Experimental manipulations blunt time-induced changes in brain monoamine levels and completely reverse stress, but not Pb+/-stress-related modifications to these trajectories

Behavioural Brain Research

Volumn 205, Issue 1, 2009, Pages 76-87

  Cory Slechta, D A ^a   Virgolini, M B ^b   Rossi George, A ^c   Weston, D ^a   Thiruchelvam, M ^d  

^a UNIVERSITY OF ROCHESTER SCHOOL OF MEDICINE AND DENTISTRY   (United States)

^b UNIVERSIDAD NACIONAL DE CÓRDOBA   (Argentina)

^c RUTGERS UNIVERSITY   (United States)

^d RUTGERS UNIVERSITY   (United States)

Author keywords

Behavior; Dopamine; Enrichment; Lead; Norepinephrine; Offspring stress; Prenatal stress; Serotonin

Indexed keywords

BRAIN MONOAMINE; DOPAMINE; DRINKING WATER; LEAD; NORADRENALIN; SEROTONIN;

ADAPTIVE BEHAVIOR; ANIMAL EXPERIMENT; ARTICLE; BRAIN REGION; CONTROLLED STUDY; CORPUS STRIATUM; ENVIRONMENTAL EXPOSURE; EXPERIMENTAL STUDY; FEMALE; FRONTAL CORTEX; MALE; NONHUMAN; NUCLEUS ACCUMBENS; OUTCOME ASSESSMENT; PRENATAL STRESS; PRIORITY JOURNAL; RAT;

AGING; ANIMALS; BIOGENIC MONOAMINES; BRAIN; CENTRAL NERVOUS SYSTEM AGENTS; CORPUS STRIATUM; DOPAMINE; FEMALE; FRONTAL LOBE; LEAD; MALE; NOREPINEPHRINE; NUCLEUS ACCUMBENS; PREGNANCY; PRENATAL EXPOSURE DELAYED EFFECTS; RANDOM ALLOCATION; RATS; RATS, LONG-EVANS; STRESS, PSYCHOLOGICAL; TIME FACTORS;

EID: 70349419542     PISSN: 01664328     EISSN: 18727549     Source Type: Journal    
DOI: 10.1016/j.bbr.2009.06.040     Document Type: Article

References (74)

1. Cory-Slechta D.A., Virgolini M.B., Thiruchelvam M., Weston D.D., and Bauter M.R. Maternal stress modulates the effects of developmental lead exposure. Environ Health Perspect 112 (2004) 717-730
2. Koehl M., Lemaire V., Vallee M., Abrous N., Piazza P.V., Mayo W., et al. Long term neurodevelopmental and behavioral effects of perinatal life events in rats. Neurotox Res 3 (2001) 65-83
3. Maccari S., Darnaudery M., Morley-Fletcher S., Zuena A.R., Cinque C., and Van Reeth O. Prenatal stress and long-term consequences: implications of glucocorticoid hormones. Neurosci Biobehav Rev 27 (2003) 119-127
4. Rossi-George A., Virgolini M., Weston D., and Cory-Slechta D.A. Alterations in glucocorticoid negative feedback following maternal Pb, prenatal stress and the combination: a potential biological unifying mechanism for their corresponding disease profiles. Toxicol Appl Pharmacol 234 (2009) 117-127
5. Vallee M., Maccari S., Dellu F., Simon H., Le Moal M., and Mayo W. Long-term effects of prenatal stress and postnatal handling on age-related glucocorticoid secretion and cognitive performance: a longitudinal study in the rat. Eur J Neurosci 11 (1999) 2906-2916
6. 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 225 (2007) 1-27
7. Kuhlmann A.C., McGlothan J.L., and Guilarte T.R. Developmental lead exposure causes spatial learning deficits in adult rats. Neurosci Lett 233 (1997) 101-104
8. Virgolini M.B., Rossi-George A., Lisek R., Weston D., Thiruchelvam M., and Cory-Slechta D.A. CNS effects of developmental Pb exposure are enhanced by combined maternal and offspring stress. Neurotoxicol 29 (2008) 812-827
9. Yang Y., Ma Y., Ni L., Zhao S., Li L., Zhang J., et al. Lead exposure through gestation-only caused long-term learning/memory deficits in young adult offspring. Exp Neurol 184 (2003) 489-495
10. Rice D.C., and Gilbert S.G. Sensitive periods for lead-induced behavioral impairment (nonspatial discrimination reversal) in monkeys. Toxicol Appl Pharmacol 102 (1990) 101-109
11. Rice D.C. Lead-induced changes in learning: evidence for behavioral mechanisms from experimental animal studies. Neurotoxicol 14 (1993) 167-178
12. Barrot M., Marinelli M., Abrous D.N., Rouge-Pont F., Le Moal M., and Piazza P.V. The dopaminergic hyper-responsiveness of the shell of the nucleus accumbens is hormone-dependent. Eur J Neurosci 12 (2000) 973-979
13. Cory-Slechta D.A., O'Mara D.J., and Brockel B.J. Nucleus accumbens dopaminergic mediation of fixed interval schedule-controlled behavior and its modulation by low-level lead exposure. J Pharmacol Exp Ther 286 (1998) 794-805
14. Diorio D., Viau V., and Meaney M.J. The role of the medial prefrontal cortex (cingulate gyrus) in the regulation of hypothalamic-pituitary-adrenal responses to stress. J Neurosci 13 (1993) 3839-3847
15. Lowy M., Gault L., and Yammamato B. Adrenalectomy attenuates stress induced elevation in extracellular glutamate concentration in hippocampus. J Neurosci 61 (1993) 1957-1960
16. Moghaddam B. Stress activation of glutamate neurotransmission in the prefrontal cortex: Implications for dopamine-associated psychiatric disorders. Biol Psychiatry 51 (2002) 775-787
17. Piazza P.V., Rouge-Pont F., Deroche V., Maccari S., Simon H., and Le Moal M. glucocorticoids have state-dependent stimulant effects on the mesencephalic dopaminergic transmission. Proc Natl Acad Sci USA 93 (1996) 8716-8720
18. Pokora M.J., Richfield E.K., and 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 67 (1996) 1540-1550
19. Anderson N.B., and Armstead C.A. Toward understanding the asociation of socioeconomic status and health: a new challenge for the biopsychosocial approach. Psychosom Med 57 (1995) 213-225
20. Iqbal S., Muntner P., Batuman V., and Rabito F.A. Estimated burden of blood lead levels 5 μg/dl in 1999-2002 and declines from 1988 to 1994. Environ Res (2008)
21. Cory-Slechta D.A., Virgolini M.B., Thiruchelvam M., Weston D.D., and Bauter M.R. Maternal stress modulates effects of developmental lead exposure. Environ Health Perspect 112 (2004) 717-730
22. Cory-Slechta D.A., Virgolini M.B., Rossi-George A., Thiruchelvam M., Lisek R., and Weston D. Lifetime consequences of combined maternal lead and stress. Basic Clin Pharmacol Toxicol 102 (2008) 218-227
23. Fox C., Merali Z., and Harrison C. Therapeutic and protective effect of environmental enrichment against psychogenic and neurogenic stress. Behav Brain Res 175 (2006) 1-8
24. Francis Dd, Diorio J., Plotsky P.M., and Meaney M.J. Environmental enrichment reverses the effects of maternal separation on stress reactivity. J Neurosci 22 (2002) 7840-7843
25. Laviola G., Rea M., Morley-Fletcher S., Di Carlo S., Bacosi A., De Simone R., et al. Beneficial effects of enriched environment on adolescent rats from stressed pregnancies. Eur J Neurosci 20 (2004) 1655-1664
26. Morley-Fletcher S., Rea M., Maccari S., and Laviola G. Environmental enrichment during adolescence reverses the effects of prenatal stress on play behaviour and HPA axis reactivity in rats. Eur J Neurosci 18 (2003) 3367-3374
27. Guilarte T.R., Toscano C.D., McGlothan J.L., and Weaver S.A. Environmental enrichment reverses cognitive and molecular deficits induced by developmental lead exposure. Ann Neurol 53 (2003) 50-56
28. Petit T.L., and Alfano D.P. Differential experience following developmental lead exposure: Effects on brain and behavior. Pharmacol Biochem Behav 11 (1979) 165-171
29. Schneider J.S., Lee M.H., Anderson D.W., Zuck L., and Lidsky T.I. Enriched environment during development is protective against lead-induced neurotoxicity. Brain Res 896 (2001) 48-55
30. Dorce V.A., and Palermo-Neto J. Behavioral and neurochemical changes induced by aging in dopaminergic systems of male and female rats. Physiol Behav 56 (1994) 1015-1019
31. Fernandez-Ruiz J., De Miguel R., Hernandez M.L., Cebeira M., and Ramos J.A. Comparisons between brain dopaminergic neurons of juvenile and aged rats: sex-related differences. Mech Ageing Dev 63 (1992) 45-55
32. Friedemann M., and Gerhardt G.A. Regional effects of aging on dopaminergic function in the Fischer-344 rat. Neurobiol Aging 13 (1992) 325-332
33. Gerhardt G.A., and Maloney Jr. R.E. Microdialysis studies of basal levels and stimulus-evoked overflow of dopamine and metabolites in the striatum of young and aged Fischer 344 rats. Brain Res 816 (1999) 68-77
34. McDermott J.L., and Dluzen D.E. Aging and sex differences in striatal dopaminergic function. Neuroscience 149 (2007) 401-408
35. Mora F., Segovia G., and del Arco A. Aging, plasticity and environmental enrichment: structural changes and neurotransmitter dynamics in several areas of the brain. Brain Res Rev 55 (2007) 78-88
36. Yurek D.M., Hipkens S.B., Hebert M.A., Gash D.M., and Gerhardt G.A. Age-related decline in striatal dopamine release and motoric function in brown Norway/Fischer 344 hybrid rats. Brain Res 791 (1998) 246-256
37. Nader M.A., and Bowen C.A. Effects of different food-reinforcement histories on cocaine self-administration by rhesus monkeys. Psychopharmacology (Berl) 118 (1995) 287-294
38. Nader M.A., and Mach R.H. Self-administration of the dopamine D3 agonist 7-OH-DPAT in rhesus monkeys is modified by prior cocaine exposure. Psychopharmacology (Berl) 125 (1996) 13-22
39. Nader M.A., and Reboussin D.M. The effects of behavioral history on cocaine self-administration by rhesus monkeys. Psychopharmacology (Berl) 115 (1994) 53-58
40. Morgan D., Brebner K., Lynch W.J., and Roberts D.C. Increases in the reinforcing efficacy of cocaine after particular histories of reinforcement. Behav Pharmacol 13 (2002) 389-396
41. Holmes A., and Rodgers R.J. Influence of spatial and temporal manipulations on the anxiolytic efficacy of chlordiazepoxide in mice previously exposed to the elevated plus-maze. Neurosci Biobehav Rev 23 (1999) 971-980
42. Holmes A., Iles J.P., Mayell S.J., and Rodgers R.J. Prior test experience compromises the anxiolytic efficacy of chlordiazepoxide in the mouse light/dark exploration test. Behav Brain Res 122 (2001) 159-167
43. Brockel B.J., and Cory-Slechta D.A. Lead, attention, and impulsive behavior: changes in a fixed-ratio waiting-for-reward paradigm. Pharmacol Biochem Behav 60 (1998) 545-552
44. Cory-Slechta D.A. Relationships between lead-induced learning impairments and changes in dopaminergic, cholinergic and glutamatergic neurotransmitter system functions. Annu Rev Pharmacol Toxicol 35 (1995) 391-415
45. Canfield R.L., Gendle M.H., and Cory-Slechta D.A. Impaired neuropsychological functioning in lead-exposed children. Dev Neuropsychol 26 (2004) 513-540
46. Canfield R.L., Henderson C.R., Cory-Slechta D.A., Cox C., Jusko T.A., and Lanphear B.P. Intellectual impairment in children with blood lead concentrations below 10 μg per deciliter. N Engl J Med 348 (2003) 1517-1526
47. Cory-Slechta D.A., Weiss B., and Cox C. Mobilization and redistribution of lead over the course of calcium disodium ethylenediamine tetracetate chelation therapy. J Pharmacol Exp Ther 243 (1987) 804-813
48. Ward I.L., and 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 114 (1984) 1635-1644
49. Baker S., Chebli M., Rees S., Lemarec N., Godbout R., and Bielajew C. Effects of gestational stress. 1. Evaluation of maternal and juvenile offspring behavior. Brain Res 1213 (2008) 98-110
50. Darnaudery M., and Maccari S. Epigenetic programming of the stress response in male and female rats by prenatal restraint stress. Brain Res Rev 57 (2008) 571-585
51. Igosheva N., Taylor P.D., Poston L., and Glover V. Prenatal stress in the rat results in increased blood pressure responsiveness to stress and enhanced arterial reactivity to neuropeptide Y in adulthood. J Physiol 582 (2007) 665-674
52. Mairesse J., Lesage J., Breton C., Breant B., Hahn T., Darnaudery M., et al. Maternal stress alters endocrine function of the feto-placental unit in rats. Am J Physiol Endocrinol Metab 292 (2007) E1526-E1533
53. Pallares M.E., Scacchi Bernasconi P.A., Feleder C., and Cutrera R.A. Effects of prenatal stress on motor performance and anxiety behavior in Swiss mice. Physiol Behav 92 (2007) 951-956
54. Cory-Slechta D.A. Comparative neurobehavioral toxicology of heavy metals. In: Suzuki T. (Ed). Toxicology of metals (1996), CRC Press, New York 537-560
55. Koolhaas J.M., Meerlo P., De Boer S.F., Strubbe J.H., and Bohus B. The temporal dynamics of the stress response. Neurosci Biobehav Rev 21 (1997) 775-782
56. Virgolini M.B., Rossi-George A., Weston D., and Cory-Slechta D.A. Influence of low level maternal Pb exposure and prenatal stress on offspring stress challenge responsivity. Neurotoxicol 29 (2008) 928-939
57. Widzowski D.V., Finkelstein J.N., Pokora M.J., and Cory-Slechta D.A. Time course of postnatal lead-induced changes in dopamine receptors and their relationship to changes in dopamine sensitivity. Neurotoxicol 15 (1994) 853-865
58. Park M., Kitahama K., Geffard M., and Maeda T. Postnatal development of the dopaminergic neurons in the rat mesencephalon. Brain Dev 22 Suppl 1 (2000) S38-S44
59. Tepper J.M., Damlama M., and Trent F. Postnatal changes in the distribution and morphology of rat substantia nigra dopaminergic neurons. Neuroscience 60 (1994) 469-477
60. Hebb D.O. The organization of behavior: a neuropsychological theory (1949), Wiley, New York
61. Rosenzweig M.R., and Bennett E.L. Psychobiology of plasticity: effects of training and experience on brain and behavior. Behav Brain Res 78 (1996) 57-65
62. Will B., Galani R., Kelche C., and Rosenzweig M.R. Recovery from brain injury in animals: relative efficacy of environmental enrichment, physical exercise or formal training (1990-2002). Prog Neurobiol 72 (2004) 167-182
63. Cirulli F., Capone F., Bonsignore L.T., Aloe L., and Alleva E. Early behavioural enrichment in the form of handling renders mouse pups unresponsive to anxiolytic drugs and increases NGF levels in the hippocampus. Behav Brain Res 178 (2007) 208-215
64. Tejedor-Real P., Sahagun M., Biguet N.F., and Mallet J. Neonatal handling prevents the effects of phencyclidine in an animal model of negative symptoms of schizophrenia. Biol Psychiatry 61 (2007) 865-872
65. Dunn A.J., Elfvin K.L., and Berridge C.W. Changes in plasma corticosterone and cerebral biogenic amines and their catabolites during training and testing of mice in passive avoidance behavior. Behav Neural Biol 46 (1986) 410-423
66. Jones B.C., Hou X., and Cook M.N. Effect of exposure to novelty on brain monoamines in C57BL/6 and DBA/2 mice. Physiol Behav 59 (1996) 361-367
67. Cabib S., Algeri S., Perego C., and Puglisi-Allegra S. Behavioral and biochemical changes monitored in two inbred strains of mice during exploration of an unfamiliar environment. Physiol Behav 47 (1990) 749-753
68. De Boer S.F., Slangen J.L., and Van der Gugten J. Plasma catecholamine and corticosterone levels during active and passive shock-prod avoidance behavior in rats: effects of chlordiazepoxide. Physiol Behav 47 (1990) 1089-1098
69. Carrasco C., Vicens P., and Redolat R. Neuroprotective effects of behavioural training and nicotine on age-related deficits in spatial learning. Behav Pharmacol 17 (2006) 441-452
70. Hougaard K.S., Andersen M.B., Kjaer S.L., Hansen A.M., Werge T., and Lund S.P. Prenatal stress may increase vulnerability to life events: comparison with the effects of prenatal dexamethasone. Brain Res Dev Brain Res 159 (2005) 55-63
71. Mastorci F., Vicentini M., Viltart O., Manghi M., Graiani G., Quaini F., et al. Long-term effects of prenatal stress: changes in adult cardiovascular regulation and sensitivity to stress. Neurosci Biobehav Rev 33 (2009) 191-203
72. Laviola G., Hannan A.J., Macri S., Solinas M., and Jaber M. Effects of enriched environment on animal models of neurodegenerative diseases and psychiatric disorders. Neurobiol Dis 31 (2008) 159-168
73. Cory-Slechta D.A., Pazmino R., and Bare C. The critical role of the nucleus accumbens dopamine systems in the mediation of fixed interval schedule-controlled operant behavior. Brain Res 764 (1997) 253-256
74. Cory-Slechta D.A., Brockel B.J., and O'Mara D.J. Lead exposure and dorsomedial striatum mediation of fixed interval schedule-controlled behavior. Neurotoxicol 23 (2002) 313-327