{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,8,1]],"date-time":"2026-08-01T06:18:13Z","timestamp":1785565093850,"version":"3.56.0"},"reference-count":68,"publisher":"Frontiers Media SA","license":[{"start":{"date-parts":[[2018,9,4]],"date-time":"2018-09-04T00:00:00Z","timestamp":1536019200000},"content-version":"unspecified","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"content-domain":{"domain":["frontiersin.org"],"crossmark-restriction":true},"short-container-title":["Front. Behav. Neurosci."],"DOI":"10.3389\/fnbeh.2018.00200","type":"journal-article","created":{"date-parts":[[2018,9,4]],"date-time":"2018-09-04T04:28:29Z","timestamp":1536035309000},"update-policy":"https:\/\/doi.org\/10.3389\/crossmark-policy","source":"Crossref","is-referenced-by-count":17,"title":["Long-Lasting Effects of Prenatal Ethanol Exposure on Fear Learning and Development of the Amygdala"],"prefix":"10.3389","volume":"12","author":[{"given":"Olga O.","family":"Kozanian","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"David J.","family":"Rohac","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Niusha","family":"Bavadian","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Alex","family":"Corches","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Edward","family":"Korzus","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Kelly J.","family":"Huffman","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1965","published-online":{"date-parts":[[2018,9,4]]},"reference":[{"key":"B1","doi-asserted-by":"publisher","first-page":"122","DOI":"10.1111\/acer.12936","article-title":"The impact of prenatal ethanol exposure on neuroanatomical and behavioral development in mice","volume":"40","author":"Abbott","year":"2016","journal-title":"Alcohol. Clin. Exp. Res."},{"key":"B2","doi-asserted-by":"publisher","first-page":"2908","DOI":"10.1093\/cercor\/bhx168","article-title":"Prenatal ethanol exposure and neocortical development: a transgenerational model of FASD","volume":"28","author":"Abbott","year":"2018","journal-title":"Cereb. Cortex"},{"key":"B3","doi-asserted-by":"publisher","first-page":"1222","DOI":"10.1016\/s0140-6736(86)92234-8","article-title":"Fetal alcohol syndrome is now leading cause of mental retardation","volume":"328","author":"Abel","year":"1986","journal-title":"Lancet"},{"key":"B4","doi-asserted-by":"publisher","first-page":"351","DOI":"10.1016\/s0166-4328(02)00020-7","article-title":"Altered performance characteristics in cognitive tasks: comparisons of the albino ICR and CD1 mouse strain","volume":"133","author":"Adams","year":"2002","journal-title":"Behav. Brain Res."},{"key":"B5","doi-asserted-by":"publisher","first-page":"179","DOI":"10.1038\/nature15698","article-title":"Basomedial amygdala mediates top-down control of anxiety and fear","volume":"527","author":"Adhikari","year":"2015","journal-title":"Nature"},{"key":"B6","doi-asserted-by":"publisher","first-page":"15481","DOI":"10.1523\/JNEUROSCI.3410-11.2011","article-title":"The fear circuit revisited: contributions of the basal amygdala nuclei to conditioned fear","volume":"31","author":"Amano","year":"2011","journal-title":"J. Neurosci."},{"key":"B7","doi-asserted-by":"publisher","first-page":"148","DOI":"10.1111\/j.1469-8749.2001.tb00179.x","article-title":"Brain dysmorphology in individuals with severe prenatal alcohol exposure","volume":"43","author":"Archibald","year":"2001","journal-title":"Dev. Med. Child Neurol."},{"key":"B8","doi-asserted-by":"publisher","first-page":"1671","DOI":"10.1111\/j.1530-0277.2009.01004.x","article-title":"Magnetic resonance imaging outcomes from a comprehensive magnetic resonance study of children with fetal alcohol spectrum disorders","volume":"33","author":"Astley","year":"2009","journal-title":"Alcohol. Clin. Exp. Res."},{"key":"B9","doi-asserted-by":"publisher","first-page":"249","DOI":"10.1016\/0006-8993(77)90310-9","article-title":"The effect of ethanol chronically administered to preweanling rats on cerebellar development: a morphological study","volume":"119","author":"Bauer-Moffett","year":"1977","journal-title":"Brain Res."},{"key":"B10","doi-asserted-by":"publisher","first-page":"457","DOI":"10.1111\/j.1530-0277.2011.01644.x","article-title":"A limited access mouse model of prenatal alcohol exposure that produces long-lasting deficits in hippocampal-dependent learning and memory","volume":"35","author":"Brady","year":"2012","journal-title":"Alcohol. Clin. Exp. Res."},{"key":"B11","doi-asserted-by":"publisher","first-page":"540","DOI":"10.1037\/0012-1649.34.3.540","article-title":"Maternal drug use during pregnancy: are preterm and full-term infants affected differently?","volume":"34","author":"Brown","year":"1998","journal-title":"Dev. Psychol."},{"key":"B12","doi-asserted-by":"publisher","first-page":"239","DOI":"10.1016\/j.alcohol.2007.03.005","article-title":"Long-term effects of prenatal alcohol exposure on the size of the whisker representation in juvenile and adult rat barrel cortex","volume":"41","author":"Chappell","year":"2007","journal-title":"Alcohol"},{"key":"B13","doi-asserted-by":"publisher","first-page":"1096","DOI":"10.1542\/peds.105.5.1096","article-title":"Structural and functional brain integrity of fetal alcohol syndrome in nonretarded cases","volume":"105","author":"Clark","year":"2000","journal-title":"Pediatrics"},{"key":"B14","doi-asserted-by":"publisher","first-page":"67","DOI":"10.1016\/j.bandc.2010.08.013","article-title":"Memory and brain volume in adults prenatally exposed to alcohol","volume":"75","author":"Coles","year":"2011","journal-title":"Brain Cogn."},{"key":"B15","doi-asserted-by":"publisher","first-page":"836","DOI":"10.1523\/JNEUROSCI.19-02-00836.1999","article-title":"Reciprocal changes in the firing probability of lateral and central medial amygdala neurons","volume":"19","author":"Collins","year":"1999","journal-title":"J. Neurosci."},{"key":"B16","doi-asserted-by":"publisher","first-page":"1092","DOI":"10.1037\/0735-7044.112.5.1092","article-title":"Both pre- and posttraining excitotoxic lesions of the basolateral amygdala abolish the expression of olfactory and contextual fear conditioning","volume":"112","author":"Cousens","year":"1998","journal-title":"Behav. Neurosci."},{"key":"B17","doi-asserted-by":"publisher","first-page":"1489","DOI":"10.1111\/j.1530-0277.2010.01234.x","article-title":"Laboratory models available to study alcohol-induced organ damage and immune variations; choosing the appropriate model","volume":"34","author":"D\u2019Souza El-Guindy","year":"2010","journal-title":"Alcohol. Clin. Exp. Res."},{"key":"B18","doi-asserted-by":"crossref","first-page":"213","DOI":"10.1093\/oso\/9780198505013.003.0006","article-title":"The role of the amygdala in conditioned and unconditioned fear and anxiety","volume-title":"The Amygdala: A Functional Analysis","author":"Davis","year":"2000"},{"key":"B19","doi-asserted-by":"publisher","first-page":"e84","DOI":"10.1038\/tp.2012.12","article-title":"Prenatal exposure to cigarette smoke or alcohol and cerebellum volume in attention-deficit\/hyperactivity disorder and typical development","volume":"2","author":"de Zeeuw","year":"2012","journal-title":"Transl. Psychiatry"},{"key":"B20","doi-asserted-by":"publisher","first-page":"18893","DOI":"10.1523\/JNEUROSCI.3721-13.2013","article-title":"Prenatal ethanol exposure disrupts intraneocortical circuitry, cortical gene expression, and behavior in a mouse model of FASD","volume":"33","author":"El Shawa","year":"2013","journal-title":"J. Neurosci."},{"key":"B21","doi-asserted-by":"crossref","first-page":"177","DOI":"10.1007\/BF03001163","article-title":"Conditional and unconditional components of post-shock freezing","volume":"15","author":"Fanselow","year":"1980","journal-title":"Pavlov. J. Biol. Sci."},{"key":"B22","doi-asserted-by":"publisher","first-page":"358","DOI":"10.1016\/j.euroneuro.2005.11.005","article-title":"Cerebral metabolic consequences in the adult brain after neonatal excitotoxic lesions of the amygdala in rats","volume":"16","author":"Gerrits","year":"2006","journal-title":"Eur. Neuropsychopharmacol."},{"key":"B23","doi-asserted-by":"publisher","first-page":"394","DOI":"10.1177\/15353702-0323006-07","article-title":"Alcohol teratogenesis. Mechanism of damage and strategies for intervention","volume":"230","author":"Goodlett","year":"2005","journal-title":"Exp. Biol. Med."},{"key":"B24","doi-asserted-by":"publisher","first-page":"107","DOI":"10.1016\/0741-8329(90)90070-s","article-title":"A single day of alcohol exposure during the brain growth spurt induces brain weight restriction and cerebellar Purkinje cell loss","volume":"7","author":"Goodlett","year":"1990","journal-title":"Alcohol"},{"key":"B25","doi-asserted-by":"publisher","first-page":"1656","DOI":"10.1111\/j.1530-0277.2009.01003.x","article-title":"Social cognitive and emotion processing abilities of children with fetal alcohol spectrum disorders: a comparison with attention deficit hyperactivity disorder","volume":"33","author":"Greenbaum","year":"2009","journal-title":"Alcohol. Clin. Exp. Res."},{"key":"B26","doi-asserted-by":"publisher","first-page":"625","DOI":"10.1001\/archneur.1980.00500590049006","article-title":"Amygdaloid changes in aging and dementia","volume":"37","author":"Herzog","year":"1980","journal-title":"Arch. Neurol."},{"key":"B27","doi-asserted-by":"publisher","first-page":"465","DOI":"10.1016\/j.alcohol.2009.08.004","article-title":"Deficits in trace fear conditioning in a rat model of fetal alcohol exposure: dose-response and timing effects","volume":"43","author":"Hunt","year":"2009","journal-title":"Alcohol"},{"key":"B28","doi-asserted-by":"publisher","first-page":"1056","DOI":"10.1126\/science.287.5455.1056","article-title":"Ethanol-induced apoptotic neurodegeneration and fetal alcohol syndrome","volume":"287","author":"Ikonomidou","year":"2000","journal-title":"Science"},{"key":"B29","first-page":"89","article-title":"Environmental influences on neural plasticity, the limbic system, emotional development and attachment: a review","volume":"3","author":"Joseph","year":"1999","journal-title":"Child Psychiatry Hum. Dev."},{"key":"B30","doi-asserted-by":"publisher","first-page":"326","DOI":"10.1016\/j.peptides.2006.07.027","article-title":"Behavioral profiling on NPY in aggression and neuropsychiatric diseases","volume":"28","author":"Karl","year":"2007","journal-title":"Peptides"},{"key":"B31","doi-asserted-by":"publisher","first-page":"155","DOI":"10.1146\/annurev.neuro.23.1.155","article-title":"Emotion circuits in the brain","volume":"23","author":"LeDoux","year":"2000","journal-title":"Annu. Rev. Neurosci."},{"key":"B32","doi-asserted-by":"publisher","first-page":"285","DOI":"10.1016\/j.alcohol.2008.04.002","article-title":"Alcohol exposure during the first two trimesters-equivalent alters the development of corpus callosum projection neurons in the rat","volume":"42","author":"Livy","year":"2008","journal-title":"Alcohol"},{"key":"B33","doi-asserted-by":"publisher","first-page":"447","DOI":"10.1016\/s0892-0362(03)00030-8","article-title":"Fetal alcohol exposure and temporal vulnerability: effects of binge-like alcohol exposure on the developing rat hippocampus","volume":"25","author":"Livy","year":"2003","journal-title":"Neurotoxicol. Teratol."},{"key":"B34","doi-asserted-by":"publisher","first-page":"49","DOI":"10.1016\/s0741-8329(00)00133-6","article-title":"Regional differences in cell loss associated with binge-like alcohol exposure during the first two trimesters equivalent in the rat","volume":"23","author":"Maier","year":"2001","journal-title":"Alcohol"},{"key":"B35","doi-asserted-by":"publisher","first-page":"8696","DOI":"10.1523\/JNEUROSCI.19-19-08696.1999","article-title":"Neurotoxic basolateral amygdala lesions impair learning and memory but not the performance of conditioned fear in rats","volume":"19","author":"Maren","year":"1999","journal-title":"J. Neurosci."},{"key":"B36","doi-asserted-by":"publisher","first-page":"167","DOI":"10.1007\/s00221-005-2287-9","article-title":"Prenatal alcohol exposure alters the size, but not the pattern, of the whisker representation in neonatal rat barrel cortex","volume":"165","author":"Margret","year":"2005","journal-title":"Exp. Brain Res."},{"key":"B37","doi-asserted-by":"publisher","first-page":"279","DOI":"10.1111\/j.1530-0277.1998.tb03651.x","article-title":"A review of the neurobehavioral deficits in children with fetal alcohol syndrome or prenatal exposure to alcohol","volume":"22","author":"Mattson","year":"1998","journal-title":"Horm. Behav."},{"key":"B38","doi-asserted-by":"publisher","first-page":"176","DOI":"10.1002\/ddrr.68","article-title":"Prevalence and epidemiologic characteristics of FASD from various research methods with an emphasis on recent in-school studies","volume":"15","author":"May","year":"2009","journal-title":"Dev. Disabil. Res. Rev."},{"key":"B39","doi-asserted-by":"publisher","first-page":"31","DOI":"10.1016\/j.reprotox.2014.02.002","article-title":"Dietary intake, nutrition, and fetal alcohol spectrum disorders in the Western Cape Province of South Africa","volume":"46","author":"May","year":"2014","journal-title":"Reprod. Toxicol."},{"key":"B40","doi-asserted-by":"publisher","first-page":"281","DOI":"10.1016\/0306-4522(93)90156-a","article-title":"Localization of GABA-like immunoreactivity in the monkey amygdala","volume":"52","author":"McDonald","year":"1993","journal-title":"Neuroscience"},{"key":"B41","first-page":"46","article-title":"Brain imaging and fetal alcohol spectrum disorders","volume":"42","author":"McGee","year":"2006","journal-title":"Ann. Ist. Super. Sanita"},{"key":"B42","doi-asserted-by":"publisher","first-page":"122","DOI":"10.1038\/nrn728","article-title":"Parallels between cerebellum- and amygdala-dependent conditioning","volume":"3","author":"Medina","year":"2002","journal-title":"Nat. Rev. Neurosci."},{"key":"B43","doi-asserted-by":"publisher","first-page":"316","DOI":"10.1016\/0006-8993(88)90445-3","article-title":"Structural and metabolic alterations in rat cerebral cortex induced by prenatal exposure to ethanol","volume":"474","author":"Miller","year":"1988","journal-title":"Brain Res."},{"key":"B44","doi-asserted-by":"publisher","first-page":"23","DOI":"10.1038\/npp.2012.112","article-title":"DNA methylation and its basic function","volume":"38","author":"Moore","year":"2013","journal-title":"Neuropsychopharmacology"},{"key":"B45","doi-asserted-by":"publisher","first-page":"686","DOI":"10.1001\/archpsyc.63.6.686","article-title":"Amygdalar volume and behavioral development in autism","volume":"63","author":"Munson","year":"2006","journal-title":"Arch. Gen. Psychiatry"},{"key":"B46","doi-asserted-by":"publisher","first-page":"1404","DOI":"10.1111\/j.1530-0277.2011.01476.x","article-title":"Extensive deep gray matter volume reductions in children and adolescents with fetal alcohol spectrum disorders","volume":"35","author":"Nardelli","year":"2011","journal-title":"Alcohol. Clin. Exp. Res."},{"key":"B47","doi-asserted-by":"publisher","first-page":"1061","DOI":"10.1016\/0306-4522(93)90049-l","article-title":"Distribution of GABA immunoreactivity in the amygdaloid complex of the cat","volume":"57","author":"Par\u00e9","year":"","journal-title":"Neuroscience"},{"key":"B48","doi-asserted-by":"publisher","first-page":"1077","DOI":"10.1016\/0306-4522(93)90050-p","article-title":"The intercalated cell masses project to the central and medial nuclei of the amygdala in cats","volume":"57","author":"Par\u00e9","year":"","journal-title":"Neuroscience"},{"key":"B49","unstructured":"RasbandW. S. Bethesda, MDNational Institutes of HealthImageJ. U.S.1997"},{"key":"B51","doi-asserted-by":"publisher","first-page":"1198","DOI":"10.1111\/j.1530-0277.1995.tb01600.x","article-title":"Abnormalities of the corpus callosum in children prenatally exposed to alcohol","volume":"19","author":"Riley","year":"1995","journal-title":"Alcohol. Clin. Exp. Res."},{"key":"B50","doi-asserted-by":"publisher","first-page":"357","DOI":"10.1177\/15353702-0323006-03","article-title":"Fetal alcohol spectrum disorders: an overview with emphasis on changes in brain and behavior","volume":"230","author":"Riley","year":"2005","journal-title":"Exp. Biol. Med."},{"key":"B52","doi-asserted-by":"publisher","first-page":"920","DOI":"10.1002\/hbm.21260","article-title":"Regional brain volume reductions relate to facial dysmorphology and neurocognitive function in fetal alcohol spectrum disorders","volume":"33","author":"Roussotte","year":"2012","journal-title":"Hum. Brain Mapp."},{"key":"B53","doi-asserted-by":"publisher","first-page":"784","DOI":"10.1111\/j.1530-0277.1995.tb01583.x","article-title":"Exposure of neonatal rats to alcohol by vapor inhalation demonstrates specificity of microcephaly and Purkinje cell loss but not astrogliosis","volume":"19","author":"Ryabinin","year":"1995","journal-title":"Alcohol. Clin. Exp. Res."},{"key":"B54","doi-asserted-by":"publisher","first-page":"9570","DOI":"10.1523\/JNEUROSCI.19-21-09570.1999","article-title":"Auditory thalamus, dorsal hippocampus, basolateral amygdala and perirhinal cortex role in the consolidation of conditioned freezing to context and to acoustic conditioned stimulus in the rat","volume":"19","author":"Sacchetti","year":"1999","journal-title":"J. Neurosci."},{"key":"B55","doi-asserted-by":"publisher","first-page":"317","DOI":"10.1002\/(sici)1096-9926(199711)56:5<317::aid-tera5>3.0.co;2-u","article-title":"Incidence of fetal alcohol syndrome and prevalence of alcohol-related neurodevelopmental disorder","volume":"56","author":"Sampson","year":"1997","journal-title":"Teratology"},{"key":"B56","doi-asserted-by":"publisher","first-page":"352","DOI":"10.1002\/dev.21035","article-title":"Deficits in tract fear conditioning induced by Neonatal alcohol persist into adulthood in female rats","volume":"55","author":"Schreiber","year":"2013","journal-title":"Dev. Psychobiol."},{"key":"B57","doi-asserted-by":"publisher","first-page":"555","DOI":"10.1002\/ana.410320412","article-title":"Amygdala cell loss and atrophy in Alzheimer\u2019s disease","volume":"32","author":"Scott","year":"1992","journal-title":"Ann. Neurol."},{"key":"B58","doi-asserted-by":"publisher","first-page":"235","DOI":"10.1212\/WNL.57.2.235","article-title":"Mapping callosal morphology and cognitive correlates: effects of heavy prenatal alcohol exposure","volume":"57","author":"Sowell","year":"2001","journal-title":"Neurology"},{"key":"B59","volume-title":"Understanding the Occurrence of Secondary Disabilities in Clients with Fetal Alcohol Syndrome (FAS) and Fetal Alcohol Effects (FAE): Final Report.","author":"Streissguth","year":"1996"},{"key":"B60","doi-asserted-by":"publisher","first-page":"341","DOI":"10.1111\/j.1399-0004.2012.01843.x","article-title":"The early-life social environment and DNA methylation","volume":"81","author":"Szyf","year":"2012","journal-title":"Clin. Genet."},{"key":"B61","doi-asserted-by":"publisher","first-page":"2","DOI":"10.1038\/nn.3286","article-title":"How do environments talk to genes?","volume":"16","author":"Szyf","year":"","journal-title":"Nat. Neurosci."},{"key":"B62","doi-asserted-by":"publisher","first-page":"331","DOI":"10.1016\/j.jgg.2013.06.004","article-title":"DNA methylation, behavior and early life adversity","volume":"40","author":"Szyf","year":"","journal-title":"J. Genet. Genomics"},{"key":"B63","doi-asserted-by":"publisher","first-page":"1042","DOI":"10.15585\/mmwr.mm6437a3","article-title":"Alcohol use and binge drinking among women of childbearing age-United States 2011\u20132013","volume":"64","author":"Tan","year":"2015","journal-title":"Morb. Mortal. Wkly. Rep."},{"key":"B64","doi-asserted-by":"publisher","first-page":"10098","DOI":"10.1523\/JNEUROSCI.5004-12.2013","article-title":"Longitudinal MRI reveals altered trajectory of brain development during childhood and adolescence in fetal alcohol spectrum disorders","volume":"33","author":"Treit","year":"2013","journal-title":"J. Neurosci."},{"key":"B65","doi-asserted-by":"publisher","first-page":"394","DOI":"10.1101\/lm.036087.114","article-title":"Prefrontal consolidation supports the attainment of fear memory accuracy","volume":"21","author":"Vieira","year":"2014","journal-title":"Learn. Mem."},{"key":"B66","doi-asserted-by":"publisher","first-page":"151","DOI":"10.1006\/nlme.2000.3994","article-title":"Fear conditioning-induced alterations of phospholipase C-\u03b21a protein level and enzyme activity in rat hippocampal formation and medial frontal cortex","volume":"76","author":"Weeber","year":"2001","journal-title":"Neurobiol. Learn. Mem."},{"key":"B67","doi-asserted-by":"publisher","first-page":"51","DOI":"10.1016\/s0924-977x(00)00138-3","article-title":"Early amygdala damage in the rat as a model for neurodevelopmental psychopathological disorders","volume":"11","author":"Wolterink","year":"2001","journal-title":"Eur. Neuropsychopharmacol."},{"key":"B68","doi-asserted-by":"publisher","first-page":"607","DOI":"10.1038\/nrm2950","article-title":"Active DNA demethylation: many roads lead to Rome","volume":"11","author":"Wu","year":"2010","journal-title":"Nat. Rev. Mol. Cell Biol."}],"container-title":["Frontiers in Behavioral Neuroscience"],"original-title":[],"link":[{"URL":"https:\/\/www.frontiersin.org\/article\/10.3389\/fnbeh.2018.00200\/full","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2024,7,9]],"date-time":"2024-07-09T22:27:23Z","timestamp":1720564043000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.frontiersin.org\/article\/10.3389\/fnbeh.2018.00200\/full"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2018,9,4]]},"references-count":68,"alternative-id":["10.3389\/fnbeh.2018.00200"],"URL":"https:\/\/doi.org\/10.3389\/fnbeh.2018.00200","relation":{},"ISSN":["1662-5153"],"issn-type":[{"value":"1662-5153","type":"electronic"}],"subject":[],"published":{"date-parts":[[2018,9,4]]},"article-number":"200"}}