Skip to main content
SpringerLink
Log in

Long-Term Brain and Behavioral Consequences of Early-Life Iron Deficiency

  • Chapter
Fetal Development

Abstract

Early-life iron deficiency anemia affects 30–50 % of pregnancies worldwide and causes deficits in cognitive development as well as socio-emotional abnormalities. More concerning, these deficits persist into adulthood, including increased risks of schizophrenia and depression, despite prompt iron repletion during childhood. Emerging evidence implicates long-term changes in the neural metabolome, proteome, and genome as potential biological bases underlying these effects. In turn, better knowledge of the underlying biology will lead to new methods of identifying young children at risk for brain iron deficiency and adjunct or rescue therapies designed to optimize their outcomes.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Log in via an institution
Chapter
EUR 29.95
Price includes VAT (Finland)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
EUR 128.39
Price includes VAT (Finland)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
EUR 175.99
Price includes VAT (Finland)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
EUR 175.99
Price includes VAT (Finland)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

Similar content being viewed by others

References

  • Aguiar, A. S., Castro, A. A., Moreira, E. L., Glaser, V., Santos, A. R. S., Tasca, C. I., … Prediger, R. D. S. (2011). Short bouts of mild-intensity physical exercise improve spatial learning and memory in aging rats: Involvement of hippocampal plasticity via AKT, CREB and BDNF signaling. Mechanisms of Ageing and Development, 132, 560–567.

    Google Scholar 

  • Aid, T., Kazantseva, A., Piirsoo, M., Palm, K., & Timmusk, T. (2007). Mouse and rat BDNF gene structure and expression revisited. Journal of Neuroscience Research, 85, 525–535.

    Article  PubMed  PubMed Central  Google Scholar 

  • Alder, J., Thakker-Varia, S., Bangasser, D. A., Kuroiwa, M., Plummer, M. R., Shors, T. J., & Black, I. B. (2003). Brain-derived neurotrophic factor-induced gene expression reveals novel actions of VGF in hippocampal synaptic plasticity. The Journal of Neuroscience, 23, 10800–10808.

    Google Scholar 

  • Algarín, C., Peirano, P. D., Garrido, M., Pizarro, F., & Lozoff, B. (2003). Iron deficiency anemia in infancy: Long-lasting effects on auditory and visual system functioning. Pediatric Research, 53, 217–223.

    Article  PubMed  Google Scholar 

  • Allen, R. (2004). Dopamine and iron in the pathophysiology of restless legs syndrome (RLS). Sleep Medicine, 5, 385–391.

    Article  PubMed  Google Scholar 

  • Amin, S. B., Orlando, M., Eddins, A., MacDonald, M., Monczynski, C., & Wang, H. (2010). In utero iron status and auditory neural maturation in premature infants as evaluated by auditory brainstem response. The Journal of Pediatrics, 156, 377–381.

    Article  PubMed  PubMed Central  Google Scholar 

  • Angulo-Kinzler, R. M., Peirano, P. D., Lin, E., Garrido, M., & Lozoff, B. (2002). Spontaneous motor activity in human infants with iron-deficiency anemia. Early Human Development, 66, 67–79.

    Article  PubMed  Google Scholar 

  • Baker, S. J., & DeMaeyer, E. M. (1979). Nutritional anemia: Its understanding and control with special reference to the work of the World Health Organization. The American Journal of Clinical Nutrition, 32, 368–417.

    PubMed  Google Scholar 

  • Beard, J. L., Chen, Q., Connor, J., & Jones, B. C. (1994). Altered monamine metabolism in caudate-putamen of iron-deficient rats. Pharmacology, Biochemistry, and Behavior, 48, 621–624.

    Article  PubMed  Google Scholar 

  • Beard, J. L., Erikson, K. M., & Jones, B. C. (2002). Neurobehavioral analysis of developmental iron deficiency in rats. Behavioural Brain Research, 134, 517–524.

    Article  PubMed  Google Scholar 

  • Beard, J. L., Erikson, K. M., & Jones, B. C. (2003). Neonatal iron deficiency results in irreversible changes in dopamine function in rats. The Journal of Nutrition, 133, 1174–1179.

    PubMed  Google Scholar 

  • Ben-Shachar, D., Ashkenazi, R., & Youdim, M. B. (1986). Long-term consequence of early iron-deficiency on dopaminergic neurotransmission in rats. International Journal of Developmental Neuroscience, 4, 81–88.

    Article  PubMed  Google Scholar 

  • Berasi, S. P., Huard, C., Li, D., Shih, H. H., Sun, Y., Zhong, W., … Martinez, R. V. (2006). Inhibition of gluconeogenesis through transcriptional activation of EGR1 and DUSP4 by AMP-activated kinase. The Journal of Biological Chemistry, 281, 27167–27177.

    Google Scholar 

  • Blegen, M. B., Kennedy, B. C., Thibert, K. A., Gewirtz, J. C., Tran, P. V., & Georgieff, M. K. (2013). Multigenerational effects of fetal-neonatal iron deficiency on hippocampal BDNF signaling. Physiological Reports, 1, e00096.

    Article  PubMed  PubMed Central  Google Scholar 

  • Boehme, F., Gil-Mohapel, J., Cox, A., Patten, A., Giles, E., Brocardo, P. S., & Christie, B. R. (2011). Voluntary exercise induces adult hippocampal neurogenesis and BDNF expression in a rodent model of fetal alcohol spectrum disorders. The European Journal of Neuroscience, 33, 1799–1811.

    Google Scholar 

  • Bourque, S. L., Iqbal, U., Reynolds, J. N., Adams, M. A., & Nakatsu, K. (2008). Perinatal iron deficiency affects locomotor behavior and water maze performance in adult male and female rats. The Journal of Nutrition, 138, 931–937.

    PubMed  Google Scholar 

  • Branchi, I., Francia, N., & Alleva, E. (2004). Epigenetic control of neurobehavioural plasticity: The role of neurotrophins. Behavioural Pharmacology, 15, 353–362.

    Article  PubMed  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, 238–248.

    Article  PubMed  PubMed Central  Google Scholar 

  • 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 Neuroscience, 35, 427–436.

    Article  PubMed  PubMed Central  Google Scholar 

  • Carlson, E. S., Magid, R., Petryk, A., & Georgieff, M. K. (2008). Iron deficiency alters expression of genes implicated in Alzheimer disease pathogenesis. Brain Research, 1237, 75–83.

    Article  PubMed  PubMed Central  Google Scholar 

  • Carlson, E. S., Stead, J. D. H., 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, 679–691.

    Article  PubMed  Google Scholar 

  • Carlson, E. S., Tkac, I., Magid, R., O’Connor, M. B., Andrews, N. C., Schallert, T., … Petryk, A. (2009). Iron is essential for neuron development and memory function in mouse hippocampus. The Journal of Nutrition, 139, 672–679.

    Google Scholar 

  • Carter, R. C., Jacobson, J. L., Burden, M. J., Armony-Sivan, R., Dodge, N. C., Angelilli, M. L., … Jacobson, S. W. (2010). Iron deficiency anemia and cognitive function in infancy. Pediatrics, 126, e427–e434.

    Google Scholar 

  • Chang, S., Wang, L., Wang, Y., Brouwer, I. D., Kok, F. J., Lozoff, B., & Chen, C. (2011). Iron-deficiency anemia in infancy and social emotional development in preschool-aged Chinese children. Pediatrics, 127, e927–e933.

    Google Scholar 

  • Chockalingam, U. M., Murphy, E., Ophoven, J. C., Weisdorf, S. A., & Georgieff, M. K. (1987). Cord transferrin and ferritin values in newborn infants at risk for prenatal uteroplacental insufficiency and chronic hypoxia. The Journal of Pediatrics, 111, 283–286.

    Article  PubMed  Google Scholar 

  • Clardy, S. L., Wang, X., Zhao, W., Liu, W., Chase, G. A., Beard, J. L., … Connor, J. R. (2006). Acute and chronic effects of developmental iron deficiency on mRNA expression patterns in the brain. Journal of Neural Transmission. Supplementum, 173–196.

    Google Scholar 

  • Connor, J. R., & Menzies, S. L. (1996). Relationship of iron to oligodendrocytes and myelination. Glia, 17, 83–93.

    Article  PubMed  Google Scholar 

  • Corapci, F., Radan, A. E., & Lozoff, B. (2006). Iron deficiency in infancy and mother-child interaction at 5 years. Journal of Developmental and Behavioral Pediatrics, 27, 371–378.

    Article  PubMed  PubMed Central  Google Scholar 

  • Cortese, S., Lecendreux, M., Bernardina, B. D., Mouren, M. C., Sbarbati, A., & Konofal, E. (2008). Attention-deficit/hyperactivity disorder, Tourette’s syndrome, and restless legs syndrome: The iron hypothesis. Medical Hypotheses, 70, 1128–1132.

    Article  PubMed  Google Scholar 

  • Dallman, P. R. (1969). Iron restriction in the nursing rat: Early effects upon tissue heme proteins, hemoglobin and liver iron. The Journal of Nutrition, 97, 475–480.

    PubMed  Google Scholar 

  • Dong, M., Wu, Y., Fan, Y., Xu, M., & Zhang, J. (2006). c-fos modulates brain-derived neurotrophic factor mRNA expression in mouse hippocampal CA3 and dentate gyrus neurons. Neuroscience Letters, 400, 177–180.

    Article  PubMed  Google Scholar 

  • Duffy, S. N., Craddock, K. J., Abel, T., & Nguyen, P. V. (2001). Environmental enrichment modifies the PKA-dependence of hippocampal LTP and improves hippocampus-dependent memory. Learning & Memory, 8, 26–34.

    Article  Google Scholar 

  • Erikson, K. M., Jones, B. C., Hess, E. J., Zhang, Q., & Beard, J. L. (2001). Iron deficiency decreases dopamine D1 and D2 receptors in rat brain. Pharmacology, Biochemistry, and Behavior, 69, 409–418.

    Article  PubMed  Google Scholar 

  • Erikson, K. M., Jones, B. C., & Beard, J. L. (2000). Iron deficiency alters dopamine transporter functioning in rat striatum. The Journal of Nutrition, 130, 2831–2837.

    PubMed  Google Scholar 

  • Eseh, R., & Zimmerberg, B. (2005). Age-dependent effects of gestational and lactational iron deficiency on anxiety behavior in rats. Behavioural Brain Research, 164, 214–221.

    Article  PubMed  Google Scholar 

  • Fabel, K., Wolf, S. A., Ehninger, D., Babu, H., Leal-Galicia, P., & Kempermann, G. (2009). Additive effects of physical exercise and environmental enrichment on adult hippocampal neurogenesis in mice. Frontiers in Neuroscience, 3, 50.

    PubMed  PubMed Central  Google Scholar 

  • Felt, B. T., Beard, J. L., Schallert, T., Shao, J., Aldridge, J. W., Connor, J. R., … Lozoff, B. (2006). Persistent neurochemical and behavioral abnormalities in adulthood despite early iron supplementation for perinatal iron deficiency anemia in rats. Behavioural Brain Research, 171, 261–270.

    Google Scholar 

  • Felt, B. T., & Lozoff, B. (1996). Brain iron and behavior of rats are not normalized by treatment of iron deficiency anemia during early development. The Journal of Nutrition, 126, 693–701.

    PubMed  Google Scholar 

  • Francis, F., Koulakoff, A., Boucher, D., Chafey, P., Schaar, B., Vinet, M. C., … Chelly, J. (1999). Doublecortin is a developmentally regulated, microtubule-associated protein expressed in migrating and differentiating neurons. Neuron, 23, 247–256.

    Google Scholar 

  • 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, 1691–1702.

    Article  PubMed  PubMed Central  Google Scholar 

  • Fretham, S. J. B., Carlson, E. S., & Georgieff, M. K. (2011). The role of iron in learning and memory. Advances in Nutrition, 2, 112–121.

    Article  PubMed  PubMed Central  Google Scholar 

  • Geguchadze, R. N., Coe, C. L., Lubach, G. R., Clardy, T. W., Beard, J. L., & Connor, J. R. (2008). CSF proteomic analysis reveals persistent iron deficiency-induced alterations in non-human primate infants. Journal of Neurochemistry, 105, 127–136.

    Article  PubMed  Google Scholar 

  • Georgieff, M. K. (2011). Long-term brain and behavioral consequences of early iron deficiency. Nutrition Reviews, 69, S43–S48.

    Article  PubMed  PubMed Central  Google Scholar 

  • Georgieff, M. K., Berry, S. A., Wobken, J. D., & Leibold, E. A. (1999). Increased placental iron regulatory protein-1 expression in diabetic pregnancies complicated by fetal iron deficiency. Placenta, 20, 87–93.

    Article  PubMed  Google Scholar 

  • Gewirtz, J. C., Hamilton, K. L., Babu, 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, 195–203.

    Article  PubMed  PubMed Central  Google Scholar 

  • Gillian, A. L., & Svaren, J. (2004). The Ddx20/DP103 dead box protein represses transcriptional activation by Egr2/Krox-20. The Journal of Biological Chemistry, 279, 9056–9063.

    Article  PubMed  Google Scholar 

  • 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, 2473–2482.

    Article  PubMed  PubMed Central  Google Scholar 

  • Golub, M. S., Hogrefe, C. E., Tarantal, A. F., Germann, S. L., Beard, J. L., Georgieff, M. K., … Lozoff, B. (2006). Diet-induced iron deficiency anemia and pregnancy outcome in rhesus monkeys. The American Journal of Clinical Nutrition, 83, 647–656.

    Google Scholar 

  • Griesbach, G. S., Hovda, D. A., & Gomez-Pinilla, F. (2009). Exercise-induced improvement in cognitive performance after traumatic brain injury in rats is dependent on BDNF activation. Brain Research, 1288, 105–115.

    Article  PubMed  PubMed Central  Google Scholar 

  • Grosse, G., Djalali, S., Deng, D. R., Höltje, M., Hinz, B., Schwartzkopff, K., … Hörtnag, H. (2005). Area-specific effects of brain-derived neurotrophic factor (BDNF) genetic ablation on various neuronal subtypes of the mouse brain. Developmental Brain Research, 156, 111–126.

    Google Scholar 

  • Guénette, S., Chang, Y., Hiesberger, T., Richardson, J. A., Eckman, C. B., Eckman, E. A., … Herz, J. (2006). Essential roles for the FE65 amyloid precursor protein-interacting proteins in brain development. The EMBO Journal, 25, 420–431.

    Google Scholar 

  • Guseva, M. V., Hopkins, D. M., Scheff, S. W., & Pauly, J. R. (2008). Dietary choline supplementation improves behavioral, histological, and neurochemical outcomes in a rat model of traumatic brain injury. Journal of Neurotrauma, 25, 975–983.

    Article  PubMed  PubMed Central  Google Scholar 

  • Hannigan, J. H., O’Leary-Moore, S. K., & Berman, R. F. (2007). Postnatal environmental or experiential amelioration of neurobehavioral effects of perinatal alcohol exposure in rats. Neuroscience and Biobehavioral Reviews, 31, 202–211.

    Article  PubMed  Google Scholar 

  • Harvey, L., & Boksa, P. (2014). Additive effects of maternal iron deficiency and prenatal immune activation on adult behaviors in rat offspring. Brain, Behavior, and Immunity, 40, 27–37.

    Article  PubMed  Google Scholar 

  • Heldt, S. A., Stanek, L., Chhatwal, J. P., & Ressler, K. J. (2007). Hippocampus-specific deletion of BDNF in adult mice impairs spatial memory and extinction of aversive memories. Molecular Psychiatry, 12, 656–670.

    Article  PubMed  PubMed Central  Google Scholar 

  • Hennigan, A., O’Callaghan, R. M., & Kelly, A. M. (2007). Neurotrophins and their receptors: Roles in plasticity, neurodegeneration and neuroprotection. Biochemical Society Transactions, 35, 424–427.

    Article  PubMed  Google Scholar 

  • Holmes, G. L., Yang, Y., Liu, Z., Cermak, J. M., Sarkisian, M. R., Stafstrom, C. E., … Blusztajn, J. K. (2002). Seizure-induced memory impairment is reduced by choline supplementation before or after status epilepticus. Epilepsy Research, 48, 3–13.

    Google Scholar 

  • Hopkins, M. E., & Bucci, D. J. (2010). BDNF expression in perirhinal cortex is associated with exercise-induced improvement in object recognition memory. Neurobiology of Learning and Memory, 94, 278–284.

    Article  PubMed  PubMed Central  Google Scholar 

  • Ikin, A. F., Sabo, S. L., Lanier, L. M., & Buxbaum, J. D. (2007). A macromolecular complex involving the amyloid precursor protein (APP) and the cytosolic adapter FE65 is a negative regulator of axon branching. Molecular and Cellular Neurosciences, 35, 57–63.

    Article  PubMed  PubMed Central  Google Scholar 

  • Iron deficiency anaemia; report of a study group. (1959). World Health Organization Technical Report Series, 182, 1–15.

    Google Scholar 

  • Jang, S.-W., LeBlanc, S. E., Roopra, A., Wrabetz, L., & Svaren, J. (2006). In vivo detection of Egr2 binding to target genes during peripheral nerve myelination. Journal of Neurochemistry, 98, 1678–1687.

    Article  PubMed  Google Scholar 

  • Jiang, B., Kitamura, A., Yasuda, H., Sohya, K., Maruyama, A., Yanagawa, Y., … Tsumoto, T. (2004). Brain-derived neurotrophic factor acutely depresses excitatory synaptic transmission to GABAergic neurons in visual cortical slices. The European Journal of Neuroscience, 20, 709–718.

    Google Scholar 

  • 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, 1094–1102.

    Article  PubMed  Google Scholar 

  • Jorgenson, L. A., Wobken, J. D., & Georgieff, M. K. (2003). Perinatal iron deficiency alters apical dendritic growth in hippocampal CA1 pyramidal neurons. Developmental Neuroscience, 25, 412–420.

    Article  PubMed  Google Scholar 

  • Jougleux, J.-L., Rioux, F. M., Church, M. W., Fiset, S., & Surette, M. E. (2014). Mild iron deficiency anaemia during pregnancy and lactation in guinea pigs alters amplitudes and auditory nerve velocity, but not brainstem transmission times in the offspring’s auditory brainstem response. Nutritional Neuroscience, 17, 37–47.

    Article  PubMed  Google Scholar 

  • Kennedy, B. C., Dimova, J. G., Siddappa, A. J. M., Tran, P. V., Gewirtz, J. C., & Georgieff, M. K. (2014). Prenatal choline supplementation ameliorates the long-term neurobehavioral effects of fetal-neonatal iron deficiency in rats. The Journal of Nutrition, 144, 1858–1865.

    Article  PubMed  PubMed Central  Google Scholar 

  • Konofal, E., Lecendreux, M., Arnulf, I., & Mouren, M.-C. (2004). Iron deficiency in children with attention-deficit/hyperactivity disorder. Archives of Pediatrics & Adolescent Medicine, 158, 1113–1115.

    Article  Google Scholar 

  • Korte, M., Carroll, P., Wolf, E., Brem, G., Thoenen, H., & Bonhoeffer, T. (1995). Hippocampal long-term potentiation is impaired in mice lacking brain-derived neurotrophic factor. Proceedings of the National Academy of Sciences of the United States of America, 92, 8856–8860.

    Google Scholar 

  • Kwik-Uribe, C. L., Golub, M. S., & Keen, C. L. (2000). Chronic marginal iron intakes during early development in mice alter brain iron concentrations and behavior despite postnatal iron supplementation. The Journal of Nutrition, 130, 2040–2048.

    PubMed  Google Scholar 

  • Lee, D. L., Strathmann, F. G., Gelein, R., Walton, J., & Mayer-Pröschel, M. (2012). Iron deficiency disrupts axon maturation of the developing auditory nerve. The Journal of Neuroscience, 32, 5010–5015.

    Article  PubMed  PubMed Central  Google Scholar 

  • Levitsky, D. A., & Barnes, R. H. (1972). Nutritional and environmental interactions in the behavioral development of the rat: Long-term effects. Science, 176, 68–71.

    Article  PubMed  Google Scholar 

  • Levitsky, D. A., & Strupp, B. J. (1995). Malnutrition and the brain: Changing concepts, changing concerns. The Journal of Nutrition, 125, 2212S–2220S.

    PubMed  Google Scholar 

  • Li, Q. (2004). Dietary prenatal choline supplementation alters postnatal hippocampal structure and function. Journal of Neurophysiology, 91, 1545–1555.

    Article  PubMed  Google Scholar 

  • Li, Y., Kim, J., Buckett, P. D., Bohlke, M., Maher, T. J., & Wessling-Resnick, M. (2011). Severe postnatal iron deficiency alters emotional behavior and dopamine levels in the prefrontal cortex of young male rats. Journal of Nutrition, 141, 2133–2138.

    Article  PubMed  PubMed Central  Google Scholar 

  • Lozoff, B. (2011). Early iron deficiency has brain and behavior effects consistent with dopaminergic dysfunction. Journal of Nutrition, 141, 740S–746S.

    Article  PubMed  PubMed Central  Google Scholar 

  • Lozoff, B., Beard, J. L., Connor, J., Felt, B. T., Georgieff, M. K., & Schallert, T. (2006). Long-lasting neural and behavioral effects of iron deficiency in infancy. Nutrition Reviews, 64, S34–43; discussion S72–91.

    Google Scholar 

  • Lozoff, B., Brittenham, G. M., Viteri, F. E., Wolf, A. W., & Urrutia, J. J. (1982). Developmental deficits in iron-deficient infants: Effects of age and severity of iron lack. The Journal of Pediatrics, 101, 948–952.

    Article  PubMed  Google Scholar 

  • Lozoff, B., Brittenham, G. M., Wolf, A. W., McClish, D. K., Kuhnert, P. M., Jimenez, E., … Krauskoph, D. (1987). Iron deficiency anemia and iron therapy effects on infant developmental test performance. Pediatrics, 79, 981–995.

    Google Scholar 

  • Lozoff, B., Castillo, M., Clark, K. M., Smith, J. B., & Sturza, J. (2014). Iron supplementation in infancy contributes to more adaptive behavior at 10 years of age. The Journal of Nutrition, 144, 838–845.

    Article  PubMed  PubMed Central  Google Scholar 

  • Lozoff, B., Clark, K. M., Jing, Y., Armony-Sivan, R., Angelilli, M. L., & Jacobson, S. W. (2008). Dose-response relationships between iron deficiency with or without anemia and infant social-emotional behavior. The Journal of Pediatrics, 152(696–702), 702.31–702.33.

    Google Scholar 

  • Lozoff, B., Corapci, F., Burden, M. J., Kaciroti, N., Angulo-Barroso, R., Sazawal, S., & Black, M. (2007). Preschool-aged children with iron deficiency anemia show altered affect and behavior. The Journal of Nutrition, 137, 683–689.

    Google Scholar 

  • Lozoff, B., De Andraca, I., Castillo, M., Smith, J. B., Walter, T., & Pino, P. (2003). Behavioral and developmental effects of preventing iron-deficiency anemia in healthy full-term infants. Pediatrics, 112, 846–854.

    PubMed  Google Scholar 

  • Lozoff, B., Jimenez, E., Hagen, J., Mollen, E., & Wolf, A. W. (2000). Poorer behavioral and developmental outcome more than 10 years after treatment for iron deficiency in infancy. Pediatrics, 105, E51.

    Article  PubMed  Google Scholar 

  • Lozoff, B., Jimenez, E., & Wolf, A. W. (1991). Long-term developmental outcome of infants with iron deficiency. The New England Journal of Medicine, 325, 687–694.

    Article  PubMed  Google Scholar 

  • Lozoff, B., Klein, N. K., Nelson, E. C., McClish, D. K., Manuel, M., & Chacon, M. E. (1998). Behavior of infants with iron-deficiency anemia. Child Development, 69, 24–36.

    Article  PubMed  Google Scholar 

  • Lozoff, B., Smith, J. B., Clark, K. M., Perales, C. G., Rivera, F., & Castillo, M. (2010). Home intervention improves cognitive and social-emotional scores in iron-deficient anemic infants. Pediatrics, 126, e884–e894.

    Article  PubMed  PubMed Central  Google Scholar 

  • Lozoff, B., Smith, J. B., Kaciroti, N., Clark, K. M., Guevara, S., & Jimenez, E. (2013). Functional significance of early-life iron deficiency: Outcomes at 25 years. The Journal of Pediatrics, 163, 1260–1266.

    Article  PubMed  Google Scholar 

  • Lozoff, B., Wolf, A. W., Urrutia, J. J., & Viteri, F. E. (1985). Abnormal behavior and low developmental test scores in iron-deficient anemic infants. Journal of Developmental and Behavioral Pediatrics, 6, 69–75.

    Article  PubMed  Google Scholar 

  • Lubach, G. R., & Coe, C. L. (2008). Selective impairment of cognitive performance in the young monkey following recovery from iron deficiency. Journal of Developmental and Behavioral Pediatrics, 29, 11–17.

    PubMed  Google Scholar 

  • Lukowski, A. F., Koss, M., Burden, M. J., Jonides, J., Nelson, C. A., Kaciroti, N., … Lozoff, B. (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, 54–70.

    Google Scholar 

  • Luo, C. X., Jiang, J., Zhou, Q. G., Zhu, X. J., Wang, W., Zhang, Z. J., … Zhu, D. Y. (2007). Voluntary exercise-induced neurogenesis in the postischemic dentate gyrus is associated with spatial memory recovery from stroke. Journal of Neuroscience Research, 85, 1637–1646.

    Google Scholar 

  • Malenka, R. C. (2003). The long-term potential of LTP. Nature Reviews. Neuroscience, 4, 923–926.

    Article  PubMed  Google Scholar 

  • Marty, S., Carroll, P., Cellerino, A., Castrén, E., Staiger, V., Thoenen, H., & Lindholm, D. (1996). Brain-derived neurotrophic factor promotes the differentiation of various hippocampal nonpyramidal neurons, including Cajal-Retzius cells, in organotypic slice cultures. The Journal of Neuroscience, 16, 675–687.

    Google Scholar 

  • McAllister, A. K., Katz, L. C., & Lo, D. C. (1999). Neurotrophins and synaptic plasticity. Annual Review of Neuroscience, 22, 295–318.

    Article  PubMed  Google Scholar 

  • McEchron, M. D., Cheng, A. Y., Liu, H., Connor, J. R., & Gilmartin, M. R. (2005). Perinatal nutritional iron deficiency permanently impairs hippocampus-dependent trace fear conditioning in rats. Nutritional Neuroscience, 8, 195–206.

    Article  PubMed  Google Scholar 

  • McLean, E., Cogswell, M., Egli, I., Wojdyla, D., & de Benoist, B. (2009). Worldwide prevalence of anaemia, WHO Vitamin and Mineral Nutrition Information System, 1993–2005. Public Health Nutrition, 12, 444–454.

    Article  PubMed  Google Scholar 

  • Meck, W. H., Williams, C. L., Cermak, J. M., & Blusztajn, J. K. (2007). Developmental periods of choline sensitivity provide an ontogenetic mechanism for regulating memory capacity and age-related dementia. Frontiers in Integrative Neuroscience, 1, 7.

    Article  PubMed  PubMed Central  Google Scholar 

  • Miyamoto, E. (2006). Molecular mechanism of neuronal plasticity: Induction and maintenance of long-term potentiation in the hippocampus. Journal of Pharmacological Sciences, 100, 433–442.

    Article  PubMed  Google Scholar 

  • Moon, J., Chen, M., Gandhy, S. U., Strawderman, M., Levitsky, D. A., Maclean, K. N., & Strupp, B. J. (2010). Perinatal choline supplementation improves cognitive functioning and emotion regulation in the Ts65Dn mouse model of Down syndrome. Behavioral Neuroscience, 124, 346–361.

    Google Scholar 

  • Morath, D. J., & Mayer-Pröschel, M. (2002). Iron deficiency during embryogenesis and consequences for oligodendrocyte generation in vivo. Developmental Neuroscience, 24, 197–207.

    Article  PubMed  Google Scholar 

  • Morley-Fletcher, S., Rea, M., Maccari, S., & Laviola, G. (2003). Environmental enrichment during adolescence reverses the effects of prenatal stress on play behaviour and HPA axis reactivity in rats. The European Journal of Neuroscience, 18, 3367–3374.

    Article  PubMed  Google Scholar 

  • Muñoz, P., Humeres, A., Elgueta, C., Kirkwood, A., Hidalgo, C., & Núñez, M. T. (2011). Iron mediates N-methyl-D-aspartate receptor-dependent stimulation of calcium-induced pathways and hippocampal synaptic plasticity. The Journal of Biological Chemistry, 286, 13382–13392.

    Article  PubMed  PubMed Central  Google Scholar 

  • Olney, D. K., Pollitt, E., Kariger, P. K., Khalfan, S. S., Ali, N. S., Tielsch, J. M., … Stoltzfus, R. J. (2007). Young Zanzibari children with iron deficiency, iron deficiency anemia, stunting, or malaria have lower motor activity scores and spend less time in locomotion. The Journal of Nutrition, 137, 2756–2762.

    Google Scholar 

  • Olson, A. K., Eadie, B. D., Ernst, C., & Christie, B. R. (2006). Environmental enrichment and voluntary exercise massively increase neurogenesis in the adult hippocampus via dissociable pathways. Hippocampus, 16, 250–260.

    Article  PubMed  Google Scholar 

  • Ortiz, E., Pasquini, J. M., Thompson, K., Felt, B. T., Butkus, G., Beard, J. L., & Connor, J. R. (2004). Effect of manipulation of iron storage, transport, or availability on myelin composition and brain iron content in three different animal models. Journal of Neuroscience Research, 77, 681–689.

    Google Scholar 

  • Patterson, S. L., Grover, L. M., Schwartzkroin, P. A., & Bothwell, M. (1992). Neurotrophin expression in rat hippocampal slices: A stimulus paradigm inducing LTP in CA1 evokes increases in BDNF and NT-3 mRNAs. Neuron, 9, 1081–1088.

    Article  PubMed  Google Scholar 

  • Patton, S. M., Coe, C. L., Lubach, G. R., & Connor, J. R. (2012). Quantitative proteomic analyses of cerebrospinal fluid using iTRAQ in a primate model of iron deficiency anemia. Developmental Neuroscience, 34, 354–365.

    Article  PubMed  PubMed Central  Google Scholar 

  • Peirano, P. D., Algarin, C., Chamorro, R., Manconi, M., Lozoff, B., & Ferri, R. (2012). Iron deficiency anemia in infancy exerts long-term effects on the tibialis anterior motor activity during sleep in childhood. Sleep Medicine, 13, 1006–1012.

    Article  PubMed  Google Scholar 

  • Peirano, P. D., Algarín, C., Garrido, M., Algarín, D., & Lozoff, B. (2007). Iron-deficiency anemia is associated with altered characteristics of sleep spindles in NREM sleep in infancy. Neurochemical Research, 32, 1665–1672.

    Article  PubMed  PubMed Central  Google Scholar 

  • Peirano, P. D., Algarín, C. R., Garrido, M. I., & Lozoff, B. (2007). Iron deficiency anemia in infancy is associated with altered temporal organization of sleep states in childhood. Pediatric Research, 62, 715–719.

    Article  PubMed  PubMed Central  Google Scholar 

  • Petry, C. D., Eaton, M. A., Wobken, J. D., Mills, M. M., Johnson, D. E., & Georgieff, M. K. (1992). Iron deficiency of liver, heart, and brain in newborn infants of diabetic mothers. The Journal of Pediatrics, 121, 109–114.

    Article  PubMed  Google Scholar 

  • Pham, T. M., Winblad, B., Granholm, A.-C., & Mohammed, A. H. (2002). Environmental influences on brain neurotrophins in rats. Pharmacology, Biochemistry, and Behavior, 73, 167–175.

    Article  PubMed  Google Scholar 

  • Piñero, D., Jones, B., & Beard, J. L. (2001). Variations in dietary iron alter behavior in developing rats. The Journal of Nutrition, 131, 311–318.

    PubMed  Google Scholar 

  • Pisansky, M. T., Wickham, R. J., Su, J., Fretham, S. J. B., Yuan, L.-L., Sun, M., … Georgieff, M. K. (2013). Iron deficiency with or without anemia impairs prepulse inhibition of the startle reflex: Iron deficiency impairs prepulse inhibition. Hippocampus, 23, 952–962.

    Google Scholar 

  • Pokorný, J., & Yamamoto, T. (1981). Postnatal ontogenesis of hippocampal CA1 area in rats. I. Development of dendritic arborisation in pyramidal neurons. Brain Research Bulletin, 7, 113–120.

    Article  PubMed  Google Scholar 

  • Pyapali, G. K., Turner, D. A., Williams, C. L., Meck, W. H., & Swartzwelder, H. S. (1998). Prenatal dietary choline supplementation decreases the threshold for induction of long-term potentiation in young adult rats. Journal of Neurophysiology, 79, 1790–1796.

    PubMed  Google Scholar 

  • Rao, R., Tkac, I., Schmidt, A. T., & Georgieff, M. K. (2011). Fetal and neonatal iron deficiency causes volume loss and alters the neurochemical profile of the adult rat hippocampus. Nutritional Neuroscience, 14, 59–65.

    Article  PubMed  PubMed Central  Google Scholar 

  • Rao, R., Tkac, I., Townsend, E. L., Ennis, K., Gruetter, R., & Georgieff, M. K. (2007). Perinatal iron deficiency predisposes the developing rat hippocampus to greater injury from mild to moderate hypoxia-ischemia. Journal of Cerebral Blood Flow and Metabolism, 27, 729–740.

    Article  PubMed  PubMed Central  Google Scholar 

  • Rao, R., Tkac, I., Townsend, E. L., Gruetter, R., & Georgieff, M. K. (2003). Perinatal iron deficiency alters the neurochemical profile of the developing rat hippocampus. The Journal of Nutrition, 133, 3215–3221.

    PubMed  Google Scholar 

  • Restivo, L., Ferrari, F., Passino, E., Sgobio, C., Bock, J., Oostra, B. A., … Ammassari-Teule, M. (2005). Enriched environment promotes behavioral and morphological recovery in a mouse model for the fragile X syndrome. Proceedings of the National Academy of Sciences of the United States of America, 102, 11557–11562.

    Google Scholar 

  • Roncagliolo, M., Garrido, M., Walter, T., Peirano, P. D., & Lozoff, B. (1998). Evidence of altered central nervous system development in infants with iron deficiency anemia at 6 mo: Delayed maturation of auditory brainstem responses. The American Journal of Clinical Nutrition, 68, 683–690.

    PubMed  Google Scholar 

  • Rössler, O. G., & Thiel, G. (2004). Brain-derived neurotrophic factor-, epidermal growth factor-, or A-Raf-induced growth of HaCaT keratinocytes requires extracellular signal-regulated kinase. American Journal of Physiology. Cell Physiology, 286, C1118–C1129.

    Article  PubMed  Google Scholar 

  • 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, 760–769.

    Article  PubMed  PubMed Central  Google Scholar 

  • Rotwein, P., Burgess, S. K., Milbrandt, J. D., & Krause, J. E. (1988). Differential expression of insulin-like growth factor genes in rat central nervous system. Proceedings of the National Academy of Sciences of the United States of America, 85, 265–269.

    Article  PubMed  PubMed Central  Google Scholar 

  • Russo-Neustadt, A. A., Beard, R. C., Huang, Y. M., & Cotman, C. W. (2000). Physical activity and antidepressant treatment potentiate the expression of specific brain-derived neurotrophic factor transcripts in the rat hippocampus. Neuroscience, 101, 305–312.

    Article  PubMed  Google Scholar 

  • 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, 91–100.

    Article  PubMed  PubMed Central  Google Scholar 

  • Salmon, H. A. (1962). The cytochrome c content of the heart, kidney, liver and skeletal muscle of iron-deficient rats. The Journal of Physiology, 164, 17–30.

    Article  PubMed  PubMed Central  Google Scholar 

  • 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, 475–482.

    Article  PubMed  Google Scholar 

  • Schneider, T., Turczak, J., & Przewłocki, R. (2006). Environmental enrichment reverses behavioral alterations in rats prenatally exposed to valproic acid: Issues for a therapeutic approach in autism. Neuropsychopharmacology, 31, 36–46.

    PubMed  Google Scholar 

  • Schratt, G. M., Nigh, E. A., Chen, W. G., Hu, L., & Greenberg, M. E. (2004). BDNF regulates the translation of a select group of mRNAs by a mammalian target of rapamycin-phosphatidylinositol 3-kinase-dependent pathway during neuronal development. The Journal of Neuroscience, 24, 7366–7377.

    Article  PubMed  Google Scholar 

  • Schrijver, N. C. A., Bahr, N. I., Weiss, I. C., & Würbel, H. (2002). Dissociable effects of isolation rearing and environmental enrichment on exploration, spatial learning and HPA activity in adult rats. Pharmacology, Biochemistry, and Behavior, 73, 209–224.

    Article  PubMed  Google Scholar 

  • Shafir, T., Angulo-Barroso, R., Jing, Y., Angelilli, M. L., Jacobson, S. W., & Lozoff, B. (2008). Iron deficiency and infant motor development. Early Human Development, 84, 479–485.

    Article  PubMed  PubMed Central  Google Scholar 

  • Siddappa, A. J. M., Georgieff, M. K., Wewerka, S., Worwa, C., Nelson, C. A., & Deregnier, R.-A. (2004). Iron deficiency alters auditory recognition memory in newborn infants of diabetic mothers. Pediatric Research, 55, 1034–1041.

    Article  PubMed  Google Scholar 

  • Siddappa, A. J. M., 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, 761–775.

    Article  PubMed  Google Scholar 

  • Soewondo, S., Husaini, M., & Pollitt, E. (1989). Effects of iron deficiency on attention and learning processes in preschool children: Bandung, Indonesia. The American Journal of Clinical Nutrition, 50, 667–673. discussion 673–674.

    PubMed  Google Scholar 

  • Sperandio, S., Fortin, J., Sasik, R., Robitaille, L., Corbeil, J., & de Belle, I. (2009). The transcription factor Egr1 regulates the HIF-1alpha gene during hypoxia. Molecular Carcinogenesis, 48, 38–44.

    Article  PubMed  Google Scholar 

  • Steward, O., & Falk, P. M. (1991). Selective localization of polyribosomes beneath developing synapses: A quantitative analysis of the relationships between polyribosomes and developing synapses in the hippocampus and dentate gyrus. The Journal of Comparative Neurology, 314, 545–557.

    Article  PubMed  Google Scholar 

  • Stoltzfus, R. (2001). Defining iron-deficiency anemia in public health terms: A time for reflection. The Journal of Nutrition, 131, 565S–567S.

    PubMed  Google Scholar 

  • Suzuki, S., Kiyosue, K., Hazama, S., Ogura, A., Kashihara, M., Hara, T., … Kojima, M. (2007). Brain-derived neurotrophic factor regulates cholesterol metabolism for synapse development. The Journal of Neuroscience, 27, 6417–6427.

    Google Scholar 

  • Sweet, D. G., Savage, G., Tubman, T. R., Lappin, T. R., & Halliday, H. L. (2001). Study of maternal influences on fetal iron status at term using cord blood transferrin receptors. Archives of Disease in Childhood. Fetal and Neonatal Edition, 84, F40–F43.

    Article  PubMed  PubMed Central  Google Scholar 

  • Tamura, T., Goldenberg, R. L., Hou, J., Johnston, K. E., Cliver, S. P., Ramey, S. L., & Nelson, K. G. (2002). Cord serum ferritin concentrations and mental and psychomotor development of children at five years of age. The Journal of Pediatrics, 140, 165–170.

    Google Scholar 

  • Tang, S. J., Reis, G., Kang, H., Gingras, A.-C., Sonenberg, N., & Schuman, E. M. (2002). A rapamycin-sensitive signaling pathway contributes to long-term synaptic plasticity in the hippocampus. Proceedings of the National Academy of Sciences of the United States of America, 99, 467–472.

    Article  PubMed  PubMed Central  Google Scholar 

  • Taylor, E. M., & Morgan, E. H. (1990). Developmental changes in transferrin and iron uptake by the brain in the rat. Developmental Brain Research, 55, 35–42.

    Article  PubMed  Google Scholar 

  • Timmusk, T., Palm, K., Metsis, M., Reintam, T., Paalme, V., Saarma, M., & Persson, H. (1993). Multiple promoters direct tissue-specific expression of the rat BDNF gene. Neuron, 10, 475–489.

    Google Scholar 

  • Todorich, B., Pasquini, J. M., Garcia, C. I., Paez, P. M., & Connor, J. R. (2009). Oligodendrocytes and myelination: The role of iron. Glia, 57, 467–478.

    Article  PubMed  Google Scholar 

  • Tran, P. V., Carlson, E. S., Fretham, S. J. B., & Georgieff, M. K. (2008). Early-life iron deficiency anemia alters neurotrophic factor expression and hippocampal neuron differentiation in male rats. The Journal of Nutrition, 138, 2495–2501.

    Article  PubMed  PubMed Central  Google Scholar 

  • Tran, P. V., Dakoji, S., Reise, K. H., Storey, K. K., & Georgieff, M. K. (2013). Fetal iron deficiency alters proteome of adult rat hippocampal synaptosomes. American Journal of Physiology. Regulatory, Integrative and Comparative Physiology, 305, R1297–R1306.

    Article  PubMed  PubMed Central  Google Scholar 

  • Tran, P. V., Fretham, S. J. B., Carlson, E. S., & Georgieff, M. K. (2009). Long-term reduction of hippocampal brain-derived neurotrophic factor activity after fetal-neonatal iron deficiency in adult rats. Pediatric Research, 65, 493–498.

    Article  PubMed  PubMed Central  Google Scholar 

  • Tran, P. V., Fretham, S. J. B., Wobken, J., Miller, B. S., & Georgieff, M. K. (2012). Gestational-neonatal iron deficiency suppresses and iron treatment reactivates IGF signaling in developing rat hippocampus. American Journal of Physiology. Endocrinology and Metabolism, 302, E316–E324.

    Article  PubMed  PubMed Central  Google Scholar 

  • Tran, P. V., Kennedy, B. C., Lien, Y.-C., Simmons, R. A., & Georgieff, M. K. (2014). Fetal iron deficiency induces chromatin remodeling at the Bdnf locus in adult rat hippocampus. American Journal of Physiology. Regulatory, Integrative and Comparative Physiology, 308(4), R276–R282.

    Article  PubMed  PubMed Central  Google Scholar 

  • Unger, E. L., Hurst, A. R., Georgieff, M. K., Schallert, T., Rao, R., Connor, J. R., … Felt, B. T. (2012). Behavior and monoamine deficits in prenatal and perinatal iron deficiency are not corrected by early postnatal moderate-iron or high-iron diets in rats. The Journal of Nutrition, 142, 2040–2049.

    Google Scholar 

  • Van Praag, H., Kempermann, G., & Gage, F. H. (2000). Neural consequences of environmental enrichment. Nature Reviews. Neuroscience, 1, 191–198.

    Article  PubMed  Google Scholar 

  • Vaynman, S., Ying, Z., & Gómez-Pinilla, F. (2004). Exercise induces BDNF and synapsin I to specific hippocampal subfields. Journal of Neuroscience Research, 76, 356–362.

    Article  PubMed  Google Scholar 

  • Wainwright, P. E., Lévesque, S., Krempulec, L., Bulman-Fleming, B., & McCutcheon, D. (1993). Effects of environmental enrichment on cortical depth and Morris-maze performance in B6D2F2 mice exposed prenatally to ethanol. Neurotoxicology and Teratology, 15, 11–20.

    Article  PubMed  Google Scholar 

  • Walter, T., De Andraca, I., Chadud, P., & Perales, C. G. (1989). Iron deficiency anemia: Adverse effects on infant psychomotor development. Pediatrics, 84, 7–17.

    PubMed  Google Scholar 

  • Ward, K. L., Tkac, I., Jing, Y., Felt, B. T., Beard, J. L., Connor, J., … Rao, R. (2007). Gestational and lactational iron deficiency alters the developing striatal metabolome and associated behaviors in young rats. The Journal of Nutrition, 137, 1043–1049.

    Google Scholar 

  • Winter, B., Breitenstein, C., Mooren, F. C., Voelker, K., Fobker, M., Lechtermann, A., … Knecht, S. (2007). High impact running improves learning. Neurobiology of Learning and Memory, 87, 597–609.

    Google Scholar 

  • Wu, L.-L., Zhang, L., Shao, J., Qin, Y.-F., Yang, R.-W., & Zhao, Z.-Y. (2008). Effect of perinatal iron deficiency on myelination and associated behaviors in rat pups. Behavioural Brain Research, 188, 263–270.

    Article  PubMed  Google Scholar 

  • Ye, P., Li, L., Richards, R. G., DiAugustine, R. P., & D’Ercole, A. J. (2002). Myelination is altered in insulin-like growth factor-I null mutant mice. The Journal of Neuroscience, 22, 6041–6051.

    PubMed  Google Scholar 

  • Youdim, M. B., Ashkenazi, R., Ben-Shachar, D., & Yehuda, S. (1984). Modulation of dopamine receptor in the striatum by iron: Behavioral and biochemical correlates. Advances in Neurology, 40, 159–170.

    PubMed  Google Scholar 

  • Youdim, M. B., & Green, A. R. (1978). Iron deficiency and neurotransmitter synthesis and function. The Proceedings of the Nutrition Society, 37, 173–179.

    Article  PubMed  Google Scholar 

  • Youdim, M. B., Yehuda, S., & Ben-Uriah, Y. (1981). Iron deficiency-induced circadian rhythm reversal of dopaminergic-mediated behaviours and thermoregulation in rats. European Journal of Pharmacology, 74, 295–301.

    Article  PubMed  Google Scholar 

  • Yu, G. S., Steinkirchner, T. M., Rao, G. A., & Larkin, E. C. (1986). Effect of prenatal iron deficiency on myelination in rat pups. The American Journal of Pathology, 125, 620–624.

    PubMed  PubMed Central  Google Scholar 

  • Zimmermann, M. B., & Hurrell, R. F. (2007). Nutritional iron deficiency. Lancet, 370, 511–520.

    Article  PubMed  Google Scholar 

Download references

Acknowledgment

Supported in part by a grant from the National Institutes of Health (R01 HD-029421) to MKG.

Author information

Authors and Affiliations

  1. Graduate Program in Neuroscience, University of Minnesota, Minneapolis, MN, USA

    Bruce C. Kennedy BS & Diana J. Wallin BS

  2. Center for Neurobehavioral Development, University of Minnesota, Minneapolis, MN, USA

    Bruce C. Kennedy BS, Diana J. Wallin BS, Phu V. Tran PhD & Michael K. Georgieff MD

  3. Department of Pediatrics, Neonatology Division, University of Minnesota, Minneapolis, MN, USA

    Phu V. Tran PhD & Michael K. Georgieff MD

Authors
  1. Bruce C. Kennedy BS
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Diana J. Wallin BS
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Phu V. Tran PhD
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Michael K. Georgieff MD
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Michael K. Georgieff MD .

Editor information

Editors and Affiliations

  1. Dept. Psychology Science Laboratories, University of Durham, Durham, United Kingdom

    Nadja Reissland

  2. Queen’s University, School of Nursing Queen’s University, KINGSTON, Ontario, Canada

    Barbara S. Kisilevsky

Rights and permissions

Reprints and permissions

Copyright information

© 2016 Springer International Publishing Switzerland

About this chapter

Cite this chapter

Kennedy, B.C., Wallin, D.J., Tran, P.V., Georgieff, M.K. (2016). Long-Term Brain and Behavioral Consequences of Early-Life Iron Deficiency. In: Reissland, N., Kisilevsky, B. (eds) Fetal Development. Springer, Cham. https://doi.org/10.1007/978-3-319-22023-9_15

Download citation

Publish with us

Policies and ethics

Search

Navigation