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Imprinting and critical periods in early development

Published online by Cambridge University Press:  02 February 2007

B. TZSCHENTKE  and
A. PLAGEMANN
B. TZSCHENTKE*
Affiliation:
Humboldt-University of Berlin, Institute of Biology, Working Group Perinatal Adaptation, Philippstr. 13, 10115Berlin, Germany
A. PLAGEMANN
Affiliation:
Charité-University Medicine Berlin, Campus Virchow-Klinikum, Clinic of Obstetrics, Division of “Experimental Obstetrics”, Augustenburger Platz 1, 13353Berlin, Germany
*
*Corresponding author: barbara.tzschentke@rz.hu-berlin.de
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Abstract

The review addresses the fundamental process of ‘imprinting’. In his classical studies on newly hatched goslings Konrad Lorenz analysed the development of social binding and established the term ‘imprinting’ to describe this process. One of his major ideas was that imprinting occurs in ‘critical periods’, which are limited and severely restricted to the animal's very early life. For some time past, the term ‘imprinting’ is also used for an epigenetic mechanism, the ‘genomic imprinting’, which can be simply defined as gamete-of-origin dependent modification of genotype. Furthermore, in the course of the perinatal period ‘imprinting’ of physiological control systems occurs. Functional systems of the organism develop from open loop systems without feedback control into closed systems controlled by feedback mechanism. During ‘critical periods’, the actual environment influences the development of the respective physiological control systems for the entire life period, especially by changes in neuroorganization and expression of related effector genes. On the one hand, these mechanisms may cause perinatal malprogramming, which has been related to, e.g., metabolic disorders and cardiovascular diseases during later life in humans as well as in animals. On the other hand, knowledge on these mechanisms might be specifically used to induce long-term adaptation of the organism, for instance, to the postnatal climatic conditions (epigenetic temperature adaptation). Furthermore, the question if ‘critical period’ and ‘sensitive period’ are synonymous or different, and problems of identifying these developmental windows are discussed. Environmental manipulation of immature physiological mechanisms may be a physiological tool for characterization of ‘critical periods’.

Keywords

imprintingmalprogrammingcritical periodphysiological control systemepigenetic adaptation
Type
Review Article
Information
World's Poultry Science Journal , Volume 62 , Issue 4 , December 2006 , pp. 626 - 637
Copyright
Copyright © World's Poultry Science Association 2006

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Footnotes

1

This review based on a presentation on the “2nd Combined Workshop on Fundamental Physiology of the European Working Group of Physiology and Perinatal Development in Poultry”, which was held at the Institute of Biology, Humboldt-University of Berlin, Germany, from the 22nd to the 25th of September 2005.

References

BALDAUF, K., BRAUN, K. and GRUSS, M. (2005) Opiate modulation of monamines in the chick forebrain: possible role in emotional regulation? Journal of Neurobiology 62: 149–163.Google Scholar
BAILY, D.B. (2001) Critical Periods. Interview, March 2001, www.bookspublishing.comGoogle Scholar
BAILY, D.B., BRUER, J.T., SYMONS, F.J. and LICHTMAN, J.W. (2001) Critical thinking about critical periods. P H Brookes Publishing Co.Google Scholar
BARKER, D.J.P. (1995) Fetal origins of coronary heart diseases. British Medical Journal 311: 171–174.CrossRefGoogle Scholar
BARTESAGHI, R., RAFFI, M. and CIANI, E. (2006) Effect of early isolation on signal transfer in the entorhinal cortex-dentate-hippocampal system. Neuroscience 137: 875–890.Google Scholar
BOCK, J. and BRAUN, K. (1998) Differential emotional experience leads to pruning of dendritic spines in the forebrain of domestic chicks. Neural Plasticity 6: 17–27.CrossRefGoogle ScholarPubMed
BOCK, J. and BRAUN, K. (1999a) Blockade of N-methyl-D-aspartate receptor activation suppresses learninginduced synaptic elimination. Proceedings of the National Academy of Sciences USA 96: 2485–2490.CrossRefGoogle ScholarPubMed
BOCK, J. and BRAUN, K. (1999b) Filial imprinting in domestic chicks is associated with spine pruning in the associative area, dorsal neostriatum. European Journal of Neuroscience 11: 2566–2570.CrossRefGoogle Scholar
BOCK, J., HELMEKE, C., OVTSCHAROFF, W. JR., GRUSS, M. and BRAUN, K. (2003) Frühkindliche emotionale Erfahrungen beeinflussen die funktionelle Entwicklung des Gehirns. Neuroforum 2: 51–55.Google Scholar
BOCK, J., GRUSS, M., BECKER, S. and BRAUN, K. (2005a) Experience-induced changes of dendritic spine densities in the prefrontal and sensory cortex: correlation with developmental time windows. Cerebral Cortex 15: 802–808.Google Scholar
BOCK, J., THODE, C., HANNEMANN, O., BRAUN, K. and DARLISON, M.G. (2005b) Early socioemotional experience induces expression of the immediate-early gene ARC/ARG3.1 (activity-regulated cytoskeleton-associated protein/activity-regulated gene) in learning-relevant brain regions of the newborn chick. Neuroscience 133: 625–633.CrossRefGoogle ScholarPubMed
BROWN, M., KEYNES, R. and LUMSDEN, A. (2004) The developing brain. Oxford University Press.Google Scholar
BUYS, N., DEWIL, E., GONZALES, E. and DECUYPERE, E. (1998) Different CO2 levels during incubation interact with hatching time and ascites susceptibility in two broiler lines selected for different growth rate. Avian Pathology 27: 605–612.Google Scholar
DAMPNEY, R.A.L., HORIUCHI, J., KILLINGER, S., SHERIFF, M.J., TAN, P.S.P. and MCDOWALL, L.M. (2005) Long-term regulation of arterial blood pressure by hypothalamic nuclei: some critical questions. Clinical and Experimental Pharmacology and Physiology 32: 419–425.CrossRefGoogle ScholarPubMed
DAVIES, W., ISLES, A.R. and WILKINSON, L.S. (2005) Imprinted gene expression in the brain. Neuroscience and Biobehavioral Reviews 29: 421–430.CrossRefGoogle ScholarPubMed
DECUYPERE, E. (1984) Incubation temperature in relation to postnatal performance in chickens. Archiv für Experimentelle Veterinärmedizin 38: 439–449.Google Scholar
DÖRNER, G. (1974) Environment-dependent brain differentiation and fundamental processes of life. Acta Biologica and Medica Germanica 33: 129–148.Google ScholarPubMed
DÖRNER, G. (1975) Perinatal hormone levels and brain organization. Anatomical Neuroendocrinology 1: 245–252.Google Scholar
DÖRNER, G. (1976) Hormones and brain differentiation. Amsterdam: Elsevier.Google Scholar
DÖRNER, G. (2002) Possible teratogenic, neuroendocrine causes of sub- and infertility. Andrologia 34: 123–153.Google Scholar
DÖRNER, G., GÖTZ, F., ROHDE, W., PLAGEMANN, A., LINDNER, R., PETERS, H. and GHANAATI, Z. (2001) Genetic and epigenetic effects on sexual brain organization mediated by sex hormones. Neuroendocrinology Letters 22: 403–409.Google Scholar
DUNCAN, J.R., COCK, M.L., HARDING, R. and REES, S.M. (2000) Relation between damage to the placenta and the fetal brain after late-gestation placental embolization and fetal growth restriction in sheep. American Journal of Obstetrics and Gynaecology 183: 10113–1022.Google Scholar
FERGUSON-SMITH, A.C. and SURANI, M.A. (2001) Imprinting and the epigenetic asymmetry between parental genomes. Science 293: 1086–1089.Google Scholar
FERSTER, D. and LEVAY, S. (1978) The axonal arborizations of the lateral geniculate neurons in the striate cortex of the cat. Journal Comparative Neurology 182: 923–944.CrossRefGoogle ScholarPubMed
FURUYA, M., SASAKI, F., HASSANIN, A.M.A., KUWAHARA, S. and TSUKAMOTO, Y. (2002) Effects of bisphenol-A on the growth of comb and testes of male chicken. The Canadian Journal of Veterinary Research 67: 68–71.Google Scholar
HARWERTH, R.S., SMITH, E.L., DUNCAN, G.C., CRAWFORD, M.L. and VON NOORDEN, G.K. (1986) Multiple sensitive periods in the development of primate visual system. Science 232: 235–238.CrossRefGoogle ScholarPubMed
HASSANZADEH, M., FARD, M.H.B., BUYSE, J., BRUGGEMAN, V. and DECUYPERE, E. (2004) Effect of chronic hypoxia during embryonic development on physiological functioning and on hatching and posthatching parameters related to ascites syndrome in broiler chickens. Avian Pathology 33: 558–564.CrossRefGoogle ScholarPubMed
HUBEL, D.H. and WIESEL, T.N. (1977) Ferrier lectures: functional architecture of macaque monkey visual cortex. Proceedings of the Royal Society London (Biology) 198: 1–59.Google Scholar
JACOBS, R., ROBINSON, J.S., OWENS, J.A., FALCONER, J. and WEBSTER, M.E. (1988) The effect of prolonged hypobaric hypoxia on growth of fetal sheep. Journal of Developmental Physiology 10: 97–112.Google Scholar
KOSKI, L.B., SASAKI, E., ROBERTS, R.D., GIBSON, J. and ETCHES, R.J. (2000) Monoalleleic transcription of the insulin-like growth factor-II gene (Igf2) in chicken embryos. Molecular reproduction and development 56: 345–352.Google Scholar
KREPPNER, J.M., O′CONNOR, T.G. and RUTTER, M. (2001) Can inattention/overactivity be an institutional deprivation syndrome? Journal of Abnormal Child Psychology 29: 513–528.Google Scholar
LEVY, G., LUTZ, I., KRÜGER, A. and KLOAS, W. (2004) Bisphenol A induces feminization in Xenopus laevis tadpoles. Environmental Research 94: 102–111.CrossRefGoogle ScholarPubMed
LI, E. (2002) Chromatin modification and epigenetic reprogramming in mammalian development. Nature Reviews Genetics 3: 662–637.Google Scholar
LOH, B., MAIER, I., WINAR, A., JANKE, O. and TZSCHENTKE, B. (2004) Prenatal development of epigenetic adaptation processes in poultry: Changes in metabolic and neuronal thermoregulatory mechanisms. Avian & Poultry Biology Reviews 15: 119–128.CrossRefGoogle Scholar
LORENZ, K. (1935) Der Kumpan in der Umwelt des Vogels. Journal für Ornithologie 83: 137–213.Google Scholar
MINNE, B. and DECUYPERE, E. (1984) Effects of late prenatal temperatures on some thermoregulatory aspects in young chickens. Archiv für Experimentelle Veterinärmedizin 38: 374–383.Google Scholar
MOORE, T. and HAIG, D. (1991) Genomic imprinting in mammalian development: a parental tug-of-war. Trends in Genetics 7: 45–49.Google Scholar
NICHELMANN, M. and TZSCHENTKE, B. (1999) Thermoregulatory heat production in precocial avian embryos. Ornis Fennica 76: 177–187.Google Scholar
NICHELMANN, M. and TZSCHENTKE, B. (2003) Efficiency of thermoregulatory control elements in precocial avian embryos (Review). Avian & Poultry Biology Reviews 14: 1–19.CrossRefGoogle Scholar
NICHELMANN, M., LANGE, B., PIROW, R., LANGBEIN, J. and HERRMANN, S. (1994) Avian thermoregulation during the perinatal period. In: Thermal Balance in Health and Disease. Advances in Pharmacological Science, Zeisberger, E., Schönbaum, E., Lomax, P. (eds.) Birkhäuser Verlag, Basel, pp. 167–173.CrossRefGoogle Scholar
NICHELMANN, M., HÖCHEL, J. and TZSCHENTKE, B. (1999) Biological rhythms in birds –development, insights and perspectives. Comparative Biochemistry and Physiology 124A: 429–437.Google Scholar
NICHELMANN, M., JANKE, O., HÖCHEL, J. and TZSCHENTKE, B. (2001) Development of physiological control systems in avian embryos. News of Biomedical Science 1: 15–25.Google Scholar
NOLAN, C.M., KILLIAN, J.K., PETITTE, J.N. and JIRTLE, R.L. (2001) Imprint status of M6P/IGF2R and IGF2 in chickens. Development Genes Evolution 211: 179–183.Google Scholar
O'Neill, M.J., INGRAM, R.S., VRANA, P.B. and TILGHAM, S.M. (2000) Allelic expression of IGF2 in marsupials and birds. Development Genes Evolution 210: 18–20.Google Scholar
OVTSCHAROFF, W. JR. and BRAUN, K. (2001) Maternal separation and social isolation modulate the postnatal development of synaptic composition in the infralimbic cortex of Octodon degus. Neuroscience 104: 33–40.CrossRefGoogle ScholarPubMed
PAKDEL, A., VAN Arendonk, J.A., VEREIJKEN, A.L. and BOVENHUIS, H. (2002) Direct and maternal genetic effects for ascites-related traits in broilers. Poultry Science 81: 1273–1279.Google Scholar
PLAGEMANN, A. (2004) ‘Fetal Programming’ and ‘functional teratogenesis’: on epigenetic mechanisms and prevention of perinatally acquired lasting health risks. Journal of Perinatal Medicine 32: 297–305.CrossRefGoogle ScholarPubMed
RUITENBEEK, K., LE Noble, F.A.C., JANSSEN, G.M.J., KESSELS, C.G.A., FAZZI, G.E., BLANCO, C.E. and DE Mey, J.G.R. (2000) Chronic hypoxia stimulates periarterial sympathetic nerve development in the chicken embryo. Circulation 102: 2892–2897.Google Scholar
SCHWABL, H. (1996) Maternal testosterone in avian egg enhances postnatal growth. Comparative Biochemistry and Physiology 114A: 271–276.Google Scholar
SCHWABL, H. (1997) Maternal steroid hormones in the egg. In: Harvey, S., Etches, R.J. (eds.) Perspectives in avian endocrinology. Bristol; Society for Endocrinology, pp. 3–13.Google Scholar
SURANI, M.A. (1998) Imprinting and initiation of gene silencing in the germ line. Cell 93: 309–312.CrossRefGoogle ScholarPubMed
THODE, C., BOCK, J., BRAUN, K. and DARLISON, M.G. (2005) The chick immediate-early gene ZENK is expressed in the medio-rostral neostriatum/hyperstriatum ventrale, a brain region involved in acoustic imprinting, and is up-regulated after exposure to an auditory stimulus. Neuroscience 130: 611–617.CrossRefGoogle Scholar
TUISKULA-HAAVISTO, M., DE KONING, D.J., HONKATUKIA, M., SCHULMAN, N.F., MAKITANILA, A. and VILKKI, J. (2004) Quantitative trait loci with parent-of-origin effects in chicken. Genetic Research 84: 57–66.Google Scholar
TZSCHENTKE, B. (2002) Stimulate body functions of embryos and get them used to the post-hatch environment. World Poultry 10: 22–25.Google Scholar
TZSCHENTKE, B. and NICHELMANN, M. (1997) Influence of prenatal and postnatal acclimation on nervous and peripheral thermoregulation. Annals of the New York Academy of Sciences 813: 87–94.Google Scholar
TZSCHENTKE, B. and NICHELMANN, M. (1999) Development of avian thermoregulatory system during the early postnatal period: development of the thermoregulatory set-point. Ornis Fennica 76: 189–198.Google Scholar
TZSCHENTKE, B. and BASTA, D. (2000) Development of hypothalamic neuronal thermosensitivity in birds during the perinatal period. Journal of Thermal Biology 25: 119–123.Google Scholar
TZSCHENTKE, B. and BASTA, D. (2002) Early development of neuronal hypothalamic thermosensitivity in birds: influence of epigenetic temperature adaptation. Comparative Biochemistry and Physiology 131A: 825–832.Google Scholar
TZSCHENTKE, B., BASTA, D., JANKE, O. and MAIER, I. (2004) Characteristics of early development of body functions and epigenetic adaptation to the environment in poultry: focused on development of central nervous mechanisms. Avian & Poultry Biology Reviews 15: 107–118.Google Scholar
VAN DEN HOVE, D.L.A., STEINBUSCH, H.W.M., SCHEEPENS, A., VAN DE Berg, W.D.J., KOOIMA, L.A.M., BOOSTEN, B.J.G., PRICKAERTS, J. and BLANCO, C.E. (2006) Prenatal stress and neonatal rat brain development. Neuroscience 137: 145–155.Google Scholar
VINKENOOG, R., BUSHELL, C., SPIELMAN, M., ADAMS, S., DICKINSON, H.G. and SCOTT, R.J. (2003) Genomic imprinting and endosperm development in flowering plants. Moleculare Biotechnology 25: 149–184.Google ScholarPubMed
WEAVER, I.C.G., CERVONI, N., CHAMPAGNE, F.A., ALESSIO, A.C.D., SHARMA, S., SECKL, J.R., DYMOV, S., SZYF, M. and MEANEY, M.J. (2004) Epigenetic programming by maternal behavior. Nature Neuroscience 8: 847–854.Google Scholar
YAHAV, S. (2000) Domestic fowl – strategies to confront environmental conditions. Avian & Poultry Biology Reviews 11: 81–95.Google Scholar
YAHAV, S. and PLAVNIK, I. (1999) Effects of early-age thermal conditioning and food restriction on performance and thermotolerance of male broiler fowl. British Poultry Sciences 40: 120–126.Google Scholar
YOKOMINE, T., SHIROHZU, H., PURBOWASITO, W., TOYODA, A., IWAMA, H., IKEO, K., HORI, T., MIZUNO, S., TSUDZUKI, M., MATSUDA, Y., HATTORI, M., SAKAKI, Y. and SASAKI, H. (2005) Structural and functional analysis of a 0.5-Mb chicken region orthologous to the imprinted mammalian Ascl2/Mash2-Igf2-H19 region. Genome Research 15: 154–165.CrossRefGoogle Scholar