Prenatal alcohol exposure: Foetal programming, the hypothalamic-pituitary-adrenal axis and sex differences in outcome

Journal of Neuroendocrinology

Volumn 20, Issue 4, 2008, Pages 470-488

  Weinberg, Joanne ^a   Sliwowska, J H ^a   Lan, N ^a   Hellemans, K G C ^a  

^a UNIVERSITY OF BRITISH COLUMBIA   (Canada)

Author keywords

Foetal alcohol spectrum disorder (FASD); Foetal programming; Hypothalamic pituitary adrenal axis; Hypothalamic pituitary gonadal axis; Prenatal ethanol; Sex differences; Stress

Indexed keywords

GLUCOCORTICOID; HYPOPHYSIS HORMONE; HYPOTHALAMUS HORMONE; METHIONINE; SEROTONIN; SEX HORMONE;

ALCOHOL CONSUMPTION; CONFERENCE PAPER; DEPRESSION; DISEASE PREDISPOSITION; ENDOCRINE DISEASE; EVIDENCE BASED MEDICINE; FETAL ALCOHOL SYNDROME; FETUS DEVELOPMENT; FETUS PROGRAMMING; GESTATION PERIOD; HIPPOCAMPUS; HORMONAL REGULATION; HUMAN; HYPOTHALAMUS HYPOPHYSIS ADRENAL SYSTEM; HYPOTHALAMUS HYPOPHYSIS GONAD SYSTEM; MATERNAL BEHAVIOR; MENTAL DISEASE; NEUROENDOCRINOLOGY; NONHUMAN; PATHOPHYSIOLOGY; PERINATAL DEVELOPMENT; PREGNANCY OUTCOME; PRENATAL EXPOSURE; PRENATAL STRESS; PRIORITY JOURNAL; PROGENY; SEROTONINERGIC SYSTEM; SEX DIFFERENCE; SEXUAL DEVELOPMENT;

ALCOHOLISM; ANIMALS; ETHANOL; FEMALE; FETAL ALCOHOL SYNDROME; FETAL DEVELOPMENT; HUMANS; HYPOTHALAMIC DISEASES; HYPOTHALAMO-HYPOPHYSEAL SYSTEM; MALE; MODELS, BIOLOGICAL; PITUITARY-ADRENAL SYSTEM; PREGNANCY; PREGNANCY COMPLICATIONS; PREGNANCY OUTCOME; PRENATAL EXPOSURE DELAYED EFFECTS; SEX CHARACTERISTICS;

EID: 41149177183     PISSN: 09538194     EISSN: 13652826     Source Type: Journal    
DOI: 10.1111/j.1365-2826.2008.01669.x     Document Type: Conference Paper

References (221)

1. Morgan MY. Alcohol and nutrition. Br Med Bull 1982; 38: 21-29.
2. Adler RA. Clinical review 33: Clinically important effects of alcohol on endocrine function. J Clin Endocrinol Metab 1992; 74: 957-960.
3. Glavas MM, Weinberg J. Stress alcohol and the hypothalamic-pituitary-adrenal axis. In: Yehuda S, Mostofsky D, eds. Stress, Nutrition and Medical Disorders. Totowa, NJ: Humana Press Inc., 2005: 165-184.
4. Anderson RA Jr. Endocrine balance as a factor in the etiology of the fetal alcohol syndrome. Neurobehav Toxicol Teratol 1981; 3: 89-104.
5. Rudeen PK, Taylor JA. Fetal alcohol neuroendocrinopathies. In: Watson RR, ed. Alcohol and Neurobiology: Brain Development and Hormone Regulation. Boca Raton, FL: CRC Press, 1992: 109-138.
6. Weinberg J. Neuroendocrine effects of prenatal alcohol exposure. Ann NY Acad Sci 1993; 697: 86-96.
7. Weinberg J. Prenatal alcohol exposure: Endocrine function of offspring. In: Zakhari S, ed. Alcohol and the Endocrine System. Research Monograph No. 23, Bethesda, MD: NIH (NIAAA), 1993: 23.
8. Weinberg J, Bezio S. Alcohol-induced changes in pituitary-adrenal activity during pregnancy. Alcohol Clin Exp Res 1987; 11: 274-280.
9. Angelucci L, Patacchioli FR, Scaccianoce S, Di Sciullo A, Cardillo A, Maccari S. A model for later-life effects of perinatal drug exposure: maternal hormone mediation. Neurobehav Toxicol Teratol 1985; 7: 511-517.
10. Bakker JM, van Bel F, Heijnen CJ. Neonatal glucocorticoids and the developing brain: Short-term treatment with life-long consequences? Trends Neurosci 2001; 24: 649-653.
11. Matthews SG. Antenatal glucocorticoids and programming of the developing CNS. Pediatr Res 2000; 47: 291-300.
12. Matthews SG, Owen D, Banjanin S, Andrews MH. Glucocorticoids, hypothalamo-pituitary-adrenal (HPA) development, and life after birth. Endocr Res 2002; 28: 709-718.
13. Welberg LA, Seckl JR. Prenatal stress, glucocorticoids and the programming of the brain. J Neuroendocrinol 2001; 13: 113-128.
14. Sliwowska JH, Zhang X, Weinberg J. Prenatal ethanol exposure and fetal programming: Implications for endocrine and immune development and long-term health. In: Miller MW, ed. Brain Development: Normal Processes and the Effects of Alcohol and Nicotine. New York, NY: Oxford University Press, 2006: 153-181.
15. Zhang X, Sliwowska JH, Weinberg J. Prenatal alcohol exposure and fetal programming: Effects on neuroendocrine and immune function. Exp Biol Med (Maywood) 2005; 230: 376-388.
16. Riley EP, McGee CL. Fetal alcohol spectrum disorders: An overview with emphasis on changes in brain and behavior. Exp Biol Med (Maywood) 2005; 230: 357-365.
17. Manning MA, Eugene Hoyme H. Fetal alcohol spectrum disorders: A practical clinical approach to diagnosis. Neurosci Biobehav Rev 2007; 31: 230-238.
18. Jones KL, Smith DW. Recognition of the fetal alcohol syndrome in early infancy. Lancet 1973; 2: 999-1001.
19. Jones KL, Smith DW, Ulleland CN, Streissguth P. Pattern of malformation in offspring of chronic alcoholic mothers. Lancet 1973; 1: 1267-1271.
20. Stratton K, Howe C, Battaglia F. Fetal Alcohol Syndrome-Diagnosis, Epidemiology, Prevention and Treatment. Washington: National Academy Press, 1996.
21. Shaywitz SE, Cohen DJ, Shaywitz BA. Behavior and learning difficulties in children of normal intelligence born to alcoholic mothers. J Pediatr 1980; 96: 978-982.
22. Streissguth AP. The behavioral teratology of alcohol: Performance, behavioral and intellectual deficits in prenatally exposed children. In: West JR, ed. Alcohol and Brain Development. New York, NY: Oxford University Press, 1986: 3-44.
23. Mattson SN, Schoenfeld AM, Riley EP. Teratogenic effects of alcohol on brain and behavior. Alcohol Res Health 2001; 25: 185-191.
24. Kodituwakku PW. Defining the behavioral phenotype in children with fetal alcohol spectrum disorders: A review. Neurosci Biobehav Rev 2007; 31: 192-201.
25. Streissguth AP, Bookstein FL, Barr HM, Sampson PD, O'Malley K, Young JK. Risk factors for adverse life outcomes in fetal alcohol syndrome and fetal alcohol effects. J Dev Behav Pediatr 2004; 25: 228-238.
26. O'Connor MJ, Kasari C. Prenatal alcohol exposure and depressive features in children. Alcohol Clin Exp Res 2000; 24: 1084-1092.
27. O'Connor MJ, Paley B. The relationship of prenatal alcohol exposure and the postnatal environment to child depressive symptoms. J Pediatr Psychol 2006; 31: 50-64.
28. O'Connor TM, O'Halloran DJ, Shanahan F. The stress response and the hypothalamic-pituitary-adrenal axis: From molecule to melancholia. QJM 2000; 93: 323-333.
29. O'Connor MJ, Shah B, Whaley S, Cronin P, Gunderson B, Graham J. Psychiatric illness in a clinical sample of children with prenatal alcohol exposure. Am J Drug Alcohol Abuse 2002; 28: 743-754.
30. Famy C, Streissguth AP, Unis AS. Mental illness in adults with fetal alcohol syndrome or fetal alcohol effects. Am J Psychiatry 1998; 155: 552-554.
31. Abel EL, Dintcheff BA. Effects of prenatal alcohol exposure on growth and development in rats. J Pharmacol Exp Ther 1978; 207: 916-921.
32. Chernoff GF. The fetal alcohol syndrome in mice: An animal model. Teratology 1977; 15: 223-229.
33. Druse MJ. Neurotransmitter function: Changes associated with in utero alcohol exposure. In: Abel EL, ed. Fetal Alcohol Syndrome: From Mechanisms to Prevention. New York: CRC Press, 1996: 171-189.
34. Leichter J, Lee M. Effect of maternal ethanol administration on physical growth of the offspring in rats. Growth 1979; 43: 288-293.
35. Randall CL, Taylor J, Walker DW. Ethanol-induced malformations in mice. Alcohol Clin Exp Res 1977; 1: 219-224.
36. Weinberg J, Gallo PV. Prenatal ethanol exposure: Pituitary-adrenal activity in pregnant dams and offspring. Neurobehav Toxicol Teratol 1982; 4: 515-520.
37. Abel EL. Prenatal effects of alcohol on adult learning in rats. Pharmacol Biochem Behav 1979; 10: 239-243.
38. Anandam N, Felegi W, Stern JM. In utero alcohol heightens juvenile reactivity. Pharmacol Biochem Behav 1980; 13: 531-535.
39. Bond NW, Di Giusto EL. Effects of prenatal alcohol consumption on open-field behaviour and alcohol preference in rats. Psychopharmacologia 1976; 46: 163-165.
40. Bond NW, Digiusto EL. Effects of prenatal alcohol consumption on shock avoidance learning in rats. Psychol Rep 1977; 41: 1269-1270.
41. Gallo PV, Weinberg J. Neuromotor development and response inhibition following prenatal ethanol exposure. Neurobehav Toxicol Teratol 1982; 4: 505-513.
42. Kim CK, Kalynchuk LE, Kornecook TJ, Mumby DG, Dadgar NA, Pinel JP, Weinberg J. Object-recognition and spatial learning and memory in rats prenatally exposed to ethanol. Behav Neurosci 1997; 111: 985-995.
43. Lochry EA, Riley EP. Retention of passive avoidance and T-maze escape in rats exposed to alcohol prenatally. Neurobehav Toxicol 1980; 2: 107-115.
44. Martin JC, Martin DC, Sigman G, Radow B. Maternal ethanol consumption and hyperactivity in cross-fostered offspring. Physiol Psychol 1978; 6: 362-365.
45. Riley EP, Baron S, Hannigan JH. Response inhibition deficits following prenatal alcohol exposure: A comparison to the effects of hippocampal lesions in rats. In: West JR, ed. Alcohol and Brain Development. New York, NY: Oxford University Press,. 1986: 7-102.
46. Riley EP, Lochry EA, Shapiro NR. Lack of response inhibition in rats prenatally exposed to alcohol. Psychopharmacology (Berl) 1979; 62: 47-52.
47. Weinberg J. Prenatal ethanol exposure alters adrenocortical response to predictable and unpredictable stressors. Alcohol 1992; 9: 427-432.
48. Streissguth AP, O'Malley K. Neuropsychiatric implications and long-term consequences of fetal alcohol spectrum disorders. Semin Clin Neuropsychiatry 2000; 5: 177-190.
49. Glavas MM, Ellis L, Yu WK, Weinberg J. Effects of prenatal ethanol exposure on basal limbic-hypothalamic-pituitary-adrenal regulation: Role of corticosterone. Alcohol Clin Exp Res 2007; 31: 1598-1610.
50. Hofmann C, Glavas M, Yu W, Weinberg J. Glucocorticoid fast feedback is not altered in rats prenatally exposed to ethanol. Alcohol Clin Exp Res 1999; 23: 891-900.
51. Redila VA, Olson AK, Swann SE, Mohades G, Webber AJ, Weinberg J, Christie BR. Hippocampal cell proliferation is reduced following prenatal ethanol exposure but can be rescued with voluntary exercise. Hippocampus 2006; 16: 305-311.
52. Weinberg J. Nutritional issues in perinatal alcohol exposure. Neurobehav Toxicol Teratol 1984; 6: 261-269.
53. Weinberg J. Effects of ethanol and maternal nutritional status on fetal development. Alcohol Clin Exp Res 1985; 9: 49-55.
54. Subcommittee on Laboratory Animal Nutrition, Committee on Animal Nutrition, Board on Agriculture and National Research Council. Nutrient Requirements of Laboratory Animals, 4th revised edn. Washington, DC: Anonymous National Academy, 1995
55. Hofmann CE, Simms W, Yu WK, Weinberg J. Prenatal ethanol exposure in rats alters serotonergic-mediated behavioral and physiological function. Psychopharmacology (Berl) 2002; 161: 379-386.
56. Yirmiya R, Chiappelli F, Tio DL, Tritt SH, Taylor AN. Effects of prenatal alcohol and pair feeding on lipopolysaccharide-induced secretion of TNF-alpha and corticosterone. Alcohol 1998; 15: 327-335.
57. Taylor AN, Branch BJ, Nelson LR, Lane LA, Poland RE. Prenatal ethanol and ontogeny of pituitary-adrenal responses to ethanol and morphine. Alcohol 1986; 3: 255-259.
58. Vieau D, Sebaai N, Leonhardt M, Dutriez-Casteloot I, Molendi-Coste O, Laborie C, Breton C, Deloof S, Lesage J. HPA axis programming by maternal undernutrition in the male rat offspring. Psychoneuroendocrinology 2007; 32 (Suppl. 1): S16-S20.
59. Symonds ME, Stephenson T, Gardner DS, Budge H. Long-term effects of nutritional programming of the embryo and fetus: Mechanisms and critical windows. Reprod Fertil Dev 2007; 19: 53-63.
60. Burdge GC, Slater-Jefferies J, Torrens C, Phillips ES, Hanson MA, Lillycrop KA. Dietary protein restriction of pregnant rats in the F0 generation induces altered methylation of hepatic gene promoters in the adult male offspring in the F1 and F2 generations. Br J Nutr 2007; 97: 435-439.
61. Fowden AL, Giussani DA, Forhead AJ. Intrauterine programming of physiological systems: Causes and consequences. Physiology (Bethesda) 2006; 21: 29-37.
62. Root AW, Reiter EO, Andriola M, Duckett G. Hypothalamic-pituitary function in the fetal alcohol syndrome. J Pediatr 1975; 87: 585-588.
63. Jacobson SW, Bihun JT, Chiodo LM. Effects of prenatal alcohol and cocaine exposure on infant cortisol levels. Dev Psychopathol 1999; 11: 195-208.
64. Ramsay DS, Bendersky MI, Lewis M. Effect of prenatal alcohol and cigarette exposure on two- and six-month-old infants' adrenocortical reactivity to stress. J Pediatr Psychol 1996; 21: 833-840.
65. Haley DW, Handmaker NS, Lowe J. Infant stress reactivity and prenatal alcohol exposure. Alcohol Clin Exp Res 2006; 30: 2055-2064.
66. Kim CK, Osborn JA, Weinberg J. Stress reactivity in fetal alcohol syndrome. In: Abel E, ed. Fetal Alcohol Syndrome: From Mechanism to Behavior. New York: CRC Press, 1996: 215-236.
67. Schneider ML, Moore CF, Kraemer GW, Roberts AD, DeJesus OT. The impact of prenatal stress, fetal alcohol exposure, or both on development: perspectives from a primate model. Psychoneuroendocrinology 2002; 27: 285-298.
68. Taylor AN, Branch BJ, van Zuylen JE, Redei E. Maternal alcohol consumption and stress responsiveness in offspring. In: Chrousos GP, Loriaux DL, Gold PW, eds. Mechanisms of Physical and Emotional Stress. Advances in Experimental Medicine and Biology. New York, NY: Plenum Press, 1988: 311-317.
69. Lee S, Imaki T, Vale W, Rivier C. Effect of prenatal exposure to ethanol on the activity of the hypothalamic-pituitary-adrenal axis of the offspring: Importance of the time of exposure to ethanol and possible modulating mechanisms. Mol Cell Neurosci 1990; 1: 168-177.
70. Eguchi Y. Interrelationships between the fetal and maternal hypophyseal-adrenal axes in rats and mice. In: Bajusz E, ed. Physiology and Pathology of Adaptation Mechanism. New York, NY: Pergamon Press, 1996: 3-27.
71. Weinberg J. Hyperresponsiveness to stress: Differential effects of prenatal ethanol on males and females. Alcohol Clin Exp Res 1988; 12: 647-652.
72. Weinberg J. Prenatal ethanol effects: Sex differences in offspring stress responsiveness. Alcohol 1992; 9: 219-223.
73. Weinberg J. In utero alcohol exposure and hypothalamic-pituitary-adrenal activity: Gender differences in outcome. In: Zakhari S, Hunt WA, eds. Stress, Gender and Alcohol-Seeking Behavior, Research Monograph 29. Bethesda, MD: National Institute on Alcohol Abuse and Alcoholism, 1995: 29.
74. Halasz I, Aird F, Li L, Prystowsky MB, Redei E. Sexually dimorphic effects of alcohol exposure in utero on neuroendocrine and immune functions in chronic alcohol-exposed adult rats. Mol Cell Neurosci 1993; 4: 343-353.
75. Lee S, Rivier C. Gender differences in the effect of prenatal alcohol exposure on the hypothalamic-pituitary-adrenal axis response to immune signals. Psychoneuroendocrinology 1996; 21: 145-155.
76. Nelson LR, Taylor AN, Lewis JW, Poland RE, Redei E, Branch BJ. Pituitary-adrenal responses to morphine and footshock stress are enhanced following prenatal alcohol exposure. Alcohol Clin Exp Res 1986; 10: 397-402.
77. Taylor AN, Branch BJ, Liu SH, Kokka N. Long-term effects of fetal ethanol exposure on pituitary-adrenal response to stress. Pharmacol Biochem Behav 1982; 16: 585-589.
78. Taylor AN, Branch BJ, Liu SH, Wiechmann AF, Hill MA, Kokka N. Fetal exposure to ethanol enhances pituitary-adrenal and temperature responses to ethanol in adult rats. Alcohol Clin Exp Res 1981; 5: 237-246.
79. Kelly SJ, Mahoney JC, Randich A, West JR. Indices of stress in rats: effects of sex, perinatal alcohol and artificial rearing. Physiol Behav 1991; 49: 751-756.
80. Taylor AN, Branch BJ, Cooley-Matthews B, Poland RE. Effects of maternal ethanol consumption in rats on basal and rhythmic pituitary-adrenal function in neonatal offspring. Psychoneuroendocrinology 1982; 7: 49-58.
81. Weinberg J, Nelson LR, Taylor AN. Hormonal effects of fetal alcohol exposure. In: West JR, ed. Alcohol and Brain Development. New York, NY: Oxford University Press, 1986: 310-342.
82. Kim CK, Giberson PK, Yu W, Zoeller RT, Weinberg J. Effects of prenatal ethanol exposure on hypothalamic-pituitary-adrenal responses to chronic cold stress in rats. Alcohol Clin Exp Res 1999; 23: 301-310.
83. Weinberg J, Taylor AN, Gianoulakis C. Fetal ethanol exposure: hypothalamic-pituitary-adrenal and beta-endorphin responses to repeated stress. Alcohol Clin Exp Res 1996; 20: 122-131.
84. Kim CK, Turnbull AV, Lee SY, Rivier CL. Effects of prenatal exposure to alcohol on the release of adenocorticotropic hormone, corticosterone, and proinflammatory cytokines. Alcohol Clin Exp Res 1999; 23: 52-59.
85. Lee S, Schmidt D, Tilders F, Rivier C. Increased activity of the hypothalamic-pituitary-adrenal axis of rats exposed to alcohol in utero: role of altered pituitary and hypothalamic function. Mol Cell Neurosci 2000; 16: 515-528.
86. Schneider ML, Moore CF, Kraemer GW. Moderate level alcohol during pregnancy, prenatal stress, or both and limbic-hypothalamic-pituitary-adrenocortical axis response to stress in rhesus monkeys. Child Dev 2004; 75: 96-109.
87. Gabriel KI, Glavas MM, Ellis LI, Weinberg J. Postnatal handling does not normalize corticotropin releasing factor mRNA levels in animals prenatally exposed to ethanol. Devel Brain Res 2005; 157: 74-82.
88. Redei E, Halasz I, Li LF, Prystowsky MB, Aird F. Maternal adrenalectomy alters the immune and endocrine functions of fetal alcohol-exposed male offspring. Endocrinology 1993; 133: 452-460.
89. Glavas MM, Hofmann CE, Yu WK, Weinberg J. Effects of prenatal ethanol exposure on hypothalamic-pituitary-adrenal regulation after adrenalectomy and corticosterone replacement. Alcohol Clin Exp Res 2001; 25: 890-897.
90. Osborn JA, Yu C, Stelzl GE, Weinberg J. Effects of fetal ethanol exposure on pituitary-adrenal sensitivity to secretagogues. Alcohol Clin Exp Res 2000; 24: 1110-1119.
91. Osborn JA, Kim CK, Yu W, Herbert L, Weinberg J. Fetal ethanol exposure alters pituitary-adrenal sensitivity to dexamethasone suppression. Psychoneuroendocrinology 1996; 21: 127-143.
92. Redei E, Branch BJ, Taylor AN. Direct effect of ethanol on adrenocorticotropin (ACTH) release in vitro. J Pharmacol Exp Ther 1986; 237: 59-64.
93. Lee S, Selvage D, Hansen K, Rivier C. Site of action of acute alcohol administration in stimulating the rat hypothalamic-pituitary-adrenal axis: Comparison between the effect of systemic and intracerebroventricular injection of this drug on pituitary and hypothalamic responses. Endocrinology 2004; 145: 4470-4479.
94. Tritt SH, Tio DL, Brammer GL, Taylor AN. Adrenalectomy but not adrenal demedullation during pregnancy prevents the growth-retarding effects of fetal alcohol exposure. Alcohol Clin Exp Res 1993; 17: 1281-1289.
95. Slone-Wilcoxon J, Redei EE. Maternal-fetal glucocorticoid milieu programs hypothalamic-pituitary-thyroid function of adult offspring. Endocrinology 2004; 145: 4068-4072.
96. Cobb CF, Van Thiel DH, Gavaler JS, Lester R. Effects of ethanol and acetaldehyde on the rat adrenal. Metabolism 1981; 30: 537-543.
97. Weinberg J, Petersen TD. Effects of prenatal ethanol exposure on glucocorticoid receptors in rat hippocampus. Alcohol Clin Exp Res 1991; 15: 711-716.
98. Kim CK, Yu W, Edin G, Ellis L, Osborn JA, Weinberg J. Chronic intermittent stress does not differentially alter brain corticosteroid receptor densities in rats prenatally exposed to ethanol. Psychoneuroendocrinology 1999; 24: 585-611.
99. Weinstock M. Gender differences in the effects of prenatal stress on brain development and behaviour. Neurochem Res 2007; 32: 1730-1740.
100. Maccari S, Darnaudery M, Morley-Fletcher S, Zuena AR, Cinque C, Van Reeth O. Prenatal stress and long-term consequences: Implications of glucocorticoid hormones. Neurosci Biobehav Rev 2003; 27: 119-127.
101. Weinstock M. The potential influence of maternal stress hormones on development and mental health of the offspring. Brain Behav Immun 2005; 19: 296-308.
102. Zagron G, Weinstock M. Maternal adrenal hormone secretion mediates behavioural alterations induced by prenatal stress in male and female rats. Behav Brain Res 2006; 175: 323-328.
103. Lee S, Rivier C. Administration of corticosterone to pregnant adrenalectomized dams does not alter the hypothalamic-pituitary-adrenal axis' acitivity of the offspring. Mol Cell Neurosci 1992; 3: 118-123.
104. Patchev VK, Hayashi S, Orikasa C, Almeida OF. Implications of estrogen-dependent brain organization for gender differences in hypothalamo-pituitary-adrenal regulation. FASEB J 1995; 9: 419-423.
105. Rivier C, Rivest S. Effect of stress on the activity of the hypothalamic-pituitary-gonadal axis: Peripheral and central mechanisms. Biol Reprod 1991; 45: 523-532.
106. Viau V. Functional cross-talk between the hypothalamic-pituitary-gonadal and -adrenal axes. J Neuroendocrinol 2002; 14: 506-513.
107. Viau V, Soriano L, Dallman MF. Androgens alter corticotropin releasing hormone and arginine vasopressin mRNA within forebrain sites known to regulate activity in the hypothalamic-pituitary-adrenal axis. J Neuroendocrinol 2001; 13: 442-452.
108. Young EA. The role of gonadal steroids in hypothalamic-pituitary-adrenal axis regulation. Crit Rev Neurobiol 1995; 9: 371-381.
109. Young EA. Sex differences in response to exogenous corticosterone: A rat model of hypercortisolemia. Mol Psychiatry 1996; 1: 313-319.
110. Carey MP, Deterd CH, de Koning J, Helmerhorst F, de Kloet ER. The influence of ovarian steroids on hypothalamic-pituitary-adrenal regulation in the female rat. J Endocrinol 1995; 144: 311-321.
111. Viau V, Meaney MJ. Variations in the hypothalamic-pituitary-adrenal response to stress during the estrous cycle in the rat. Endocrinology 1991; 129: 2503-2511.
112. Dallman MF, Viau V, Bhatnagar S, Gomez F, Laugero K, Bell ME. Corticotropin-releasing factor (CRF), corticosteroids, and sugar: Energy balance, the brain and behavior. In: Pffaf DW, Arnold AP, Etgen AM, Fahrback SE, Rubin RT, eds. Mammalian hormone systems. San Diego: Academic Press, 2002: 571-632.
113. Handa RJ, Burgess LH, Kerr JE, O'Keefe JA. Gonadal steroid hormone receptors and sex differences in the hypothalamo-pituitary-adrenal axis. Horm Behav 1994; 28: 464-476.
114. Williamson M, Bingham B, Viau V. Central organization of androgen-sensitive pathways to the hypothalamic-pituitary-adrenal axis: implications for individual differences in responses to homeostatic threat and predisposition to disease. Prog Neuropsychopharmacol Biol Psychiatry 2005; 29: 1239-1248.
115. Karandrea D, Kittas C, Kitraki E. Contribution of sex and cellular context in the regulation of brain corticosteroid receptors following restraint stress. Neuroendocrinology 2000; 71: 343-353.
116. Kerr JE, Beck SG, Handa RJ. Androgens modulate glucocorticoid receptor mRNA, but not mineralocorticoid receptor mRNA levels, in the rat hippocampus. J Neuroendocrinol 1996; 8: 439-447.
117. Kerr JE, Allore RJ, Beck SG, Handa RJ. Distribution and hormonal regulation of androgen receptor (AR) and AR messenger ribonucleic acid in the rat hippocampus. Endocrinology 1995; 136: 3213-3221.
118. Viau V, Meaney MJ. The inhibitory effect of testosterone on hypothalamic-pituitary-adrenal responses to stress is mediated by the medial preoptic area. J Neurosci 1996; 16: 1866-1876.
119. Bingaman EW, Magnuson DJ, Gray TS, Handa RJ. Androgen inhibits the increases in hypothalamic corticotropin-releasing hormone (CRH) and CRH-immunoreactivity following gonadectomy. Neuroendocrinology 1994; 59: 228-234.
120. Handa RJ, Nunley KM, Lorens SA, Louie JP, McGivern RF, Bollnow MR. Androgen regulation of adrenocorticotropin and corticosterone secretion in the male rat following novelty and foot shock stressors. Physiol Behav 1994; 55: 117-124.
121. Kelly SJ, Ostrowski NL, Wilson MA. Gender differences in brain and behavior: Hormonal and neural bases. Pharmacol Biochem Behav 1999; 64: 655-664.
122. McGivern RF, Raum WJ, Salido E, Redei E. Lack of prenatal testosterone surge in fetal rats exposed to alcohol: Alterations in testicular morphology and physiology. Alcohol Clin Exp Res 1988; 12: 243-247.
123. McGivern RF, Handa RJ, Raum WJ. Ethanol exposure during the last week of gestation in the rat: Inhibition of the prenatal testosterone surge in males without long-term alterations in sex behavior. Neurotoxicol Teratol 1998; 20: 483-490.
124. McGivern RF, Handa RJ, Redei E. Decreased postnatal testosterone surge in male rats exposed to ethanol during the last week of gestation. Alcohol Clin Exp Res 1993; 17: 1215-1222.
125. Kakihana R, Butte JC, Moore JA. Endocrine effects of meternal alcoholization: Plasma and brain testosterone, dihydrotestosterone, estradiol, and corticosterone. Alcohol Clin Exp Res 1980; 4: 57-61.
126. Kelce WR, Rudeen PK, Ganjam VK. Prenatal ethanol exposure alters steroidogenic enzyme activity in newborn rat testes. Alcohol Clin Exp Res 1989; 13: 617-621.
127. Chen JJ, Smith ER. Effects of perinatal alcohol on sexual differentiation and open-field behavior in rats. Horm Behav 1979; 13: 219-231.
128. McGivern RF. Influence of prenatal exposure to cimetidine and alcohol on selected morphological parameters of sexual differentiation: A preliminary report. Neurotoxicol Teratol 1987; 9: 23-26.
129. Parker S, Udani M, Gavaler JS, Van Thiel DH. Adverse effects of ethanol upon the adult sexual behavior of male rats exposed in utero. Neurobehav.Toxicol.Teratol. 1984; 6: 289-293.
130. Rudeen PK. Reduction of the volume of the sexually dimorphic nucleus of the preoptic area by in utero ethanol exposure in male rats. Neurosci Lett 1986; 72: 363-368.
131. Udani M, Parker S, Gavaler J, Van Thiel DH. Effects of in utero exposure to alcohol upon male rats. Alcohol Clin Exp Res 1985; 9: 355-359.
132. Jungkuntz-Burgett L, Paredez S, Rudeen PK. Reduced sensitivity of hypothalamic-preoptic area norepinephrine and dopamine to testosterone feedback in adult fetal ethanol-exposed male rats. Alcohol 1990; 7: 513-516.
133. Hard E, Dahlgren IL, Engel J, Larsson K, Lindh AS, Musi B. Impairment of reproductive behavior in prenatally ethanol-exposed rats. In: Rydberg U, ed. Alcohol and the Developing Brain. New York, NY: Raven Press, 1985: 93-108.
134. McGivern RF, Clancy AN, Hill MA, Noble EP. Prenatal alcohol exposure alters adult expression of sexually dimorphic behavior in the rat. Science 1984; 224: 896-898.
135. McGivern RF, Ervin MG, McGeary J, Somes C, Handa RJ. Prenatal ethanol exposure induces a sexually dimorphic effect on daily water consumption in prepubertal and adult rats. Alcohol Clin Exp Res 1998; 22: 868-875.
136. Meyer LS, Riley EP. Social play in juvenile rats prenatally exposed to alcohol. Teratology 1986; 34: 1-7.
137. Barron S, Tieman SB, Riley EP. Effects of prenatal alcohol exposure on the sexually dimorphic nucleus of the preoptic area of the hypothalamus in male and female rats. Alcohol Clin Exp Res 1988; 12: 59-64.
138. Boggan WO, Randall CL, Dodds HM. Delayed sexual maturation in female C57BL/6J mice prenatally exposed to alcohol. Res Commun Chem Pathol Pharmacol 1979; 23: 117-125.
139. Esquifino AI, Sanchis R, Guerri C. Effect of prenatal alcohol exposure on sexual maturation of female rat offspring. Neuroendocrinology 1986; 44: 483-487.
140. Farry K, Tittmar HG. Alcohol as a teratogen: Effects of maternal administration in rats on sexual development in female offspring. Irc Med Sci Reprod Obstet Gynecol 1975; 3: 620.
141. Wilson ME, Handa RJ. Gonadotropin secretion in infantile rats exposed to ethanol in utero. Alcohol 1997; 14: 497-501.
142. McGivern RF, Yellon SM. Delayed onset of puberty and subtle alterations in GnRH neuronal morphology in female rats exposed prenatally to ethanol. Alcohol 1992; 9: 335-340.
143. Handa RJ, McGivern RF, Noble ES, Gorski RA. Exposure to alcohol in utero alters the adult patterns of luteinizing hormone secretion in male and female rats. Life Sci 1985; 37: 1683-1690.
144. Li Y, McGivern RF, Nagahara AH, Handa RJ. Alterations in the estrogen sensitivity of hypothalamic proenkephalin mRNA expression with age and prenatal exposure to alcohol. Brain Res Mol Brain Res 1997; 47: 215-222.
145. Wilson ME, Marshall MT, Bollnow MR, McGivern RF, Handa RJ. Gonadotropin-releasing hormone mRNA and gonadotropin beta-subunit mRNA expression in the adult female rat exposed to ethanol in utero. Alcohol Clin Exp Res 1995; 19: 1211-1218.
146. Creighton-Taylor JA, Rudeen PK. Fetal alcohol exposure and effects of LHRH and PMA on LH beta-mRNA expression in the female rat. Alcohol Clin Exp Res 1991; 15: 1031-1035.
147. McGivern RF, McGeary J, Robeck S, Cohen S, Handa RJ. Loss of reproductive competence at an earlier age in female rats exposed prenatally to ethanol. Alcohol Clin Exp Res 1995; 19: 427-433.
148. Barron S, Riley EP. Pup-induced maternal behavior in adult and juvenile rats exposed to alcohol prenatally. Alcohol Clin Exp Res 1985; 9: 360-365.
149. Aird F, Halasz I, Redei E. Ontogeny of hypothalamic corticotropin-releasing factor and anterior pituitary pro-opiomelanocortin expression in male and female offspring of alcohol-exposed and adrenalectomized dams. Alcohol Clin Exp Res 1997; 21: 1560-1566.
150. Lan N, Yamashita F, Halpert AG, Ellis L, Yu WK, Viau V, Weinberg J. Prenatal ethanol exposure alters the effects of gonadectomy on hypothalamic-pituitary-adrenal activity in male rats. J Neuroendocrinol 2006; 18: 672-684.
151. Aguilera G. Regulation of pituitary ACTH secretion during chronic stress. Front Neuroendocrinol 1994; 15: 321-350.
152. Gillies GE, Linton EA, Lowry PJ. Corticotropin releasing activity of the new CRF is potentiated several times by vasopressin. Nature 1982; 299: 355-357.
153. Ma XM, Lightman SL, Aguilera G. Vasopressin and corticotropin-releasing hormone gene responses to novel stress in rats adapted to repeated restraint. Endocrinology 1999; 140: 3623-3632.
154. Kalra PS, Simpkins JW, Kalra SP. Testosterone raises LHRH levels exclusively in the median eminence of castrated rats. Neuroendocrinology 1984; 39: 45-48.
155. Lan N, Hellemans KGC, Ellis LI, Viau V, Weinberg J. Role of testosterone in mediating prenatal ethanol effects on hypothalamic-pituitary-adrenal activity in male rats. Psychoneuroendocrinology submitted.
156. Lan N, Bach P, Westendorp S, Ellis L, Yu WK, Viau V, Weinberg J. Role of testosterone in hippocampal mineralocorticoid (MR) and glucocorticoid (GR) receptor mRNA levels in male rats prenatally exposed to ethanol. Endocrine Soc Abstr 2007: 3-57.
157. Lan N, Westendorp S, Bach P, Ellis L, O'Neill R, O'Rourke D, Yu WK, Vogl W, Weinberg J. Prenatal ethanol exposure delays testes seminiferous tubule development. Alcohol Clin Exp Res 2007; 31: 100A.
158. Lan N, Yamashita F, Halpert AH, Sliwowska JH, Ellis L, Yu W, O'Rourke D, Viau V, Weinberg J. Prenatal ethanol effects on the hypothalmic-pituitary-adrenal response to stress across the estrus cycle. Alcohol Clin Exp Res 2006; 30: 880A.
159. Sliwowska JH, Lee J, Ellis LI, Yu W, Weinberg J. The decrease of kisspeptin-ir cells in the arcuate nucleus of the hypothalamus in adult female rats prenatally exposed to ethanol is estradiol-dependent. Soc Neurosci 2007: (Abstract 194.8).
160. Kotani M, Detheux M, Vandenbogaerde A, Communi D, Vanderwinden JM, Le PoulE, Brezillon S, Tyldesley R, Suarez-Huerta N, Vandeput F, Blanpain C, Schiffmann SN, Vassart G, Parmentier M. The metastasis suppressor gene KiSS-1 encodes kisspeptins, the natural ligands of the orphan G protein-coupled receptor GPR54. J Biol Chem 2001; 276: 34631-34636.
161. Muir AI, Chamberlain L, Elshourbagy NA, Michalovich D, Moore DJ, Calamari A, Szekeres PG, Sarau HM, Chambers JK, Murdock P, Steplewski K, Shabon U, Miller JE, Middleton SE, Darker JG, Larminie CG, Wilson S, Bergsma DJ, Emson P, Faull R, Philpott KL, Harrison DC. AXOR12, a novel human G protein-coupled receptor, activated by the peptide KiSS-1. J Biol Chem 2001; 276: 28969-28975.
162. Ohtaki T, Shintani Y, Honda S, Matsumoto H, Hori A, Kanehashi K, Terao Y, Kumano S, Takatsu Y, Masuda Y, Ishibashi Y, Watanabe T, Asada M, Yamada T, Suenaga M, Kitada C, Usuki S, Kurokawa T, Onda H, Nishimura O, Fujino M. Metastasis suppressor gene KiSS-1 encodes peptide ligand of a G-protein-coupled receptor. Nature 2001; 411: 613-617.
163. Gottsch ML, Cunningham MJ, Smith JT, Popa SM, Acohido BV, Crowley WF, Seminara S, Clifton DK, Steiner RA. A role for kisspeptins in the regulation of gonadotropin secretion in the mouse. Endocrinology 2004; 145: 4073-4077.
164. Smith JT, Cunningham MJ, Rissman EF, Clifton DK, Steiner RA. Regulation of Kiss1 gene expression in the brain of the female mouse. Endocrinology 2005; 146: 3686-3692.
165. Clarkson J, Herbison AE. Postnatal development of kisspeptin neurons in mouse hypothalamus; sexual dimorphism and projections to gonadotropin-releasing hormone neurons. Endocrinology 2006; 147: 5817-5825.
166. Dhillo WS, Chaudhri OB, Patterson M, Thompson EL, Murphy KG, Badman MK, McGowan BM, Amber V, Patel S, Ghatei MA, Bloom SR. Kisspeptin-54 stimulates the hypothalamic-pituitary gonadal axis in human males. J Clin Endocrinol Metab 2005; 90: 6609-6615.
167. Messager S, Chatzidaki EE, Ma D, Hendrick AG, Zahn D, Dixon J, Thresher RR, Malinge I, Lomet D, Carlton MB, Colledge WH, Caraty A, Aparicio SA. Kisspeptin directly stimulates gonadotropin-releasing hormone release via G protein-coupled receptor 54. Proc Natl Acad Sci USA 2005; 102: 1761-1766.
168. Shahab M, Mastronardi C, Seminara SB, Crowley WF, Ojeda SR, Plant TM. Increased hypothalamic GPR54 signaling: A potential mechanism for initiation of puberty in primates. Proc Natl Acad Sci USA 2005; 102: 2129-2134.
169. Thompson EL, Patterson M, Murphy KG, Smith KL, Dhillo WS, Todd JF, Ghatei MA, Bloom SR. Central and peripheral administration of kisspeptin-10 stimulates the hypothalamic-pituitary-gonadal axis. J Neuroendocrinol 2004; 16: 850-858.
170. Kauffman AS, Clifton DK, Steiner RA. Emerging ideas about kisspeptin- GPR54 signaling in the neuroendocrine regulation of reproduction. Trends
171. Herbison AE, Pape JR. New evidence for estrogen receptors in gonadotropin-releasing hormone neurons. Front Neuroendocrinol 2001; 22: 292-308.
172. Adachi S, Yamada S, Takatsu Y, Matsui H, Kinoshita M, Takase K, Sugiura H, Ohtaki T, Matsumoto H, Uenoyama Y, Tsukamura H, Inoue K, Maeda K. Involvement of anteroventral periventricular metastin/kisspeptin neurons in estrogen positive feedback action on luteinizing hormone release in female rats. J Reprod Dev 2007; 53: 367-378.
173. Navarro VM, Castellano JM, Fernandez-Fernandez R, Tovar S, Roa J, Mayen A, Nogueiras R, Vazquez MJ, Barreiro ML, Magni P, Aguilar E, Dieguez C, Pinilla L, Tena-Sempere M. Characterization of the potent luteinizing hormone-releasing activity of KiSS-1 peptide, the natural ligand of GPR54. Endocrinology 2005; 146: 156-163.
174. Lowry CA. Functional subsets of serotonergic neurones: Implications for control of the hypothalamic-pituitary-adrenal axis. J Neuroendocrinol 2002; 14: 911-923.
175. Druse MJ, Kuo A, Tajuddin N. Effects of in utero ethanol exposure on the developing serotonergic system. Alcohol Clin Exp Res 1991; 15: 678-684.
176. Rathbun W, Druse MJ. Dopamine, serotonin, and acid metabolites in brain regions from the developing offspring of ethanol-treated rats. J Neurochem 1985; 44: 57-62.
177. Sari Y, Zhou FC. Prenatal alcohol exposure causes long-term serotonin neuron deficit in mice. Alcohol Clin Exp Res 2004; 28: 941-948.
178. Zafar H, Shelat SG, Redei E, Tejani-Butt S. Fetal alcohol exposure alters serotonin transporter sites in rat brain. Brain Res 2000; 856: 184-192.
179. Tajuddin NF, Druse MJ. Treatment of pregnant alcohol-consuming rats with buspirone: Effects on serotonin and 5-hydroxyindoleacetic acid content in offspring. Alcohol Clin Exp Res 1993; 17: 110-114.
180. Kelly SJ. Alcohol exposure during development alters hypothalamic neurotransmitter concentrations. J Neural Transm 1996; 103: 55-67.
181. Tran TD, Kelly SJ. Alterations in hippocampal and hypothalamic monoaminergic neurotransmitter systems after alcohol exposure during all three trimester equivalents in adult rats. J Neural Transm 1999; 106: 773-786.
182. Hofmann CE, Ellis L, Yu WK, Weinberg J. Hypothalamic-pituitary-adrenal responses to 5-HT1A and 5-HT2A/C agonists are differentially altered in female and male rats prenatally exposed to ethanol. Alcohol Clin Exp Res 2007; 31: 345-355.
183. Sliwowska JH, Lan N, Yamashita F, Halpert AG, Viau V, Weinberg J. Prenatal ethanol exposure induces long-term changes in hippocampal MR but not GR mRNA levels in adult female rats. Alcohol Clin Exp Res; 30: 119A.
184. Lopez JF, Chalmers DT, Little KY, Watson SJ. A.E. Bennett Research Award. Regulation of serotonin1A, glucocorticoid, and mineralocorticoid receptor in rat and human hippocampus: Implications for the neurobiology of depression. Biol Psychiatry 1998; 43: 547-573.
185. Lopez JF, Vazquez DM, Chalmers DT, Watson SJ. Regulation of 5-HT receptors and the hypothalamic-pituitary-adrenal axis. Implications for the neurobiology of suicide. Ann NY Acad Sci 1997; 836: 106-134.
186. Heinz A, Mann K, Weinberger DR, Goldman D. Serotonergic dysfunction, negative mood states, and response to alcohol. Alcohol Clin Exp Res 2001; 25: 487-495.
187. Thase ME. Depression and sleep: Pathophysiology and treatment. Dialogues Clin Neurosci 2006; 8: 217-226.
188. Tyrer P, Baldwin D. Generalised anxiety disorder. Lancet 2006; 368: 2156-2166.
189. Pariante CM, Thomas SA, Lovestone S, Makoff A, Kerwin RW. Do antidepressants regulate how cortisol affects the brain? Psychoneuroendocrinology 2004; 29: 423-447.
190. Swaab DF, Bao AM, Lucassen PJ. The stress system in the human brain in depression and neurodegeneration. Ageing Res Rev 2005; 4: 141-194.
191. de Kloet E.R, Vreugdenhil E, Oitzl MS, Joels M. Brain corticosteroid receptor balance in health and disease. Endocr Rev 1998; 19: 269-301.
192. Gillespie CF, Nemeroff CB. Hypercortisolemia and depression. Psychosom Med 2005; 67 (Suppl. 1): S26-S28.
193. Heim C, Plotsky PM, Nemeroff CB. Importance of studying the contributions of early adverse experience to neurobiological findings in depression. Neuropsychopharmacology 2004; 29: 641-648.
194. Heim C, Nemeroff CB. The role of childhood trauma in the neurobiology of mood and anxiety disorders: Preclinical and clinical studies. Biol Psychiatry 2001; 49: 1023-1039.
195. Meaney MJ, Szyf M, Seckl JR. Epigenetic mechanisms of perinatal programming of hypothalamic-pituitary-adrenal function and health. Trends Mol Med 2007; 13: 269-277.
196. Gluckman PD, Hanson MA. The developmental origins of the metabolic syndrome. Trends Endocrinol Metab 2004; 15: 183-187.
197. Liu L, Li A, Matthews SG. Maternal glucocorticoid treatment programs HPA regulation in adult offspring: Sex-specific effects. Am J Physiol Endocrinol Metab 2001; 280: E729-E739.
198. Weaver IC, Cervoni N, Champagne FA, D'Alessio AC, Sharma S, Seckl JR, Dymov S, Szyf M, Meaney MJ. Epigenetic programming by maternal behavior. Nat Neurosci 2004; 7: 847-854.
199. Phillips DI, Barker DJ, Fall CH, Seckl JR, Whorwood CB, Wood PJ, Walker BR. Elevated plasma cortisol concentrations: A link between low birth weight and the insulin resistance syndrome? J Clin Endocrinol Metab 1998; 83: 757-760.
200. Phillips DI, Walker BR, Reynolds RM, Flanagan DE, Wood PJ, Osmond C, Barker DJ, Whorwood CB. Low birth weight predicts elevated plasma cortisol concentrations in adults from 3 populations. Hypertension 2000; 35: 1301-1306.
201. Schalinske KL, Nieman KM. Disruption of methyl group metabolism by ethanol. Nutr Rev 2005; 63: 387-391.
202. O'Neill R, Lan N, Innis S, Devlin A, Ellis L, Chan B, Weinberg J. Metabolic effects of prenatal ethanol exposure and epigenetic reprogramming of the HPA axis. Alcohol Clin Exp Res 2007; 31: 100A.
203. Streissguth AP, Barr HM, Kogan J, Bookstein FL. Understanding the Occurrence of Secondary Disabilities in Clients with Fetal Alcohol Syndrome (FAS) and Fetal Alcohol Effects (FAE). Final Report, CDCP Grant No. RO4/CCROO8515, Fetal Alcohol and Drug Unit, Seattle, 1996.
204. Bertoglio LJ, Joca SR, Guimaraes FS. Further evidence that anxiety and memory are regionally dissociated within the hippocampus. Behav Brain Res 2006; 175: 183-188.
205. de KloetER, Joels M, Holsboer F. Stress and the brain: From adaptation to disease. Nat Rev Neurosci 2005; 6: 463-475.
206. Heim C, Nemeroff CB. The impact of early adverse experiences on brain systems involved in the pathophysiology of anxiety and affective disorders. Biol Psychiatry 1999; 46: 1509-1522.
207. Heim C, Newport DJ, Heit S, Graham YP, Wilcox M, Bonsall R, Miller AH, Nemeroff CB. Pituitary-adrenal and autonomic responses to stress in women after sexual and physical abuse in childhood. JAMA 2000; 284: 592-597.
208. Hauger RL, Lorang M, Irwin M, Aguilera G. CRF receptor regulation and sensitization of ACTH responses to acute ether stress during chronic intermittent immobilization stress. Brain Res 1990; 532: 34-40.
209. Bernet CZ, Stein MB. Relationship of childhood maltreatment to the onset and course of major depression in adulthood. Depress Anxiety 1999; 9: 169-174.
210. Matthews K, Christmas D, Swan J, Sorrell E. Animal models of depression: navigating through the clinical fog. Neurosci Biobehav Rev 2005; 29: 503-513.
211. Gutman DA, Nemeroff CB. Persistent central nervous system effects of an adverse early environment: Clinical and preclinical studies. Physiol Behav 2003; 79: 471-478.
212. Nemeroff CB, Vale WW. The neurobiology of depression: Inroads to treatment and new drug discovery. J Clin Psychiatry 2005; 66: 5-13.
213. Dungan HM, Clifton DK, Steiner RA. Minireview: KISS peptin neurons as central processors in the regulation of gonadotropin - releasing hormone secretion. Endocrinology 2006; 147: 1154-1158.
214. Glavas MM, Yu WK, Weinberg J. Effects of mineralcorticoid and glucocorticoid receptor blockade on the hypothalmic-pituitary-adrenal function in rats prenatally exposed to ethanol. Alcohol Clin Exp Res 2006; 30: 1916-1924.
215. Rudeen PK, Weinberg J. Prenatal ethanol exposure: Changes in regional brain catecholamine content following stress. J Neurochem 1993; 61: 1907-1915.
216. Hofmann CE, Patyk IA, Weinberg J. Prenatal ethanol exposure: Sex differences in anxiety and anxiolytic response to a 5-HT1A agonist. Pharmacol Biochem Behav 2005; 82: 549-558.
217. Porsolt RD. Animal model of depression. Biomedicine 1979; 30: 139-140.
218. Cameron OG, Abelson JL, Young EA. Anxious and depressive disorders and their comorbidity: Effect on central nervous system noradrenergic function. Biol Psychiatry 2004; 56: 875-883.
219. Gorman JM. Comorbid depression and anxiety spectrum disorders. Depress Anxiety 1996; 4: 160-168.
220. Nemeroff CB. Comorbidity of mood and anxiety disorders: The rule, not the exception? Am J Psychiatry 2002; 159: 3-4.
221. Willner P. Validity, reliability and utility of the chronic mild stress model of depression: A 10-year review and evaluation. Psychopharmacology (Berl) 1997; 134: 319-329.