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.
Access this chapter
Tax calculation will be finalised at checkout
Purchases are for personal use only
Preview
Unable to display preview. Download preview PDF.
Similar content being viewed by others
References
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.
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.
Altman, J., & Bayer, S. A. (1986). The development of the rat hypothalamus. Advances in Anatomy Embryology and Cell Biology, 100, 1–178.
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.
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.
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.
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.
Armstrong, S. M. (1989). Melatonin and circadian control in mammals Experientia, 45, 933–938.
Aschoff, J. (1960). Exogenous and endogenous components in circadian rhythms. Cold Spring Harbor Symposium on Quantitative Biology, 25, 11–28.
Aschoff, J., Gerecke, U., & Weyer, R. (1967). Desynchronization of human circadian rhythms. Japanese Journal of Physiology, 17, 450–457.
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.
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.
Barr, M. J. (1973). Prenatal growth of wistar rats: Circadian periodicity of fetal growth late in gestation. Teratology, 7, 283–287.
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.
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.
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.
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.
Cambras, T., & Diez-Noguera, A. (1991). Evolution of rat motor activity circadian rhythm under three different light patterns. Physiology and Behavior, 49, 63–68.
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.
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.
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.
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.
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.
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.
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.
Cooper, Z. K. (1939). Mitotic rhythm in human epidermis. Journal oflnvestigativeDermatology, 2, 289–300.
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.
Darwin, C. (1896). The power of movement in plants. New York: Appleton.
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.
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: Karger
Davis, F. C. (1989). Daily variation in maternal and fetal weight gain in mice and hamsters. Journal of Experimental Zoology, 250, 273–282.
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.
Davis, F. C., & Gorski, R. A. (1986). Development of hamster circadian rhythms: Prenatal entrainment of the pacemaker. Journal of Biological Rhythms, 1, 77–89.
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.
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.
Davis, F. C., & Menaker, M. (1981). Development of the mouse circadian pacemaker: Independence from environmental cycles. Journal of Comparative Physiology A, 143, 527–539.
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.
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.
Davis, F. C., Boada, R., & LeDeaux, J. (1990). Neurogenesis of the hamster suprachiasmatic nucleus. Brain Research, 519, 192–199.
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.
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.
Decavel, C., & Van den Pol, A. N. (1990). GABA: A dominant neurotransmitter in the hypothalamus. Journal of Comparative Neurology, 302, 1019–1037.
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.
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.
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.
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.
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.
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.
Duncan, M. J., Banister, M. J., & Reppert, S. M. (1986). Developmental appearance of light-dark entrainment in the rat. Brain Research, 369, 326–330.
Ehrstrom, C. (1984). Circadian rhythm of fetal movements. Acta Obstetrica et Gynecologica Scandinavica, 63, 539–541.
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.
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.
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.
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.
Ganzhorn, J. U., & Wright, P. C. (1994). Temporal patterns in primate leaf eating: The possible role of leaf chemistry. Folia Primatologica, 63, 203–208.
Gibson, A. A. M. (1992). Current epidemiology of SIDS. Journal of Clinical Pathology, 45 (Supplement), 7–10.
Glotzbach, S. T., Sollars, P., Ariagno, R. L., & Pickard, G. E. (1992). Development of the human retinohypothalamic tract. Society for Neuroscience Abstracts, 18, 875.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
Hoffman, K. (1959). Die aktivitatsperiodik von im 18- und 36-stunden-tag erfruteten eidechsen. Zeitschriftfur vergleichende Physiologie, 42, 422–432.
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.
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.
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 Press
Horton, T. H. (1983). Growth and maturation in Microtus montanus: Effects of photoperiods before and after weaning. Canadian Journal of Zoology, 62, 1741–1746.
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 Press
Ibuka, N. (1987). Circadian rhythms in sleep-wakefullness and wheel-running activity in a congenitally anophthalmic rat mutant. Physiology and Behavior, 39, 321–326.
Illnerovã, H., Buresovã, M., & Presl, J. (1993). Melatonin rhythm in human milk. Journal of Clinical Endocrinology and Metabolism, 77, 838–841.
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.
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.
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.
Jilge, B. (1993). The ontogeny of circadian rhythms in the rabbit. Journal of Biological Rhythms, 8, 247–260.
Jilge, B. (1995). Ontogeny of the rabbit’s circadian rhythms without an external zeitgeber. Physiology and Behavior, 58, 131–140.
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.
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.
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.
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.
Kaufman, C. M., & Menaker, M. (1994). Ontogeny of light-induced Fos-like immunoreactivity in the hamster suprachiasmatic nucleus. Brain Research, 633, 162–166.
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.
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.
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.
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.
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.
Krieger, D. T. (1972). Circadian corticosteroid periodicity: Critical period for abolition by neonatal injection of corticosteroid. Science, 178, 1205–1207.
Krieger, D. T., & Hauser, H. (1977). Suprachiasmatic nuclear lesions do not abolish food-shifted circadian adrenal and temperature rhythmicity. Science, 197, 398–399.
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.
Laemle, L. K., & Rusa, R. (1992). VIP-like immunoreactivity in the suprachiasmatic nuclei of a mutant anophthalmic mouse. Brain Research, 589, 124–128.
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.
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.
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.
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.
LeSauter, J., Lehman, M. N., & Silver, R. (1996). Restoration of circadian rhythmicity by transplants of SCN “micropunches.” Journal of Biological Rhythms, 11, 163–171.
Lewy, A. J. (1992). Melatonin shifts human circadian rhythms according to a phase-response curve. Chronobiology International, 9, 380–392.
Magnin, M., Cooper, H. M., & Mick, G. (1989). Retinohypothalamic pathway: A breach in the law of Newton-Muller-Gudden? Brain Research, 488, 390–397.
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.
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.
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.
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.
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.
Miller, J. D., Morin, L. P., Schwartz, F.J., & Moore, R. Y. (1996). New insights into the mammalian circadian clock. Sleep, 19, 641–667.
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.
Mirmiran, M., & Kok, J. H. (1991). Circadian rhythms in early human development. Early Human Development, 26, 121–128.
Moore, R. Y. (1973). Retinohypothalamic projection in mammals: A comparative study. Brain Research, 49, 403–409.
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.
Moore, R. Y., & Lenn, N. J. (1972). A retinohypothalamic projection in the rat. Journal of Comparative Neurology, 146, 1–14.
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.
Morin, L. P. (1994). The circadian visual system. Brain Research Reviews, 19, 102–127.
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.
Mosko, S., & Moore, R. Y. (1979). Retinohypothalamic tract development: Alteration by suprachiasmatic lesions in the neonatal rat. Brain Research, 164, 1–15.
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.
Ninkina, N. N. (1995). Nerve growth factor-regulated properties of sensory neurones in Oct-2 null mutant mice. Molecular Brain Research, 33, 233–244.
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.
Nuesslein, B., & Schmidt, I. (1990). Development of circadian cycle of core temperature in juvenile rats. American Journal of Physiology, 259, R270–R276.
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.
Nurminen, T. (1989). Shift work, fetal development and course of pregnancy. Scandinavian Journal of Work and Environmental Health, 15, 395–403.
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.
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.
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.
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.
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.
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.
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.
Pollak, C. P. (1994). Regulation of sleep rate and circadian consolidation of sleep and wakefulness in aninfant. Sleep, 17, 567–575.
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.
Redman, J., Armstrong, S., & Ng, K. T. (1983). Free-running activity rhythms in the rat: Entrainment by melatonin. Science, 219, 1089–1091.
Reh, T. A. (1992). Generation of neuronal diversity in the vertebrate retina. In Determinants of neural identity (pp. 433–467). New York: Academic Press.
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.
Reppert, S. M., & Schwartz, W. J. (1983). Maternal coordination of the fetal biological clock in utero. Science, 220, 969–971.
Reppert, S. M., & Schwartz, W. J. (1984). Functional activity of the suprachiasmatic nuclei in the fetal primate. Neuroscience Letters, 46, 145–149.
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.
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.
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.
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.
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.
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.
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.
Rivkees, S. A. & Reppert, S. M. (1991). Appearance of melatonin receptors during embryonic life in Siberian hamsters (Phodopus sungorous). Brain Research, 568, 345–349.
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.
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.
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.
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.
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.
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.
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.
Sauerbier, I. (1986). Circadian variation in teratogenic response to dexamethasone in mice. Drug and Chemical Toxicology, 9, 25–31.
Sauerbier, I. (1987). Circadian modification of ethanol damage in utero to mice. American Journal of Anatomy, 178, 170–174.
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.
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.
Serón-Ferré, M., Ducsay, C. A., Sc Valenzuela, G. J. (1993). Circadian rhythms during pregnancy. Endocrine Reviews, 14, 594–609.
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.
Shibata, S., & Moore, R. Y. (1987). Development of neuronal activity in the rat suprachiasmatic nucleus. Developmental Brain Research, 34, 311–315.
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.
Shimada, M., & Nakamura, T. (1973). Time of neuron origin in mouse hypothalamic nuclei. Experimental Neurology, 41, 163–173.
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.
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.
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.
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.
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.
Speh, J. C., & Moore, R. Y. (1993). Retinohypothalamic tract development in the hamster and rat. Developmental Brain Research, 76, 171–181.
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.
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.
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.
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.
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.
Takahashi, K., & Deguchi, T. (1983). Entrainment of the circadian rhythms of blinded infant rats by nursing mothers. Physiology and Behavior, 31, 373–378.
Takahashi, K, Hayafuji, C., & Murakami, N. (1982). Foster mother rat entrains circadian adrenocortical rhythm in blinded pups. American Journal of Physiology, 243, 443–449.
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.
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.
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.
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.
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.
Tosini, G. & Menaker, M. (1996). Circadian rhythms in cultured mammalian retina. Science, 272, 419–421.
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.
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.
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.
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.
Updike, P. A., Accurso, F. J., & Jones, R. H. (1985). Physiologic ciradian rhythmicity in preterm infants. Nursing Research, 34, 160–163.
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.
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.
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.
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.
Viswanathan, N., & Chandrashekaran, M. K. (1985). Cycles of presence and absence of mother mouse entrain the circadian clock of pups. Nature, 317, 530–531.
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.
Viswanathan, N., & Davis, F. C. (1995). Suprachiasmatic nucleus grafts restore circadian function in aged hamsters. Brain Research, 686, 10–16.
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.
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.
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.
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.
Weaver, D. R., & Reppert, S. M. (1986). Maternal melatonin communicates daylength to the fetus in djungarian hamsters. Endocrinology, 119, 2861–2863.
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.
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.
Weaver, D. R. & Reppert, S. M. (1989b). Direct in utero perception of light by the mammalian fetus. Developmental Brain Research, 47, 151–155.
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.
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.
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.
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.
Weinert, D., Sitka, U., Minors, D. S., & Waterhouse, J. M. (1994). The development of circadian rhythmicity in neonates. Early Human Development, 36, 117–126.
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.
Weyer, R. A. (1984). Sex differences in human circadian rhythms: Intrinsic periods and sleep fractions. Experientia, 40, 1226–1234.
Whitnall, M. H., Key, S., Ben-Barak, Y., Ozato, K., & Gainer, H. (1985). Neurophysin in the hypothalamoneurohypophysial system. Journal of Neuroscience, 5, 98–109.
Wiegand, S. J., & Gash, D. M. (1988). Organization and efferent connections of transplanted suprachiasmatic nuclei. Journal of Comparative Neurology, 267, 562–579.
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.
Wray, S., Castel, M., & Gainer, H. (1993). Characterization of the suprachiasmatic nucleus in organotypic slice explant cultures. Microscopy Research and Technique, 25, 46–60.
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.
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.
Author information
Authors and Affiliations
Editor information
Editors and Affiliations
Rights and permissions
Copyright information
© 2001 Springer Science+Business Media New York
About this chapter
Cite this chapter
Davis, F.C., Reppert, S.M. (2001). Development of Mammalian Circadian Rhythms. In: Takahashi, J.S., Turek, F.W., Moore, R.Y. (eds) Circadian Clocks. Handbook of Behavioral Neurobiology, vol 12. Springer, Boston, MA. https://doi.org/10.1007/978-1-4615-1201-1_10
Download citation
DOI: https://doi.org/10.1007/978-1-4615-1201-1_10
Publisher Name: Springer, Boston, MA
Print ISBN: 978-1-4613-5438-3
Online ISBN: 978-1-4615-1201-1
eBook Packages: Springer Book Archive