Sex and rearing condition modify the effects of perinatal lead exposure on learning and memory

NeuroToxicology

Volumn 33, Issue 5, 2012, Pages 985-995

  Anderson, D W ^a   Pothakos, K ^a   Schneider, J S ^a  

^a THOMAS JEFFERSON UNIVERSITY   (United States)

Author keywords

Environment; Lead; Learning; Memory; Sex

Indexed keywords

LEAD; LEAD ACETATE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CHILD REARING; CONTROLLED STUDY; ENVIRONMENTAL ENRICHMENT; ENVIRONMENTAL EXPOSURE; FEMALE; LEAD POISONING; LEARNING DISORDER; MALE; MAZE TEST; MEMORY DISORDER; NEUROTOXICITY; NONHUMAN; PERINATAL PERIOD; PRIORITY JOURNAL; RAT; REFERENCE MEMORY; SEX DIFFERENCE; SPATIAL MEMORY;

AGE FACTORS; ANALYSIS OF VARIANCE; ANIMALS; ANIMALS, NEWBORN; AVOIDANCE LEARNING; BRAIN; DIETARY SUPPLEMENTS; DISEASE MODELS, ANIMAL; ENVIRONMENT; FEMALE; LEAD; LEAD POISONING; LEARNING DISORDERS; MALE; MAZE LEARNING; MEMORY DISORDERS; RATS; RATS, LONG-EVANS; REACTION TIME; SEX CHARACTERISTICS;

ANIMALIA; RATTUS; RODENTIA;

EID: 84867233301     PISSN: 0161813X     EISSN: 18729711     Source Type: Journal    
DOI: 10.1016/j.neuro.2012.04.016     Document Type: Article

References (68)

1. Astur R.S., Ortiz M.L., Sutherland R.J. A characterization of performance by men and women in a virtual Morris water task: a large and reliable sex difference. Behav Brain Res 1998, 93:185-190.
2. Beiko J., Lander R., Hampson E., Boon F., Cain D.P. Contribution of sex differences in the acute stress response to sex differences in water maze performance in the rat. Behav Brain Res 2004, 151:239-253.
3. Bellinger D., Leviton A., Sloman J. Antecedents and correlates of improved cognitive performance in children exposed in utero to low levels of lead. Environ Health Perspect 1990, 89:5-11.
4. Bellinger D., Sloman J., Leviton A., Rabinowitz M., Needleman H.L., Waternaux C. Low-level lead exposure and children's cognitive function in the preschool years. Pediatrics 1991, 87:219-227.
5. Blokland A., Rutten K., Prickaerts J. Analysis of spatial orientation strategies of male and female Wistar rats in a Morris water escape task. Behav Brain Res 2006, 171:216-224.
6. Bradley R.H., Corwyn R.F. Socioeconomic status and child development. Ann Rev Psychol 2002, 53:371-379.
7. Bradley R.H., Corwyn R.F., McAdoo H.P., Coll C.G. The home environments of children in the United States part I: variations by age, ethnicity, and poverty status. Child Dev 2001, 72:1844-1867.
8. Braga M.F., Pereira E.F., Marchioro M. Albuquerque ex lead increases tetrodotoxin-insensitive spontaneous release of glutamate and GABA from hippocampal neurons. Brain Res 1999, 826:10-21.
9. Brooks-Gunn J., Duncan G.J. The effects of poverty on children. Future Children 1997, 7:55-71.
10. Cao X., Huang S., Ruan D. Enriched environment restores impaired hippocampal long-term potentiation and water maze performance induced by developmental lead exposure in rats. Dev Psychobiol 2008, 50:307-313.
11. Cory-Slechta D.A., Virgolini M.B., Thiruchelvam M., Weston D.D., Bauter M.R. Maternal stress modulates the effects of developmental lead exposure. Environ Health Perspect 2004, 112:717-730.
12. Dahlqvist P., Ronnback A., Bergstrom S.A., Soderstrom I., Olsson T. Environmental enrichment reverses learning impairment in the Morris water maze after focal cerebral ischemia in rats. Eur J Neurosci 2004, 19:2288-2298.
13. Dalla C., Shors T.J. Sex differences in learning processes of classical and operant conditioning. Physiol Behav 2009, 97:229-238.
14. Davis J.M., Svendsgaard D.J. U-Shaped dose response curves: their occurrence and implications for risk assessment. J Toxicol Environ Health 1990, 30:71-83.
15. de Souza Lisboa S.F., Gonzalves G., Komatsu F., Salci Queiroz C.A., Aparecido Almeida A., Gastaldello Moreira E.N. Developmental lead exposure induces depressive-like behavior in female rats. Drug Chem Toxicol 2005, 28:67-77.
16. Dietrich K.N., Krafft K.M., Bornschein R.L., Hammond P.B., Berger O., Succop P.A. Low-level fetal lead exposure effect on neurobehavioral development in early infancy. Pediatrics 1987, 80:721-730.
17. Duff S.J., Hampson E. A sex difference on a novel spatial working memory task in humans. Brain Cogn 2001, 47:470-493.
18. Farah M.J., Shera D.M., Savage J.H., Betancourt L., Giannetta J.M., Brodsky N.L., et al. Specific associations with neurocognitive development. Brain Res 2006, 1110:166-174.
19. Farrell R., Evans S., Corbett D. Environmental enrichment enhances recovery of function but exacerbates ischemic cell death. Neuroscience 2001, 107:585-592.
20. Frye C.A. Estrus-associated decrements in a water maze task are limited to acquisition. Physiol Behav 1995, 57:5-14.
21. Frye C.A., Sturgis J.D. Neurosteroids affect spatial/reference, working, and long-term memory of female rats. Neurobiol Learn Mem 1995, 64:83-96.
22. Galea L.A., Kavaliers M., Ossenkopp K.P. Sexually dimorphic spatial learning in meadow voles Microtus pennsylvanicus and deer mice Peromyscus maniculatus. J Exp Biol 1996, 199:195-200.
23. Gilbert M.E., Kelly M.E., Samsam T.E., Goodman J.H. Chronic developmental lead exposure reduces neurogenesis in adult rat hippocampus but does not impair spatial learning. Toxicol Sci 2005, 86:365-374.
24. Gobbo O.L., O'Mara S.M. Impact of enriched-environment housing on brain-derived neurotrophic factor and on cognitive performance after a transient global ischemia. Behav Brain Res 2004, 152:231-241.
25. 2+-exposed rats: implications for synaptic targeting and cell surface expression of NMDAR complexes. Brain Res Mol Brain Res 2003, 113:37-43.
26. Guilarte T.R., Toscano C.D., McGlothan J.L., Weaver S.A. Environmental enrichment reverses cognitive and molecular deficits induced by developmental lead exposure. Ann Neurol 2003, 53:50-56.
27. Hoffmann L.C., Schutte S.R., Koch M., Schwabe K. Effect of "enriched environment" during development on adult rat behavior and response to the dopamine receptor agonist apomorphine. Neuroscience 2009, 158:1589-1598.
28. Jett D.A., Kuhlmann A.C., Farmer S.J., Guilarte T.R. Age-dependent effects of developmental lead exposure on performance in the Morris water maze. Pharmacol Biochem Behav 1997, 57:271-279.
29. Jonasson Z. Meta-analysis of sex differences in rodent models of learning and memory: a review of behavioral and biological data. Neurosci Biobehav Rev 2005, 28:811-825.
30. Kolb B., Gibb R. Environmental enrichment and cortical injury: behavioral and anatomical consequences of frontal cortex lesions. Cereb Cortex 1991, 1:189-198.
31. Lanphear B.P., Dietrich K., Auinger P., Cox C. Cognitive deficits associated with blood lead concentrations <10μg/dL in US children and adolescents. Public Health Rep 2000, 115:521-529.
32. Lanphear B.P., Hornung R., Khoury J., Yolton K., Baghurst P., Bellinger D.C., et al. Low-level environmental lead exposure and children's intellectual function: an international pooled analysis. Environ Health Perspect 2005, 113:894-899.
33. Lasley S.M., Gilbert M.E. Rat hippocampal glutamate and GABA release exhibit biphasic effects as a function of chronic lead exposure level. Toxicol Sci 2002, 66:139-147.
34. Lucas M.M., Lenck-Santini P.-P., Holmes G.L., Scott R.C. Impaired cognition in rats with cortical dysplasia: additional impact of early-life seizures. Brain 2011, 134:1684-1693.
35. Markovac J., Goldstein G.W. Picomolar concentrations of lead stimulate brain protein kinase C. Nature 1988, 334:71-73.
36. McCloyd V.C. Socioeconomic disadvantage and child development. Am Psychol 1988, 53:185-204.
37. McMichael A.J., Baghurst P.A., Vimpani G.V., Robertson E.F., Wigg N.R., Tong S.L. Sociodemographic factors modifying the effect of environmental lead on neuropsychological development in early childhood. Neurotoxicol Teratol 1992, 14:321-327.
38. Mendez-Lupez M., Mendez M., Lupez L., Arias J.L. Spatial working memory learning in young male and female rats: involvement of different limbic system regions revealed by cytochrome oxidase activity. Neurosci Res 2009, 65:28-34.
39. Moncek F., Duncko R., Johansson B.B., Jezova D. Effect of environmental enrichment on stress related systems in rats. J Neuroendocrinol 2004, 16:423-431.
40. Morris R. Developments of a water-maze procedure for studying spatial learning in the rat. J Neurosci Methods 1984, 11:47-60.
41. Newhouse P., Newhouse C., Astur R.S. Sex differences in visual-spatial learning using a virtual water maze in pre-pubertal children. Behav Brain Res 2007, 183:1-7.
42. Rabinowitz M.B., Wang J.D., Soong W.T. Dentine lead and child intelligence in Taiwan. Arch Environ Health 1991, 46:351-360.
43. Rizk-Jackson A.M., Acevedo S.F., Inman D., Howieson D., Benice T.S., Raber J. Effects of sex on object recognition and spatial navigation in humans. Behav Brain Res 2006, 173:181-190.
44. Roof R.L., Stein D.G. Gender differences in Morris water maze performance depend on task parameters. Physiol Behav 1999, 68:81-86.
45. Roof R.L., Zhang Q., Glasier M.M., Stein D.G. Gender-specific impairment on Morris water maze task after entorhinal cortex lesion. Behav Brain Res 1993, 57:47-51.
46. Rose Fd, Al-Khamees K., Davey M.J., Attree E.A. Environmental enrichment following brain damage: an aid to recovery or compensation. Behav Brain Res 1993, 56:93-100.
47. Rose F.D., Davey M.J., Attree E.A. How does environmental enrichment aid performance following cortical injury in the rat. Neuroreport 1993, 4:163-166.
48. Rosenzweig M.R., Bennett E.L., Hebert M., Morimoto H. Social grouping cannot account for cerebral effects of enriched environments. Brain Res 1978, 153:563-576.
49. Rothenberg S.J., Rothenberg J.C. Testing the dose-response specification in epidemiology: public health and policy consequences for lead. Environ Health Perspect 2005, 113:1190-1195.
50. Sandstrom N.J., Kaufman J., Huettel S.A. Males and females use different distal cues in a virtual environment navigation task. Brain Res Cogn Brain Res 1998, 6:351-360.
51. Saucier D.M., Green S.M., Leason J., Macfadden A., Bell S., Elias L.J. Are sex differences in navigation caused by sexually dimorphic strategies or by differences in the ability to use the strategies. Behav Neurosci 2002, 116:403-410.
52. Saucier D.M., Shultz S.R., Keller A.J., Cook C.M., Binsted G. Sex differences in object location memory and spatial navigation in Long-Evans rats. Anim Cogn 2008, 11:129-137.
53. Savic M.M., Milinkovic M.M., Rallapalli S., Clayton T., Joksimovic S., Van Linn M. The differential role of alpha1- and alpha5-containing GABA(A) receptors in mediating diazepam effects on spontaneous locomotor activity and water-maze learning and memory in rats. Int J Neuropsychopharmacol 2009, 12:1179-1193.
54. Schneider J.S., Anderson D.W., Sonnenahalli H., Vadigepalli R. Sex-based differences in gene expression in hippocampus following postnatal lead exposure. Toxicol Appl Pharmacol 2011, 256:179-190.
55. Schneider J.S., Lee M.H., Anderson D.W., Zuck L., Lidsky T.I. Enriched environment during development is protective against lead-induced neurotoxicity. Brain Res 2001, 896:48-55.
56. Surkan P.J., Zhang A., Trachtenberg F., Daniel D.B., McKinlay S., Bellinger D.C. Neuropsychological function in children with blood lead levels <10microg/dL. Neurotoxicology 2007, 28:1170-1177.
57. van Praag H., Kempermann G., Gage F.H. Neural consequences of environmental enrichment. Nat Rev Neurosci 2000, 1:191-198.
58. Virgolini M.B., Cancela L.M., Fulginiti S. Behavioral responses to ethanol in rats perinatally exposed to low lead levels. Neurotoxicol Teratol 1999, 21:551-557.
59. Virgolini M.B., Volosin M., Fulginiti A.S., Cancela L.M. Amphetamine and stress responses in developmentally lead-exposed rats. Neurotoxicol Teratol 2004, 26:291-303.
60. Vorhees C.V., Williams M.T. Morris water maze: procedures for assessing spatial and related forms of learning and memory. Nat Protoc 2006, 1:848-858.
61. Warren S.G., Juraska J.M. Spatial and nonspatial learning across the rat estrous cycle. Behav Neurosci 1997, 111:259-266.
62. White L.D., Cory-Slechta D.A., Gilbert M.E., Tiffany-Castiglioni E., Zawia N.H., Virgolini M., et al. New and evolving concepts in the neurotoxicology of lead. Toxicol Appl Pharmacol 2007, 225:1-27.
63. Will B., Galani R., Kelche C., Rosenzweig M.R. Recovery from brain injury in animals: relative efficacy of environmental enrichment, physical exercise or formal training (1990-2002). Prog Neurobiol 2004, 72:167-182.
64. Will B.E., Sutter A.R., Offerlin M.R. Effects of methamphetamine and enriched experience on behavioral recovery after brain damage [author's transl]. Psychopharmacology (Berl) 1977, 51:273-277.
65. Williams C.L., Meck W.H. The organizational effects of gonadal steroids on sexually dimorphic spatial ability. Psychoneuroendocrinology 1991, 16:155-176.
66. Xu J., Yan H.C., Yang B., Tong L.S., Zou Y.X., Tian Y. Effects of lead exposure on hippocampal metabotropic glutamate receptor subtype 3 and 7 in developmental rats. J Negat Results Biomed 2009, 8:5.
67. Yu S.Y., Mizinga K.M., Nonavinakere V.K., Soliman K.F. Decreased endurance to cold water swimming and delayed sexual maturity in the rat following neonatal lead exposure. Toxicol Lett 1996, 85:135-141.
68. Zakharova E., Miller J., Unterwald E., Wade D., Izenwasser S. Social and physical environment alter cocaine conditioned place preference and dopaminergic markers in adolescent male rats. Neuroscience 2009, 163:890-897.