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Nutrition and neurodevelopment: mechanisms of developmental dysfunction and disease in later life

Published online by Cambridge University Press:  14 December 2007

M. J. Dauncey  and
R. J. Bicknell
M. J. Dauncey*
Affiliation:
Developmental Genetics Programme and Neurobiology Programme, The Babraham Institute, Cambridge CB2 4AT, UK
R. J. Bicknell
Affiliation:
Developmental Genetics Programme and Neurobiology Programme, The Babraham Institute, Cambridge CB2 4AT, UK
*
*Corresponding author: Dr M. J. Dauncey, fax +44 (0) 1223 496032, email joy.dauncey@bbsrc.ac.uk
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Abstract

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Nutrition plays a central role in linking the fields of developmental neurobiology and cognitive neuroscience. It has a profound impact on the development of brain structure and function and malnutrition can result in developmental dysfunction and disease in later life. A number of diseases, including schizophrenia, may be related to neurodevelopmental insults such as malnutrition, hypoxia, viruses or in utero drug exposure. Some of the most significant findings on nutrition and neurodevelopment during the last three decades, and especially during the last few years, are discussed in this review. Attention is focused on the underlying cellular and molecular mechanisms by which diet exerts its effects. Randomized intervention studies have revealed important effects of early nutrition on later cognitive development, and recent epidemiological findings show that both genetics and environment are risk factors for schizophrenia. Particularly important is the effect of early nutrition on development of the hippocampus, a brain structure important in establishing learning and memory, and hence for cognitive performance. A major aim of future research should be to elucidate the molecular mechanisms underlying nutritionally-induced impairment of neurodevelopment and specifically to determine the mechanisms by which early nutritional experience affects later cognitive performance. Key research objectives should include: (1) increased understanding of mechanisms underlying the normal processes of ageing and neurodegenerative disorders; (2) assessment of the role of susceptibility genes in modulating the effects of early nutrition on neurodevelopment; and (3) development of nutritional and pharmaceutical strategies for preventing and/or ameliorating the adverse effects of early malnutrition on long-term programming.

Keywords

NeurodevelopmentFetal nutritionInfant nutrition

Information

Type
Research Article
Information
Nutrition Research Reviews , Volume 12 , Issue 2 , December 1999 , pp. 231 - 253
Copyright
Copyright © CABI Publishing 1999

References

Albright, CD, Tsai, AY, Mar, MH & Zeisel, SH (1998) Choline availability modulates the expression of TGFβ1 and cytoskeletal proteins in the hippocampus of developing rat brain. Neurochemical Research 23, 751–758.CrossRefGoogle ScholarPubMed
Almeida, SS, Tonkiss, J & Galler, JR (1996 a) Prenatal protein malnutrition affects avoidance but not escape behavior in the elevated T-maze test. Physiology and Behavior 60, 191–195.CrossRefGoogle Scholar
Almeida, SS, Tonkiss, J & Galler, JR (1996 b) Prenatal protein malnutrition affects exploratory behavior of female rats in the elevated plus-maze test. Physiology and Behavior 60, 675–680.CrossRefGoogle ScholarPubMed
Almeida, SS, Tonkiss, J & Galler, JR (1996 c) Prenatal protein malnutrition affects the social interactions of juvenile rats. Physiology and Behavior 60, 197–201.CrossRefGoogle ScholarPubMed
Atallah, MT, Barbeau, IS & Pellett, PL (1977) Metabolic and development changes in growing rats born to dams restricted in protein and/or energy intake. Journal of Nutrition 107, 650–655.CrossRefGoogle ScholarPubMed
Austin, KB, Bronzino, J & Morgane, PJ (1986) Prenatal protein malnutrition affects synaptic potentiation in the dentate gyrus of rats in adulthood. Brain Research 394, 267–273.CrossRefGoogle ScholarPubMed
Austin-Lafrance, RJ, Morgane, PJ & Bronzino, JD (1991) Prenatal protein malnutrition and hippocampal function: rapid kindling. Brain Research Bulletin 27, 815–818.CrossRefGoogle ScholarPubMed
Barker, DJ (1995) The Wellcome Foundation Lecture, 1994. The fetal origins of adult disease. Proceedings of the Royal Society of London. Series B: Biological Sciences 262, 37–43.Google ScholarPubMed
Bedi, KS, Massey, RF & Smart, JL (1989) Neuronal and synaptic measurements in the visual cortex of adult rats after undernutrition during normal or artificial rearing. Journal of Comparative Neurology 289, 89–98.CrossRefGoogle ScholarPubMed
Bedi, KS, Thomas, YM, Davies, CA & Dobbing, J (1980) Synapse-to-neuron ratios of the frontal and cerebellar cortex of 30-day-old and adult rats undernourished during early postnatal life. Journal of Comparative Neurology 193, 49–56.CrossRefGoogle ScholarPubMed
Bicknell, RJ (1998) Sex-steroid actions on neurotransmission. Current Opinion in Neurology 11, 667–671.CrossRefGoogle ScholarPubMed
Bliss, TV & Collingridge, GL (1993) A synaptic model of memory: long-term potentiation in the hippocampus. Nature 361, 31–39.CrossRefGoogle ScholarPubMed
Bronzino, JD, Austin, K, Siok, CJ, Cordova, C & Morgane, PJ (1983) Spectral analysis of neocortical and hippocampal EEG in the protein malnourished rat. Electroencephalography and Clinical Neurophysiology 55, 699–709.CrossRefGoogle ScholarPubMed
Bronzino, JD, Austin-LaFrance, RJ, Mokler, D & Morgane, PJ (1997) Effects of prenatal protein malnutrition on hippocampal long-term potentiation in freely moving rats. Experimental Neurology 148, 317–323.CrossRefGoogle ScholarPubMed
Bronzino, JD, Austin-LaFrance, RJ & Morgane, PJ (1990) Effects of prenatal protein malnutrition on perforant path kindling in the rat. Brain Research 515, 45–50.Google Scholar
Bronzino, JD, Austin-LaFrance, RJ, Morgane, PJ & Galler, JR (1991 a) Effects of prenatal protein malnutrition on kindling-induced alterations in dentate granule cell excitability. I. Synaptic transmission measures. Experimental Neurology 112, 206–215.CrossRefGoogle ScholarPubMed
Bronzino, JD, Austin-LaFrance, RJ, Morgane, PJ & Galler, JR (1991 b) Effects of prenatal protein malnutrition on kindling-induced alterations in dentate granule cell excitability. II. Paired-pulse measures. Experimental Neurology 112, 216–223.CrossRefGoogle ScholarPubMed
Bronzino, JD, Austin-LaFrance, RJ, Morgane, PJ & Galler, JR (1996 a) Diet-induced alterations in the ontogeny of long-term potentiation. Hippocampus 6, 109–117.3.0.CO;2-K>CrossRefGoogle ScholarPubMed
Bronzino, JD, Austin-LaFrance, RJ, Siok, CJ & Morgane, PJ (1986) Effect of protein malnutrition on hippocampal kindling: electrographic and behavioral measures. Brain Research 384, 348–354.CrossRefGoogle ScholarPubMed
Bronzino, JD, Kehoe, P, Austin-LaFrance, RJ, Rushmore, RJ & Kurdian, J (1996 b) Neonatal isolation alters LTP in freely moving juvenile rats: sex differences. Brain Research Bulletin 41, 175–183.CrossRefGoogle ScholarPubMed
Bronzino, JD, Stisser, P, Forbes, WB, Tracy, C, Resnick, O & Morgane, PJ (1980) Power spectral analysis of the EEG following protein malnutrition. Brain Research Bulletin 5, 51–60.CrossRefGoogle ScholarPubMed
Brown, AS, Susser, ES, Butler, PD, Richardson Andrews, R, Kaufmann, CA & Gorman, JM (1996) Neurobiological plausibility of prenatal nutritional deprivation as a risk factor for schizophrenia. Journal of Nervous and Mental Disease 184, 71–85.CrossRefGoogle ScholarPubMed
Brown, JL & Pollitt, E (1996) Malnutrition, poverty and intellectual development. Scientific American 274, 38–43.CrossRefGoogle ScholarPubMed
Carlson, SE, Clandinin, MT, Cook, HW, Emken, EA & Filer, LJ Jr (1997) Trans fatty acids: infant and fetal development. American Journal of Clinical Nutrition 66, 715S–736S.CrossRefGoogle ScholarPubMed
Carughi, A, Carpenter, KJ & Diamond, MC (1989) Effect of environmental enrichment during nutritional rehabilitation on body growth, blood parameters and cerebral cortical development of rats. Journal of Nutrition 119, 2005–2016.CrossRefGoogle ScholarPubMed
Chen, JC, Turiak, G, Galler, J & Volicer, L (1997) Postnatal changes of brain monoamine levels in prenatally malnourished and control rats. International Journal of Developmental Neuroscience 15, 257–263.CrossRefGoogle ScholarPubMed
Chen, YC, Chen, QS, Lei, JL & Wang, SL (1998) Physical training modifies the age-related decrease of GAP-43 and synaptophysin in the hippocampal formation in C57BL/6J mouse. Brain Research 806, 238–245.CrossRefGoogle ScholarPubMed
Cintra, L, Aguilar, A, Granados, L, Galvan, A, Kemper, T, DeBassio, W, Galler, J, Morgane, P, Duran, P & Diaz-Cintra, S (1997 a) Effects of prenatal protein malnutrition on hippocampal CA1 pyramidal cells in rats of four age groups. Hippocampus 7, 192–203.3.0.CO;2-P>CrossRefGoogle ScholarPubMed
Cintra, L, Granados, L, Aguilar, A, Kemper, T, DeBassio, W, Galler, J, Morgane, P, Duran, P & Diaz-Cintra, S (1997 b) Effects of prenatal protein malnutrition on mossy fibers of the hippocampal formation in rats of four age groups. Hippocampus 7, 184–191.3.0.CO;2-N>CrossRefGoogle ScholarPubMed
Cirulli, F, Micera, A, Alleva, E & Aloe, L (1998) Early maternal separation increases NGF expression in the developing rat hippocampus. Pharmacology, Biochemistry and Behavior 59, 853–858.Google Scholar
Coffey, ET, Akerman, KE & Courtney, MJ (1997) Brain derived neurotrophic factor induces a rapid upregulation of synaptophysin and tau proteins via the neurotrophin receptor TrkB in rat cerebellar granule cells. Neuroscience Letters 227, 177–180.CrossRefGoogle ScholarPubMed
Cordero, ME, D'Acuna, E, Benveniste, S, Prado, R, Nunez, JA & Colombo, M (1993) Dendritic development in neocortex of infants with early postnatal life undernutrition. Pediatric Neurology 9, 457–464.CrossRefGoogle ScholarPubMed
Crawford, MA, Costeloe, K, Ghebremeskel, K & Phylactos, A (1998) The inadequacy of the essential fatty acid content of present preterm feeds. European Journal of Pediatrics 157, S23–S27.CrossRefGoogle ScholarPubMed
Crawford, MA, Doyle, W, Drury, P, Lennon, A, Costeloe, K & Leighfield, M (1989) n-6 and n-3 fatty acids during early human development. Journal of Internal Medicine Suppl., 159–169.CrossRefGoogle ScholarPubMed
Crawford, MA, Doyle, W, Leaf, A, Leighfield, M, Ghebremeskel, K & Phylactos, A (1993) Nutrition and neurodevelopmental disorders. Nutrition and Health 9, 81–97.CrossRefGoogle ScholarPubMed
Dauncey, MJ (1990) Thyroid hormones and thermogenesis. Proceedings of the Nutrition Society 49, 203–215.CrossRefGoogle ScholarPubMed
Dauncey, MJ (1997) From early nutrition and later development … to underlying mechanisms and optimal health. British Journal of Nutrition 78, S113–S123.Google Scholar
Davidsson, P & Blennow, K (1998) Neurochemical dissection of synaptic pathology in Alzheimer's disease. International Psychogeriatrics 10, 11–23.Google Scholar
de Andraca, I & Uauy, R (1995) Breastfeeding for optimal mental development. The alpha and the omega in human milk. World Review of Nutrition and Dietetics 78, 1–27.Google Scholar
Debassio, WA, Kemper, TL, Tonkiss, J & Galler, JR (1996) Effect of prenatal protein deprivation on postnatal granule cell generation in the hippocampal dentate gyrus. Brain Research Bulletin 41, 379–383.CrossRefGoogle ScholarPubMed
Diaz-Cintra, S, Garcia-Ruiz, M, Corkidi, G & Cintra, L (1994) Effects of prenatal malnutrition and postnatal nutritional rehabilitation on CA3 hippocampal pyramidal cells in rats of four ages. Brain Research 662, 117–126.Google Scholar
Dobbing, J (1990) Boyd Orr memorial lecture. Early nutrition and later achievement. Proceedings of the Nutrition Society 49, 103–118.Google Scholar
Duffy, PH, Leakey, JE, Pipkin, JL, Turturro, A & Hart, RW (1997) The physiologic, neurologic, and behavioral effects of caloric restriction related to aging, disease, and environmental factors. Environmental Research 73, 242–248.CrossRefGoogle ScholarPubMed
Eriksson, PS, Perfilieva, E, Bjork-Eriksson, T, Alborn, AM, Nordborg, C, Peterson, DA & Gage, FH (1998) Neurogenesis in the adult human hippocampus. Nature Medicine 4, 1313–1317.Google Scholar
Farquharson, J, Cockburn, F, Patrick, WA, Jamieson, EC & Logan, RW (1992) Infant cerebral cortex phospholipid fatty-acid composition and diet. Lancet 340, 810–813.CrossRefGoogle ScholarPubMed
Fernald, LC & Grantham-McGregor, SM (1998) Stress response in school-age children who have been growth retarded since early childhood. American Journal of Clinical Nutrition 68, 691–698.Google Scholar
Ferrer, I, Marti, E, Tortosa, A & Blasi, J (1998) Dystrophic neurites of senile plaques are defective in proteins involved in exocytosis and neurotransmission. Journal of Neuropathology and Experimental Neurology 57, 218–225.Google Scholar
Forbes, WB, Resnick, O, Stern, WC, Bronzino, JD & Morgane, PJ (1975) The effect of chronic protein malnutrition on trans-callosal evoked responses in the rat. Developmental Psychobiology 8, 503–509.CrossRefGoogle ScholarPubMed
Fowden, AL, Li, J & Forhead, AJ (1998) Glucocorticoids and the preparation for life after birth: are there long-term consequences of the life insurance?. Proceedings of the Nutrition Society 57, 113–122.CrossRefGoogle ScholarPubMed
Franklin, KBJ & Paxinos, G (1997) The Mouse Brain in Stereotaxic Coordinates. San Diego, CA: Academic Press.Google Scholar
Franzek, E & Beckmann, H (1996) Gene-environment interaction in schizophrenia: season-of-birth effect reveals etiologically different subgroups. Psychopathology 29, 14–26.Google Scholar
Gibson, RA & Makrides, M (1998) The role of long chain polyunsaturated fatty acids (LCPUFA) in neonatal nutrition. Acta Paediatrica 87, 1017–1022.Google ScholarPubMed
Gibson, RA, Neumann, MA & Makrides, M (1997) Effect of increasing breast milk docosahexaenoic acid on plasma and erythrocyte phospholipid fatty acids and neural indices of exclusively breast fed infants. European Journal of Clinical Nutrition 51, 578–584.CrossRefGoogle ScholarPubMed
Glantz, LA & Lewis, DA (1997) Reduction of synaptophysin immunoreactivity in the prefrontal cortex of subjects with schizophrenia. Regional and diagnostic specificity. Archives of General Psychiatry 54, 943–952.CrossRefGoogle ScholarPubMed
Gordon, N (1997) Nutrition and cognitive function. Brain and Development 19, 165–170.CrossRefGoogle ScholarPubMed
Gottschalk, W, Pozzo-Miller, LD, Figurov, A & Lu, B (1998) Presynaptic modulation of synaptic transmission and plasticity by brain-derived neurotrophic factor in the developing hippocampus. Journal of Neuroscience 18, 6830–6839.CrossRefGoogle ScholarPubMed
Gramsbergen, A & Westerga, J (1992) Locomotor development in undernourished rats. Behavioural Brain Research 48, 57–64.Google Scholar
Grantham-McGregor, S, Schofield, W & Powell, C (1987) Development of severely malnourished children who received psychosocial stimulation: six-year follow-up. Pediatrics 79, 247–254.Google Scholar
Grosse, G, Tapp, R, Wartenberg, M, Sauer, H, Fox, PA, Grosse, J, Gratzl, M & Bergmann, M (1998) Prenatal hippocampal granule cells in primary cell culture form mossy fiber boutons at pyramidal cell dendrites. Journal of Neuroscience Research 51, 602–611.3.0.CO;2-J>CrossRefGoogle ScholarPubMed
Guesry, P (1998) The role of nutrition in brain development. Preventive Medicine 27, 189–194.CrossRefGoogle ScholarPubMed
Hansen, LA, Daniel, SE, Wilcock, GK & Love, S (1998) Frontal cortical synaptophysin in Lewy body diseases: relation to Alzheimer's disease and dementia. Journal of Neurology, Neurosurgery and Psychiatry 64, 653–656.CrossRefGoogle ScholarPubMed
Hatten, ME (1999) Central nervous system neuronal migration. Annual Review of Neuroscience 22, 511–539.CrossRefGoogle ScholarPubMed
Hay, WW Jr (1994) Nutritional requirements of extremely low birthweight infants. Acta Paediatrica Suppl., 40294–99.Google Scholar
Heffernan, JM, Eastwood, SL, Nagy, Z, Sanders, MW, McDonald, B & Harrison, PJ (1998) Temporal cortex synaptophysin mRNA is reduced in Alzheimer's disease and is negatively correlated with the severity of dementia. Experimental Neurology 150, 235–239.CrossRefGoogle ScholarPubMed
Hesen, W, Karten, YJ, van de Witte, SV & Joels, M (1998) Serotonin and carbachol induced suppression of synaptic excitability in rat CA1 hippocampal area: effects of corticosteroid receptor activation. Journal of Neuroendocrinology 10, 9–19.Google Scholar
Hoet, JJ & Hanson, MA (1999) Intrauterine nutrition: its importance during critical periods for cardiovascular and endocrine development. Journal of Physiology (London) 514, 617–627.CrossRefGoogle ScholarPubMed
Innis, SM (1994) The 1993 Borden Award Lecture. Fatty acid requirements of the newborn. Canadian Journal of Physiology and Pharmacology 72, 1483–1492.CrossRefGoogle ScholarPubMed
Ishimura, K, Takeuchi, Y, Fujiwara, K, Yoshioka, H, Sawada, T & Kusunoki, T (1989) Effects of undernutrition on the serotonin neuron system in the developing brain: an immunohistochemical study. Brain Research. Developmental Brain Research 50, 225–231.Google Scholar
Kandel, ER & Sahwartz, JH (editors) (1985) Principles of Neural Science, 2nd ed. New York: Elsevier.Google Scholar
Karp, R, Martin, R, Sewell, T, Manni, J & Heller, A (1992) Growth and academic achievement in inner-city kindergarten children. The relationship of height, weight, cognitive ability, and neurodevelopmental level. Clinical Pediatrics (Philadelphia) 31, 336–340.CrossRefGoogle ScholarPubMed
Katsumata, M, Burton, KA, Li, J & Dauncey, MJ (1999) Suboptimal energy balance selectively up-regulates muscle GLUT gene expression but reduces insulin-dependent glucose uptake during postnatal development. FASEB Journal 13, 1405–1413.CrossRefGoogle ScholarPubMed
Kehoe, P, Hoffman, JH, Austin-LaFrance, RJ & Bronzino, JD (1995) Neonatal isolation enhances hippocampal dentate response to tetanization in freely moving juvenile male rats. Experimental Neurology 136, 89–97.Google Scholar
Kolb, B & Gibb, R (1990) Anatomical correlates of behavioural change after neonatal prefrontal lesions in rats. Progress in Brain Research 85, 241–255.CrossRefGoogle ScholarPubMed
Kolb, B & Whishaw, IQ (1989) Plasticity in the neocortex: mechanisms underlying recovery from early brain damage. Progress in Neurobiology 32, 235–276.Google Scholar
Kretchmer, N, Beard, JL & Carlson, S (1996) The role of nutrition in the development of normal cognition. American Journal of Clinical Nutrition 63, 997S–1001S.CrossRefGoogle ScholarPubMed
Krigman, MR & Hogan, EL (1976) Undernutrition in the developing rat: effect upon myelination. Brain Research 107, 239–255.CrossRefGoogle ScholarPubMed
Kuroda, Y & McEwen, BS (1998) Effect of chronic restraint stress and tianeptine on growth factors, growth-associated protein-43 and microtubule-associated protein 2 mRNA expression in the rat hippocampus. Brain Research. Molecular Brain Research 59, 35–39.CrossRefGoogle ScholarPubMed
Laban, O, Markovic, BM, Dimitrijevic, M & Jankovic, BD (1995) Maternal deprivation and early weaning modulate experimental allergic encephalomyelitis in the rat. Brain, Behavior, and Immunity 9, 9–19.Google Scholar
Lai, M & Lewis, PD (1980) Effects of undernutrition on myelination in rat corpus callosum. Journal of Comparative Neurology 193, 973–982.Google Scholar
Lai, M, Lewis, PD & Patel, AJ (1980) Effects of undernutrition on gliogenesis and glial maturation in rat corpus callosum. Journal of Comparative Neurology 193, 965–972.Google Scholar
Lanting, CI & Boersma, ER (1996) Lipids in infant nutrition and their impact on later development. Current Opinion in Lipidology 7, 43–47.Google Scholar
Lanting, CI, Fidler, V, Huisman, M, Touwen, BC & Boersma, ER (1994) Neurological differences between 9-year-old children fed breast-milk or formula-milk as babies. Lancet 344, 1319–1322.CrossRefGoogle ScholarPubMed
Levitsky, DA & Strupp, BJ (1995) Malnutrition and the brain: changing concepts, changing concerns. Journal of Nutrition 125, 2212S–2220S.Google Scholar
Lucas, A (1994) Role of nutritional programming in determining adult morbidity. Archives of Disease in Childhood 71, 288–290.Google Scholar
Lucas, A (1998) Programming by early nutrition: an experimental approach. Journal of Nutrition 128, 401S–406S.CrossRefGoogle ScholarPubMed
Lucas, A, Fewtrell, MS, Morley, R, Lucas, PJ, Baker, BA, Lister, G & Bishop, NJ (1996) Randomized outcome trial of human milk fortification and developmental outcome in preterm infants. American Journal of Clinical Nutrition 64, 142–151.Google Scholar
Lucas, A, Morley, R, Cole, TJ, Gore, SM, Davis, JA, Bamford, MF & Dossetor, JF (1989) Early diet in preterm babies and developmental status in infancy. Archives of Disease in Childhood 64, 1570–1578.CrossRefGoogle ScholarPubMed
Lucas, A, Morley, R, Cole, TJ, Lister, G & Leeson-Payne, C (1992) Breast milk and subsequent intelligence quotient in children born preterm. Lancet 339, 261–264.Google Scholar
Lupien, SJ, de Leon, M, de Santi, S, Convit, A, Tarshish, C, Nair, NP, Thakur, M, McEwen, BS, Hauger, RL & Meaney, MJ (1998) Cortisol levels during human aging predict hippocampal atrophy and memory deficits. Nature Neuroscience 1, 69–73.Google Scholar
Magnusson, KR (1998) The aging of the NMDA receptor complex. Frontiers in Biosciences 3, e70–e80.Google Scholar
Major, DE, Kesslak, JP, Cotman, CW, Finch, CE & Day, JR (1997) Life-long dietary restriction attenuates age-related increases in hippocampal glial fibrillary acidic protein mRNA. Neurobiology of Aging 18, 523–526.Google Scholar
Makrides, M, Neumann, MA, Byard, RW, Simmer, K & Gibson, RA (1994) Fatty acid composition of brain, retina, and erythrocytes in breast- and formula-fed infants. American Journal of Clinical Nutrition 60, 189–194.CrossRefGoogle ScholarPubMed
Marcus, J, Auerbach, J, Wilkinson, L & Burack, CM (1981) Infants at risk for schizophrenia. The Jerusalem Infant Development Study. Archives of General Psychiatry 38, 703–713.CrossRefGoogle ScholarPubMed
Marin, MC, De Tomas, ME, Serres, C & Mercuri, O (1995) Protein-energy malnutrition during gestation and lactation in rats affects growth rate, brain development and essential fatty acid metabolism. Journal of Nutrition 125, 1017–1024.Google ScholarPubMed
Martin, LJ, Furuta, A & Blackstone, CD (1998) AMPA receptor protein in developing rat brain: glutamate receptor-1 expression and localization change at regional, cellular, and subcellular levels with maturation. Neuroscience 83, 917–928.CrossRefGoogle ScholarPubMed
Martinez, M (1992) Tissue levels of polyunsaturated fatty acids during early human development. Journal of Pediatrics 120, S129–S138.CrossRefGoogle ScholarPubMed
Matthews, K, Wilkinson, LS & Robbins, TW (1996) Repeated maternal separation of preweanling rats attenuates behavioral responses to primary and conditioned incentives in adulthood. Physiology and Behavior 59, 99–107.Google Scholar
Meberg, A (1981) Somatic growth and brain development. Effects of intrauterine malnutrition and hypoxia in mice. Biology of the Neonate 39, 272–284.Google Scholar
Morgane, PJ, Austin, K, Siok, C, LaFrance, R & Bronzino, JD (1985) Power spectral analysis of hippocampal and cortical EEG activity following severe prenatal protein malnutrition in the rat. Brain Research 354, 211–218.CrossRefGoogle ScholarPubMed
Morgane, PJ, Austin-LaFrance, R, Bronzino, J, Tonkiss, J, Diaz-Cintra, S, Cintra, L, Kemper, T & Galler, JR (1993) Prenatal malnutrition and development of the brain. Neuroscience and Biobehavioral Reviews 17, 91–128.Google Scholar
Morley, R (1996) The influence of early diet on later development. Journal of Biosocial Science 28, 481–487.Google Scholar
Morley, R & Lucas, A (1994) Influence of early diet on outcome in preterm infants. Acta Paediatrica Suppl., 405123–126.Google Scholar
Morovat, A & Dauncey, MJ (1995) Regulation of porcine skeletal muscle nuclear 3,5,3′-triiodothyronine receptor binding capacity by thyroid hormones: modification by energy balance. Journal of Endocrinology 144, 233–242.CrossRefGoogle ScholarPubMed
Mortensen, PB, Pedersen, CB, Westergaard, T, Wohlfahrt, J, Ewald, H, Mors, O, Andersen, PK & Melbye, M (1999) Effects of family history and place and season of birth on the risk of schizophrenia. New England Journal of Medicine 340, 603–608.Google Scholar
Nathanielsz, PW (1996) Fetal and neonatal environment has influence on brain development. Lancet 347, 314.Google Scholar
Nyirenda, MJ & Seckl, JR (1998) Intrauterine events and the programming of adulthood disease: The role of fetal glucocorticoid exposure. International Journal of Molecular Medicine 2, 607–614.Google Scholar
Pastor, R, Bernal, J & Rodriguez-Pena, A (1994) Unliganded c-erbA/thyroid hormone receptor induces trkB expression in neuroblastoma cells. Oncogene 9, 1081–1089.Google Scholar
Pavey, DE & Widdowson, EM (1980) Body lipids of guinea pigs exposed to different dietary fats from mid-gestation to 3 months of age. V. The fatty acid composition of brain lipids at birth. Nutrition and Metabolism 24, 357–366.Google Scholar
Peeling, AN & Smart, JL (1994 a) Review of literature showing that undernutrition affects the growth rate of all processes in the brain to the same extent. Metabolic Brain Disease 9, 33–42.CrossRefGoogle Scholar
Peeling, AN & Smart, JL (1994 b) Successful prediction of immediate effects of undernutrition throughout the brain growth spurt on capillarity and synapse-to-neuron ratio of cerebral cortex in rats. Metabolic Brain Disease 9, 81–95.Google Scholar
Petridou, E, Koussouri, M, Toupadaki, N, Youroukos, S, Papavassiliou, A, Pantelakis, S, Olsen, J & Trichopoulos, D (1998) Diet during pregnancy and the risk of cerebral palsy. British Journal of Nutrition 79, 407–412.CrossRefGoogle ScholarPubMed
Phillips, DI, Barker, DJ, Fall, CH, Seckl, JR, Whorwood, CB, Wood, PJ & Walker, BR (1998) Elevated plasma cortisol concentrations: a link between low birth weight and the insulin resistance syndrome?. Journal of Clinical Endocrinology and Metabolism 83, 757–760.Google Scholar
Rizzo, TA, Metzger, BE, Dooley, SL & Cho, NH (1997) Early malnutrition and child neurobehavioral development: insights from the study of children of diabetic mothers. Child Development 68, 26–38.Google Scholar
Rushmore, J, Luebke, J & Galler, JR (1998) Electrophysiological properties of rat hippocampal principal cells are unaltered by prenatal protein malnutrition. Hippocampus 8, 380–389.3.0.CO;2-L>CrossRefGoogle ScholarPubMed
Salas, M, Torrero, C & Pulido, S (1984) Long-term alterations in the maternal behavior of neonatally undernourished rats. Physiology and Behavior 33, 273–278.CrossRefGoogle ScholarPubMed
Saste, MD, Carver, JD, Stockard, JE, Benford, VJ, Chen, LT & Phelps, CP (1998) Maternal diet fatty acid composition affects neurodevelopment in rat pups. Journal of Nutrition 128, 740–743.Google Scholar
Schull, WJ & Otake, M (1999) Cognitive function and prenatal exposure to ionizing radiation. Teratology 59, 222–226.Google Scholar
Seidler, FJ, Bell, JM & Slotkin, TA (1990) Undernutrition and overnutrition in the neonatal rat: long-term effects on noradrenergic pathways in brain regions. Pediatric Research 27, 191–197.Google Scholar
Shimohama, S, Kamiya, S, Taniguchi, T, Akagawa, K & Kimura, J (1997) Differential involvement of synaptic vesicle and presynaptic plasma membrane proteins in Alzheimer's disease. Biochemical and Biophysical Research Communications 236, 239–242.CrossRefGoogle ScholarPubMed
Shultz, PL, Tonkiss, J, Morgane, PJ, Bronzino, JD & Galler, JR (1995) Effects of an every other day rapid kindling procedure in prenatally protein malnourished rats. Brain Research 682, 35–40.Google Scholar
Smart, JL (1990) Vulnerability of developing brain to undernutrition. Uppsala Journal of Medical Sciences Suppl., 48 21–41.Google ScholarPubMed
Smart, JL (1991) Critical periods in brain development. CIBA Foundation Symposium 156, 109–124.Google Scholar
Soto-Moyano, R, Belmar, J, Perez, H, Ruiz, S & Hernandez, A (1995) Central noradrenergic hyperactivity early in life: a hypothesis on the origin of morpho-functional brain disorders induced by malnutrition. Biological Research 28, 105–111.Google ScholarPubMed
Stern, WC, Forbes, WB, Resnick, O & Morgane, PJ (1974) Seizure susceptibility and brain amine levels following protein malnutrition during development in the rat. Brain Research 79, 375–384.CrossRefGoogle ScholarPubMed
Stewart, RJC (1974) Experimental studies on nutrition and brain development. Nutrition 28, 151–162.Google Scholar
Sun, XZ, Takahashi, S, Fukui, Y, Hisano, S, Kuboda, Y, Sato, H & Inouye, M (1999) Different patterns of abnormal neuronal migration in the cerebral cortex of mice prenatally exposed to irradiation. Brain Research. Developmental Brain Research 114, 99–108.Google Scholar
Sze, CI, Troncoso, JC, Kawas, C, Mouton, P, Price, DL & Martin, LJ (1997) Loss of the presynaptic vesicle protein synaptophysin in hippocampus correlates with cognitive decline in Alzheimer disease. Journal of Neuropathology and Experimental Neurology 56, 933–944.CrossRefGoogle ScholarPubMed
Thomas, YM, Peeling, A, Bedi, KS, Davies, CA & Dobbing, J (1980) Deficits in synapse-to-neuron ratio due to early undernutrition show evidence of catch-up in later life. Experientia 36, 556–557.Google Scholar
Tonkiss, J, Galler, J, Morgane, PJ, Bronzino, JD & Austin-LaFrance, RJ (1993) Prenatal protein malnutrition and postnatal brain function. Annals of the New York Academy of Sciences 678, 215–227.Google Scholar
Uauy, R & de Andraca, I (1995) Human milk and breast feeding for optimal mental development. Journal of Nutrition 125, 2278S–2280S.Google Scholar
Uauy-Dagach, R & Mena, P (1995) Nutritional role of omega-3 fatty acids during the perinatal period. Clinics in Perinatology 22, 157–175.Google Scholar
van Houwelingen, AC, Sorensen, JD, Hornstra, G, Simonis, MM, Boris, J, Olsen, SF & Secher, NJ (1995) Essential fatty acid status in neonates after fish-oil supplementation during late pregnancy. British Journal of Nutrition 74, 723–731.Google Scholar
Wainwright, PE, Xing, HC, Ward, GR, Huang, YS, Bobik, E, Auestad, N & Montalto, M (1999) Water maze performance is unaffected in artificially reared rats fed diets supplemented with arachidonic acid and docosahexaenoic acid. Journal of Nutrition 129, 1079–1089.Google Scholar
Wang, W & Dow, KE (1998) Quantitative analysis of mRNA expression of neuron-specific growth-associated genes in rat primary neurons by competitive RT-PCR. Brain Research. Brain Research Protocols 2, 199–208.Google Scholar
Ward, GR & Wainwright, PE (1988) Reductions in maternal food and water intake account for prenatal stress effects on neurobehavioral development in B6D2F2 mice. Physiology and Behavior 44, 781–786.Google Scholar
Wasantwisut, E (1997) Nutrition and development: other micronutrients' effect on growth and cognition. Southeast Asian Journal of Tropical Medicine and Public Health 28, 78–82.Google Scholar
Wauben, IP & Wainwright, PE (1999) The influence of neonatal nutrition on behavioral development: a critical appraisal. Nutrition Reviews 57, 35–44.Google Scholar
Wheal, HV, Chen, Y, Mitchell, J, Schachner, M, Maerz, W, Wieland, H, Rossum, DV & Kirsch, J (1998) Molecular mechanisms that underlie structural and functional changes at the postsynaptic membrane during synaptic plasticity. Progress in Neurobiology 55, 611–640.Google Scholar
White, P & Dauncey, MJ (1998) Postnatal undernutrition markedly upregulates cardiac α1 and α2 thyroid hormone receptor gene expression Proceedings of the Nutrition Society 57, 79A.Google Scholar
White, P & Dauncey, MJ (1999) Differential expression of thyroid hormone receptor isoforms is strikingly related to cardiac and skeletal muscle phenotype during postnatal development. Journal of Molecular Endocrinology 23,(In the Press).Google Scholar
Widdowson, EM, Dauncey, MJ, Gairdner, DM, Jonxis, JH & Pelikan-Filipkova, M (1975) Body fat of British and Dutch infants. British Medical Journal 1, 653–655.Google Scholar
Wiggins, RC, Fuller, G & Enna, SJ (1984) Undernutrition and the development of brain neurotransmitter systems. Life Sciences 35, 2085–2094.Google Scholar
Woltil, HA, van Beusekom, CM, Schaafsma, A, Muskiet, FA & Okken, A (1998) Long-chain polyunsaturated fatty acid status and early growth of low birth weight infants. European Journal of Pediatrics 157, 146–152.Google Scholar
Xu, L, Holscher, C, Anwyl, R & Rowan, MJ (1998) Glucocorticoid receptor and protein/RNA synthesis-dependent mechanisms underlie the control of synaptic plasticity by stress. Proceedings of the National Academy of Sciences USA 95, 3204–3208.Google Scholar
Young, CE, Arima, K, Xie, J, Hu, L, Beach, TG, Falkai, P & Honer, WG (1998) SNAP-25 deficit and hippocampal connectivity in schizophrenia. Cerebral Cortex 8, 261–268.Google Scholar
Zeisel, SH (1986) Dietary influences on neurotransmission. Advances in Pediatrics 33, 23–47.CrossRefGoogle ScholarPubMed