Persistent neurochemical and behavioral abnormalities in adulthood despite early iron supplementation for perinatal iron deficiency anemia in rats

Behavioural Brain Research

Volumn 171, Issue 2, 2006, Pages 261-270

  Felt, Barbara T ^a   Beard, John L ^b   Schallert, Timothy ^c   Shao, Jie ^a   Aldridge, J Wayne ^d   Connor, James R ^e   Georgieff, Michael K ^f   Lozoff, Betsy ^a  

^a UNIVERSITY OF MICHIGAN   (United States)

^b PENNSYLVANIA STATE UNIVERSITY   (United States)

^c UNIVERSITY OF TEXAS AT AUSTIN   (United States)

^d UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

^e PENN STATE MILTON S HERSHEY MEDICAL CENTER   (United States)

^f UNIVERSITY OF MINNESOTA   (United States)

Author keywords

Behavior; Brain; Dopamine; Iron deficiency anemia; Rat; Serotonin

Indexed keywords

BRAIN MONOAMINE; DOPAMINE; DOPAMINE RECEPTOR; DOPAMINE TRANSPORTER; IRON; SEROTONIN TRANSPORTER;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BEHAVIOR; BEHAVIOR DISORDER; BRAIN DYSFUNCTION; BRAIN REGION; CONCENTRATION (PARAMETERS); CONTROLLED STUDY; CORPUS STRIATUM; DIET SUPPLEMENTATION; DOPAMINE BRAIN LEVEL; FEMALE; GESTATION PERIOD; HIPPOCAMPUS; IRON DEFICIENCY ANEMIA; IRON RESTRICTION; IRON THERAPY; LACTATION; MALE; MAZE TEST; MENTAL DEFICIENCY; MONOAMINERGIC SYSTEM; NEUROCHEMISTRY; NEWBORN; NONHUMAN; PERINATAL PERIOD; PRIORITY JOURNAL; PROGENY; RAT; SENSORIMOTOR FUNCTION; TASK PERFORMANCE; THALAMUS; VIBRISSA; WEANING;

ANEMIA, IRON-DEFICIENCY; ANIMALS; BEHAVIOR, ANIMAL; DOPAMINE; FEMALE; HIPPOCAMPUS; IRON; MALE; MAZE LEARNING; MOTOR ACTIVITY; NEOSTRIATUM; PREGNANCY; PRENATAL EXPOSURE DELAYED EFFECTS; RANDOM ALLOCATION; RATS; RATS, SPRAGUE-DAWLEY; SEX FACTORS;

EID: 33745402807     PISSN: 01664328     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bbr.2006.04.001     Document Type: Article

References (59)

1. Grantham-McGregor S., and Ani C. A review of studies on the effect of iron deficiency on cognitive development in children. J Nutr 131 (2001) 649S-668S
2. Lozoff B., Brittenham G.M., Wolf A.W., McClish D.K., Kuhnert P.M., Jimenez E., et al. Iron deficiency anemia and iron therapy: effects on infant developmental test performance. Pediatrics 79 (1987) 981-995
3. Lozoff B., Jimenez E., and Wolf A.W. Long-term developmental outcome of infants with iron deficiency. N Engl J Med 325 (1991) 687-694
4. Lozoff B., Jimenez E., Hagen J., Mollen E., and Wolf A.W. Poorer behavioral and developmental outcome more than 10 years after treatment for iron deficiency in infancy. Pediatrics 105 (2000) E51
5. Beard J.L., and Connor J.R. Iron status and neural functioning. Ann Rev Nutr 23 (2003) 41-58
6. Youdim M.B.H., Ben-Shachar D., and Yehuda S. Putative biological mechanisms of the effect of iron deficiency on brain biochemistry and behavior. Am J Clin Nutr 50 (1989) 607-617
7. Pinero D., Jones B., and Beard J.L. Variations in dietary iron alter behavior in developing rats. J Nutr 131 (2001) 311-318
8. Felt B.T., and Lozoff B. Brain iron and behavior of rats are not normalized by treatment of iron deficiency anemia during early development. J Nutr 126 (1996) 693-701
9. Kwik-Uribe C.L., Gietzen D., German J.B., Golub M.S., and Keen C.L. Chronic marginal iron intakes during early development in mice result in persistent changes in dopamine metabolism and myelin composition. J Nutr 130 (2000) 2821-2830
10. Weinberg J., Dallman P.R., and Levine S. Iron deficiency during early development in the rat: behavioral and physiological consequences. Pharmacol Biochem Behav 12 (1980) 493-502
11. Findlay E., Reid R.L., Ng K.T., and Armstrong S.M. The effect of iron deficiency during development on passive avoidance learning in the adult rat. Physiol Behav 27 (1981) 1089-1096
12. Weinberg J., Levine S., and Dallman P.R. Long-term consequences of early iron deficiency in the rat. Pharmacol Biochem Behav 11 (1979) 631-638
13. Pinero D.J., Li N.Q., Connor J.R., and Beard J.L. Alterations in brain iron metabolism in response to dietary iron changes. J Nutr 130 (2000) 254-263
14. Erikson K.M., Jones B.C., Hess E.J., Zhang Q., and Beard J.L. Iron deficiency decreases dopamine D1 and D2 receptors in rat brain. Pharmacol Biochem Behav 69 (2001) 409-418
15. Rao R., Tkac I., Townsend E.L., Gruetter R., and Georgieff M.K. Perinatal iron deficiency alters the neurochemical profile of the developing rat hippocampus. J Nutr 133 (2003) 3215-3221
16. Beard J.L., Erikson K.M., and Jones B.C. Neurobehavioral analysis of developmental iron deficiency in rats. Behav Brain Res 134 (2002) 517-524
17. Beard JL, Felt B, Schallert T, Burhans M, Connor JR, Georgieff MK. Moderate iron deficiency in young rats: alterations in biology and behavior; 2005 [in revision].
18. Dobbing J., and Sands J. Comparative aspects of the brain growth spurt. Early Hum Dev 3 (1979) 79-83
19. Jorgenson L.A., Wobken J.D., and Georgieff M.K. Perinatal iron deficiency alters apical dendritic growth in hippocampal CA1 pyramidal neurons. Dev Neurosci 25 (2003) 412-420
20. DeUngria M., Rao R., Wobken J.D., Luciana M., Nelson C.A., and Georgieff M.K. Perinatal iron deficiency decreases cytochrome c oxidase (CytOx) activity in selected regions of neonatal rat brain. Pediatr Res 48 (2000) 169-176
21. Ortiz E., Pasquini J.M., Thompson K., Felt B., Butkus G., Beard J., et al. Effect of manipulation of iron storage, transport, or availability on myelin composition and brain iron content in three different animal models. J Neurosci Res 77 (2004) 681-689
22. Yu G.S., Steinkirchner T.M., Rao G.A., and Larkin E.C. Effect of prenatal iron deficiency on myelination in rat pups. Am J Pathol 125 (1986) 620-624
23. Erikson K., Jones B., and Beard J.L. Iron deficiency alters dopamine transporter functioning in rat striatum. J Nutr 130 (2000) 2831-2837
24. Nelson C., Erikson K., Pinero D.J., and Beard J.L. In vivo dopamine metabolism is altered in iron-deficient anemic rats. J Nutr 127 (1997) 2282-2288
25. Beard J.L., Chen Q., Connor J.R., and Jones B.C. Altered monoamine metabolism in caudate nucleus on iron deficient rats. Pharmacol Biochem Behav 48 (1994) 621-624
26. Glover J., and Jacobs A. Activity pattern of iron-deficient rats. BMJ 2 (1972) 627-628
27. Edgerton V.R., Bryant S.L., Gillespie C.A., and Gardner G.W. Iron deficiency anemia and physical performance and activity in rats. J Nutr 102 (1972) 381-400
28. Hunt J.R., Zito C.A., Erjavec J., and Johson L.K. Severe or marginal iron deficiency affects spontaneous physical activity in rats. Am J Clin Nutr 59 (1994) 413-418
29. Yehuda S., Youdim M.B.H., and Mostofsky D.I. Brain iron deficiency causes reduced learning capacity in rats. Pharmacol Biochem Behav 25 (1986) 141-144
30. Siddappa A.J., Rao R., Wobken J.D., Casperson K., Liebold E.A., Connor J., et al. Iron deficiency alters iron regulatory protein and iron transport protein expression in the perinatal rat brain. Pediatr Res 53 (2003) 800-807
31. Schallert T., Petrie B.F., and Whishaw I.Q. Neonatal dopamine depletion: spared and unspared sensorimotor and attentional disorders and effects of further depletion in adulthood. Psychobiology 17 (1989) 386-396
32. Schallert T., Fleming S.M., Leasure J.L., Tillerson J.L., and Bland S.T. CNS plasticity and assessment of forelimb sensorimotor outcome in unilateral rat models of stroke, cortical ablation, parkinsonism and spinal cord injury. Neuropharmacology 39 (2000) 777-787
33. Schallert T., and Woodlee M.T. Brain-dependent movements and cerebral-spinal connections: key targets of cellular and behavioral enrichment in CNS injury models. J Rehab Res Dev 40 (2003) 9-17
34. Felt B.T., Schallert T., Shao J., Liu Y., Li X., and Barks J.D. Early appearance of functional deficits after neonatal excitotoxic and hypoxic-ischemic injury: fragile recovery after development and role of the NMDA receptor. Dev Neurosci 24 (2002) 418-425
35. Aldridge J.W., and Berridge K.C. Coding of serial order by neostriatal neurons: a "natural action" approach to movement sequence. J Neurosci 18 (1998) 2777-2787
36. Cromwell H.C., and Berridge K.C. Implementation of action sequences by a neostriatal site: a lesion mapping study of grooming syntax. J Neurosci 16 (1996) 3444-3458
37. Maren S., Patel K., Thompson R.F., and Mitchell D. Individual differences in emergence neophobia predict magnitude of perforant-path long-term potentiation (LTP) and plasma corticosterone levels in rats. Psychobiology 21 (1993) 2-10
38. Spinetta M.J., Woodlee M.T., Hester N.W., Heymann J.C., Feinberg L.M., Rajagopalan K.N., et al. A simple and sensitive odor recognition test for rats and mice detects retrograde amnesia caused by ethanol or other drugs that interfere with memory consolidation (2005), Society for Neuroscience, Washington, DC
39. Prut L., and Belzung C. The open field as a paradigm to measure the effects of drugs on anxiety-like behaviors: a review. Eur J Pharmacol 463 (2003) 3-33
40. Alber S.A., and Strupp B.J. An in-depth analysis of lead effects in a delayed spatial alternation task: assessment of mnemonic effects, side bias, and proactive interference. Neurotoxicol Teratol 18 (1996) 3-15
41. Hilson J., and Strupp B. Analyses of response patterns clarify lead effects in ilfactory reversal and extradimensional shift tasks: assessment of inhibitory control, associative ability and memory. Behav Neurosci 111 (1997) 532-542
42. Day L.B., and Schallert T. Anticholinergic effects on acquisition of place learning in the morris water task: spatial mapping deficit or inability to inhibit nonplace strategies?. Behav Neurosci 110 (1996) 998-1005
43. Day L.B., Weisend M., Sutherland R.J., and Schallert T. The hippocampus is not necessary for a place response but may be necessary for pliancy. Behav Neurosci 113 (1999) 914-924
44. Lindner M.D., and Schallert T. Aging and atropine effects on spatial navigation in the Morris water task. Behav Neurosci 102 (1988) 621-634
45. Whishaw I.Q. Posterior neocortical (visual cortex) lesions in the rat impair matching-to-place navigation in a swimming pool: a reevaluation of cortical contributions to spatial behavior using a new assessment of spatial versus non-spatial behavior. Behav Brain Res 155 (2004) 177-184
46. Littell R.C., Milliken G.A., Stroup W.W., and Wolfinger R.D. SAS system for mixed models (1996), SAS Institute, Cary, NC
47. Beard JL. Personal communication.
48. Schallert T., Upchurch M., Lobaugh N., Farrar S.B., Spirduso W.W., Gilliam P., et al. Tactile extinction: distinguishing between sensorimotor and motor asymmetries in rats with unilateral nigrostriatal damage. Pharmacol Biochem Behav 16 (1982) 455-462
49. Beard J. Personal communication.
50. Lozoff B., Smith J., Liberzon T., Angulo-Barroso A., Calatroni A., and Jimenez E. Longitudinal analysis of cognitive and motor effects of iron deficiency in infancy. APA plenary presentation. Pediatr Res 55 (2004) 23A
51. Eseh R., and Zimmerberg B. Age-dependent effects of gestational and lactational iron deficiency on anxiety behavior in rats. Behav Brain Res 164 (2005) 214-221
52. Fox N.A., Bell M.A., and Jones N.A. Individual differences in response to stress and cerebral asymmetry. Dev Neuropsychol 8 (1992) 161-184
53. Golub M.S., Hogrefe C.E., Germann S.L., Capitanio J.L., and Lozoff B. Behavioral consequences of developmental iron deficiency in infant rhesus monkeys. Neurotoxicol Teratol 28 (2005) 3-17
54. Treit D., and Fundytus M. Thigmotaxis as a test for anxiolytic activity in rats. Pharmacol Biochem Behav 31 (1989) 959-962
55. Erikson K., Pinero D.J., Connor J.R., and Beard J.L. Regional brain iron, ferritin and transferrin concentrations during iron deficiency and iron repletion in developing rats. J Nutr 127 (1997) 2030-2038
56. Zhang K., Davids E., Tarazi F.I., and Baldessarini R.J. Serotonin transporter binding increases in caudate-putamen and nucleus accumbens after neonatal 6-hydroxydopamine lesions in rats: implications for motor hyperactivity. Brain Res 137 (2002) 135-138
57. Avale M.E., Nemirovsky S.I., Raisman-Vozari R., and Rubinstein M. Elevated serotonin is involved in hyperactivity but not in the paradoxical effect of amphetamine in mice neonatally lesioned with 6-hydroxydopamine. J Neurosci Res 78 (2004) 289-296
58. Levine S. Maternal and environmental influences on the adrenocortical response to stress in weanling rats. Science 156 (1967) 258-260
59. Caldji C., Tannenbaum B., Sharma S., Francis D., Plotsky P.M., and Meaney M.J. Maternal care during infancy regulates the development of neural systems mediating the expression of fearfulness in the rat. PNAS 95 (1998) 5335-5340