Hostname: page-component-7c8c6479df-fqc5m Total loading time: 0 Render date: 2024-03-28T09:53:21.773Z Has data issue: false hasContentIssue false

Early life nutrition and neural plasticity

Published online by Cambridge University Press:  06 May 2015

Michael K. Georgieff*
Affiliation:
University of Minnesota
Katya E. Brunette
Affiliation:
Boys' Town USA
Phu V. Tran
Affiliation:
University of Minnesota
*
Address correspondence and reprint requests to: Michael K. Georgieff, Division of Neonatology, University of Minnesota Children's Hospital, 2450 Riverside Avenue, Sixth Floor, East Building, MB-630, Minneapolis, MN 55454; E-mail: georg001@umn.edu.

Abstract

The human brain undergoes a remarkable transformation during fetal life and the first postnatal years from a relatively undifferentiated but pluripotent organ to a highly specified and organized one. The outcome of this developmental maturation is highly dependent on a sequence of environmental exposures that can have either positive or negative influences on the ultimate plasticity of the adult brain. Many environmental exposures are beyond the control of the individual, but nutrition is not. An ever-increasing amount of research demonstrates not only that nutrition shapes the brain and affects its function during development but also that several nutrients early in life have profound and long-lasting effects on the brain. Nutrients have been shown to alter opening and closing of critical and sensitive periods of particular brain regions. This paper discusses the roles that various nutrients play in shaping the developing brain, concentrating specifically on recently explicated biological mechanisms by which particularly salient nutrients influence childhood and adult neural plasticity.

Type
Regular Articles
Copyright
Copyright © Cambridge University Press 2015 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Armstrong, V. L., Brunet, P. M., He, C., Nishimura, M., Poole, H. L., & Spector, F. J. (2006). What is so critical? A commentary on the reexamination of critical periods. Developmental Psychobiology, 48, 326331.CrossRefGoogle ScholarPubMed
Artavanis-Tsakonas, S., Rand, M. D., & Lake, R. J. (1999). Notch signaling: Cell fate control and signal integration in development. Science, 284, 770776.CrossRefGoogle ScholarPubMed
Bagot, R. C., van Hasselt, F. N., Champagne, D. L., Meaney, M. J., Krugers, H. J., & Joels, M. (2009). Maternal care determines rapid effects of stress mediators on synaptic plasticity in adult rat hippocampal dentate gyrus. Neurobiology of Learning and Memory, 92, 292300.CrossRefGoogle ScholarPubMed
Balmer, T. S., Carels, V. M., Frisch, J. L., & Nick, T. A. (2009). Modulation of perineuronal nets and parvalbumin with developmental song learning. Journal of Neuroscience, 29, 1287812885.CrossRefGoogle ScholarPubMed
Bekenstein, J. W., & Lothman, E. W. (1991). An in vivo study of the ontogeny of long-term potentiation (LTP) in the CA1 region and in the dentate gyrus of the rat hippocampal formation. Developmental Brain Research, 63, 245251.CrossRefGoogle Scholar
Blegen, M. B., Kennedy, B. C., Thibert, K. A., Tran, P. V., & Georgieff, M. K. (2013). Multigenerational effects of fetal–neonatal iron deficiency on hippocampal BDNF signaling. Physiological Reports, 1(5), e00096.CrossRefGoogle ScholarPubMed
Bornstein, M. H. (1989). Sensitive periods in development: Structural characteristics and causal interpretations. Psychological Bulletin, 105, 179197.CrossRefGoogle ScholarPubMed
Bretin, S., Reibel, S., Charrier, E., Maus-Moatti, M., Auvergnon, N., Thevenoux, A., et al. (2005). Differential expression of CRMP1, CRMP2A, CRMP2B, and CRMP5 in axons or dendrites of distinct neurons in the mouse brain. Journal of Comparative Neurology, 486, 117.CrossRefGoogle ScholarPubMed
Bronfenbrenner, U., & Morris, P. (2006). The bioecological model of human development. In Lerner, R. (Ed.), Handbook of child psychology: Vol. 1. Theoretical models of human development (6th ed., pp. 793828). Hoboken, NJ: Wiley.Google Scholar
Brunette, K. E., Tran, P. V., Wobken, J. D., Carlson, E. S., & Georgieff, M. K. (2010). Gestational and neonatal iron deficiency alters apical dendrite structure of CA1 pyramidal neurons in adult rat hippocampus. Developmental Neuroscience, 32, 238248.CrossRefGoogle ScholarPubMed
Callahan, L. S. N., Thibert, K. A., Wobken, J. D., & Georgieff, M. K. (2013). Early life iron deficiency anemia alters the development and long-term expression of parvalbumin and perineuronal nets in the rat hippocampus. Developmental Neurscience, 35, 427436.CrossRefGoogle ScholarPubMed
Carlson, E. S., Stead, J. D., Neal, C. R., Petryk, A., & Georgieff, M. K. (2007). Perinatal iron deficiency results in altered developmental expression of genes mediating energy metabolism and neuronal morphogenesis in hippocampus. Hippocampus, 17, 679691.CrossRefGoogle ScholarPubMed
Carvin, C. D., Parr, R. D., & Kladde, M. P. (2003). Site-selective in vivo targeting of cytosine-5 DNA methylation by zinc-finger proteins. Nucleic Acids Research, 31, 64936501.CrossRefGoogle ScholarPubMed
Celio, M. R., Spreafico, R., De Biasi, S., & Vitellaro-Zuccarello, L. (1998). Perineuronal nets: Past and present. Trends in Neurosciences, 21, 510515.CrossRefGoogle ScholarPubMed
Champagne, D. L., Bagot, R. C., van Hasselt, F., Ramakers, G., Meaney, M. J., deKloet, E. R., et al. (2008). Maternal care and hippocampal plasticity: Evidence for experience-dependent structural plasticity, altered synaptic functioning, and differential responsiveness to glucocorticoids and stress. Journal of Neuroscience, 28, 60376045.CrossRefGoogle ScholarPubMed
Christian, P., Morgan, M. E., Murray-Kolb, L., LeClerq, S. C., Khatry, S. K., Schaefer, B., et al. (2011). Preschool iron–folic acid and zinc supplementation in children exposed to iron–folic acid in utero confers no added cognitive benefit in early school-age. Journal of Nutrition, 141, 20422048.CrossRefGoogle ScholarPubMed
Christian, P., Murray-Kolb, L. E., Khatry, S. K., Katz, J., Schaefer, B. A., Cole, P. M., et al. (2010). Prenatal micronutrient supplementation and intellectual and motor function in early school-aged children in Nepal. Journal of the American Medical Association, 304, 27162723.CrossRefGoogle ScholarPubMed
Cicchetti, D., & Tucker, D. (Eds.) (1994). Neural plasticity, sensitive periods, and psychopathology [Special Issue]. Development and Psychopathology, 6, 531814.Google Scholar
Colombo, J. (1982). The critical period concept: Research, methodology and theoretical issues. Psychological Bulletin, 91, 260275.CrossRefGoogle ScholarPubMed
Cusick, S. E., & Georgieff, M. K. (2012). Nutrient supplementation and neurodevelopment: Timing is the key. Archives of Pediatric and Adolescent Medicine, 155, 481482.Google Scholar
Dallman, P. R., & Schwartz, H. C. (1964). Cytochrome C concentrations during rat and guinea pig development. Pediatrics, 33, 106110.CrossRefGoogle Scholar
deKloet, E. R., Vreugdenhil, E., Oitzl, M. S., & Joels, M. (1998). Brain corticosteroid receptor balance in health and disease. Endocrine Reviews, 19, 269301.Google Scholar
Donato, F., Rompani, S. R., & Caroni, P. (2013). Parvalbumin-expressing basket-cell network plasticity induced by experience regulates adult learning. Nature, 504, 272277.CrossRefGoogle ScholarPubMed
Encío, I. J., & Detera-Wadleigh, S. D. (1991). The genomic structure of the human glucocorticoid receptor. Journal of Biological Chemistry, 266, 71827188.CrossRefGoogle ScholarPubMed
Felt, B. T., & Lozoff, B. (1996). Brain iron and behavior of rats are not normalized by treatment of iron deficiency anemia during early development. Journal of Nutrition, 126, 693701.CrossRefGoogle Scholar
Fisher, M. C., Zeisel, S. H., Mar, M.-H., & Sadler, T. W. (2002). Perturbations in choline metabolism cause neural tube defects in mouse embryos in vitro. FASEB Journal, 16, 619621.CrossRefGoogle ScholarPubMed
Fretham, S. J. B., Carlson, E. S., & Georgieff, M. K. (2011). The role of iron in learning and memory. Advances in Nutrition, 2, 110.CrossRefGoogle ScholarPubMed
Fretham, S. J. B., Carlson, E. S., Wobken, J., Tran, P. V., Petryk, A., & Georgieff, M. K. (2012). Temporal manipulation of transferrin receptor-1 dependent iron uptake identifies a sensitive period in mouse hippocampal neurodevelopment. Hippocampus, 22, 16911702.CrossRefGoogle ScholarPubMed
Fuglestad, A. J., Ramel, S. E., & Georgieff, M. K. (2010). Miconutrient needs of the developing brain: Priorities and assessment. In Packer, L. (Ed.), Micronutrients and brain health: Oxidative stress and disease (pp. 93115). Boca Raton, FL: CRC Press.Google Scholar
Georgieff, M. K. (2008). The role of iron in neurodevelopment: Fetal iron deficiency and the developing hippocampus. Biochemical Society Transactions, 36, 12671271.CrossRefGoogle ScholarPubMed
Gewirtz, J. C., Hamilton, K. L., Babuh, M. A., Wobken, J. D., & Georgieff, M. K. (2008). Effects of gestational iron deficiency on fear conditioning in juvenile and adult rats. Brain Research, 1237, 195203.CrossRefGoogle ScholarPubMed
Glenn, M. J., Gibson, E. M., Kirby, E. D., Mellott, T. J., Blusztajn, J. K., & Williams, C. L. (2007). Prenatal choline availability modulates hippocampal neurogenesis and neurogenic responses to enriching experiences in adult female rats. European Journal of Neuroscience, 25, 24732482.CrossRefGoogle ScholarPubMed
Gluckman, P. D., & Hanson, M. A. (2004). Living with the past: Evolution, development and patterns of disease. Science, 305, 17331736.CrossRefGoogle ScholarPubMed
Hebb, D. O. (1949). The organization of behavior:A neuropsychological theory. New York: Wiley.Google Scholar
Hensch, T. (2004). Critical period regulation. Annual Reviews Neuroscience, 27, 549579.CrossRefGoogle ScholarPubMed
Huang, Z. J., Kirkwood, A., Pizzorusso, T., Porciatti, V., Morales, B., Bear, M. F., et al. (1999). BDNF regulates the maturation of inhibition and the critical period of plasticity in mouse visual cortex. Cell, 98, 739755.Google Scholar
Insel, B. J., Schaefer, C. A., McKeague, I. W., Susser, E. S., & Brown, A. S. (2008) Maternal iron deficiency and the risk of schizophrenia in offspring. Archives of General Psychiatry, 65, 11361144.CrossRefGoogle ScholarPubMed
Isaacsom, J. S., & Scanziani, M. (2011). How inhibition shapes cortical activity. Neuron, 72, 231243.CrossRefGoogle Scholar
Jaworski, J., Spangler, S., Seeburg, D. P., Hoogenraad, C. C., & Sheng, M. (2005). Control of dendritic arborization by the phosphoinositide-3'-kinase-Akt-mammalian target of rapamycin pathway. Journal of Neuroscience, 25, 1130011312.CrossRefGoogle ScholarPubMed
Johnson, M. (2005). Sensitive periods in functional brain development: Problems and prospects. Developmental Psychobiology, 46, 287292.CrossRefGoogle ScholarPubMed
Jorgenson, L. A., Sun, M., O'Connor, M., & Georgieff, M. K. (2005). Fetal iron deficiency disrupts the maturation of synaptic function and efficacy in area CA1 of the developing rat hippocampus. Hippocampus, 15, 10941102.CrossRefGoogle ScholarPubMed
Kennedy, B. C., Dimova, J. G., Tran, P. V., Gewirtz, J. C., Siddappa, A. J. M., & Georgieff, M. K. (2014). Protective effects of prenatal choline supplementation on long-term alterations in behavior and hippocampal gene expression resulting from fetal–neonatal iron deficiency. Journal of Nutrition. Advance online publication.CrossRefGoogle Scholar
Knox, S., Ge, H., Dimitroff, B. D., Ren, Y., Howe, K. A., Arsham, A. M., et al. (2007). Mechanisms of TSC-mediated control of synapse assembly and axon guidance. PLoS One, 2, e375.CrossRefGoogle ScholarPubMed
Kretchmer, N., Beard, J. L., & Carlson, S. (1996). The role of nutrition in the development of normal cognition. American Journal of Clinical Nutrition, 63, 997S1001S.CrossRefGoogle ScholarPubMed
Kuzawa, C. W. (1998). Adipose tissue in human infancy and childhood: An evolutionary perspective. Yearbook of Physical Anthropology, 41, 177209.3.0.CO;2-B>CrossRefGoogle Scholar
Lerner, R. (2011). Structure and process in relational, developmental systems theories: A commentary on contemporary changes in the understanding of developmental changes across the life span. Human Development, 54, 3443.CrossRefGoogle Scholar
Liu, D., Diorio, J., Tannenbaum, B., Caldji, C., Francis, D., Freedman, A., et al. (1997). Maternal care, hippocampal glucocorticoid receptors, and hypothalamic–pituitary–adrenal responses to stress. Science, 277, 16591662.CrossRefGoogle ScholarPubMed
Lozoff, B., & Georgieff, M. K. (2006). Iron deficiency and brain development. Seminars in Pediatric Neurology, 13, 158165.CrossRefGoogle ScholarPubMed
Lubin, F. D., Roth, T. L., & Sweatt, J. D. (2008). Epigenetic regulation of BDNF gene during memory consolidation. Journal of Neuroscience, 28, 1057610586.CrossRefGoogle Scholar
Lucassen, P. J., Naninck, E. F., van Goudoever, J. B., Fitzsimons, C., Joels, M., & Korosi, A. (2013). Perinatal programming of adult hippocampal structure and function: Emerging roles of stress, nutrition and epigenetics. Trends in Neuroscience, 36, 621631.CrossRefGoogle ScholarPubMed
Lukowski, A. F., Koss, M., Burden, M. J., Jonides, J., Nelson, C. A., Kaciroti, N., et al. (2010). Iron deficiency in infancy and neurocognitive functioning at 19 years: Evidence of long-term deficits in executive function and recognition memory. Nutritional Neuroscience, 13, 5470.CrossRefGoogle Scholar
Markram, H., Toledo-Rodriguez, M., Wang, Y., Gupta, A., Silberberg, G., & Wu, C. (2004). Interneurons of the neocortical inhibitory system. Nature Reviews Neuroscience, 5, 793807.CrossRefGoogle ScholarPubMed
McEchron, M. D., Cheng, A. Y., Liu, H., Connor, J. R., & Gilmartin, M. R. (2005). Nutritional iron deficiency permanently impairs hippocampus-dependent trace fear conditioning in rats. Nutritional Neuroscience, 8, 195206.CrossRefGoogle ScholarPubMed
Meaney, M. J., Diorio, J., Francis, D., Weaver, S., Yau, J., Chapman, K., et al. (2000). Postnatal handling increases the expression of cAMP-inducible transcription factors in the rat hippocampus: The effects of thyroid hormones and serotonin. Journal of Neuroscience, 20, 39263935.CrossRefGoogle ScholarPubMed
Meck, W. H., Smith, R. A., & Williams, C. L. (1988). Pre- and postnatal choline supplementation produces long-term facilitation of special memory. Developmental Psychobiology, 21, 339353.CrossRefGoogle Scholar
Meck, W. H., Smith, R. A., & Williams, C. L. (1989). Organizational changes in cholinergic activity and enhanced visuospatial memory as a function of choline administered prenatally or postnatally or both. Behavioral Neuroscience, 103, 12341241.CrossRefGoogle ScholarPubMed
Meck, W. H., Williams, C. L., Cermak, J. M., & Blusztajn, J. K. (2008). Developmental periods of choline sensitivity provide an ontogenetic mechanism for regulating memory capacity and age-related dementia. Frontiers in Integrative Neuroscience, 1, 7.CrossRefGoogle ScholarPubMed
Michel, G., & Tyler, A. (2005). Critical period: A history of the transition from questions of when, to what, to how. Developmental Psychobiology, 46, 163183.CrossRefGoogle Scholar
Moon, J., Chen, M., Gandhy, S. U., Strawderman, M., Levitsky, D. A., Maclean, K. N., et al. (2010). Perinatal choline supplementation improves cognitive functioning and emotion regulation in the Ts65Dn mouse model of Down syndrome. Behavioral Neuroscience, 124, 346361.CrossRefGoogle ScholarPubMed
Morishita, H., & Hensch, T. K. (2008). Critical period revisited: Impact on vision. Current Opinion in Neurobiology, 18, 101107.CrossRefGoogle ScholarPubMed
Murray-Kolb, L. E., Khatry, S. K., Katz, J., Schaefer, B. A., Cole, P. M., LeClerq, S. C., et al. (2012). Preschool micronutrient supplementation effects on intellectual and motor function in school-aged Nepalese children. Archives of Pediatric and Adolescent Medicine, 166, 404410.Google ScholarPubMed
Pisansky, M. T., Wickham, R. J., Su, J., Fretham, S., Yuan, L.-L., Sun, M., et al. (2013). Iron deficiency with or without anemia impairs prepulse inhibition of the startle reflex. Hippocampus, 23, 952962.CrossRefGoogle ScholarPubMed
Plato. (1993). Republic (pp. 377a–b), Waterfield, R. (Trans.). New York: Oxford University Press.Google Scholar
Pokorny, J., & Yamamoto, T. (1981). Postnatal ontogenesis of hippocampal CA1 area in rats: I. Development of dendritic arborization in pyramidal neurons. Brain Research Bulletin, 7, 113120.CrossRefGoogle Scholar
Pongcharoen, T., Ramakrishnan, U., DiGirolamo, A. M., Winichagoon, P., Flores, R., Singkhornard, J., et al. (2012). Influence of prenatal and postnatal growth on intellectual functioning in school-aged children. Archives of Pediatric and Adolescent Medicine, 166, 411416.Google ScholarPubMed
Ramel, S. E., Demerath, E. W., Gray, H. L., Younge, N., Boys, C., & Georgieff, M. K. (2012). The relationship of poor linear growth velocity with neonatal illness and two-year neurodevelopment in preterm infants. Neonatology, 102, 1924.CrossRefGoogle ScholarPubMed
Rao, R., Tkac, I., Schmidt, A., & Georgieff, M. (2011). Fetal and neonatal iron deficiency causes volume loss and alters the neurochemical profile of the adult rat hippocampus. Nutritional Neuroscience, 14, 5965.CrossRefGoogle ScholarPubMed
Rice, D., & Barone, S. Jr., (2000). Critical periods of vulnerability for the developing nervous system: Evidence from humans and animal models. Environmental Health Perspectives, 108(Suppl 3), 511533.Google ScholarPubMed
Ricceri, L., De Filippis, B., & Laviola, G. (2013) Rett syndrome treatment in mouse models: Searching for effective targets and strategies. Neuropharmacology, 68, 106115.CrossRefGoogle ScholarPubMed
Riggins, T., Miller, N. C., Bauer, P. B., Georgieff, M. K., & Nelson, C. A. (2009). Consequences of low neonatal iron status due to maternal diabetes mellitus on explicit memory performance in childhood. Developmental Neuropsychlogy, 34, 762779.CrossRefGoogle ScholarPubMed
Roth, T. L., Lubin, F. D., Funk, A. J., & Sweatt, J. D. (2009). Lasting epigenetic influence of early-life adversity on the BDNF gene. Biological Psychiatry, 65, 760769.CrossRefGoogle ScholarPubMed
Ryan, S. H., Williams, J. K., & Thomas, J. D. (2008) Choline supplementation attenuates learning deficits associated with neonatal alcohol exposure in the rat: Effects of varying the timing of choline administration. Brain Research, 1237, 91100.CrossRefGoogle ScholarPubMed
Schmidt, A. T., Waldow, K. J., Grove, W. M., Salinas, J. A., & Georgieff, M. K. (2007). Dissociating the long-term effects of fetal/neonatal iron deficiency on three types of learning in the rat. Behavioral Neuroscience, 121, 475482.CrossRefGoogle ScholarPubMed
Siddappa, A. J., Rao, R. B., Wobken, J. D., Leibold, E. A., Connor, J. R., & Georgieff, M. K. (2002). Developmental changes in the expression of iron regulatory proteins and iron transport proteins in the perinatal rat brain. Journal of Neuroscience Research, 68, 761775.CrossRefGoogle ScholarPubMed
Siddappa, A. M., Georgieff, M. K., Wewerka, S., Worwa, C., Nelson, C. A., & deRegnier, R.-A. (2004). Auditory recognition memory in iron-deficient infants of diabetic mothers. Pediatric Research, 55, 10341041.CrossRefGoogle Scholar
Silveira, P. P., Portella, A. K., Goldani, M. Z., & Barbieri, M. A. (2007). Developmental origins of health and disease (DOHaD). Jornal De Pediatria, 83, 494504.CrossRefGoogle ScholarPubMed
Sugiyama, S., Di Nardo, A. A., Aizawa, S., Matsuo, I., Volovitch, M., Prochiantz, A., et al. (2008). Experience-dependent transfer of Otx2 homeoprotein into the visual cortex activates postnatal plasticity. Cell, 134, 508520.CrossRefGoogle ScholarPubMed
Tang, B. L. (2003). Inhibitors of neuronal regeneration: Mediators and signaling mechanisms. Neurochemistry International, 42, 189203.CrossRefGoogle ScholarPubMed
Thompson, R. A., & Nelson, C. A. (2001). Developmental science and the media: Early brain development. American Psychologist, 56, 515.CrossRefGoogle ScholarPubMed
Townsend, E. L., Georgieff, M. K., & Nelson, C. A. (2005). Neurobehavioral functioning in five-year-old children born to diabetic mothers. Cognite, Creier, Comportament, 9, 363381.Google Scholar
Tran, P. V., Carlson, E. S., Fretham, S. J., & Georgieff, M. K. (2008). Early-life iron deficiency anemia alters neurotrophic factor expression and hippocampal neuron differentiation in male rats. Journal of Nutrition, 138, 24952501.CrossRefGoogle ScholarPubMed
Tran, P. V., Fretham, S. J. B., Carlson, E. S., & Georgieff, M. K. (2009). Long-term reduction of hippocampal BDNF activity following fetal-neonatal iron deficiency in adult rats. Pediatric Research, 65, 493498.CrossRefGoogle Scholar
Wachs, T. D., Georgieff, M., Cusick, S., & McEwan, B. (2014). Issues in the timing of integrated early interventions: Contributions from nutrition, neuroscience and psychological research. Annals of the New York Academy of Sciences, 1308, 89106.CrossRefGoogle ScholarPubMed
Walker, S. P., Wachs, T. D., Gardner, J. M., Lozoff, B., Wasserman, G. A., Pollit, E. A., et al. (2007). Child development: Risk factors for adverse outcomes in developing countries. Lancet, 369, 145157.CrossRefGoogle ScholarPubMed
Wiesel, T. N., & Hubel, D. H. (1963). Effects of visual deprivation on morphology and physiology of cells in the cat's lateral geniculate body. Journal of Neurophysiology, 26, 978993.CrossRefGoogle Scholar
Wong, O. L., & Ghosh, A. (2002). Activity-dependent regulation of dendritic growth and patterning. Nature Reviews Neuroscience, 3, 803812.CrossRefGoogle ScholarPubMed
Wong, R. O. (1999). Retinal waves and visual system development. Annual Review of Neuroscience, 22, 2947.CrossRefGoogle ScholarPubMed
Wullschleger, S., Loewith, R., & Hall, M. N. (2006). TOR signaling in growth and metabolism. Cell, 124, 471484.CrossRefGoogle ScholarPubMed
Yiu, G., & He, Z. (2006). Glial inhibition of CNS axon regeneration. Nature Reviews Neuroscience, 7, 76177627.CrossRefGoogle ScholarPubMed
Zeisel, S. H. (2010). Choline: Clinical nutrigenetic/nutrigenomic approaches for identification of functions and dietary requirements. Journal of Nutrigenetics and Nutrigenomics, 3, 209219.CrossRefGoogle ScholarPubMed