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. 2004 May;112(6):717–730. doi: 10.1289/ehp.6481

Maternal stress modulates the effects of developmental lead exposure.

Deborah A Cory-Slechta 1, Miriam B Virgolini 1, Mona Thiruchelvam 1, Doug D Weston 1, Mark R Bauter 1
PMCID: PMC1241967  PMID: 15121516

Abstract

Lead exposure is higher among children with low socioeconomic status (SES) compared with other children in the United States. Low SES itself is a known risk factor for various diseases and dysfunctions, effects that have been ascribed to chronic stress and associated elevation of glucocorticoids. Chronically elevated glucocorticoids and Pb provoke similar behavioral changes, and both can act on mesocorticolimbic systems of the brain. In this study we examined the hypothesis that these co-occurring risk factors, Pb and environmental stress, would interact and modulate each others' effects. Using a rodent model, we focused on the specific contributions of maternal stress (restraint) and maternal Pb exposure (150 ppm in drinking water) on corticosterone levels of offspring, as well as on neurotransmitter changes and a behavioral baseline (fixed-interval schedule-controlled performance) with known sensitivities to Pb. We observed interactions of Pb and stress that differed in relation to outcome measure and sex. In addition, potentiated effects (effects of Pb plus stress but showing no changes produced by either alone) were observed more frequently in females. Importantly, Pb alone (in males) and Pb plus stress (in females) permanently elevated corticosterone levels in offspring; even short-term Pb exposure to dams could cause this effect. Such increases could suggest a potential new mechanism by which Pb exposure could directly or indirectly enhance susceptibility to diseases and dysfunctions and induce cognitive deficits. Moreover, the interactive effects of Pb and stress, and particularly the potentiated effects of Pb plus stress, raise questions about whether current risk assessment strategies sufficiently consider the potential for modulation of toxicity that can accrue from intercurrent risk factors.

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Selected References

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  1. Adelstein A. M. Life-style in occupational cancer. J Toxicol Environ Health. 1980 Sep-Nov;6(5-6):953–962. doi: 10.1080/15287398009529916. [DOI] [PubMed] [Google Scholar]
  2. Alonso S. J., Navarro E., Rodriguez M. Permanent dopaminergic alterations in the n. accumbens after prenatal stress. Pharmacol Biochem Behav. 1994 Oct;49(2):353–358. doi: 10.1016/0091-3057(94)90433-2. [DOI] [PubMed] [Google Scholar]
  3. Anderson N. B., Armstead C. A. Toward understanding the association of socioeconomic status and health: a new challenge for the biopsychosocial approach. Psychosom Med. 1995 May-Jun;57(3):213–225. doi: 10.1097/00006842-199505000-00003. [DOI] [PubMed] [Google Scholar]
  4. Armando I., Tjurmina O. A., Li Q., Murphy D. L., Saavedra J. M. The serotonin transporter is required for stress-evoked increases in adrenal catecholamine synthesis and angiotensin II AT(2) receptor expression. Neuroendocrinology. 2003 Oct;78(4):217–225. doi: 10.1159/000073705. [DOI] [PubMed] [Google Scholar]
  5. Barrot M., Marinelli M., Abrous D. N., Rougé-Pont F., Le Moal M., Piazza P. V. The dopaminergic hyper-responsiveness of the shell of the nucleus accumbens is hormone-dependent. Eur J Neurosci. 2000 Mar;12(3):973–979. doi: 10.1046/j.1460-9568.2000.00996.x. [DOI] [PubMed] [Google Scholar]
  6. Bellinger D., Hu H., Titlebaum L., Needleman H. L. Attentional correlates of dentin and bone lead levels in adolescents. Arch Environ Health. 1994 Mar-Apr;49(2):98–105. doi: 10.1080/00039896.1994.9937461. [DOI] [PubMed] [Google Scholar]
  7. Bellinger D., Leviton A., Waternaux C., Needleman H., Rabinowitz M. Longitudinal analyses of prenatal and postnatal lead exposure and early cognitive development. N Engl J Med. 1987 Apr 23;316(17):1037–1043. doi: 10.1056/NEJM198704233161701. [DOI] [PubMed] [Google Scholar]
  8. Bellinger D., Leviton A., Waternaux C., Needleman H., Rabinowitz M. Low-level lead exposure, social class, and infant development. Neurotoxicol Teratol. 1988 Nov-Dec;10(6):497–503. doi: 10.1016/0892-0362(88)90084-0. [DOI] [PubMed] [Google Scholar]
  9. Bland Sondra T., Twining Carin, Watkins Linda R., Maier Steven F. Stressor controllability modulates stress-induced serotonin but not dopamine efflux in the nucleus accumbens shell. Synapse. 2003 Sep 1;49(3):206–208. doi: 10.1002/syn.10229. [DOI] [PubMed] [Google Scholar]
  10. Bradley Robert H., Corwyn Robert F. Socioeconomic status and child development. Annu Rev Psychol. 2002;53:371–399. doi: 10.1146/annurev.psych.53.100901.135233. [DOI] [PubMed] [Google Scholar]
  11. Brosschot J. F., Benschop R. J., Godaert G. L., de Smet M. B., Olff M., Heijnen C. J., Ballieux R. E. Effects of experimental psychological stress on distribution and function of peripheral blood cells. Psychosom Med. 1992 Jul-Aug;54(4):394–406. doi: 10.1097/00006842-199207000-00002. [DOI] [PubMed] [Google Scholar]
  12. Calabrese J. R., Kling M. A., Gold P. W. Alterations in immunocompetence during stress, bereavement, and depression: focus on neuroendocrine regulation. Am J Psychiatry. 1987 Sep;144(9):1123–1134. doi: 10.1176/ajp.144.9.1123. [DOI] [PubMed] [Google Scholar]
  13. Canfield Richard L., Henderson Charles R., Jr, Cory-Slechta Deborah A., Cox Christopher, Jusko Todd A., Lanphear Bruce P. Intellectual impairment in children with blood lead concentrations below 10 microg per deciliter. N Engl J Med. 2003 Apr 17;348(16):1517–1526. doi: 10.1056/NEJMoa022848. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Chou-Green Jennifer M., Holscher Todd D., Dallman Mary F., Akana Susan F. Repeated stress in young and old 5-HT(2C) receptor knockout mice. Physiol Behav. 2003 Jul;79(2):217–226. doi: 10.1016/s0031-9384(03)00096-9. [DOI] [PubMed] [Google Scholar]
  15. Cohn J., Cox C., Cory-Slechta D. A. The effects of lead exposure on learning in a multiple repeated acquisition and performance schedule. Neurotoxicology. 1993 Summer-Fall;14(2-3):329–346. [PubMed] [Google Scholar]
  16. Cory-Slechta D. A., McCoy L., Richfield E. K. Time course and regional basis of Pb-induced changes in MK-801 binding: reversal by chronic treatment with the dopamine agonist apomorphine but not the D1 agonist SKF-82958. J Neurochem. 1997 May;68(5):2012–2023. doi: 10.1046/j.1471-4159.1997.68052012.x. [DOI] [PubMed] [Google Scholar]
  17. Cory-Slechta D. A., O'Mara D. J., Brockel B. J. Nucleus accumbens dopaminergic medication of fixed interval schedule-controlled behavior and its modulation by low-level lead exposure. J Pharmacol Exp Ther. 1998 Aug;286(2):794–805. [PubMed] [Google Scholar]
  18. Cory-Slechta D. A., Pazmino R., Bare C. The critical role of nucleus accumbens dopamine systems in the mediation of fixed interval schedule-controlled operant behavior. Brain Res. 1997 Aug 1;764(1-2):253–256. doi: 10.1016/s0006-8993(97)00591-x. [DOI] [PubMed] [Google Scholar]
  19. Cory-Slechta D. A., Pokora M. J., Fox R. A., O'Mara D. J. Lead-induced changes in dopamine D1 sensitivity: modulation by drug discrimination training. Neurotoxicology. 1996 Summer;17(2):445–457. [PubMed] [Google Scholar]
  20. Cory-Slechta D. A., Pokora M. J., Widzowski D. V. Postnatal lead exposure induces supersensitivity to the stimulus properties of a D2-D3 agonist. Brain Res. 1992 Dec 11;598(1-2):162–172. doi: 10.1016/0006-8993(92)90180-h. [DOI] [PubMed] [Google Scholar]
  21. Cory-Slechta D. A., Weiss B., Cox C. Delayed behavioral toxicity of lead with increasing exposure concentration. Toxicol Appl Pharmacol. 1983 Dec;71(3):342–352. doi: 10.1016/0041-008x(83)90021-2. [DOI] [PubMed] [Google Scholar]
  22. Cory-Slechta D. A., Weiss B., Cox C. Mobilization and redistribution of lead over the course of calcium disodium ethylenediamine tetraacetate chelation therapy. J Pharmacol Exp Ther. 1987 Dec;243(3):804–813. [PubMed] [Google Scholar]
  23. Cory-Slechta D. A., Weiss B., Cox C. Performance and exposure indices of rats exposed to low concentrations of lead. Toxicol Appl Pharmacol. 1985 Apr;78(2):291–299. doi: 10.1016/0041-008x(85)90292-3. [DOI] [PubMed] [Google Scholar]
  24. Cory-Slechta Deborah A., Brockel B. J., O'Mara D. J. Lead exposure and dorsomedial striatum mediation of fixed interval schedule-controlled behavior. Neurotoxicology. 2002 Sep;23(3):313–327. doi: 10.1016/s0161-813x(02)00059-1. [DOI] [PubMed] [Google Scholar]
  25. Davis J. M., Svendsgaard D. J. U-shaped dose-response curves: their occurrence and implications for risk assessment. J Toxicol Environ Health. 1990 Jun;30(2):71–83. doi: 10.1080/15287399009531412. [DOI] [PubMed] [Google Scholar]
  26. Devoto P., Flore G., Ibba A., Fratta W., Pani L. Lead intoxication during intrauterine life and lactation but not during adulthood reduces nucleus accumbens dopamine release as studied by brain microdialysis. Toxicol Lett. 2001 May 19;121(3):199–206. doi: 10.1016/s0378-4274(01)00336-8. [DOI] [PubMed] [Google Scholar]
  27. Dietrich K. N., Succop P. A., Berger O. G., Hammond P. B., Bornschein R. L. Lead exposure and the cognitive development of urban preschool children: the Cincinnati Lead Study cohort at age 4 years. Neurotoxicol Teratol. 1991 Mar-Apr;13(2):203–211. doi: 10.1016/0892-0362(91)90012-l. [DOI] [PubMed] [Google Scholar]
  28. Diorio D., Viau V., Meaney M. J. The role of the medial prefrontal cortex (cingulate gyrus) in the regulation of hypothalamic-pituitary-adrenal responses to stress. J Neurosci. 1993 Sep;13(9):3839–3847. doi: 10.1523/JNEUROSCI.13-09-03839.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Dohrenwend B. P. Socioeconomic status (SES) and psychiatric disorders. Are the issues still compelling? Soc Psychiatry Psychiatr Epidemiol. 1990 Jan;25(1):41–47. doi: 10.1007/BF00789069. [DOI] [PubMed] [Google Scholar]
  30. Dohrenwend B. S. Social status and stressful life events. J Pers Soc Psychol. 1973 Nov;28(2):225–235. doi: 10.1037/h0035718. [DOI] [PubMed] [Google Scholar]
  31. Dyer A. R., Stamler J., Shekelle R. B., Schoenberger J. The relationship of education to blood pressure: findings on 40,000 employed Chicagoans. Circulation. 1976 Dec;54(6):987–992. doi: 10.1161/01.cir.54.6.987. [DOI] [PubMed] [Google Scholar]
  32. Egbuonu L., Starfield Child health and social status. Pediatrics. 1982 May;69(5):550–557. [PubMed] [Google Scholar]
  33. Faraday Martha M. Rat sex and strain differences in responses to stress. Physiol Behav. 2002 Apr 1;75(4):507–522. doi: 10.1016/s0031-9384(02)00645-5. [DOI] [PubMed] [Google Scholar]
  34. Finlay J. M., Zigmond M. J. The effects of stress on central dopaminergic neurons: possible clinical implications. Neurochem Res. 1997 Nov;22(11):1387–1394. doi: 10.1023/a:1022075324164. [DOI] [PubMed] [Google Scholar]
  35. Haile C. N., GrandPre T., Kosten T. A. Chronic unpredictable stress, but not chronic predictable stress, enhances the sensitivity to the behavioral effects of cocaine in rats. Psychopharmacology (Berl) 2001 Mar 1;154(2):213–220. doi: 10.1007/s002130000650. [DOI] [PubMed] [Google Scholar]
  36. Hanley N. R., Van de Kar L. D. Serotonin and the neuroendocrine regulation of the hypothalamic--pituitary-adrenal axis in health and disease. Vitam Horm. 2003;66:189–255. doi: 10.1016/s0083-6729(03)01006-9. [DOI] [PubMed] [Google Scholar]
  37. Henry C., Guegant G., Cador M., Arnauld E., Arsaut J., Le Moal M., Demotes-Mainard J. Prenatal stress in rats facilitates amphetamine-induced sensitization and induces long-lasting changes in dopamine receptors in the nucleus accumbens. Brain Res. 1995 Jul 10;685(1-2):179–186. doi: 10.1016/0006-8993(95)00430-x. [DOI] [PubMed] [Google Scholar]
  38. Hirschfeld R. M., Cross C. K. Epidemiology of affective disorders. Arch Gen Psychiatry. 1982 Jan;39(1):35–46. doi: 10.1001/archpsyc.1982.04290010013003. [DOI] [PubMed] [Google Scholar]
  39. Joëls M., de Kloet E. R. Mineralocorticoid and glucocorticoid receptors in the brain. Implications for ion permeability and transmitter systems. Prog Neurobiol. 1994 May;43(1):1–36. doi: 10.1016/0301-0082(94)90014-0. [DOI] [PubMed] [Google Scholar]
  40. Kala S. V., Jadhav A. L. Region-specific alterations in dopamine and serotonin metabolism in brains of rats exposed to low levels of lead. Neurotoxicology. 1995 Summer;16(2):297–308. [PubMed] [Google Scholar]
  41. Kennedy S., Kiecolt-Glaser J. K., Glaser R. Immunological consequences of acute and chronic stressors: mediating role of interpersonal relationships. Br J Med Psychol. 1988 Mar;61(Pt 1):77–85. doi: 10.1111/j.2044-8341.1988.tb02766.x. [DOI] [PubMed] [Google Scholar]
  42. Kerr D. S., Campbell L. W., Applegate M. D., Brodish A., Landfield P. W. Chronic stress-induced acceleration of electrophysiologic and morphometric biomarkers of hippocampal aging. J Neurosci. 1991 May;11(5):1316–1324. doi: 10.1523/JNEUROSCI.11-05-01316.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  43. Lasley S. M., Green M. C., Gilbert M. E. Rat hippocampal NMDA receptor binding as a function of chronic lead exposure level. Neurotoxicol Teratol. 2001 Mar-Apr;23(2):185–189. doi: 10.1016/s0892-0362(01)00116-7. [DOI] [PubMed] [Google Scholar]
  44. Lasley S. M., Lane J. D. Diminished regulation of mesolimbic dopaminergic activity in rat after chronic inorganic lead exposure. Toxicol Appl Pharmacol. 1988 Sep 30;95(3):474–483. doi: 10.1016/0041-008x(88)90365-1. [DOI] [PubMed] [Google Scholar]
  45. Lowy M. T., Gault L., Yamamoto B. K. Adrenalectomy attenuates stress-induced elevations in extracellular glutamate concentrations in the hippocampus. J Neurochem. 1993 Nov;61(5):1957–1960. doi: 10.1111/j.1471-4159.1993.tb09839.x. [DOI] [PubMed] [Google Scholar]
  46. Lupie S. J., King S., Meaney M. J., McEwen B. S. Can poverty get under your skin? basal cortisol levels and cognitive function in children from low and high socioeconomic status. Dev Psychopathol. 2001 Summer;13(3):653–676. doi: 10.1017/s0954579401003133. [DOI] [PubMed] [Google Scholar]
  47. Lupien S. J., McEwen B. S. The acute effects of corticosteroids on cognition: integration of animal and human model studies. Brain Res Brain Res Rev. 1997 Jun;24(1):1–27. doi: 10.1016/s0165-0173(97)00004-0. [DOI] [PubMed] [Google Scholar]
  48. Lustberg Mark, Silbergeld Ellen. Blood lead levels and mortality. Arch Intern Med. 2002 Nov 25;162(21):2443–2449. doi: 10.1001/archinte.162.21.2443. [DOI] [PubMed] [Google Scholar]
  49. Ma T., Chen H. H., Lim D. K., Hume A. S., Ho I. K. Excitatory amino acids and lead-induced neurotoxicity. J Toxicol Sci. 1998 Jul;23 (Suppl 2):181–183. doi: 10.2131/jts.23.supplementii_181. [DOI] [PubMed] [Google Scholar]
  50. Maccari S., Darnaudery M., Morley-Fletcher S., Zuena A. R., Cinque C., Van Reeth O. Prenatal stress and long-term consequences: implications of glucocorticoid hormones. Neurosci Biobehav Rev. 2003 Jan-Mar;27(1-2):119–127. doi: 10.1016/s0149-7634(03)00014-9. [DOI] [PubMed] [Google Scholar]
  51. Mangiavacchi S., Masi F., Scheggi S., Leggio B., De Montis M. G., Gambarana C. Long-term behavioral and neurochemical effects of chronic stress exposure in rats. J Neurochem. 2001 Dec;79(6):1113–1121. doi: 10.1046/j.1471-4159.2001.00665.x. [DOI] [PubMed] [Google Scholar]
  52. Marmot M. G., Shipley M. J., Rose G. Inequalities in death--specific explanations of a general pattern? Lancet. 1984 May 5;1(8384):1003–1006. doi: 10.1016/s0140-6736(84)92337-7. [DOI] [PubMed] [Google Scholar]
  53. McEwen B. S. Plasticity of the hippocampus: adaptation to chronic stress and allostatic load. Ann N Y Acad Sci. 2001 Mar;933:265–277. doi: 10.1111/j.1749-6632.2001.tb05830.x. [DOI] [PubMed] [Google Scholar]
  54. McEwen B. S., Weiss J. M., Schwartz L. S. Selective retention of corticosterone by limbic structures in rat brain. Nature. 1968 Nov 30;220(5170):911–912. doi: 10.1038/220911a0. [DOI] [PubMed] [Google Scholar]
  55. McMichael A. J., Baghurst P. A., Wigg N. R., Vimpani G. V., Robertson E. F., Roberts R. J. Port Pirie Cohort Study: environmental exposure to lead and children's abilities at the age of four years. N Engl J Med. 1988 Aug 25;319(8):468–475. doi: 10.1056/NEJM198808253190803. [DOI] [PubMed] [Google Scholar]
  56. Miller D. B., Chernoff N. Restraint-induced stress in pregnant mice--degree of immobilization affects maternal indices of stress and developmental outcome in offspring. Toxicology. 1995 Apr 12;98(1-3):177–186. doi: 10.1016/0300-483x(94)02988-7. [DOI] [PubMed] [Google Scholar]
  57. Moghaddam Bita. Stress activation of glutamate neurotransmission in the prefrontal cortex: implications for dopamine-associated psychiatric disorders. Biol Psychiatry. 2002 May 15;51(10):775–787. doi: 10.1016/s0006-3223(01)01362-2. [DOI] [PubMed] [Google Scholar]
  58. Monteiro F., Abraham M. E., Sahakari S. D., Mascarenhas J. F. Effect of immobilization stress on food intake, body weight and weights of various organs in rat. Indian J Physiol Pharmacol. 1989 Jul-Sep;33(3):186–190. [PubMed] [Google Scholar]
  59. Munck A., Guyre P. M., Holbrook N. J. Physiological functions of glucocorticoids in stress and their relation to pharmacological actions. Endocr Rev. 1984 Winter;5(1):25–44. doi: 10.1210/edrv-5-1-25. [DOI] [PubMed] [Google Scholar]
  60. Needleman H. L., Riess J. A., Tobin M. J., Biesecker G. E., Greenhouse J. B. Bone lead levels and delinquent behavior. JAMA. 1996 Feb 7;275(5):363–369. [PubMed] [Google Scholar]
  61. Nihei M. K., Desmond N. L., McGlothan J. L., Kuhlmann A. C., Guilarte T. R. N-methyl-D-aspartate receptor subunit changes are associated with lead-induced deficits of long-term potentiation and spatial learning. Neuroscience. 2000;99(2):233–242. doi: 10.1016/s0306-4522(00)00192-5. [DOI] [PubMed] [Google Scholar]
  62. Orsini Cristina, Ventura Rossella, Lucchese Franco, Puglisi-Allegra Stefano, Cabib Simona. Predictable stress promotes place preference and low mesoaccumbens dopamine response. Physiol Behav. 2002 Feb 1;75(1-2):135–141. doi: 10.1016/s0031-9384(01)00629-1. [DOI] [PubMed] [Google Scholar]
  63. Pappas G., Queen S., Hadden W., Fisher G. The increasing disparity in mortality between socioeconomic groups in the United States, 1960 and 1986. N Engl J Med. 1993 Jul 8;329(2):103–109. doi: 10.1056/NEJM199307083290207. [DOI] [PubMed] [Google Scholar]
  64. Pincus T., Callahan L. F., Burkhauser R. V. Most chronic diseases are reported more frequently by individuals with fewer than 12 years of formal education in the age 18-64 United States population. J Chronic Dis. 1987;40(9):865–874. doi: 10.1016/0021-9681(87)90186-x. [DOI] [PubMed] [Google Scholar]
  65. Pirkle J. L., Kaufmann R. B., Brody D. J., Hickman T., Gunter E. W., Paschal D. C. Exposure of the U.S. population to lead, 1991-1994. Environ Health Perspect. 1998 Nov;106(11):745–750. doi: 10.1289/ehp.98106745. [DOI] [PMC free article] [PubMed] [Google Scholar]
  66. Pokora M. J., Richfield E. K., Cory-Slechta D. A. Preferential vulnerability of nucleus accumbens dopamine binding sites to low-level lead exposure: time course of effects and interactions with chronic dopamine agonist treatments. J Neurochem. 1996 Oct;67(4):1540–1550. doi: 10.1046/j.1471-4159.1996.67041540.x. [DOI] [PubMed] [Google Scholar]
  67. Rahe R. H., Lind E. Psychosocial factors and sudden cardiac death: a pilot study. J Psychosom Res. 1971 Mar;15(1):19–24. doi: 10.1016/0022-3999(71)90069-9. [DOI] [PubMed] [Google Scholar]
  68. Sapolsky R. M., Krey L. C., McEwen B. S. The neuroendocrinology of stress and aging: the glucocorticoid cascade hypothesis. Endocr Rev. 1986 Aug;7(3):284–301. doi: 10.1210/edrv-7-3-284. [DOI] [PubMed] [Google Scholar]
  69. Scheggi Simona, Leggio Benedetta, Masi Flavio, Grappi Silvia, Gambarana Carla, Nanni Giulio, Rauggi Riccardo, De Montis Maria Graziella. Selective modifications in the nucleus accumbens of dopamine synaptic transmission in rats exposed to chronic stress. J Neurochem. 2002 Nov;83(4):895–903. doi: 10.1046/j.1471-4159.2002.01193.x. [DOI] [PubMed] [Google Scholar]
  70. Shalev U., Weiner I. Gender-dependent differences in latent inhibition following prenatal stress and corticosterone administration. Behav Brain Res. 2001 Nov 29;126(1-2):57–63. doi: 10.1016/s0166-4328(01)00250-9. [DOI] [PubMed] [Google Scholar]
  71. Takahashi L. K., Turner J. G., Kalin N. H. Prenatal stress alters brain catecholaminergic activity and potentiates stress-induced behavior in adult rats. Brain Res. 1992 Mar 6;574(1-2):131–137. doi: 10.1016/0006-8993(92)90809-n. [DOI] [PubMed] [Google Scholar]
  72. Tennes K., Kreye M. Children's adrenocortical responses to classroom activities and tests in elementary school. Psychosom Med. 1985 Sep-Oct;47(5):451–460. doi: 10.1097/00006842-198509000-00005. [DOI] [PubMed] [Google Scholar]
  73. Thiruchelvam M., Richfield E. K., Baggs R. B., Tank A. W., Cory-Slechta D. A. The nigrostriatal dopaminergic system as a preferential target of repeated exposures to combined paraquat and maneb: implications for Parkinson's disease. J Neurosci. 2000 Dec 15;20(24):9207–9214. doi: 10.1523/JNEUROSCI.20-24-09207.2000. [DOI] [PMC free article] [PubMed] [Google Scholar]
  74. Tong S., McMichael A. J., Baghurst P. A. Interactions between environmental lead exposure and sociodemographic factors on cognitive development. Arch Environ Health. 2000 Sep-Oct;55(5):330–335. doi: 10.1080/00039890009604025. [DOI] [PubMed] [Google Scholar]
  75. Vinokur A., Selzer M. L. Desirable versus undesirable life events: their relationship to stress and mental distress. J Pers Soc Psychol. 1975 Aug;32(2):329–337. doi: 10.1037//0022-3514.32.2.329. [DOI] [PubMed] [Google Scholar]
  76. Virgolini M. B., Cancela L. M., Fulginiti S. Behavioral responses to ethanol in rats perinatally exposed to low lead levels. Neurotoxicol Teratol. 1999 Sep-Oct;21(5):551–557. doi: 10.1016/s0892-0362(99)00020-3. [DOI] [PubMed] [Google Scholar]
  77. Vázquez D. M. Stress and the developing limbic-hypothalamic-pituitary-adrenal axis. Psychoneuroendocrinology. 1998 Oct;23(7):663–700. doi: 10.1016/s0306-4530(98)00029-8. [DOI] [PubMed] [Google Scholar]
  78. Walkowiak J., Altmann L., Krämer U., Sveinsson K., Turfeld M., Weishoff-Houben M., Winneke G. Cognitive and sensorimotor functions in 6-year-old children in relation to lead and mercury levels: adjustment for intelligence and contrast sensitivity in computerized testing. Neurotoxicol Teratol. 1998 Sep-Oct;20(5):511–521. doi: 10.1016/s0892-0362(98)00010-5. [DOI] [PubMed] [Google Scholar]
  79. Ward I. L., Weisz J. Differential effects of maternal stress on circulating levels of corticosterone, progesterone, and testosterone in male and female rat fetuses and their mothers. Endocrinology. 1984 May;114(5):1635–1644. doi: 10.1210/endo-114-5-1635. [DOI] [PubMed] [Google Scholar]
  80. Weinstock M., Poltyrev T., Schorer-Apelbaum D., Men D., McCarty R. Effect of prenatal stress on plasma corticosterone and catecholamines in response to footshock in rats. Physiol Behav. 1998 Jun 15;64(4):439–444. doi: 10.1016/s0031-9384(98)00056-0. [DOI] [PubMed] [Google Scholar]
  81. Widzowski D. V., Cory-Slechta D. A. Homogeneity of regional brain lead concentrations. Neurotoxicology. 1994 Summer;15(2):295–307. [PubMed] [Google Scholar]
  82. Wyler A. R., Masuda M., Holmes T. H. Magnitude of life events and seriousness of illness. Psychosom Med. 1971 Mar-Apr;33(2):115–122. doi: 10.1097/00006842-197103000-00003. [DOI] [PubMed] [Google Scholar]
  83. 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 Jun;85(3):135–141. doi: 10.1016/0378-4274(96)03655-7. [DOI] [PubMed] [Google Scholar]
  84. Zhang Xiao-yan, Liu Ai-Ping, Ruan Di-Yun, Liu Jin. Effect of developmental lead exposure on the expression of specific NMDA receptor subunit mRNAs in the hippocampus of neonatal rats by digoxigenin-labeled in situ hybridization histochemistry. Neurotoxicol Teratol. 2002 Mar-Apr;24(2):149–160. doi: 10.1016/s0892-0362(01)00210-0. [DOI] [PubMed] [Google Scholar]
  85. Zuch C. L., O'Mara D. J., Cory-Slechta D. A. Low-level lead exposure selectively enhances dopamine overflow in nucleus accumbens: an in vivo electrochemistry time course assessment. Toxicol Appl Pharmacol. 1998 May;150(1):174–185. doi: 10.1006/taap.1998.8396. [DOI] [PubMed] [Google Scholar]

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