Animal models of fetal alcohol spectrum disorders: Impact of the social environment

Developmental Disabilities Research Reviews

Volumn 15, Issue 3, 2009, Pages 200-208

  Kelly, Sandra J ^a   Goodlett, Charles R ^b   Hannigan, John H ^c  

^a UNIVERSITY OF SOUTH CAROLINA   (United States)

^b INDIANA UNIVERSITY   (United States)

^c WAYNE STATE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Environmental enrichment; Epigenetics; Fetal alcohol spectrum disorder; Maternal; Rat; Social behavior; Voluntary exercise

Indexed keywords

ALCOHOL;

DEVELOPMENTAL DISORDER; EMBRYO DEVELOPMENT; EMOTIONAL STRESS; EPIGENETICS; EXPERIENCE; EXPERIMENTAL MODEL; FETAL ALCOHOL SPECTRUM DISORDER; FETUS DISEASE; LIFESPAN; MATERNAL BEHAVIOR; MATERNAL CARE; NONHUMAN; PRENATAL EXPOSURE; PRIORITY JOURNAL; PROGENY; REVIEW; SOCIAL BEHAVIOR; SOCIAL ENVIRONMENT; SOCIAL INTERACTION; SOCIAL PROBLEM; SOCIAL STRESS; TERATOGENESIS;

EID: 70149122592     PISSN: 19405510     EISSN: 10982779     Source Type: Journal    
DOI: 10.1002/ddrr.69     Document Type: Review

References (120)

1. Abel EL. 1995. An update on incidence of FAS: FAS is not an equal opportunity birth defect. Neurotoxicol Teratol 17:437-443.
2. Ackerman SH, Hofer MA, Weiner H. 1977. Some effects of a split litter cross foster design applied to 15 day old rat pups. Physiol Behav 19:433-436. (Pubitemid 8243266)
3. Barron S, Kelly SJ, Riley EP. 1991. Neonatal alcohol exposure alters suckling behavior in neonatal rat pups. Pharmacol Biochem Behav 39:423-427.
4. Barron S, Riley EP. 1985. Pup-induced maternal behavior in adult and juvenile rats exposed to alcohol prenatally. Alcohol Clin Exp Res 9:360-365. (Pubitemid 16247131)
5. Barron S, Segar TM, Yahr JS, Baseheart BJ, Willford JA. 2000. The effects of neonatal ethanol and/or cocaine exposure on isolationinduced ultrasonic vocalizations. Pharmacol Biochem Behav 67:1-9.
6. Bayer SA, Altman J, Russo RJ, et al. 1993. Timetables of neurogenesis in the human brain based on experimentally determined patterns in the rat. Neurotoxicology 14:83-144. (Pubitemid 23195769)
7. Berman RF, Hannigan JH. 2000. Effects of prenatal alcohol exposure on the hippocampus: spatial behavior, electrophysiology, and neuroanatomy. Hippocampus 10:94-110. (Pubitemid 30107595)
8. Berman RF, Hannigan JH, Sperry MA, et al. 1996. Prenatal alcohol exposure and the effects of environmental enrichment on hippocampal dendritic spine density. Alcohol 13:209-216.
9. Bertrand J, Floyd LL, Weber MK. 2005. Guidelines for identifying and referring persons with fetal alcohol syndrome. MMWR Recomm Rep 54:1-14.
10. Bishop S, Gahagan S, Lord C. 2007. Re-examining the core features of autism: a comparison of autism spectrum disorder and fetal alcohol spectrum disorder. J Child Psychol Psychiatry 48:1111-1121. (Pubitemid 350086158)
11. Blanchard BA, Riley EP, Hannigan JH. 1987. Deficits on a spatial navigation task following prenatal exposure to ethanol. Neurotoxicol Teratol 9:253-258.
12. Bogdarina I, Welham S, King PJ, et al. 2007. Epigenetic modification of the renin-angiotensin system in the fetal programming of hypertension. Circ Res 100:520-526. (Pubitemid 46673261)
13. Brain PF, Ajarem JS, Petkov VV. 1987. The utility of ethological assessments of murin agonistic interactions in behavioural teratology: the fetal alcohol syndrome. In: Olivier B, Mos J, Brain PF, editors. Ethopharmacology of agnoistic behaviour in animals and humans. Boston: Martinus Nijhoff Publishers. p 110-121.
14. Cameron NM, Shahrokh D, Del Corp A, Dhir SK, Szyf M, Champagne FA, Meaney MJ. 2008. Epigenetic programming of phenotypic variations in reproductive strategies in the rat through maternal care. J Neuroendocrinol 20:795-801. (Pubitemid 351858731)
15. Champagne FA, Meaney MJ. 2007. Transgenerational effects of social environment on variations in maternal care and behavioral response to novelty. Behav Neurosci 121: 1353-1363.
16. Chen JS, Driscoll CD, Riley EP. 1982. Ontogeny of suckling behavior in rats prenatally exposed to alcohol. Teratology 26:145-153. (Pubitemid 13203981)
17. Christie BR, Swann SE, Fox CJ, Froc D, Lieblich SE, Redila V, Webber A. 2005. Voluntary exercise rescues deficits in spatial memory and long-term potentiation in prenatal ethanol- exposed male rats. Eur J Neurosci 21: 1719-1726. (Pubitemid 40646617)
18. Church MW. 1987. Chronic in utero alcohol exposure affects auditory function in rats and humans. Alcohol 4:231-239.
19. Coggins TE, Timler GR, Olsang LB. 2007. A state of double jeopardy: impact of prenatal alcohol exposure and adverse environments on the social communicative abilities of school-age children with fetal alcohol spectrum disorder. Lang Speech Hear Serv Sch 38:117-127.
20. Cooney CA. 2007. Epigenetics-DNA-based mirror of our environment? Dis Markers 23: 121-137.
21. Cronise K, Marino MD, Tran TD, Kelly SJ. 2001. Critical periods for the effects of alcohol exposure on learning in rats. Behav Neurosci 115:138-145. (Pubitemid 32185157)
22. de Jong JG, van der Vegt BJ, Buwalda B, et al. 2005. Social environment determines the long-term effects of social defeat. Physiol Behav 84:87-95. (Pubitemid 40092069)
23. DeBeukelaer MM, Randall CL, Stroud DR. 1977. Renal anomalies in the fetal alcohol syndrome. J Pediatr 91:759-760. (Pubitemid 8207601)
24. Douglas LA, Varlinskaya EI, Spear LP. 2004. Rewarding properties of social interactions in adolescent and adult male and female rats: impact of social versus isolate housing of subjects and partners. Dev Psychobiol 45: 153-162.
25. Driscoll CD, Streissguth AP, Riley EP. 1990. Prenatal alcohol exposure: comparability of effects in humans and animal models. Neurotoxicol Teratol 12:231-237. (Pubitemid 20344187)
26. Fernandez K, Caul WF, Haenlein M, et al. 1983. Effects of prenatal alcohol on homing behavior, maternal responding, and open-field activity in rats. Neurobehav Toxicol Teratol 5: 351-356.
27. File SE, Seth P. 2003. A review of 25 years of the social interaction test. Eur J Pharmacol 463: 35-53. (Pubitemid 36205071)
28. Filgueiras CC, Krahe TE, Medina AE. 2009. Alcohol exposure during the third trimester equivalent reduces play behavior of juvenile ferrets. Alcohol Clin Exp Res 33:35a.
29. Fleming AS, Kraemer GW, Gonzalez A, et al. 2002. Mothering begets mothering: the transmission of behavior and its neurobiology across generations. Pharmacol Biochem Behav 73:61-75. (Pubitemid 34669905)
30. Fleming AS, O'Day DH, Kraemer GW. 1999. Neurobiology of mother-infant interactions: experience and central nervous system plasticity across development and generations. Neurosci Biobehav Rev 23:673-685.
31. Floyd RL, O'Connor MJ, Bertrand J, et al. 2006. Reducing adverse outcomes from prenatal alcohol exposure: a clinical plan of action. Alcohol Clin Exp Res 30:1271-1275. (Pubitemid 44114677)
32. Francis DD, Liu D, Caldji C, et al. 1999. Variations in maternal care and the development of stress responses. In: Yamashita H, Funder JW, Verbalis JG, Ueta Y, and Endo Y, editors. Control mechanisms of stress and emotion: neuroendocrine-based studies. New York: Elsevier Science B.V. p 11-28.
33. Frankel F, Paley B, Marquardt R, et al. 2006. Stimulants, neuroleptics, and children's friendship training for children with fetal alcohol spectrum disorders. J Child Adolesc Psychopharmacol 16:777-789. (Pubitemid 46175432)
34. Goodlett CR, Johnson RB. 1997. Neonatal binge ethanol exposure using intubation: timing and dose effects on place learning. Neurotoxicol Teratol 19:435-446.
35. Haley DW, Handmaker NS, Lowe J. 2006. Infant stress reactivity and prenatal alcohol exposure. Alcohol Clin Exp Res 30:2055-2064. (Pubitemid 44749533)
36. Ham J, Tronick E. 2006. Infant resilience to the stress of the still-face: infant and maternal psychophysiology are related. Ann N Y Acad Sci 1094:297-302,297-302. (Pubitemid 47092415)
37. Hannigan JH, Berman RF, Zajac CS. 1993. Environmental enrichment and the behavioral effects of prenatal exposure to alcohol in rats. Neurotoxicol Teratol 15:261-266. (Pubitemid 23233621)
38. Hannigan JH, O'Leary-Moore SK, Berman RF. 2007. Postnatal environmental or experiential amelioration of neurobehavioral effects of perinatal alcohol exposure in rats. Neurosci Biobehav Rev 31:202-211.
39. Hashimoto H, Saito TR, Furudate S, et al. 2001. Prolactin levels and maternal behavior induced by ultrasonic vocalizations of the rat pup. Exp Anim 50:307-312. (Pubitemid 33620394)
40. Haycock PC. 2009. Fetal alcohol spectrum disorders: the epigenetic perspective. Biol Reprod. DOI 10.1095/bioreprod.108.074682.
41. Haycock PC, Ramsay M. 2009. Exposure of mouse embryos to ethanol during preimplantation development: effect on DNA methylation in the H19 imprinting control region. Biol Reprod. DOI 10.1095/bioreprod. 108.074690.
42. Hofer MA, Brunelli SA, Masmela J, et al 1996. Maternal interactions prior to separation potentiate isolation-induced calling in rat pups. Behav Neurosci 110:1158-1167. (Pubitemid 26365814)
43. Hofer MA, Shair HN, Brunelli SA. 2002. Ultrasonic vocalizations in rat and mouse pups. Curr Protoc Neurosci Chapter 8: Unit 8.14.
44. Hoyme HE, May PA, Kalberg WO, et al. 2005. A practical clinical approach to diagnosis of fetal alcohol spectrum disorders: clarification of the 1996 institute of medicine criteria. Pediatrics 115:39-47. (Pubitemid 43046280)
45. Johnson TB, Stanton ME, Goodlett CR, et al. 2008. Eyeblink classical conditioning in the preweanling lamb. Behav Neurosci 122:722-729.
46. Kehoe P, Shoemaker WJ. 1991. Opioid-dependent behavior in infant rats: effects of prenatal exposure to ethanol. Pharmacol Biochem Behav 39:389-394.
47. Kelly SJ, Day N, Streissguth AP. 2000. Effects of prenatal alcohol exposure on social behavior in humans and other species. Neurotoxicol Teratol 22:143-149. (Pubitemid 30176070)
48. Kelly SJ, Dillingham RR. 1994. Sexually dimorphic effects of perinatal alcohol exposure on social interactions and amygdala DNA and DOPAC concentrations. Neurotoxicol Teratol 16:377-384.
49. Kelly SJ, Tran TD. 1997. Alcohol exposure during development alters social recognition and social communication in rats. Neurotoxicol Teratol 19:383-389. (Pubitemid 27404670)
50. Kleinfeld J, Wescott S. 1993. Fantastic antone succeeds: experiences in educating children with fetal alcohol syndrome. Anchorage: University of Alaska Press.
51. Klintsova AY, Cowell RM, Swain RA, et al. 1998. Therapeutic effects of complex motor training on motor performance deficits induced by neonatal binge-like alcohol exposure in rats. I. Behavioral results. Brain Res 800:48-61.
52. Klintsova AY, Helfer JL, Calizo LH, et al. 2007. Persistent impairment of hippocampal neurogenesis in young adult rats following early postnatal alcohol exposure. Alcohol Clin Exp Res 31:2073-2082.
53. Klintsova AY, Scamra C, Hoffman M, et al. 2002. Therapeutic effects of complex motor training on motor performance deficits induced by neonatal binge-like alcohol exposure in rats. II. A quantitative stereological study of synaptic plasticity in female rat cerebellum. Brain Res 937:83-93.
54. Kodituwakku PW. 2007. Defining the behavioral phenotype in children with fetal alcohol spectrum disorders: a review. Neurosci Biobehav Rev 31:192-201. (Pubitemid 46074142)
55. Kršiak M, Elis J, Pöschlová N, Mašek K. 1977. Increased aggressiveness and lower brain serotonin levels in offspring of mice given alcohol during gestation. J Stud Alcohol 38:1696-1704. (Pubitemid 8203861)
56. Lam MK, Homewood J, Taylor AJ, et al. 2000. Second generation effects of maternal alcohol consumption during pregnancy in rats. Prog Neuropsychopharmacol Biol Psychiatry 24:619-631. (Pubitemid 30419084)
57. Leasure JL, Decker L. 2009. Social isolation prevents exercise-induced proliferation of hippocampal progenitor cells in female rats. Hippocampus. DOI 10.1002/hipo.20563.
58. Leuner B, Gould E, Shors TJ. 2006. Is there a link between adult neurogenesis and learning? Hippocampus 16:216-224.
59. Lugo JN Jr, Marino MD, Gass JT, et al. 2006. Ethanol exposure during development reduces resident aggression and testosterone in rats. Physiol Behav 87:330-337.
60. Maier SE, Chen WJ, Miller JA, et al. 1997. Fetal alcohol exposure and temporal vulnerability regional differences in alcohol-induced microencephaly as a function of the timing of binge-like alcohol exposure during rat brain development. Alcohol Clin Exp Res 21:1418-1428.
61. Maier SE, Miller JA, Blackwell JM, et al. 1999. Fetal alcohol exposure and temporal vulnerability: regional differences in cell loss as a function of the timing of binge-like alcohol exposure during brain development. Alcohol Clin Exp Res 23:726-734.
62. Marino MD, Cronise K, Lugo JN Jr, Kelly SJ. 2002. Ultrasonic vocalizations and maternalinfant interactions in a rat model of fetal alcohol syndrome. Dev Psychobiol 41:341-351. (Pubitemid 35403400)
63. May PA, Gossage JP. 2001. Estimating the prevalence of fetal alcohol syndrome. A summary. Alcohol Res Health 25:159-167. (Pubitemid 33708978)
64. May PA, Gossage JP, Marais AS, et al. 2007. The epidemiology of fetal alcohol syndrome and partial FAS in a South African community. Drug Alcohol Depend 88:259-271.
65. May PA, Gossage JP, Marais AS, et al. 2008. Maternal risk factors for fetal alcohol syndrome and partial fetal alcohol syndrome in South Africa: a third study. Alcohol Clin Exp Res 32:738-753. (Pubitemid 351589390)
66. McCann JC, Hudes M, Ames BN. 2006. An overview of evidence for a causal relationship between dietary availability of choline during development and cognitive function in offspring. Neurosci Biobehav Rev 30: 696-712. (Pubitemid 44294477)
67. McGee CL, Fryer SL, Bjorkquist OA, et al. 2008. Deficits in social problem solving in adolescents with prenatal exposure to alcohol. Am J Drug Alcohol Abuse 34:423-431.
68. McGowan PO, Sasaki A, D'Alessio AC, et al. 2009. Epigenetic regulation of the glucocorticoid receptor in human brain associates with childhood abuse. Nat Neurosci 12: 342-348.
69. Meaney MJ. 2001. Maternal care, gene expression, and the transmission of individual differences in stress reactivity across generations. Ann Rev Neurosci 24:1161-1192.
70. Miczek KA, Yap JJ, Covington HE III. 2008. Social stress, therapeutics and drug abuse: preclinical models of escalated and depressed intake. Pharmacol Ther 120:102-128.
71. Misanin JR, Zawacki DM, Drieger WG. 1977. Differential maternal behavior of the rat dam toward natural and foster pups: Implications for nutrition research. Bull Psychon Soc 10: 313-316.
72. Nash K, Rovet J, Greenbaum R, Fantus E, Nulman I, Koren G. 2006. Identifying the behavioural phenotype in fetal alcohol spectrum disorder: sensitivity, specificity and screening potential. Arch Womens Ment Health 9:181-186. (Pubitemid 43974453)
73. Ness JW, Franchina JJ. 1990. Effects of prenatal alcohol exposure on rat pups' ability to elicit retrieval behavior from dams. Dev Psychobiol 23:85-99.
74. Numan M, Sheehan TP. 1997. Neuroanatomical circuitry for mammalian maternal behavior. Ann NY Acad Sci 807:101-125. (Pubitemid 27135488)
75. O'Connor MJ, Frankel F, Paley B, et al. 2006. A controlled social skills training for children with fetal alcohol spectrum disorders. J Consult Clin Psychol 74:639-648. (Pubitemid 44199116)
76. O'Connor MJ, Kogan N, Findlay R. 2002. Prenatal alcohol exposure and attachment behavior in children. Alcohol Clin Exp Res 26: 1592-1602. (Pubitemid 35192322)
77. O'Connor MJ, Sigman M, Kasari C. 1992. Attachment behavior of infants exposed to alcohol prenatally: mediating effects of infant affect and mother-infant interaction. Dev Psychopathol 4:243-256.
78. O'Leary CM. 2004. Fetal alcohol syndrome: diagnosis, epidemiology, and developmental outcomes. J Paediatr Child Health 40:2-7.
79. O'Leary-Moore SK, McMechan AP, Mathison SN, et al. 2006a. Reversal learning after prenatal or early postnatal alcohol exposure in juvenile and adult rats. Alcohol 38:99-110.
80. Ouko LA, Shantikumar K, Knezovich J, et al. 2009. Effect of alcohol consumption on CpG methylation in the differentially methylated regions of H19 and IG-DMR in male gametes-implications for fetal alcohol spectrum disorders. Alcohol Clin Exp Res. DOI 10.111/j.1530-0277.2009.00993.x
81. Rasmussen C, Talwar V, Loomes C, et al. 2008. Brief report: lie-telling in children with fetal alcohol spectrum disorder. J Pediatr Psychol 33:220-225. (Pubitemid 351197734)
82. Redila VA, Olson AK, Swann SE, et al. 2006. Hippocampal cell proliferation is reduced following prenatal ethanol exposure but can be rescued with voluntary exercise. Hippocampus 16:305-311.
83. Rockwood GA, Riley EP. 1986. Suckling deficits in rat pups exposed to alcohol in utero. Teratology 33:145-151.
84. Rockwood GA, Riley EP. 1990. Nipple attachment behavior in rat pups exposed to alcohol in utero. Neurotoxicol Teratol 12: 383-389.
85. Ryan SH, Williams JK, Thomas JD. 2008. Choline supplementation attenuates learning deficits associated with neonatal alcohol exposure in the rat: effects of varying the timing of choline administration. Brain Res 1237:91-100.
86. Sampson PD, Streissguth AP, Bookstein FL, et al. 1997. Incidence of fetal alcohol syndrome and prevalence of alcohol-related neurodevelopmental disorder. Teratology 56:317-326.
87. Schneider ML, Moore CF, Kraemer GW, et al. 2002. The impact of prenatal stress, fetal alcohol exposure, or both on development: perspectives from a primate model. Psychoneuroendocrinology 27:285-298.
88. Schonfeld AM, Mattson SN, Riley EP. 2005. Moral maturity and delinquency after prenatal alcohol exposure. J Stud Alcohol 66: 545-554. (Pubitemid 41193162)
89. Schonfeld AM, Paley B, Frankel F, et al. 2006. Executive functioning predicts social skills following prenatal alcohol exposure. Child Neuropsychol 12:439-452. (Pubitemid 44343991)
90. Schonfeld AM, Paley B, Frankel F, et al. 2009. Behavioral regulation as a predictor of response to children's friendship training in children with fetal alcohol spectrum disorders. Clin Neuropsychol 23:428-445.
91. Shukla SD, Velazquez J, French SW, et al. 2008. Emerging role of epigenetics in the actions of alcohol. Alcohol Clin Exp Res 32: 1525-1534.
92. Sokol RJ, Delaney-Black V, Nordstrom B. 2003. Fetal alcohol spectrum disorder. JAMA 290: 2996-2999.
93. Spadoni AD, McGee CL, Fryer SL, et al. 2007. Neuroimaging and fetal alcohol spectrum disorders. Neurosci Biobehav Rev 31: 239-245. (Pubitemid 46074148)
94. Stanton ME, Goodlett CR. 1998. Neonatal ethanol exposure impairs eyeblink conditioning in weanling rats. Alcohol Clin Exp Res 22: 270-275.
95. Stranahan AM, Khalil D, Gould E. 2006. Social isolation delays the positive effects of running on adult neurogenesis. Nat Neurosci 9: 526-533.
96. Streissguth AP, Aase JM, Clarren SK, et al. 1991. Fetal alcohol syndrome in adolescents and adults. JAMA 265:1961-1967.
97. Streissguth AP, Bookstein FL, Barr HM, et al. 1998. A fetal alcohol behavior scale. Alcohol Clin Exp Res 22:325-333.
98. Subramanian M. 1992. Lactation and prolactin release in foster dams suckling prenatally ethanol exposed pups. Alcohol Clin Exp Res 16:891-894.
99. Thomas JD, Garrison M, O'Neill TM. 2004. Perinatal choline supplementation attenuates behavioral alterations associated with neonatal alcohol exposure in rats. Neurotoxicol Teratol 26:35-45. (Pubitemid 38299107)
100. Thomas JD, Goodlett CR, West JR. 1998a. Alcohol- induced Purkinje cell loss depends on developmental timing of alcohol exposure and correlates with motor performance. Brain Res Dev Brain Res 105:159-166.
101. Thomas JD, La Fiette MH, Quinn VR, et al. 2000. Neonatal choline supplementation ameliorates the effects of prenatal alcohol exposure on a discrimination learning task in rats. Neurotoxicol Teratol 22:703-711.
102. Thomas JD, Sather TM, Whinery LA. 2008. Voluntary exercise influences behavioral development in rats exposed to alcohol during the neonatal brain growth spurt. Behav Neurosci 122:1264-1273.
103. Thomas JD, Wasserman EA, West JR, et al. 1996. Behavioral deficits induced by bingelike exposure to alcohol in neonatal rats: importance of developmental timing and number of episodes. Dev Psychobiol 29:433-452.
104. Thomas SE, Kelly SJ, Mattson SN, et al. 1998b. 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 22:528-533.
105. Tran TD, Cronise K, Marino MD, et al. 2000. Critical periods for the effects of alcohol exposure on brain weight, body weight, activity, and investigation. Behav Brain Res 116: 99-110. (Pubitemid 30945546)
106. Tran TD, Kelly SJ. 2003. Critical periods for ethanol- induced cell loss in the hippocampal formation. Neurotoxicol Teratol 25:519-528.
107. Tran TD, Stanton ME, Goodlett CR. 2007. Binge-like ethanol exposure during the early postnatal period impairs eyeblink conditioning at short and long CS-US intervals in rats. Dev Psychobiol 49:589-605.
108. Valzelli L, Garattini S. 1972. Biochemical and behavioural changes induced by isolation in rats. Neuropharmacology 11:17-22.
109. van den Berg CL, Pijlman FTA, Koning HAM, et al. 1999a. Isolation changes the incentive value of sucrose and social behaviour in juvenile and adult rats. Behav Brain Res 106: 133-142.
110. van den Berg CL, Van Ree JM, Spruijt BM. 1999b. Sequential analysis of juvenile isolationinduced decreased social behavior in the adult rat. Physiol Behav 67:483-488.
111. Wainwright PE, Levesque S, Krempulec L, et al. 1993. Effects of environmental enrichment on cortical depth and Morris-maze performance in B6D2F2 mice exposed prenatally to ethanol. Neurotoxicol Teratol 15:11-20. (Pubitemid 23043228)
112. Weinberg J. 1988. Hyperresponsiveness to stress: differential effects of prenatal ethanol on males and females. Alcohol Clin Exp Res 12:647-652. (Pubitemid 19000771)
113. Weinberg J, Bezio S. 1987. Alcohol-induced changes in pituitary-adrenal activity during pregnancy. Alcohol Clin Exp Res 11: 274-280. (Pubitemid 18005372)
114. Weinberg J, Kim CK, Yu W. 1995. Early handling can attenuate adverse effects of fetal ethanol exposure. Alcohol 12:317-327.
115. Weinberg J, Sliwowska JH, Lan N, et al. 2008. Prenatal alcohol exposure: foetal programming, the hypothalamic-pituitary-adrenal axis and sex differences in outcome. J Neuroendocrinol 20:470-488.
116. West JR. 1987. Fetal alcohol-induced brain damage and the problem of determining temporal vulnerability: a review. Alcohol Drug Res 7:423-441.
117. Wilson JH, Kelly SJ, Wilson MA. 1996. Early postnatal alcohol exposure in rats: maternal behavior and estradiol levels. Physiol Behav 59:287-293.
118. Wongwitdecha N, Marsden CA. 1996. Social isolation increases aggressive behaviour and alters the effects of diazepam in the rat social interaction test. Behav Brain Res 75:27-32. (Pubitemid 26078011)
119. Zeisel SH. 2006. The fetal origins of memory: the role of dietary choline in optimal brain development. J Pediatr 149:S131-S136.
120. Zimmerberg B, Drucker PC, Weider JM. 1995. Differential behavioral effects of the neuroactive steroid allogprenanolone on neonatal rats prenatally exposed to alcohol. Pharmacol Biochem Behav 51:463-468.