Brain hemispheric differences in the neurochemical effects of lead, prenatal stress, and the combination and their amelioration by behavioral experience

Toxicological Sciences

Volumn 132, Issue 2, 2013, Pages 419-430

  Cory slechta, Deborah A ^a   Weston, Douglas ^a   Liu, Sue ^a   Allen, Joshua L ^a  

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

Author keywords

Dopamine; Glutamate; Laterality; Lead; Prenatal stress; Sex

Indexed keywords

AMINO ACID; GLUTAMIC ACID; LEAD; MONOAMINE; NEUROTRANSMITTER;

ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ARTICLE; COGNITION; CONTROLLED STUDY; CORPUS STRIATUM; FEMALE; FRONTAL CORTEX; GESTATIONAL AGE; HEMISPHERIC DOMINANCE; LEARNING; LEFT HEMISPHERE; MALE; MESENCEPHALON; NONHUMAN; NUCLEUS ACCUMBENS; PRENATAL EXPOSURE; PRENATAL STRESS; RAT; RIGHT HEMISPHERE; SEX DIFFERENCE;

ANIMALS; BEHAVIOR, ANIMAL; BRAIN; FEMALE; LEAD; MALE; PREGNANCY; RATS; RATS, LONG-EVANS; STRESS, PHYSIOLOGICAL;

EID: 84875259284     PISSN: 10966080     EISSN: 10960929     Source Type: Journal    
DOI: 10.1093/toxsci/kft015     Document Type: Article

References (100)

1. Abrahams, S., Pickering, A., Polkey, C. E., and Morris, R. G. (1997). Spatial memory deficits in patients with unilateral damage to the right hippocampal formation. Neuropsychologia 35, 11-24.
2. Afonso, D., Santana, C., and Rodriguez, M. (1993). Neonatal lateralization of behavior and brain dopaminergic asymmetry. Brain Res. Bull. 32, 11-16.
3. Barrot, M., Marinelli, M., Abrous, D. N., Rouge-Pont, F., Le Moal, M., and Piazza, P. V. (2000). The dopaminergic hyper-responsiveness of the shell of the nucleus accumbens is hormone-dependent. Eur. J. Neurosci. 12, 973-979.
4. Belcheva, I., Bryer, J. B., Starkstein, S. E., Honig, M., Moran, T. H., and Robinson, R. G. (1990). Hemispheric asymmetry in behavioral response to D1 and D2 receptor agonists in the nucleus accumbens. Brain Res. 533, 286-291.
5. Berrebi, A. S., Fitch, R. H., Ralphe, D. L., Denenberg, J. O., Friedrich, V. L., Jr, and Denenberg, V. H. (1988). Corpus callosum: Region-specific effects of sex, early experience and age. Brain Res. 438, 216-224.
6. Broca, P. (1861). Remarques sur le siege de la faculte du langage articule suivies d'une observation d'aphemie (perte de la parole). Bull. Soc. Anthropol. 6, 330-357.
7. Brockel, B. J., and Cory-Slechta, D. A. (1998). Lead, attention, and impulsive behavior: Changes in a fixed-ratio waiting-for-reward paradigm. Pharmacol. Biochem. Behav. 60, 545-552.
8. Canfield, R. L., Gendle, M. H., and Cory-Slechta, D. A. (2004). Impaired neuropsychological functioning in lead-exposed children. Dev. Neuropsychol. 26, 513-540.
9. Canfield, R. L., Henderson, C. R., Jr, Cory-Slechta, D. A., Cox, C., Jusko, T. A., and Lanphear, B. P. (2003). Intellectual impairment in children with blood lead concentrations below 10 microg per deciliter. N. Engl. J. Med. 348, 1517-1526.
10. Capper-Loup, C., Rebell, D., and Kaelin-Lang, A. (2009). Hemispheric lateralization of the corticostriatal glutamatergic system in the rat. J. Neural Transm. 116, 1053-1057.
11. Carlson, J. N., Fitzgerald, L. W., Keller, R. W., Jr, and Glick, S. D. (1993). Lateralized changes in prefrontal cortical dopamine activity induced by controllable and uncontrollable stress in the rat. Brain Res. 630, 178-187.
12. Cohn, J., and Cory-Slechta, D. A. (1993). Subsensitivity of lead-exposed rats to the accuracy-impairing and rate-altering effects of MK-801 on a multiple schedule of repeated learning and performance. Brain Res. 600, 208-218.
13. Cohn, J., and Cory-Slechta, D. A. (1994a). Assessment of the role of dopaminergic systems in lead-induced learning impairments using a repeated acquisition and performance baseline. Neurotoxicology 15, 913-926.
14. Cohn, J., and Cory-Slechta, D. A. (1994b). Lead exposure potentiates the effects of NMDA on repeated learning. Neurotoxicol. Teratol. 16, 455-465.
15. Cohn, J., Cox, C., and Cory-Slechta, D. A. (1993). The effects of lead exposure on learning in a multiple repeated acquisition and performance schedule. Neurotoxicology 14, 329-346.
16. Cory-Slechta, D. A. (1995). Relationships between lead-induced learning impairments and changes in dopaminergic, cholinergic, and glutamatergic neurotransmitter system functions. Annu. Rev. Pharmacol. Toxicol. 35, 391-415.
17. Cory-Slechta, D. A., Merchant-Borna, K., Allen, J., Liu, S., Weston, D., and Conrad, K. (2012a). Enhanced stimulus sequence-dependent repeated learning in male offspring after prenatal stress alone or in conjunction with lead exposure. Neurotoxicology 33, 1188-1202.
18. Cory-Slechta, D. A., Merchant-Borna, K., Allen, J. L., Liu, S., Weston, D., and Conrad, K. (2012b). Variations in the nature of behavioral experience can differentially alter the consequences of developmental exposures to lead, prenatal stress, and the combination. Toxicol. Sci. 131, 194-205.
19. Cory-Slechta, D. A., O'Mara, D. J., and Brockel, B. J. (1998). Nucleus accumbens dopaminergic medication of fixed interval schedule-controlled behavior and its modulation by low-level lead exposure. J. Pharmacol. Exp. Ther. 286, 794-805.
20. Cory-Slechta, D. A., O'Mara, D. J., and Brockel, B. J. (1999). Learning versus performance impairments following regional administration of MK-801 into nucleus accumbens and dorsomedial striatum. Behav. Brain Res. 102, 181-194.
21. Cory-Slechta, D. A., Pazmino, R., and Bare, C. (1997). The critical role of nucleus accumbens dopamine systems in the mediation of fixed interval schedule-controlled operant behavior. Brain Res. 764, 253-256.
22. Cory-Slechta, D. A., Pokora, M. J., and Preston, R. A. (1996). The effects of dopamine agonists on fixed interval schedule-controlled behavior are selectively altered by low-level lead exposure. Neurotoxicol. Teratol. 18, 565-575.
23. Cory-Slechta, D. A., Stern, S., Weston, D., Allen, J. L., and Liu, S. (2010). Enhanced learning deficits in female rats following lifetime pb exposure combined with prenatal stress. Toxicol. Sci. 117, 427-438.
24. Cory-Slechta, D. A., Virgolini, M. B., Liu, S., and Weston, D. (2012c). Enhanced stimulus sequence-dependent repeated learning in male offspring after prenatal stress alone or in conjunction with lead exposure. Neurotoxicology
25. Cory-Slechta, D. A., Virgolini, M. B., Liu, S., and Weston, D. (2012d). Enhanced stimulus sequence-dependent repeated learning in male offspring after prenatal stress alone or in conjunction with lead exposure. Neurotoxicology 33, 1188-1202.
26. Cory-Slechta, D. A., Virgolini, M. B., Rossi-George, A., Weston, D., and Thiruchelvam, M. (2009). Experimental manipulations blunt time-induced changes in brain monoamine levels and completely reverse stress, but not Pb+/-stress-related modifications to these trajectories. Behav. Brain Res. 205, 76-87.
27. Cory-Slechta, D. A., Virgolini, M. B., Thiruchelvam, M., Weston, D. D., and Bauter, M. R. (2004). Maternal stress modulates the effects of developmental lead exposure. Environ. Health Perspect. 112, 717-730.
28. Czeh, B., Perez-Cruz, C., Fuchs, E., and Flugge, G. (2008). Chronic stress-induced cellular changes in the medial prefrontal cortex and their potential clinical implications: Does hemisphere location matter? Behav. Brain Res. 190, 1-13.
29. de Freitas Silva, D. M., Ferraz, V. P., and Ribeiro, A. M. (2009). Improved highperformance liquid chromatographic method for GABA and glutamate determination in regions of the rodent brain. J. Neurosci. Methods 177, 289-293.
30. Denenberg, V. H. (1983). Lateralization of function in rats. Am. J. Physiol. 245, R505-R509.
31. Denenberg, V. H. (1984). Some statistical and experimental considerations in the use of the analysis-of-variance procedure. Am. J. Physiol. 246(4 Pt 2), R403-R408.
32. Denenberg, V. H., Hofmann, M., Garbanati, J. A., Sherman, G. F., Rosen, G. D., and Yutzey, D. A. (1980). Handling in infancy, taste aversion, and brain laterality in rats. Brain Res. 200, 123-133.
33. Diaz, R., Sokoloff, P., and Fuxe, K. (1997). Codistribution of the dopamine D3 receptor and glucocorticoid receptor mRNAs during striatal prenatal development in the rat. Neurosci. Lett. 227, 119-122.
34. Diorio, D., Viau, V., and Meaney, M. J. (1993). The role of the medial prefrontal cortex (cingulate gyrus) in the regulation of hypothalamic-pituitary-adrenal responses to stress. J. Neurosci. 13, 3839-3847.
35. Drew, K. L., Lyon, R. A., Titeler, M., and Glick, S. D. (1986). Asymmetry in D-2 binding in female rat striata. Brain Res. 363, 192-195.
36. Fox, C., Merali, Z., and Harrison, C. (2006). Therapeutic and protective effect of environmental enrichment against psychogenic and neurogenic stress. Behav. Brain Res. 175, 1-8.
37. Froehlich, T. E., Lanphear, B. P., Dietrich, K. N., Cory-Slechta, D. A., Wang, N., and Kahn, R. S. (2007). Interactive effects of a DRD4 polymorphism, lead, and sex on executive functions in children. Biol. Psychiatry 62, 243-249.
38. Gasbarri, A., Campana, E., Pacitti, C., Hajdu, F., and Tombol, T. (1991). Organization of the projections from the ventral tegmental area of Tsai to the hippocampal formation in the rat. J. Hirnforsch. 32, 429-437.
39. Geschwind, N., and Galaburda, A. M. (1985). Cerebral lateralization. Biological mechanisms, associations, and pathology: I. A hypothesis and a program for research. Arch. Neurol. 42, 428-459.
40. Grizenko, N., Shayan, Y. R., Polotskaia, A., Ter-Stepanian, M., and Joober, R. (2008). Relation of maternal stress during pregnancy to symptom severity and response to treatment in children with ADHD. J. Psychiatry Neurosci. 33, 10-16.
41. Guilarte, T. R., Toscano, C. D., McGlothan, J. L., and Weaver, S. A. (2003). Environmental enrichment reverses cognitive and molecular deficits induced by developmental lead exposure. Ann. Neurol. 53, 50-56.
42. Hashimoto, K., Engberg, G., Shimizu, E., Nordin, C., Lindstrom, L. H., and Iyo, M. (2005). Elevated glutamine/glutamate ratio in cerebrospinal fluid of first episode and drug naive schizophrenic patients. BMC Psychiatry 5, 6.
43. Hausmann, M., and Gunturkun, O. (2000). Steroid fluctuations modify functional cerebral asymmetries: The hypothesis of progesterone-mediated interhemispheric decoupling. Neuropsychologia 38, 1362-1374.
44. Hirnstein, M., Leask, S., Rose, J., and Hausmann, M. (2010). Disentangling the relationship between hemispheric asymmetry and cognitive performance. Brain Cogn. 73, 119-127.
45. Jett, D. A., Kuhlmann, A. C., Farmer, S. J., and Guilarte, T. R. (1997). Agedependent effects of developmental lead exposure on performance in the Morris water maze. Pharmacol. Biochem. Behav. 57, 271-279.
46. Keune, P. M., Schonenberg, M., Wyckoff, S., Mayer, K., Riemann, S., Hautzinger, M., and Strehl, U. (2011). Frontal alpha-asymmetry in adults with attention deficit hyperactivity disorder: Replication and specification. Biol. Psychol. 87, 306-310.
47. King, S., and Laplante, D. P. (2005). The effects of prenatal maternal stress on children's cognitive development: Project Ice Storm. Stress 8, 35-45.
48. Klur, S., Muller, C., Pereira de Vasconcelos, A., Ballard, T., Lopez, J., Galani, R., Certa, U., and Cassel, J. C. (2009). Hippocampal-dependent spatial memory functions might be lateralized in rats: An approach combining gene expression profiling and reversible inactivation. Hippocampus 19, 800-816.
49. Kuhlmann, A. C., McGlothan, J. L., and Guilarte, T. R. (1997). Developmental lead exposure causes spatial learning deficits in adult rats. Neurosci. Lett. 233, 101-104.
50. Lange, N., Dubray, M. B., Lee, J. E., Froimowitz, M. P., Froehlich, A., Adluru, N., Wright, B., Ravichandran, C., Fletcher, P. T., Bigler, E. D., et al. (2010). Atypical diffusion tensor hemispheric asymmetry in autism. Autism Res. 3, 350-358.
51. Lanphear, B. P., Hornung, R., Khoury, J., Yolton, K., Baghurst, P., Bellinger, D. C., Canfield, R. L., Dietrich, K. N., Bornschein, R., Greene, T., et al. (2005). Low-level environmental lead exposure and children's intellectual function: An international pooled analysis. Environ. Health Perspect. 113, 894-899.
52. Laplante, D. P., Barr, R. G., Brunet, A., Galbaud du Fort, G., Meaney, M. L., Saucier, J. F., Zelazo, P. R., and King, S. (2004). Stress during pregnancy affects general intellectual and language functioning in human toddlers. Pediatr. Res. 56, 400-410.
53. Leonard, C. M., and Eckert, M. A. (2008). Asymmetry and dyslexia. Dev. Neuropsychol. 33, 663-681.
54. Lim, S. Y., Doherty, J. D., McBride, K., Miller-Ihli, N. J., Carmona, G. N., Stark, K. D., and Salem, N., Jr. (2005). Lead exposure and (n-3) fatty acid deficiency during rat neonatal development affect subsequent spatial task performance and olfactory discrimination. J. Nutr. 135, 1019-1026.
55. Lo, Y. C., Soong, W. T., Gau, S. S., Wu, Y. Y., Lai, M. C., Yeh, F. C., Chiang, W. Y., Kuo, L. W., Jaw, F. S., and Tseng, W. Y. (2011). The loss of asymmetry and reduced interhemispheric connectivity in adolescents with autism: A study using diffusion spectrum imaging tractography. Psychiatry Res. 192, 60-66.
56. Lordi, B., Patin, V., Protais, P., Mellier, D., and Caston, J. (2000). Chronic stress in pregnant rats: Effects on growth rate, anxiety and memory capabilities of the offspring. Int. J. Psychophysiol. 37, 195-205.
57. Lui, C. C., Wang, J. Y., Tain, Y. L., Chen, Y. C., Chang, K. A., Lai, M. C., and Huang, L. T. (2011). Prenatal stress in rat causes long-term spatial memory deficit and hippocampus MRI abnormality: Differential effects of postweaning enriched environment. Neurochem. Int. 58, 434-441.
58. Majkutewicz, I., Cecot, T., Jerzemowska, G., Myślińska, D., Plucińska, K., Trojniar, W., and Wrona, D. (2010). Lesion of the ventral tegmental area amplifies stimulation-induced Fos expression in the rat brain. Brain Res. 1320, 95-105.
59. Maliszewska-Scisło, M., and Trojniar, W. (1999). Augmentation of ventral tegmental area stimulation-induced feeding by both stimulation and lesion of the contralateral ventral tegmental area in the rat. Acta Neurobiol. Exp. (Wars). 59, 287-293.
60. Motlagh, M. G., Katsovich, L., Thompson, N., Lin, H., Kim, Y. S., Scahill, L., Lombroso, P. J., King, R. A., Peterson, B. S., and Leckman, J. F. (2010). Severe psychosocial stress and heavy cigarette smoking during pregnancy: An examination of the pre- and perinatal risk factors associated with ADHD and Tourette syndrome. Eur. Child Adolesc. Psychiatry 19, 755-764.
61. Nigg, J. T., Knottnerus, G. M., Martel, M. M., Nikolas, M., Cavanagh, K., Karmaus, W., and Rappley, M. D. (2008). Low blood lead levels associated with clinically diagnosed attention-deficit/hyperactivity disorder and mediated by weak cognitive control. Biol. Psychiatry 63, 325-331.
62. Nigg, J. T., Nikolas, M., Mark Knottnerus, G., Cavanagh, K., and Friderici, K. (2010). Confirmation and extension of association of blood lead with attention-deficit/hyperactivity disorder (ADHD) and ADHD symptom domains at population-typical exposure levels. J. Child Psychol. Psychiatry. 51, 58-65.
63. Nottebohm, F. (1970). Ontogeny of bird song. Science 167, 950-956.
64. Nottebohm, F. (1971). Neural lateralization of vocal control in a passerine bird. I. Song. J. Exp. Zool. 177, 229-261.
65. Oades, R. D., and Halliday, G. M. (1987). Ventral tegmental (A10) system: Neurobiology. 1. Anatomy and connectivity. Brain Res. 434, 117-165.
66. Oertel-Knochel, V., and Linden, D. E. (2011). Cerebral asymmetry in schizophrenia. Neuroscientist 17, 456-467.
67. Petroff, O. A., Errante, L. D., Rothman, D. L., Kim, J. H., and Spencer, D. D. (2002). Glutamate-glutamine cycling in the epileptic human hippocampus. Epilepsia 43, 703-710.
68. Piazza, P. V., Rouge-Pont, F., Deroche, V., Maccari, S., Simon, H., and Le Moal, M. (1996). Glucocorticoids have state-dependent stimulant effects on the mesencephalic dopaminergic transmission. Proc. Natl. Acad. Sci. U.S.A. 93, 8716-8720.
69. Pokora, M. J., Richfield, E. K., and Cory-Slechta, D. A. (1996). 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, 1540-1550.
70. Rodriguez, M., Castellano, M. A., and Palarea, M. D. (1990). Interhemispheric regulation of dopaminergic ascending systems. Life Sci. 47, 377-384.
71. Rogers, L. J., Zucca, P., and Vallortigara, G. (2004). Advantages of having a lateralized brain. Proc. Biol. Sci. 271(Suppl. 6), S420-S422.
72. Rosen, G. D., Finklestein, S., Stoll, A. L., Yutzey, D. A., and Denenberg, V. H. (1984). Neurochemical asymmetries in the albino rat's cortex, striatum, and nucleus accumbens. Life Sci. 34, 1143-1148.
73. Schneider, J. S., Lee, M. H., Anderson, D. W., Zuck, L., and Lidsky, T. I. (2001). Enriched environment during development is protective against leadinduced neurotoxicity. Brain Res. 896, 48-55.
74. Schuepbach, D., Skotchko, T., Duschek, S., Theodoridou, A., Grimm, S., Boeker, H., and Seifritz, E. (2012). Gender and rapid alterations of hemispheric dominance during planning. Neuropsychobiology 66, 149-157.
75. Scott, L. L., and Nguyen, L. M. (2011). Geographic region of residence and blood lead levels in US children: Results of the National Health and Nutrition Examination Survey. Int. Arch. Occup. Environ. Health 84, 513-522.
76. Sesack, S. R., and Grace, A. A. (2010). Cortico-Basal Ganglia reward network: Microcircuitry. Neuropsychopharmacology 35, 27-47.
77. Shaw, P., Lalonde, F., Lepage, C., Rabin, C., Eckstrand, K., Sharp, W., Greenstein, D., Evans, A., Giedd, J. N., and Rapoport, J. (2009). Development of cortical asymmetry in typically developing children and its disruption in attention-deficit/hyperactivity disorder. Arch. Gen. Psychiatry 66, 888-896.
78. Sherman, G. F., Garbanati, J. A., Rosen, G. D., Hofmann, M., Yutzey, D. A., and Denenberg, V. H. (1983). Lateralization of spatial preference in the female rat. Life Sci. 33, 189-193.
79. Sherman, G. F., Garbanati, J. A., Rosen, G. D., Yutzey, D. A., and Denenberg, V. H. (1980). Brain and behavioral asymmetries for spatial preference in rats. Brain Res. 192, 61-67.
80. Shinohara, Y., Hosoya, A., Yamasaki, N., Ahmed, H., Hattori, S., Eguchi, M., Yamaguchi, S., Miyakawa, T., Hirase, H., and Shigemoto, R. (2012). Righthemispheric dominance of spatial memory in split-brain mice. Hippocampus 22, 117-121.
81. Simpson, J., and Kelly, J. P. (2011). The impact of environmental enrichment in laboratory rats-behavioural and neurochemical aspects. Behav. Brain Res. 222, 246-264.
82. Simpson, J., and Kelly, J. P. (2012). An investigation of whether there are sex differences in certain behavioural and neurochemical parameters in the rat. Behav. Brain Res. 229, 289-300.
83. Sullivan, R. M. (2004). Hemispheric asymmetry in stress processing in rat prefrontal cortex and the role of mesocortical dopamine. Stress 7, 131-143.
84. Sullivan, R. M., Chehab, S. L., Dufresne, M. M., and Laplante, F. (2012). Role of sex in the neurochemical and neuroendocrine correlates of paw preference in the rat. Neuroscience 202, 192-201.
85. Sullivan, R. M., and Dufresne, M. M. (2006). Mesocortical dopamine and HPA axis regulation: Role of laterality and early environment. Brain Res. 1076, 49-59.
86. Sullivan, R. M., Dufresne, M. M., and Waldron, J. (2009). Lateralized sex differences in stress-induced dopamine release in the rat. Neuroreport 20, 229-232.
87. Sun, L., Zhao, Z. Y., Hu, J., and Zhou, X. L. (2005). Potential association of lead exposure during early development of mice with alteration of hippocampus nitric oxide levels and learning memory. Biomed. Environ. Sci. 18, 375-378.
88. Tecchio, F., Zappasodi, F., Tombini, M., Caulo, M., Vernieri, F., and Rossini, P. M. (2007). Interhemispheric asymmetry of primary hand representation and recovery after stroke: A MEG study. Neuroimage 36, 1057-1064.
89. Tian, L., Wang, J., Yan, C., and He, Y. (2011). Hemisphere- and gender-related differences in small-world brain networks: A resting-state functional MRI study. Neuroimage 54, 191-202.
90. Toga, A. W., and Thompson, P. M. (2003). Mapping brain asymmetry. Nat. Rev. Neurosci. 4, 37-48.
91. Trojniar, W., and Klejbor, I. (1999). Facilitatory effect of unilateral lesion of the ventral tegmental area on locomotor response to stimulation of the contralateral ventral tegmental area: Involvement of GABAergic transmission. Brain Res. 842, 419-430.
92. Vallortigara, G. and Rogers, L. J. (2005). Survival with an asymmetrical brain: advantages and disadvantages. Behav. Brain Sci. 28, 575-589.
93. Virgolini, M. B., Rossi-George, A., Lisek, R., Weston, D. D., Thiruchelvam, M., and Cory-Slechta, D. A. (2008a). CNS effects of developmental Pb exposure are enhanced by combined maternal and offspring stress. Neurotoxicology 29, 812-827.
94. Virgolini, M. B., Rossi-George, A., Weston, D., and Cory-Slechta, D. A. (2008b). Influence of low level maternal Pb exposure and prenatal stress on offspring stress challenge responsivity. Neurotoxicology 29, 928-939.
95. Vogel, J. J., Bowers, C. A., and Vogel, D. S. (2003). Cerebral lateralization of spatial abilities: A meta-analysis. Brain Cogn. 52, 197-204.
96. Ward, I. L., and Weisz, J. (1984). Differential effects of maternal stress on circulating levels of corticosterone, progesterone, and testosterone in male and female rat fetuses and their mothers. Endocrinology 114, 1635-1644.
97. Wisniewski, A. B. (1998). Sexually-dimorphic patterns of cortical asymmetry, and the role for sex steroid hormones in determining cortical patterns of lateralization. Psychoneuroendocrinology 23, 519-547.
98. Yang, J., Hou, C., Ma, N., Liu, J., Zhang, Y., Zhou, J., Xu, L., and Li, L. (2007). Enriched environment treatment restores impaired hippocampal synaptic plasticity and cognitive deficits induced by prenatal chronic stress. Neurobiol. Learn. Mem. 87, 257-263.
99. Yi, S. J., Masters, J. N., and Baram, T. Z. (1994). Glucocorticoid receptor mRNA ontogeny in the fetal and postnatal rat forebrain. Mol. Cell. Neurosci. 5, 385-393.
100. Zimmerberg, B., and Reuter, J. M. (1989). Sexually dimorphic behavioral and brain asymmetries in neonatal rats: Effects of prenatal alcohol exposure. Brain Res. Dev. Brain Res. 46, 281-290.