system. Journal of Neuroscience, 5, 98–109.PubMedGoogle Scholar
  208. Wiegand, S. J., & Gash, D. M. (1988). Organization and efferent connections of transplanted suprachiasmatic nuclei. Journal of Comparative Neurology, 267, 562–579.PubMedGoogle Scholar
  209. Williams, L. M., Martinoli, M. G., Titchener, L. T., & Pelletier, G. (1991). The ontogeny of central melatonin binding sites in the rat. Endocrinology, 128, 2083–2090.PubMedGoogle Scholar
  210. Wray, S., Castel, M., & Gainer, H. (1993). Characterization of the suprachiasmatic nucleus in organotypic slice explant cultures. Microscopy Research and Technique, 25, 46–60.PubMedGoogle Scholar
  211. Yellon, S. M., & Longo, L. D. (1988). Effect of maternal pinealectomy and reverse photoperiod on the circadian melatonin rhythm in the sheep and fetus during the last trimester of pregnancy. Biology of Reproduction, 39, 1093–1099.PubMedGoogle Scholar
  212. Zucker, I., Fitzgerald, K. M., & Morin, L. P. (1980). Sex differentiation of the circadian system in the golden hamster. American Journal of Physiology, 238, R97—R101.PubMedGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2001

Authors and Affiliations

  • Fred C. Davis
    • 1
  • Steven M. Reppert
    • 2
  1. 1.Department of BiologyNortheastern UniversityBoston
  2. 2.Laboratory of Developmental Chronobiology, Children’s ServiceMassachusetts General Hospital, Harvard Medical SchoolBoston

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