Effects of Exogenous Agents on Brain Development: Stress, Abuse and Therapeutic Compounds

CNS Neuroscience and Therapeutics

Volumn 17, Issue 5, 2011, Pages 470-489

  Archer, Trevor ^a  

^a UNIVERSITY OF GOTHENBURG   (Sweden)

Author keywords

Abnormality; Agent; Alcohol; Anesthetics; Anxiolytics; Exogenous; Infection; Neurodevelopment; Nicotine; Stress

Indexed keywords

4 AMINOBUTYRIC ACID A RECEPTOR; 4,4' ISOPROPYLIDENEDIPHENOL; ALCOHOL; ANESTHETIC AGENT; ANTICONVULSIVE AGENT; ANXIOLYTIC AGENT; BARBITURIC ACID DERIVATIVE; BENZODIAZEPINE DERIVATIVE; BRAIN DERIVED NEUROTROPHIC FACTOR; DEXAMETHASONE; DEXAMPHETAMINE; DIAZEPAM; DIZOCILPINE; DOPAMINE; ENDOCRINE DISRUPTOR; GLUTAMIC ACID; KETAMINE; METHAMPHETAMINE; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; NICOTINE; NITROUS OXIDE; PHENCYCLIDINE; PHENOBARBITAL; PROPOFOL; SCATTER FACTOR; SCATTER FACTOR RECEPTOR; SEDATIVE AGENT; SEVOFLURANE; TOBACCO SMOKE; UNINDEXED DRUG;

ADULTHOOD; APOPTOSIS; ATTENTION DEFICIT DISORDER; AUTISM; BACTERIAL INFECTION; BEHAVIOR DISORDER; BRAIN DEVELOPMENT; BRAIN DYSFUNCTION; BRAIN GROWTH; DRUG ABUSE; DRUG MECHANISM; FETAL ALCOHOL SYNDROME; GABAERGIC SYSTEM; GENOTYPE ENVIRONMENT INTERACTION; HUMAN; MATERNAL SMOKING; MATERNAL STRESS; MENTAL STRESS; NERVE DEGENERATION; NEUROTOXICITY; NONHUMAN; OXIDATIVE STRESS; PATHOGENESIS; PROTEIN EXPRESSION; PSYCHOPATHY; REVIEW; SCHIZOPHRENIA; VIRUS INFECTION;

ANESTHETICS; ANIMALS; ANTI-ANXIETY AGENTS; BRAIN; HUMANS; MENTAL DISORDERS; OXIDATIVE STRESS; PHARMACEUTICAL PREPARATIONS; STRESS, PSYCHOLOGICAL; SUBSTANCE-RELATED DISORDERS; TREATMENT OUTCOME;

EID: 80053208443     PISSN: 17555930     EISSN: 17555949     Source Type: Journal    
DOI: 10.1111/j.1755-5949.2010.00171.x     Document Type: Review

References (300)

1. Bayer SA, Altman J, Russo RJ, Zhang X. Timetables of neurogenesis in the human brain based on experimentally determined patterns in the rat. Neurotoxicology 1993;14:83-144.
2. Herschkowitz N, Kagan J, Zilles K. Neurobiological bases of behavioural development in the first year. Neuropediatrics 1997;28:296-306.
3. Martí J, Santa-Cruz MC, Bayer SA, Ghetti B, Hervás JP. Generation and survival of midbrain dopaminergic neurons in weaver mice. Int J Dev Neurosci 2007;25:299-307.
4. Chen WJ, Parnell SE, West JR. Effects of alcohol and nicotine on developing olfactory bulb: Loss of mitral cells and alterations in neurotransmitter levels. Alcohol Clin Exp Res 1999;23:18-25.
5. Eriksson P, Ankarberg E, Fredriksson A. Exposure to nicotine during a defined period in neonatal life induces permanent changes in brain nicotine receptors and in behavior of adult mice. Brain Res 2000;853:41-48.
6. Fredriksson A, Eriksson P, Ankarberg E, Palomo T, Archer T. Neonatal nicotine administration influences ethanol-induced behaviours. Alcohol 2000;21:107-115.
7. Fredriksson A, Schröder N, Eriksson P, Izquierdo I, Archer T. Neonatal iron potentiates adult MPTP-induced neurodegenerative and functional deficits. Parkinsonism Relat Disord 2001;7:97-105.
8. Stanwood GD, Levitt P. Drug exposure early in life: Functional repercussions of changing neuropharmacology during sensitive periods of brain development. Curr Opin Neuropharmacol 2004;4:65-71.
9. Connors SL, Levitt P, Matthews SG, et al. Fetal mechanisms in neurodevelopmental disorers. Pediatr Neurol 2008;38:163-176.
10. Costa LG, Aschner M, Vitalone A, Syversen T, Soldin OP. Developmental neuropathology of environmental agents. Ann Rev Pharmacol Toxicol 2004;44:87-110.
11. Bouchard M, Laforest F, Vandelac L, Bellinger D, Mergler D. Hair manganese and hyperactive behaviours: Pilot study of school age children exposed through tap water. Environ Health Perspect 2007;115:122-127.
12. Rodier PM. Environment causes of central nervous system maldevelopment. Pediatrics 2004;113:1076-1083.
13. Wasserman GA, Liu X, Parvez F, et al. Water manganese exposure and children's intellectual function in Araihazar, Banbladesh. Environ Health Perspect 2006;114:124-129.
14. Bada HS, Das A, Bauer CR, et al. Impact of prenatal cocaine exposure on child behaviour problems through school age. Pediatrics 2007;119:348-359.
15. Harvey JA. Cocaine effects on the developing brain: Current status. Neurosci Biobehav Rev 2004;27:751-764.
16. Linares TJ, Singer LT, Kirchner HL, Short EJ, Min MO, Hussey P, Minnes S. Mental health outcomes of cocaine-exposed children at 6 years of age. J Pediatr Psychol 2006;31:85-97.
17. Malanga CJ, Kosofsky BE. Does drug abuse beget drug abuse? Behavioral analysis of addiction liability in animal models of prenatal drug exposure. Brain Res Dev Brain Res 2003;147:47-57.
18. Malanga CJ, Riday TT, Carlezon WA, Kosofsky BE. Prenatal exposure to cocaine increases the rewarding potency of cocaine and selective dopaminergic agonists in adult mice. Biol Psychiatr 2008;63:214-221.
19. Mayes LC. A behavioural teratogenic model of the impact of prenatal cocaine exposure on arousal regulatory systems. Neurotoxicol Teratol 2002;24:385-395.
20. Mayes LC, Cicchetti D, Acharyya S, Zhang H. Developmental trajectories of cocaine-and-other-drug-exposed and non-cocaine-exposed children. J Dev Behav Pediatr 2003;24:323-335.
21. Singer LT, Minnes S, Short E, et al. Cognitive outcomes of preschool children with prenatal cocaine exposure. JAMA 2004;291:2448-2456.
22. Singer LT, Nelson S, Short E, Min MO, Lewis B, Russ S, Minnes S. Prenatal cocaine exposure: Drug and environmental effects at 9 years. J Pediatr 2008;153:105-111.
23. 1 receptor activity and subcellular distribution. J Neurosci 2007;27:152-157.
24. Dobbing J, Sands J. The brain growth spurt in various mammalian species. Early Hum Dev 1979;3:79-84.
25. Giedd JN. The teen brain: Insights from neuroimaging. J Adolesc Health 2008;42:335-343.
26. Byrnes ML, Reynolds JN, Brien JF. Effect of prenatal alcohol exposure during the brain growth spurt of the guinea pig. Neurotoxicol Teratol 2001;23:355-364.
27. Ikonomidou C. Triggers of apoptosis in the immature brain. Brain Dev 2009;31:488-492.
28. Committee on Substance Abuse and Committee on Children with Disabilities. Fetal alcohol syndrome and alcohol-related neurodevelopmental disorders. Pediatrics 2000;106:358-361.
29. Ishimaru MJ, Ikonomidou C, Tenkova TI, Der TC, Dikranian K, Sesma MA, Olney JW. Distinguishing exitotoxic from apoptotic neurodegeneration in the developing brain. J Comp Neurol 1999;408:461-476.
30. Lockshin RA, Zakeri Z. Cell death during development. J Immunol Methods 2002;265:3-20.
31. Penaloza C, Lin L, Lockshin RA, Zakeri Z. Cell death in development: Shaping the embryo. Review. Histochem Cell Biol 2006;126:149-158.
32. Penaloza C, Orlanski S, Ye Y, Entezari-Zaher T, Javdan M, Zakeri Z. Cell death in mammalian development. Curr Pharm Des 2008;14:184-196.
33. Twomey C, McCarthy JV. Pathways of apoptosis and importance in development. J Cell Mol Med 2005;9:345-359.
34. Agnello M, Roccheri MC. Apoptosis: Focus on sea urchin development. Apoptosis 2010;15:322-330.
35. Hengartner MO. The biochemistry of apoptosis. Nature 2000;407:770-776.
36. Kerr JF, Wyllie AH, Currie AR. Apoptosis: A basic biological phenomenon with wide-ranging implications in tissue kinetics. Br J Cancer 1972;26:239-257.
37. Olney JW. New insights and new issues in developmental neurotoxicology. Neurotoxicology 2002;23:659-668.
38. Bittigau P, Genz K, Engelbrechten S, Hoerster F, Dikranian K, Olney JW, Ikonomidou C. Antiepileptics which enhance GABAergic inhibition cause neuronal apoptosis in the developing CNS. Soc Neurosci Abstr 1999;26:323.
39. Bittigau P, Sifringer M, Pohl D, et al. Apoptotic neurodegeneration following trauma is markedly enhanced in the immature brain. Ann Neurol 2000;45:724-735.
40. Bittigau P, Sifringer M, Genz K, et al. Antiepileptics drugs and apoptotic neurodegeneration in the developing brain. Proc Nat Acad Sci 2002;99:15089-15094.
41. Edwards AD, Azzopardi DV. Perinatal hypoxia-ischemia and brain injury. Pediatr Res 2000;47:431-432.
42. Olney JW. Excitotoxicity, apoptosis and neuropsychiatric disorders. Curr Opin Pharmacol 2003;3:101-109.
43. Olney JW, Farber NB, Wozniak DF, Jevtovic-Todorovic V, Ikonomidou C. Environmental agents that have the potential to trigger massive apoptotic neurodegeneration in the developing brain. Environ Health Perspect 2000;108(Suppl. 3):383-388.
44. Jevtovic-Todorovic V, Olney JW. PRO: Anesthesia-induced developmental neuroapoptosis: Status of the evidence. Anesthesia Analgesis 2008;106:1659-1663.
45. Jevtovic-Todorovic V, Hartman RE, Izumi Y, et al. Early exposure to common anesthetic agents causes neurodegeneration in the developing rat brain and persistent learning deficits. J Neurosci 2003;23:876-882.
46. Lu LX, Yon JH, Carter LB, Jevtovic-Todorovic V. General anesthesia activates BDNF-dependent neuroapoptosis in the developing rat brain. Apoptosis 2006;11:1603-1615.
47. Young C, Jevtovic-Todorovic V, Qin YQ, Tenkova T, Wang H, Labruyere J, Olney JW. Potential of ketamine and midazolam, individually or in combination, to induce apoptotic neurodegeneration in the infant mouse brain. Br J Pharmacol 2005;146:189-197.
48. Frederick AL, Stanwood GD. Drugs, biogenic amine targets and the developing brain. Dev Neurosci 2009;31:7-22.
49. Ruediger T, Bolz J. Neurotransmitters and the development of neuronal circuits. Adv Exp Med Biol 2007;621:104-115.
50. Zimmer G, Garcez P, Rudolph J, Niehage R, Weth F, Lent R, Bolz J. Ephrin-A5 acts as a repulsive cue for migrating cortical interneurons. Eur J Heurosci 2008;28:62-73.
51. Hensch TK, Fagiolini M. Excitatory-inhibitory balance and critical period plasticity in developing visual cortex. Prog Brain Res 2005;147:115-124.
52. Johnston MV, Ishida A, Ishida WN, Matsushita HB, Nishimura A, Tsuji M. Plasticity and injury in the developing brain. Brain Dev 2009;31:1-10.
53. Ibi D, Nagai T, Kitahara Y, et al. Neonatal polyI:C treatment in mice results in schizophrenia-like behavioral and neurochemical abnormalities in adulthood. Neurosci Res 2009;64:297-305.
54. Meyer U, Feldon J. Neural basis of psychosis-related behaviour in the infection model of schizophrenia. Behav Brain Res 2009;204:322-334.
55. Sanderson JL, Donald Partridge J, Valenzuela CE. Modulation of GABAergic and glutamatergic transmission by ethanol in the developing neocortex: An intro test of the excessive inhibition hypothesis of fetal alcohol spectrum disorder. Neuropharmacology 2009;56:541-555.
56. Teng KK, Hempstead BL. Neurotrophins and their receptors: Signaling trios in complex biological systems. Cell Mol Life Sci 2004;61:35-48.
57. Vicario-Abejon C, Owens D, McKay R, Segal M. Role of neurotrophins in central synapse formation and stabilization. Nat Rev Neurosci 2002;3:965-974.
58. Zweifel LS, Kuruvilla R, Ginty DD. Functions and mechanisms of retrograde neurotrophin signaling. Nat Rev Neurosci 2005;6:615-625.
59. Singh B, Henneberger C, Betances D, Arevalo MA, Rodrigurz-Tebar A, Meier JC, Grantyn R. Altered balance of glutamatergic/GABAergic synaptic input and associated changes in dendrite morphology after BDNF expression in BDNF-deficient hippocampal neurons. J Neurosci 2006;26:7189-7200.
60. Manthey D, Asimiadou S, Stefovska V, Kaindl AM, Fassbender J, Ikonomidou C, Bittigau P. Sulthiame but not levetiracetam exerts neurotoxic effect in the developing rat brain. Exp Neurol 2005;193:497-503.
61. Bittigau P, Sifringer M, Ikonomidou C. Antiepileptic drugs and apoptosis in the developing brain. Ann N Y Acad Sci 2003;993:103-114.
62. Kaindl AM, Koppelstaetter A, Nebrich G, et al. Brief alteration of NMDA or GABAA receptor-mediated neurotransmission has long term effects on the developing cerebral cortex. Mol Cell Proteomics 2008;7:2293-2310.
63. Bercker S, Bert B, Bittigau P, et al. Neurodegeneration in newborn rats following propofol and sevoflurane anesthesia. Neurotox Res 2009;16:140-147.
64. Asimiadou S, Bittigau P, Felderhoff-Mueser U, et al. Protection with estradiol in developmental models of apoptotic neurodegeneration. Ann Neurol 2005;58:266-276.
65. Hansen HH, Briem T, Dzietko M, et al. Mechanisms leading to disseminated apoptosis following NMDA receptor blockade in the developing rat brain. Neurobiol Dis 2004;16:440-453.
66. Olney JW, Young C, Wozniak DF, Ikonomidou C, Jevtovic-Todorovic V. Anesthesia-induced developmental neuroapoptosis. Does it happen in humans? Anesthesiology 2004;101:273-275.
67. Li Y, Liang G, Wang S, Meng Q, Wang Q, Wei H. Effects of fetal exposure to isoflurane on postnatal memory and learning in rats. Neuropharmacology 2007;53:942-950.
68. Sanders RD, Xu J, Shu Y, Fidalgo A, Ma D, Maze M. General anesthetics induce apoptotic neurodegeneration in the neonatal rat spinal cord. Anesth Analg 2008;106:1708-1711.
69. Zou X, Sadovova N, Patterson TA, et al. The effects of L-carnitine on the combination of, inhalation anesthetic-induced developmental, neuronal apoptosis in the rat frontal cortex. Neuroscience 2008;151:1053-1065.
70. Stratmann G, Sall JW, May LD, et al. Isoflurane differentially affects neurogenesis and long-term neurocognitive function in 60-day-old and 7-day-old rats. Anesthesiology 2009;110:834-848.
71. Schmued LC, Hopkins KJ. Flouro-Jade B: A high affinity fluorescent marker for the localization of neuronal degeneration. Brain Res 2000a;874:123-130.
72. Schmued LC, Hopkins KJ. Fluoro-Jade: Novel fluorochromes for detecting toxicant-induced neuronal degeneration. Toxicol Pathol 2000b;28:91-99.
73. De Roo M, Klauser P, Briner A, et al. Anesthetics rapidly promote synaptogenesis during a critical period of brain development. PLoS One 2009;4:7043.
74. Ba YC, Dai P, Zhou HL, Liu J, Wang TH. Spatiotemporal Changes of NGF, BDNF and NT-3 in the Developing Spinal Cords of Embryonic Chicken. Neurochem Res 2010;35:273-278.
75. Cao D, Kevala K, Kim J, Moon HS, Jun SB, Lovinger D, Kim HY. Docosahexaenoic acid promotes hippocampal neuronal development and synaptic function. J Neurochem 2009;111:510-521.
76. Desfeux A, El Ghazi F, Jégou S, Legros H, Marret S, Laudenbach V, Gonzalez BJ. Dual Effect of Glutamate on GABAergic Interneuron Survival during Cerebral Cortex Development in Mice Neonates. Cereb Cortex 2010;20:1092-1108.
77. Raol YH, Lynch DR, Brooks-Kayal AR. Role of excitatory amino acids in developmental epilepsies. Ment Retard Dev Disabil Res Rev 2001;7:254-260.
78. Sallert M, Rantamäki T, Vesikansa A, et al. Brain-derived neurotrophic factor controls activity-dependent maturation of CA1 synapses by downregulating tonic activation of presynaptic kainate receptors. J Neurosci 2009;29:11294-11303.
79. Noctor SC, Martínez-Cerdeño V, Kriegstein AR. Contribution of intermediate progenitor cells to cortical histogenesis. Arch. Neurol 2007;64:639-642.
80. Seaberg RM, Van Der Kooy D. Stem and progenitor cells: The premature desertion of rigorous definitions. Trends in Neurosciences 2003;26:125-131.
81. Sun W, Salvi RJ. Brain derived neurotrophic factor and neurotrophic factor 3 modulate neurotransmitter receptor expressions on developing spiral ganglion neurons. Neuroscience 2009;164:1854-1866.
82. Pohl D, Bittigau P, Ishimaru MJ, Stadthaus D, Hubner C. N-methyl-D-aspartate antagonists and apoptotic cell death triggered by head trauma in developing rat brain. Proc Natl Acad Sci USA 1999;96:2508-2513.
83. DeSilva TM, Kabakov AY, Goldhoff PE, Volpe JJ, Rosenberg PA. Regulation of glutamate transport in developing rat oligodendrocytes. J Neurosci 2009;29:7898-908.
84. Olney JW, Labruyere J, Wang G, Wozniak DF, Price MT, Sesma MA. NMDA antagonist neurotoxicity: Mechanism and prevention. Science 1991;254:1515-1518.
85. Olney JW, Wozniak DF, Jevtovic-Todorovic V, Ikonomidou C. Glutamate signaling and the fetal alcohol syndrome. Ment Retard Dev Disabil Res Rev 2001;7:267-275.
86. Nakatani-Pawlak A, Yamaguchi K, Tatsumi Y, Mizoguchi H, Yoneda Y. Neonatal phencyclidine treatment in mice induces behavioral, histological and neurochemical abnormalities in adulthood. Biol Pharm Bull 2009;32:1576-1583.
87. Takahashi M, Negishi T, Imamura M, Sawano E, Kuroda Y, Yoshikawa Y, Tashiro T. Alterations in gene expression of glutamate receptors and exocytosis-related factors by a hydroxylated-polychlorinated biphenyl in the developing rat brain. Toxicology 2009;257:17-24.
88. Ikonomidou C, Bosch F, Miksa M, et al. Blockade of NMDA receptors and apoptotic neurodegeneration in the developing brain. Science 1999;283:70-74.
89. Ikonomidou C, Bittigau P, Ishimaru MJ, et al. Ethanol-induced apoptotic neurodegeneration and fetal alcohol syndrome. Science 2000;287:1056-1060.
90. Fredriksson A, Archer T, Alm H, Gordh T, Eriksson P. Neurofunctional deficits and potentiated apoptosis by neonatal NMDA antagonist administration. Behav Brain Res 2004;153:367-376.
91. Fredriksson A, Dahlgren L, Danielsson B, Eriksson P, Dencker L, Archer T. Behavioural effects of neonatal metallic mercury exposure in rats. Toxicology 1992;74:151-160.
92. Fredriksson A, Archer T. Neurobehavioural deficits associated with apoptotic neurodegeneration and vulnerability for ADHD. Neurotoxicity Res 2004;6:435-456.
93. du Bois TM, Huang XF. Early brain development disruption from NMDA receptor hypofunction: Relevance to schizophrenia. Brain Res Rev 2007;53:260-270.
94. Teneti L, Lipton SA. Involvment of activated caspase-3-like proteases in N-methyl-D-aspartate-induced apoptosis in cerebrocortical neurons. J Neurochem 2000;74:134-142.
95. Thomas JD, Fleming SL, Riley EP. Administration of low doses of MK-801 during ethanol withdrawal in the developing rat pup attenuates alcohol's teratogenic effects. Alcohol Clin Exp Res 2002;26:1307-1313.
96. Abekawa T, Ito K, Nakagawa S, Koyama T. Prenatal exposure to an NMDA receptor antagonist, MK-801 reduces density of parvalbumin-immunoreactive GABAergic neurons in the medial prefrontal cortex and enhances phencyclidine-induced hyperlocomotion but not behavioral sensitization to methamphetamine in postpubertal rats. Psychopharmacology 2007;192:303-316.
97. Fredriksson A, Archer T. Hyperactivity following postnatal NMDA antagonist treatment: Reversal by D-amphetamine. Neurotox Res 2003;5:549-564.
98. Jensen V, Rinholm JE, Johansen TJ, et al. N-methyl-D-aspartate receptor subunit dysfunction at hippocampal glutamatergic synapses in an animal model of attention-deficit/hyperactivity disorder. Neuroscience 2009;158:353-364.
99. Carrey NJ, MacMaster FP, Gaudet L, Schmidt MH. Striatal creatine and glutamate/glutamine in attention-deficit/hyperactivity disorder. J Child Adolesc Psychopharmacol 2007;17:11-17.
100. Perlov E, Philipsen A, Hesslinger B, et al. Reduced cingulate glutamate/glutamine-to-creatine ratios in adult patients with attention deficit/hyperactivity disorder-a magnet resonance spectroscopy study. J Psychiatr Res 2007;41:934-941.
101. Lindahl JS, Kjellsen BR, Tigert J, Miskimins R. In utero PCP exposure alters oligodendrocyte differentiation and myelination in developing rat frontal cortex. Brain Res 2008;1234:137-147.
102. D'Hulst C, Kooy RF. Fragile X syndrome: From molecular genetics to therapy. J Med Genet 2009;46:577-584.
103. Elia J, Gai X, Xie HM, et al. Rare structural variants found in attention-deficit hyperactivity disorder are preferentially associated with neurodevelopmental genes. Mol Psychiatry 2009;PMID:19546859.
104. Hagerman RJ, Berry-Kravis E, Kaufmann WE, et al. Advances in the treatment of fragile X syndrome. Pediatrics 2009;123:378-390.
105. Mick E, Neale B, Middleton FA, McGough JJ, Faraone SV. Genome-wide association study of response to methylphenidate in 187 children with attention-deficit/hyperactivity disorder. Am J Med Genet B Neuropsychiatr Genet 2008;147B:1412-1418.
106. Goodlett CR, Horn KH, Zhou FC. Alcohol teratogenesis: Mechanisms of damage and strategies for intervention. Exp Biol Med 2005;230:394-406.
107. Jang MH, Shin MC, Jung SB, et al. Alcohol and nicotine reduce cell proliferation and enhance apoptosis in the dentate gyrus. NeuroReport 2002;13:1509-1513.
108. Roy TS, Andrews JE, Seidler FJ, Slotkin TA. Nicotine evokes cell death in embryonic rat brain during neurulation. J Pharmacol Exp Ther 1998;287:1136-1144.
109. Berger F, Gage FH, Vijayaraghaven S. Nicotinic receptor-induced apoptotic cell death of hippocampal progenitor cells. J Neurosci 1998;18:6871-6881.
110. Klintsova AY, Helfer JL, Calizo LH, Dong WK, Goodlett CR, Greenough WT. Persistent impairment of hippocampal neurogenesis in young adult rats following early postnatal alcohol exposure. Alcohol Clin Exp Res 2007;31:2073-2082.
111. Milotova M, Riljak V, Jandova K, Bortelova J, Maresova D, Pokorny L, Landmeier M. Changes of hippocampal neurons after perinatal exposure to ethanol. Physiol Res 2008;57:275-282.
112. Crews FT, Nixon K. Mechanisms of neurodegeneration and regeneration in alcoholism. Alcohol Alcohol 2009;44:115-127.
113. Spear LP. The adolescent brain and age-related behavioural manifestations. Neurosci Biobehav Rev 2000;24:417-463.
114. Tizabi Y, Al-Namaeh M, Manaye KF, Taylor RE. Protective effects of nicotine on ethanol-induced toxicity in cultured cerebellar granule cells. Neurotoxicity Res 2003;5:315-321.
115. Abreu-Villaca Y, Seidler FJ, Tate CA, Slotkin TA. Nicotine is a neurotoxin in the adolescent brain: Critical periods, patterns of exposure, regional selectivity, and dose thresholds for macromolecular alterations. Brain Res 2003;979:114-128.
116. Adriani W, Granstrom O, Macri S, Izykenova G, Dambinova S, Laviola G. Behavioural and neurochemical vulnerability during adolescence in mice: Studies with nicotine. Neuropsychopharmacology 2004;29:869-878.
117. Xu Z, Seidler FJ, Tate CA, Garcia SJ, Slikker W, Slotkin TA. Sex-selective hippocampal alterations after adolescent nicotine administration: Effects on neurospecific proteins. Nicotin Tob Res 2003;5:955-960.
118. Crews FT, Braun CJ, Hoplight B, Switzer RC, Knapp DJ. Binge ethanol consumption causes differential brain damage in young adolescent rats compared with adult rats. Alcohol Clin Exp Res 2000;24:1712-1723.
119. Crews FT, Mdzinarishvili A, Kim D, He J, Nixon K. Neurogenesis in adolescent brain is potently inhibited by ethanol. Neuroscience 2006;137:437-445.
120. Evrard SG, Duhalde-Veja M, Tagliaferro P, Mirochnic S, Caltana LR, Brusco A. A low chronic ethanol exposure induces morphological changes in the adolescent rat brain that are not fully recovered even after a long abstinence: An immunohistochemical study. Exp Neurol 2006;200:438-459.
121. Pascual M, Blanco AM, Cauli O, Minarro J, Guerri C. Intermittent ethanol exposure induces inflammatory brain damage and causes long-term behavioural alterations in adolecent rats. Eur J Neurosci 2007;25:541-550.
122. Abreu-Villaca Y, Medeiros AH, Lima CS, Faria FP, Filgueiras CC, Manhaes AC. Combined exposure to nicotine and ethanol in adolescent mice differentially affects memory and learning during exposure and withdrawal. Behav Brain Res 2007;181:136-146.
123. Abreu-Villaca Y, Nunes F, Queiroz-Gomes FE, Manhaes AC, Filgueiras CC. Combined exposure to nicotine and ethanol in adolescent mice differentially affects anxiety levels during exposure, short term and long term withdrawal. Neuropsychopharmacology 2008;33:599-610.
124. Chen WJ, Harle LK. Interactive effect of alcohol and nicotine on developing cerebellum: An investigation of the temporal pattern of alcohol and nicotine administration. Alcohol Clin Exp Res 2005;29:437-442.
125. Gilbertson RJ, Barron S. Neonatal ethanol and nicotine exposure causes locomotor activity changes in preweanling animals. Pharmacol Biochem Behav 2005;81:54-64.
126. Larsson A, Engel JA. Neurochemical and behavioural studies on ethanol and nicotine interactions. Neurosci Biobehav Rev 2004;27:713-720.
127. Meyerhoff DJ, Tizabi Y, Staley JK, Durazzo TC, Glass JM, Nixon SJ. Smoking comorbidity in alcoholism: Neurobiological and neurocognitive consequences. Alcohol Clin Exp Res 2006;30:253-264.
128. Ribeiro-Carvelho A, Lima CS, Filgueiras CC, Manhaes A, Abreu-Villaca Y. Nicotine and ethanol interact during adolescence: Effects on central cholinergic systems. Brain Res 2008;1232:48-60.
129. Oliveira-da-Silva A, Vieira FB, Cristina-Rodrigues F, Filgueiras CC, Manhaes A, Abreu-Villaca Y. Increased apoptosis and reduced neuronal and glial densities in the hippocampus due to nicotine and ethanol exposure in adolescent mice. Int J Devel Neurosci 2009;27:539-548.
130. Hughes JR. Craving among long-abstinent smokers: An Internet survey. Nicotine Tob Res 2010;12:459-462.
131. Piper ME, Smith SS, Schlam TR, Fiore MC, Jorenby DE, Fraser D, Baker TB. A randomized placebo-controlled clinical trial of 5 smoking cessation pharmacotherapies. Arch Gen Psychiatry 2009;66:1253-1262.
132. Hutchinson J, Pickett KE, Green J, Wakschlag LS. Smoking in pregnancy and disruptive behavior in 3-year old boys and girls: An analysis of the UK Millenium cohort study. J Epidemiol Community Health 2010;64:82-88.
133. Kum-Nji P, Meloy L, Herrod HG. Envirnmental tobacco smoke exposure: Prevalence and mechanisms of causation of infections in children. Pediatrics 2006;117:1745-1754.
134. Reeves S, Bernstein I. Effects of maternal tobacco-smoke exposure on fetal growth and neonatal size. Expert Rev Obstet Gynecol 2009;3:719-730.
135. Rogers JM. Tobacco and pregnancy: Overview of exposures and effects. Birth Defects Res C Embryol Today 2008;84:1-15.
136. Slotkin TA. If nicotine is a developmental neurotoxicant in animal studies, dare we recommend nicotine replacement therapy in pregnant women and adolescents? Neurotoxicol Teratol 2008;30:1-19.
137. Sasaki S, Kishi R. Adverse birth outcomes of maternal smoking during pregnancy and genetic polymorphisms: Exploiting gene-environment interaction. Nippon Eiseigaku Zasshi 2009;64:759-764.
138. Wu LT, Anthony JC. Tobacco smoking and depressed mood in late childhood and early adolescence. Am J Public Health 1999;89:1837-1840.
139. Onal A, Uysal A, Ulker S, Delen Y, Yurtseven ME, Evinc A. Alterations of brain tissue in fetal rats exposed to nicotine in utero: Possible involvement of nitric oxide and catecholamines. Neurotoxicol Teratol 2004;26:103-112.
140. Slotkin TA. Cholinergic systems in brain development and disruption by neurotoxicants: Nicotine, environmental tobacco smoke, organophosphates. Toxicol Appl Pharmacol 2004;198:132-151.
141. Slotkin TA, Orband-Miller L, Queen KL, Whitmore WL, Seidler FJ. Effects of prenatal nicotine exposure on biochemical development of the rat brain regions: Maternal drug infusions via osmotic minipumps. J Pharmacol Exp Ther 1987;240:602-611.
142. Slotkin TA. Fetal nicotine or cocaine exposure: Which one is worse? J Pharmacol Exp Ther 1998;285:931-945.
143. Shea AK, Steiner M. Cigarette smoking during pregnancy. Nicotine Tob Res 2008;10:267-278.
144. Wickström R. Effects of nicotine during pregnancy: Human and experimental evidence. Curr Neuropharmacol 2007;5:213-222.
145. Jacobsen LK, Picciotto MR, Heath CJ, et al. Prenatal and adolescent exposure to tobacco smoke modulates the development of white matter microstructure. J Neurosci 2007;27:13491-13498.
146. Slotkin TA, MacKillop EA, Rudder CL, Ryde IT, Tate CA, Seidler FJ. Permanent, sex-selective effects of prenatal or adolescent nicotine exposure, separately or sequentially, in rat brain regions: Indices of cholinergic and serotonergic synaptic function, cell signaling, and neural cell number and size at 6 months of age. Neuropsychopharmacology 2007;32:1082-1097.
147. Pahl K, Brook DW, Morojele NK, Brook JS. Nicotine dependence and problem behaviors among urban South African adolescents. J Behav Med 2010;33:101-109.
148. Rose JS, Dierker LC, Donny E. Nicotine dependence symptoms among recent onset adolescent smokers. Drug Alcohol Depend 2010;106:126-132.
149. Thomas JD, Garrison ME, Slawecki CJ, Ehlers CL, Riley EP. Nicotine exposure during the neonatal brain growth spurt produces hyperactivity in preweanling rats. Neurotoxicol Teratol 2000;22:695-701.
150. Dwyer JB, McQuown SC, Leslie FM. The dynamic effects of nicotine on the developing brain. Pharmacol Ther 2009;122:125-139.
151. Abreu-Villaça Y, Seidler FJ, Slotkin TA. Does prenatal nicotine exposure sensitize the brain to nicotine-induced neurotoxicity in adolescence? Neuropsychopharmacology 2004;29:1440-1450.
152. Ernst M, Moolchan ET, Robinson ML. Behavioral and neural consequences of prenatal exposure to nicotine. J Am Acad Child Adolesc Psychiatry 2001;40:630-641.
153. Trask CL, Kosofsky BE. Developmental considerations of neurotoxic exposures. Neurol Clin 2000;18:541-562.
154. Parnell SE, O'Leary-Moore SK, Godin EA, et al. Magnetic resonance microscopy defines ethanol-induced brain abnormalities in prenatal mice: Effects of acute insult on gestational day 8. Alcohol Clin Exp Res 2009;33:1001-1011.
155. Riley EP, McGee CL. Fetal alcohol spectrum disorders: An overview with emphasis on changes in brain and behavior. Exp Biol Med 2005;230:357-365.
156. Abel EL, Berman RF. Long-term behavioral effects of prenatal alcohol exposure in rats. Neurotoxicol Teratol 1994;16:467-470.
157. Clarren SK, Alvord EC, Sumi SM, Streissguth AP, Smith DW. Brain malformations related to prenatal exposure to ethanol. J Pediatr 1978;92:64-67.
158. Jones KL, Smith DW. The fetal alcohol syndrome. Teratology 1975;12:1-10.
159. Jones KL, Smith DW, Ulleland CN, Striessguth AP. Pattern of malformation in offspring of chronic alcoholic mothers. Lancet 1973;1:1267-1271.
160. Komatsu S, Sakata-Haga H, Sawada K, Hisano S, Fukui Y. Prenatal exposure to ethanol induces leptomeningeal heterotopia in the cerebral cortex of the rat fetus. Acta Neuropathol 2001;101:22-26.
161. Sakata-Haga H, Sawada K, Hisano S, Fukui Y. Abnormalities of cerebellar foliation in rats prenatally exposed to ethanol. Acta Neuropath 2001;102:36-40.
162. Sakata-Haga H, Sawada K, Hisano S, Fukui Y. Administration schedule for an ethanol-containing diet in pregnancy affects types of offspring brain malformations. Acta Neuropath 2002;104:305-312.
163. Sakata-Haga H, Sawada K, Ohta K, Cui C, Hisano S, Fukui Y. Adverse effects of maternal alcohol consumption on development of dorsal hippocampus in rat offspring. Acta Neuropath 2003;105:30-36.
164. Sakata-Haga H, Sawada K, Takamasa O, Fukui Y. Hydrocephalus following prenatal exposure to ethanol. Acta Neuropath 2004;108:393-398.
165. Sakata-Haga H, Dominguez HD, Sei H, Fukui Y, Riley EP, Thomas JD. Alterations in circadian rhythm phase shifting ability in rats following ethanol exposure during the third trimester brain growth spurt. Alcohol Clin Exp Res 2006;30:899-907.
166. Fukui Y, Sakata-Haga H. Intrauterine environment-genome interaction and children's development (1): Ethanol: A teratogen in developing brain. J Toxicol Sci 2009;34:SP273-SP278.
167. rd Edition. Seattle, WA University of Washington Publication Services 2004.
168. Astley SJ, Aylward EH, Olson HC, et al. Magnetic resonance imaging outcomes from a comprehensive magnetic resonance study of children with fetal alcohol spectrum disorders. Alcohol Clin Exp Res 2009a;33:1671-1689.
169. Astley SJ, Aylward EH, Olson HC, et al. Functional magnetic resonance imaging outcomes from a comprehensive magnetic resonance study of children with fetal alcohol spectrum disorders. J Neurodev Disorder 2009b;1:61-80.
170. Astley SJ, Olson HC, Kerns K, et al. Neuropsychological and behavioural outcomes from a comprehensive magnetic resonance study of children with fetal alcohol spectrum disorders. Can J Pharmacol 2009c; 16:e178-e201.
171. Bonthius DJ, West JR. Alcohol-induced neuronal loss in developing rats: Increased brain damage with binge exposure. Alcohol Clin Exp Res 1990;14:107-118.
172. Pierce DR, West JR. Differential deficits in regional brain growth induced by postnatal alcohol. Neurotoxicol Teratol 1987;9:129-141.
173. Zharkovsky T, Kaasik A, Jaako K, Zharkovsky A. Neurodegeneration and production of the new cells in the dentate gyrus of juvenile rat hippocampus after a single administration of ethanol. Brain Res 2003;978:115-123.
174. Abdelrahman A, Conn R. Eye abnormalities in fetal alcohol syndrome. Ulster Med J 2009;78:164-165.
175. Arzumanyan A, Anni H, Rubin R, Rubin E. Effects of Ethanol on Mouse Embryonic Stem Cells. Alcohol Clin Exp Res 2009;33:2172-2179.
176. Domellöf E, Rönnqvist L, Titran M, Esseily R, Fagard J. A typical functional lateralization in children with fetal alcohol syndrome. Dev Psychobiol 2009.
177. Famy C, Streissguthy AS, Unis AS. Mental illness in adults with fetal alcohol syndrome or fetal alcohol effects. Am J Psychiatr 1998;155:552-554.
178. Godin EA, O'Leary-Moore SK, Khan AA, et al. Magnetic resonance microscopy defines ethanol-induced brain abnormalities in prenatal mice: Effects of acute insult on gestational day 7. Alcohol Clin Exp Res 2010;34:98-111.
179. Kerns KA, Don A, Mateer CA, Streissguth AP. Cognitive deficits in nonretarded adults with fetal alcohol syndrome. J Learn Disabil 1997;30:685-693.
180. Mansouri A, Demelliers C, Amsellem S, Pessayre D, Fromenty B. Acute ethanol administration oxidatively damages and depletes mitochondrial DNA in mouse liver, brain, heart, and skeletal muscles: Protective effects of antioxidants. J Pharmacol Exp Ther 2001;298:737-743.
181. Somani SM, Husain K, Diaz-Phillips L, Lanzotti DJ, Kareti KR, Trammell GL. Interaction of exercise and ethanol on antioxidant enzymes in brain regions of the rat. Alcohol 1996;13:603-610.
182. Dame C, Juul SE, Christensen RD. The biology of erythropoietin in the central nervous system and its neurotrophic and neuroprotective potential. Biol Neonate 2001;79:228-235.
183. Marti HH, Wenger RH, Rivas LA, et al. Erythropoietin gene expression in human, monkey and murine brain. Eur J Neurosci 1996;8:666-676.
184. Kumral A, Gonene S, Acikgoz O, et al. Erythropoietin increases gluthione peroxidase enzyme activity and decreases lipid peroxidation levels in hypoxic-ischemic brain injury in neonatal rats. Biol Neonate 2005;87:15-18.
185. Chakraborty M, Ghosal J, Biswas T, Data AG. Effect of erythropoietin on membrane lipid peroxidation, superoxide dismutase, catalase, and glutathione of rat. Biochem Med Metab Biol 1988;40:8-18.
186. Genc S, Akhisaroglu M, Kuralay F, Genc K. Erythropoietin restores gluthione peroxidase activity in 1-methyl-4-phenyl-1, 2, 5, 6-tetrahydropyridine-induced neurotoxicity in C57BL mice and stimulates mural astroglial gluthione peroxidase production in vitro. Neurosci Lett 2002;312:73-76.
187. Akisu M, Tuzun S, Arslanoglu S, Yalaz M, Kultursay N. Effect of recombinant human erythropoietin administration on lipid peroxidation and antioxidant enzyme(s) activities in preterm infants. Acta Med Okayama 2001;55:357-362.
188. Conry J. Neuropsychological deficits in fetal alcohol syndrome and fetal alcohol effects. Alcohol Clin Exp Res 1990;14:650-655.
189. Kodituwakku PW. Defining the behavioural phenotype in children with fetal alcohol spectrum disorders: A review. Neurosci Biobehav Rev 2007;31:192-201.
190. Streissguth AP, Barr HM, Sampson PD. Moderate prenatal alcohol exposure: Effects on child IQ and learning problems at age 71/2 years. Alcohol Clin Exp Res 1990;14:662-669.
191. Kelly SJ, Day N, Striessguth AP. Effects of prenatal alcohol exposure on social behaviour in humans and other species. Neurotoxicol Teratol 2000;22:143-149.
192. Thomas JD, Kelly SJ, Mattson SN, Riley EP. Comparison of social abilities of children with fetal alcohol syndrome to those of children with similar IQ scores and normal controls. Alcohol Clin Exp Res 1998;22:528-533.
193. Goodlett CR, Horn KH. Mechanisms of alcohol-induced damage to the developing nervous system. Alcohol Res Health 2001;25:175-184.
194. Kelly SJ, Tran TD. Alcohol exposure during development alters social recognition and social communication in rats. Neurotoxicol Teratol 1997;19:383-389.
195. Lawrence RC, Bonner HC, Newsom RJ, Kelly SJ. Effects of alcohol exposure during development on play behaviour and c-fos expression in response to play behavior. Behav Brain Res 2008;188:209-218.
196. Lugo JN, Marino MD, Cronise K, Kelly SJ. Effects of alcohol exposure during development on social behavior in rats. Physiol Behav 2003;78:185-194.
197. Hamilton DA, Akers KG, Rice JP, et al. Prenatal exposure to moderate levels of ethanol alters social behavior in adult rats: Relationship to structural plasticity and immediate early gene expression in frontal cortex. Behav Brain Res 2010;207:290-304.
198. Kolb B, Sutherland RJ, Wishaw IQ. A comparison of the contribution of frontal and parietal association cortex to spatial localization in rats. Behav Neurosci 1983;97:13-27.
199. Riley EP, Lochry EA, Shapiro NR, Baldwin J. Response perseveration in rats exposed to alcohol prenatally. Pharmacol Biochem Behav 1979;10:255-259.
200. Thomas JD, Garcia GG, Domininguez HD, Riley EP, Administration of eliprodil during ethanol withdrawal in the neonatal rat attenuates alcohol-induced learning deficits. Psychopharmacology 2004a;175:189-195.
201. Thomas JD, Garrison ME, O'Neill TM. Perinatalcholine supplementation attenuates behavioral alterations associated with neonatal alcohol exposure in rats. Neurotoxicol Teratol 2004b;26:35-45.
202. Thomas JD, Abou EJ, Dominguez HD. Prenatal choline supplementation mitigates the adverse effects of prenatal alcohol exposure on development in rats. Neurotoxicol Teratol 2009;31:303-311.
203. Mazur-Kolecka B, Cohen IL, Jenkins EC, Kacmarski W, Flory M, Frackowiak J. Altered development of neuronal progenitor cells after stimulation with autistic blood sera. Brain Res 2007;1168C:11-20.
204. Mazur-Kolecka B, Cohen IL, Jenkins EC, Flory M, Merz G, Ted Brown W, Frackowiak J. Sera from children with autism alter proliferation of human neuronal progenitor cells exposed to oxidation. Neurotox Res 2009;16:87-95.
205. Lan F, Xu J, Zhang X, et al. Hepatocyte growth factor promotes proliferation and migration in immortalized progenitor cells. Neuroreport 2008;19:765-769.
206. Beversdorf DQ, Manning SE, Hillier A, et al. Timing of prenatal stressors and autism. J Autism Dev Disord 2005;35:471-478.
207. Miller MT, Stromland K, Ventura L, Johansson M, Bandim JN, Gillberg C. Autism associated with conditions characterized by developmental errors in early embryogenesis: A mini review. Int Dev Neurosci 2005;23:201-219.
208. Kern JK, Jones AM. Evidence of toxicity, oxidative stress, and neuronal insult in autism. J Toxicol Environ Health B Crit Rev 2006;9:485-499.
209. McGinnis WR. Oxidative stresses in autism. Altern Ther Health Med 2005;11:19-25.
210. Ming X, Stein TP, Brimacombe M, Johnson WG, Lambert GH, Wagner GC. Increased excretion of lipid peroxidation biomarker in autism. Prostaglandins Leukot Essent Fatty Acids 2005;73:379-384.
211. Archer T, Palomo, T, Fredriksson, A. Functional deficits following neonatal dopamine depletion and isolation housing: Circular water maze acquisition under pre-exposure conditions and motor activity. Neurotoxicity Res 2002;4:503-522.
212. Pathye U. Excess dietary iron is the root cause for increase in childhood autism and allergies. Med Hypotheses 2003;61:220-222.
213. Rola R, Zou Y, Huang TT, et al. Lack of extracellular superoxide dismutase (EC-SOD) in the microenvironment impacts radiation-induced changes in neurogenesis. Free Radic Biol Med 2007;42:1133-1145.
214. Pierce K, Glatt SJ, Liptak GS, McIntyre LL. The power and promise of identifying autism early: Insights from the search for clinical and biological markers. Ann Clin Psychiatry 2009;21:132-147.
215. Mazur-Kolecka B, Golabek A, Nowicki K, Flory M, Frackowiak J. Amyloid-β impairs development of neuronal progenitor cells by oxidative mechanisms. Neurobiol Aging 2006;27:1181-1192.
216. Kim K, Son TG, Kim SJ, Kim HS, Kim TS, Han SY, Lee J. Suppressive effects of bisphenol A on the proliferation of neural progenitor cells. J Toxicol Environ Health A 2007;70:1288-1295.
217. Castro SL, Zigmond MJ. Stress-induced increase in cellular dopamine in striatum: Role of glutamatergic action via N-methyl-D-aspartate receptors in substantia nigra. Brain Res 2001;901:47-54.
218. Darnaudery M, Dutriez I, Viltart O, Morley-Fletcher S, Maccari S. Stress during gestation induces lasting effects on emotional reactivity of the dam rat. Behav Brain Res 2004;153:211-216.
219. Lesage J, Dufourny L, Laborie C, et al. Perinatal malnutrition programs sympathoadrenal and hypothalamic-pituitary-adrenal axis responsiveness to restraint stress in adult male rats. J Neuroendocrinol 2002;14:135-143.
220. Fumagalli F, Molteni R, Racagni G, Riva MA. Stress during development: Impact on neuroplasticity and relevance to psychopathology. Prog Neurobiol 2007;81:197-217.
221. Kippin TE, Szumlinski KK, Kapasova Z, Rezner B, See RE. Prenatal stress enhances responsiveness to cocaine. Neuropsychopharmacology 2008;33:769-782.
222. Koehl M, Lemaire V, Vallee M, et al. Long term developmental and behavioral effects of perinatal life events in rats. Neurotoxicity Res 2001;3:65-83.
223. Maccari S, Morley-Fletcher S. Effects of prenatal restraint stress on the hypothalamic-pituitary-adrenal axis and related behavioural and neurobiological alterations. Psychoneuroendocrinology 2007;32(Suppl. 1):S10-S15.
224. Spauwen J, Krabbendam L, Lieb R, Wittchen H, van Os J. Early maternal stress and health behaviours and offspring expression of psychosis in adolescence. Acta Psychiatr Scand 2004;110:356-364.
225. Weinstock M. Alterations induced by gestational stress in brain morphology and behaviour of the offspring. Prog Neurobiol 2001;65:427-451.
226. Weinstock M. Gender differences in the effects of prenatal stress on brain development and behaviour. Neurochem Res 2007;32:1730-1740.
227. Dallman MF. Editorial: Moments in time-The neonatal rat hypothalamic-pituitary-adrenal axis. Endocrinology 2000;141:1590-1592.
228. Kapoor A, Dunn E, Kostaki A, Andrews MH, Matthews SG. Fetal programming of hypothalamic-pituitary-adrenal function: Prenatal stress and glucocorticoids. J Physiol 2006;572:31-44.
229. Kofman O. The role of prenatal stress in the etiology of develop behavioral disorders. Neurosci Biobehav Rev 2002;26:457-470.
230. Buitelaar JK, Huizink AC, Mulder EJ, de Medina PG, Visser GH. Prenatal stress and cognitive development and temperament in infants. Neurobiol Aging 2003;24:S53-S60.
231. De Kloet ER, Joëls M, Holsboer F. Stress and the brain: From adaptation to disease. Nat Rev Neurosci 2005;6:463-475.
232. Ward HE, Johnson EA, Salm AK, Birkle DL. Effects of prenatal stress on defensive withdrawal behavior and corticotrophin releasing factor systems in rat brain. Physiol Behav 2000;70:359-366.
233. Mabandla MV, Dobson B, Johnson S, Kellaway LA, Daniels WM, Russell VA. Development of a mild prenatal stress rat model to study long term effects on neural function and survival. Metab Brain Dis 2008;23:31-42.
234. Canlon B, Erichsen S, Nemlander E, Chen M, Hossain A, Celsi G, Ceccatelli S. Alterations in the intrauterine environment by glucocorticoids modifies the developmental programme of the auditory system. Eur J Neurosci 2003;17:2035-2041.
235. Levitt NS, Lindsay RS, Holmes MC, Seckl JR. Dexamethasone in the last week of pregnancy attenuates hippocampal glucocorticoid receptor gene expression and elevates blood pressure in the adult offspring of the rat. Neuroendocrinology 1996;64:412-418.
236. Richardson HN, Zorrilla EP, Mandyam CD, Rivier CL. Exposure to repetitive versus varied stress during prenatal development generates two distinct anxiogenic and neuroendocrine profiles in adulthood. Endocrinology 2006;147:2506-2517.
237. Zimmerberg B, Blaskey LG. Prenatal stress effects are partially ameliorated by prenatal administration of the neurosteriod allopregnanolone. Pharmacol Biochem Behav 1998;59:819-827.
238. Hossain A, Hajman K, Charitidi K, Erhardt S, Zimmermann U, Knipper M, Canlon B. Prenatal dexamethasone impairs behavior and the activation of the BDNF exon IV promoter in the paraventricular nucleus in adult offspring. Endocrinology 2008a;149:6356-6365.
239. Hossain WA, D'Sa C, Morest DK. Interactive roles of fibroblast growth factor 2 and neurotrophin 3 in the sequence of migration, process outgrowth, and axonal differentiation of mouse cochlear ganglion cells. J Neurosci Res 2008b;86:2376-2391.
240. Fumagalli F, Bedogni F, Perez J, Racagni G, Riva MA. Corticostriatal brain-derived neurotrophic factor dysregulation in adult rats following prenatal stress. Eur J Neurosci 2004;20:1348-1354.
241. Fumagalli F, Bedogni F, Slotkin TA, Racagni G, Riva MA. Prenatal stress elicits regionally selective changes in basal FGF-2 gene expression in adulthood and alters the adult response to acute or chronic stress. Neurobiol Dis 2005;20:731-737.
242. Lemaire V, Koehl M, Le Moal M, Abrous DN. Prenatal stress produces learning deficits associated with an inhibition of neurogenesis in the hippocampus. Proc Natl Acad Sci USA 2000;97:11032-11037.
243. Lemaire V, Lamarque S, Le Moal M, Piazza PV, Abrous DN. Postnatal stimulation of the pups counteracts prenatal stress-induced deficits in hippocampal neurogenesis. Biol Psychiatr 2006;59:786-792.
244. Son GH, Geum D, Chung S, et al. Maternal stress produces learning deficits associated with NMDA receptor-mediated synaptic plasticity. J Neurosci 2006;26:3309-3318.
245. Fumagalli F, Pasini M, Frasca A, Drago F, Racagni G, Riva MA. Prenatal stress alters glutamatergic system responsiveness in adult rat prefrontal cortex. J Neurochem 2009;109:1733-1744.
246. Daniels WM, Pietersen CY, Carstens ME, Stein DJ. Maternal separation in rats leads to anxiety-like behavior and a blunted ACTH response and altered neurotransmitter levels in response to a subsequent stressor. Metab Brain Dis 2004;19:3-14.
247. Ishiwata H, Shiga T, Okado N. Selective serotonin reuptake inhibitor treatment of early postnatal mice reverses their prenatal stress-induced brain dysfunction. Neuroscience 2005;133:893-901.
248. Olausson H, Uvnäs-Moberg K, Sohlström A. Postnatal oxytocin alleviates adverse effects in adult rat offspring caused by maternal malnutrition. Am J Physiol Endocrinol Metab 2003;284:E475-E480.
249. Walker CD, Scribner KA, Cascio CS, Dallman MF. The pituitaryadrenocortical system of neonatal rats is responsive to stress throughout development in a time-dependent and stressor-specific fashion. Endocrinology 1991;128:1385-1395.
250. Uysal N, Acikgoz O, Gonene S, Kayatekin BM, Kiray M, Sonmez A, Semin I. Effects of acute footshock stress on antioxidant enzyme activities in the adolescent rat brain. Physiol Res 2005;54:437-442.
251. Arborelius L, Eklund MB. Both long and brief maternal separation produces persistent changes in tissue levels of brain monoamines in middle-aged female rats. Neuroscience 2007;145:738-750.
252. Gartside SE, Johnson DA, Leitch MM, Troakes C, Ingram CD. Early life adversity programs changes in central 5-HT neuronal function in adulthood. Eur J Neurosci 2003;17:2401-2408.
253. Meaney MJ, Aitken DH, van Berkel C, Bhatnagar S, Sapolsky RM. Effect of neonatal handling on age-related impairments associated with the hippocampus. Science 1988;239:766-768.
254. Mesquita AR, Pego JM, Summavielle T, Maciel P, Almeida OF, Sousa N. Neurodevelopmental milestone abnormalities in rats exposed to stress in early life. Neuroscience 2007;147:1022-1033.
255. Knuth ED, Etgen AM. Long-term behavioural consequences of brief, repeated neonatal isolation. Brain Res 2007;1128:139-147.
256. Meaney MJ, Aitken DH. The effects of early postnatal handling on hippocampal glucocorticoid receptor concentrations: Temporal parameters. Brain Res 1985;354:301-304.
257. Mirescu C, Peters JD, Gould E. Early life experience alters response of adult neurogenesis to stress. Nat Neurosci 2004;7:841-846.
258. Rice D, Stan BJ. Critical periods of vulnerability for the developing nervous system: Evidence from human and animal models. Environ Health Perspect 2000;108:511-533.
259. McIntosh J, Anisman H, Merali Z. Short- and long-periods of neonatal maternal separation differentially affect anxiety and feeding in adult rats: Gender-dependent effects. Dev Brain Res 1999;113:97-106.
260. Post RM. Mechanisms of illness progression in the recurrent affective disorders. Neurotoxicity Res 2010, in press.
261. Tamborski A, Lucot JB, Hennessey MB. Central dopamine turnover in guinea pig pups during separation from their mothers in a novel environment. Behav Neurosci 1990;104:607-611.
262. Oitzl MS, Champagne DL, Van Der Veen R, de Kloet ER. Brain development under stress: Hypotheses of glucocorticoid actions revisited. Neurosci Biobehav Rev 2010;34:853-866.
263. Enthoven L, de Kloet ER, Oitzl MS. Differential development of stress system (re)activity at weaning dependent on time of disruption of maternal care. Brain Res 2008;1217:62-69.
264. Oitzl MS, Workel JO, Fluttert M, Frosch F, de Kloet ER. Maternal deprivation affects behaviour from youth to senescence: Amplification of individual differences in spatial learning and memory in senescent Brown Norway rats. Eur J Neurosci 2000;12:3771-3780.
265. Lehmann J, Pryce CR, Bettschen D, Feldon J. The maternal separation paradigm and adult emotionality and cognition in male and female Wistar rats. Pharmacol Biochem Behav 1999;64:705-715.
266. Sapolsky RM, Meaney MJ. Maturation of the adrenocortical stress response: Neuroendocrine control mechanisms and stress hyporesponsive period. Brain Res Rev 1986;11:65-76.
267. Schapiro S, Geller E, Eiduson S. Neonatal adrenal cortical response to stress and vasopressin. Proc Soc Exp Biol Med 1962;109:937-941.
268. Matsumoto M, Higuchi K, Togashi H, et al. Early postnatal stress alters the 5-HTergic modulation to emotional stress atpostadolescent periods of rats. Hippocampus 2005;15:775-781.
269. Heisler lK, Pronchuk N, Nonogaki K, et al. Serotonin activates the hypothalamic-pituitary-adrenal axis via serotonin 2C receptor stimulation. J Neurosci 2007;27:6956-6964.
270. Dent G, Choi DC, Herman JP, Levine S. GABAergic circuits and the stress hyporesponsive period in the rat: Ontogeny of glutamic acid decarboxylase (GAD) 67 mRNA expression in limbic-hypothalamic stress pathways. Brain Res 2007;1138:1-9.
271. Schmidt MV, Levine S, Oitzl MS, Van Der Mark M, Müller MB, Holsboer F, de Kloet ER. Glucocorticoid receptor blockade disinhibits pituitary-adrenal activity during the stress hyporesponsive period of the mouse. Endocrinology 2005;146:1458-1464.
272. Sutanto W. Multifaceted interaction of corticosteroids with the intracellular receptors and with membrane GABA-A receptor complex in the rat brain. J Neuroendocrinol 1989;1:243-247.
273. Matsui F, Morimoto M, Yoshimoto K, et al. Effects of postnatal development on corticosterone, serotonin and behavioral changes. Brain Dev 2009:PMID:19818569.
274. Uysal N, Gonene S, Acikgoz O, Pekcetin C, Kayatekin BM, Sonmez A, Semin I. Age-dependent effects of maternal deprivation on oxidative stress in infant rat. Neurosci Lett 2005;384:98-101.
275. Koontz T, Bralic M, Tomac J, Pernjak-Pugel E, Bantug G, Jonjic S, Britt WJ. Altered development of the brain after focal herpesvirus infection of the central nervous system. J Exp Med 2008;205:423-435.
276. Zerrate MC, Pletnikov M, Conners SL, Vargas DL, Seidler FJ, Zimmerman AW, Slotkin TA. Neuroinflammation and behavioral abnormalities after terbutaline treatment in rats: Implications for autism. J Pharmacol Exp Ther 2007;322:16-22.
277. Babulas V, Factor-Litvak P, Goetz R, Schaefer CA, Brown AS. Prenatal exposure to maternal genital and reproductive infections and adult schizophrenia. Am J Psychiatr 2006;163:927-929.
278. Brown AS, Susser ES. In utero infection and adult schizophrenia. Ment Retard Dev Disabil Res Rev 2002;8:51-57.
279. Patterson PH. Maternal infection: Window on neuroimmune interactions in fetal brain development and mental illness. Curr Opin Neurobiol 2002;12:115-118.
280. Smith SE, Li J, Garbett K, Mirnics K, Patterson PH. Maternal immune activation alters fetal brain development through interleukin-6. J Neurosci 2007;27:10695-10702.
281. Borrell J, Vela JM, Arevalo-Martin A, Molina-Holgado E, Guaza C. Prenatal immune challenge disrupts sensorimotor gating in adult rats: Implications for the etiopathogenesis of schizophrenia. Neuropsychopharmacology 2002;26:204-221.
282. Fortier ME, Joober R, Luheshi GN, Boksa P. Maternal exposure to bacterial endotoxin during pregnancy enhances amphetamine-induced locomotion and startle responses in adult rat offspring. J Psychiatr Res 2004;38:335-345.
283. Fortier ME, Luheshi GN, Boksa P. Effects of prenatal infection on prepulse inhibition in the rat depend on the nature of the infectious agent and the stage of pregnancy. Behav Brain Res 2007;181:270-277.
284. Meyer U, Feldon J, Schedlowski M, Yee BK. Immunological stress at the maternal-foetal interface: A link between neurodevelopment and adult psychopathology. Brain Behav Immun 2006;20:378-388.
285. Meyer U, Nyffeler M, Schwendener S, KnueselI, Yee BK, Feldon J. Relative prenatal and postnatal maternal contributions to schizophrenia-related neurochemical dysfunction after in utero immune challenge. Neuropsychopharmacology 2008a;33:441-456.
286. Meyer U, Nyffeler M, Yee BK, Knuesel I, Feldon J. Adult brain and behavioural pathological markers of prenatal immune challenge during early/middle and late fetal development. Brain Behav Immun 2008b;22:469-486.
287. Meyer U, Yee BK, Feldon J. The neurodevelopmental impact of prenatal infections at different of pregnancy: The earlier the worse? Neuroscientist 2007;13:241-256.
288. Romero E, Ali C, Molina-Holgado E, Castellano B, Guaza C, Borrell J. Neurobehavioural and immunological consequences of prenatal immune activation in rats: Influence of antipsychotics. Neuropsychopharmacology 2007;32:1791-1804.
289. Shi L, Fatemi SH, Sidwell RW, Patterson PH. Maternal influenza infection causes marked behavioral and pharmacological changes in the offspring. J Neurosci 2003;23:297-302.
290. Zuckerman L, Rehavi M, Nachman R, Weiner I. Immune activation during pregnancy in rats leads to a postpubertal emergence of disrupted latent inhibition, dopaminergic hyperfunction, and altered limb morphology in the offspring: A novel neurodevelopmental model of schizophrenia. Neuropsychopharmacology 2003;28:1778-1789.
291. Winter C, Djodari-Irani A, Sohr R, Morgenstern R, Feldon J, Juckel G, Meyer U. Prenatal immune activation leads to multiple changes in basal neurotransmitter levels in the adult brain: Implications for brain disorders of neurodevelopmental origin such as schizophrenia. Int J Neuropsychopharmacol 2009;12:513-524.
292. Fatemi SH. Potential microbial origins of schizophrenia and their treatments. Drugs Today 2009;45:305-318.
293. Fatemi SH, Folsom TD, Reutiman TJ, Huang H, Oishi K, Mori S. Prenatal viral infection of mice at E16 causes changes in gene expression in hippocampi of the offspring. Eur Neuropsychopharmacol 2009;19:648-653.
294. Nawa H, Takei N. Recent progress in animal modeling of immune inflammatory processes in schizophrenia: Implications of specific cytokines. Neurosci Res 2006;56:2-13.
295. Ozawa K, Hashimoto K, Kishimoto T, Shimizu E, Ishikura H, Masaomi L. Immune activation during pregnancy in mice leads to dopaminergic hyperfunction and cognitive impairment in the offspring: A neurodevelopmental animal model of schizophrenia. Biol Psychiatr 2006;59:546-554.
296. Patterson PH. Immune involvement in schizophrenia and autism: Etiology, pathology and animal models. Behav Brain Res 2009;204:313-321.
297. Shi S, Smith SEP, Malkova N, Tse D, Su Y, Patterson PH. Activation of the maternal immune system alters cerebellar development in the offspring. Brain Behav Immun 2009;23:116-123.
298. Winter C, Reutiman TJ, Folsom TD, Sohr R, Wolf RJ, Juckel G, Fatemi SH. Dopamine and serotonin levels following prenatal viral infection in mouse-Implications for psychiatric disorders such as schizophrenia and autism. Eur Neuropsychopharmacol 2008;18:712-716.
299. Palomo T, Beninger RJ, Kostrzewa RM, Archer T. Neurodevelopmental Liabilities in Brain Disorders. Tennessee Graham Publishing, Mountain View, 2003.
300. Kinney DK, Hintz K, Shearer EM, Barch DH, Riffin C, Whitley K, Butler R. A unifying hypothesis of schizophrenia: Abnormal immune system development may help explain roles of prenatal hazards, post-pubertal onset, stress, genes, climate, infections, and brain dysfunction. Med Hypoth 2010;74:555-563.