{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,9,26]],"date-time":"2026-09-26T09:00:35Z","timestamp":1790413235095,"version":"4.1.0"},"reference-count":57,"publisher":"Oxford University Press (OUP)","issue":"5","license":[{"start":{"date-parts":[[2020,3,14]],"date-time":"2020-03-14T00:00:00Z","timestamp":1584144000000},"content-version":"vor","delay-in-days":0,"URL":"http:\/\/www.nationalarchives.gov.uk\/doc\/open-government-licence\/version\/2\/"}],"funder":[{"DOI":"10.13039\/100000002","name":"National Institutes of Health","doi-asserted-by":"publisher","award":["AA019443"],"award-info":[{"award-number":["AA019443"]}],"id":[{"id":"10.13039\/100000002","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/100000027","name":"National Institute on Alcohol Abuse and Alcoholism","doi-asserted-by":"publisher","id":[{"id":"10.13039\/100000027","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":[],"published-print":{"date-parts":[[2020,5,27]]},"abstract":"<jats:title>Abstract<\/jats:title>\n               <jats:sec>\n                  <jats:title>Background<\/jats:title>\n                  <jats:p>Alcohol consumption during pregnancy is widespread and contributes to pediatric neurological defects, including hippocampal and neocortex dysfunction, causing cognitive deficits termed fetal alcohol spectrum disorders. However, the critical mechanisms underlying these brain abnormalities remain poorly described.<\/jats:p>\n               <\/jats:sec>\n               <jats:sec>\n                  <jats:title>Methods<\/jats:title>\n                  <jats:p>Using a postnatal ethanol exposure (PEE) animal model and pharmacological, epigenetic, synaptic plasticity-related and behavioral approaches, we discovered a novel persistent epigenetic mechanism of neurodegeneration in neonatal hippocampus and neocortex brain regions and of cognitive decline in adult animals.<\/jats:p>\n               <\/jats:sec>\n               <jats:sec>\n                  <jats:title>Results<\/jats:title>\n                  <jats:p>PEE, which activates caspase-3 (CC3, a neurodegeneration marker), enhanced histone deacetylase (HDAC1\u2013HDAC3) levels and reduced histone 3 (H3) and 4 (H4) acetylation (ac) in mature neurons. PEE repressed the expression of several synaptic plasticity genes, such as brain-derived neurotrophic factor, C-Fos, early growth response 1 (Egr1), and activity-regulated cytoskeleton-associated protein (Arc). Detailed studies on Egr1 and Arc expression revealed HDAC enrichment at their promoter regions. HDAC inhibition with trichostatin A (TSA) before PEE rescued H3ac\/H4ac levels and prevented CC3 formation. Antagonism\/null mutation of cannabinoid receptor type-1 (CB1R) before PEE to inhibit CC3 production prevented Egr1 and Arc loss via epigenetic events. TSA administration before PEE prevented postnatal ethanol-induced loss of Egr1 and Arc expression and neurobehavioral defects in adult mice via epigenetic remodeling. In adult mice, 3-day TSA administration attenuated PEE-induced behavioral defects.<\/jats:p>\n               <\/jats:sec>\n               <jats:sec>\n                  <jats:title>Conclusions<\/jats:title>\n                  <jats:p>These findings demonstrate that CB1R\/HDAC-mediated epigenetic remodeling disrupts gene expression and is a critical step in fetal alcohol spectrum disorder-associated cognitive decline but is reversed by restoration of histone acetylation in the brain.<\/jats:p>\n               <\/jats:sec>","DOI":"10.1093\/ijnp\/pyaa017","type":"journal-article","created":{"date-parts":[[2020,3,12]],"date-time":"2020-03-12T20:30:33Z","timestamp":1584045033000},"page":"324-338","source":"Crossref","is-referenced-by-count":36,"title":["Postnatal Ethanol Exposure Activates HDAC-Mediated Histone Deacetylation, Impairs Synaptic Plasticity Gene Expression and Behavior in Mice"],"prefix":"10.1093","volume":"23","author":[{"given":"Madhu","family":"Shivakumar","sequence":"first","affiliation":[{"name":"Division of Analytical Psychopharmacology, Nathan Kline Institute for Psychiatric Research, Orangeburg, New York"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Shivakumar","family":"Subbanna","sequence":"first","affiliation":[{"name":"Division of Analytical Psychopharmacology, Nathan Kline Institute for Psychiatric Research, Orangeburg, New York"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Vikram","family":"Joshi","sequence":"first","affiliation":[{"name":"Division of Analytical Psychopharmacology, Nathan Kline Institute for Psychiatric Research, Orangeburg, New York"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Balapal S","family":"Basavarajappa","sequence":"first","affiliation":[{"name":"Division of Analytical Psychopharmacology, Nathan Kline Institute for Psychiatric Research, Orangeburg, New York"},{"name":"New York State Psychiatric Institute, New York, New York"},{"name":"Department of Psychiatry, College of Physicians and Surgeons, Columbia University, New York, New York"},{"name":"Department of Psychiatry, New York University Langone Medical Center, New York, New York"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"286","published-online":{"date-parts":[[2020,3,14]]},"reference":[{"key":"2020052705595934100_CIT0001","first-page":"1550","article-title":"Effects of alcohol on histone deacetylase 2 (HDAC2) and the neuroprotective role of trichostatin A (TSA)","volume":"35","author":"Agudelo","year":"2011","journal-title":"Alcohol Clin Exp Res"},{"key":"2020052705595934100_CIT0002","doi-asserted-by":"crossref","first-page":"635","DOI":"10.1016\/j.alcohol.2012.03.005","article-title":"Alcohol-induced serotonergic modulation: the role of histone deacetylases","volume":"46","author":"Agudelo","year":"2012","journal-title":"Alcohol"},{"key":"2020052705595934100_CIT0003","doi-asserted-by":"crossref","first-page":"35444","DOI":"10.1074\/jbc.M112.394544","article-title":"Histone deacetylase-1 (HDAC1) is a molecular switch between neuronal survival and death","volume":"287","author":"Bardai","year":"2012","journal-title":"J Biol Chem"},{"key":"2020052705595934100_CIT0004","doi-asserted-by":"crossref","first-page":"456","DOI":"10.3390\/brainsci5040456","article-title":"Fetal alcohol spectrum disorder: potential role of endocannabinoids signaling","volume":"5","author":"Basavarajappa","year":"2015","journal-title":"Brain Sci"},{"key":"2020052705595934100_CIT0005","doi-asserted-by":"crossref","first-page":"73","DOI":"10.1016\/S0014-2999(03)01557-7","article-title":"Chronic ethanol inhibits the anandamide transport and increases extracellular anandamide levels in cerebellar granule neurons","volume":"466","author":"Basavarajappa","year":"2003","journal-title":"Eur J Pharmacol"},{"key":"2020052705595934100_CIT0006","doi-asserted-by":"crossref","first-page":"12","DOI":"10.3390\/brainsci6020012","article-title":"Epigenetic mechanisms in developmental alcohol-induced neurobehavioral deficits","volume":"6","author":"Basavarajappa","year":"2016","journal-title":"Brain Sciences"},{"key":"2020052705595934100_CIT0007","doi-asserted-by":"crossref","first-page":"1133","DOI":"10.1111\/acer.12082","article-title":"Gestational choline supplementation normalized fetal alcohol-induced alterations in histone modifications, DNA methylation, and proopiomelanocortin (POMC) gene expression in \u03b2-endorphin-producing POMC neurons of the hypothalamus","volume":"37","author":"Bekdash","year":"2013","journal-title":"Alcohol Clin Exp Res"},{"key":"2020052705595934100_CIT0008","doi-asserted-by":"crossref","first-page":"94","DOI":"10.1002\/(SICI)1098-1063(2000)10:1<94::AID-HIPO11>3.0.CO;2-T","article-title":"Effects of prenatal alcohol exposure on the hippocampus: spatial behavior, electrophysiology, and neuroanatomy","volume":"10","author":"Berman","year":"2000","journal-title":"Hippocampus"},{"key":"2020052705595934100_CIT0009","doi-asserted-by":"crossref","first-page":"147","DOI":"10.1002\/tera.1420440203","article-title":"Permanent neuronal deficits in rats exposed to alcohol during the brain growth spurt","volume":"44","author":"Bonthius","year":"1991","journal-title":"Teratology"},{"key":"2020052705595934100_CIT0010","doi-asserted-by":"crossref","first-page":"47","DOI":"10.1007\/BF02686117","article-title":"Distribution of histone deacetylases 1-11 in the rat brain","volume":"31","author":"Broide","year":"2007","journal-title":"J Mol Neurosci"},{"key":"2020052705595934100_CIT0011","doi-asserted-by":"crossref","first-page":"243","DOI":"10.1002\/dev.20178","article-title":"Neonatal alcohol exposure impairs acquisition of eyeblink conditioned responses during discrimination learning and reversal in weanling rats","volume":"49","author":"Brown","year":"2007","journal-title":"Dev Psychobiol"},{"key":"2020052705595934100_CIT0012","doi-asserted-by":"crossref","first-page":"132","DOI":"10.1038\/ncb2013","article-title":"Histone deacetylase and Cullin3-REN(KCTD11) ubiquitin ligase interplay regulates Hedgehog signalling through Gli acetylation","volume":"12","author":"Canettieri","year":"2010","journal-title":"Nat Cell Biol"},{"key":"2020052705595934100_CIT0013","author":"CDC","year":"2016"},{"key":"2020052705595934100_CIT0014","doi-asserted-by":"crossref","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":"2020052705595934100_CIT0015","doi-asserted-by":"crossref","first-page":"737","DOI":"10.1042\/bj20021321","article-title":"Histone deacetylases (HDACs): characterization of the classical HDAC family","volume":"370","author":"de Ruijter","year":"2003","journal-title":"Biochem J"},{"key":"2020052705595934100_CIT0016","doi-asserted-by":"crossref","first-page":"63","DOI":"10.1016\/j.semcdb.2017.09.023","article-title":"The Arc of cognition: signaling cascades regulating Arc and implications for cognitive function and disease","volume":"77","author":"Epstein","year":"2018","journal-title":"Semin Cell Dev Biol"},{"key":"2020052705595934100_CIT0017","doi-asserted-by":"crossref","first-page":"193","DOI":"10.1002\/ddrr.75","article-title":"Prevention of fetal alcohol spectrum disorders","volume":"15","author":"Floyd","year":"2009","journal-title":"Dev Disabil Res Rev"},{"key":"2020052705595934100_CIT0018","doi-asserted-by":"crossref","first-page":"300","DOI":"10.1111\/j.1530-0277.2000.tb04611.x","article-title":"Early postnatal ethanol exposure has long-term effects on the performance of male rats in a delayed matching-to-place task in the Morris water maze","volume":"24","author":"Girard","year":"2000","journal-title":"Alcohol Clin Exp Res"},{"key":"2020052705595934100_CIT0019","doi-asserted-by":"crossref","first-page":"378","DOI":"10.1016\/j.biopsych.2012.04.006","article-title":"Male germline transmits fetal alcohol adverse effect on hypothalamic proopiomelanocortin gene across generations","volume":"72","author":"Govorko","year":"2012","journal-title":"Biol Psychiatry"},{"key":"2020052705595934100_CIT0020","doi-asserted-by":"crossref","first-page":"E338","DOI":"10.1111\/j.1530-0277.2012.01886.x","article-title":"Prenatal alcohol exposure, attention-deficit\/hyperactivity disorder, and sluggish cognitive tempo","volume":"37","author":"Graham","year":"2013","journal-title":"Alcohol Clin Exp Res"},{"key":"2020052705595934100_CIT0021","doi-asserted-by":"crossref","first-page":"e19351","DOI":"10.1371\/journal.pone.0019351","article-title":"Alcohol exposure decreases CREB binding protein expression and histone acetylation in the developing cerebellum","volume":"6","author":"Guo","year":"2011","journal-title":"PLoS One"},{"key":"2020052705595934100_CIT0022","doi-asserted-by":"crossref","first-page":"e99467","DOI":"10.1371\/journal.pone.0099467","article-title":"Epigenetic regulations of immediate early genes expression involved in memory formation by the amyloid precursor protein of Alzheimer disease","volume":"9","author":"Hendrickx","year":"2014","journal-title":"PLoS One"},{"key":"2020052705595934100_CIT0023","doi-asserted-by":"crossref","first-page":"597","DOI":"10.1016\/j.nbd.2007.02.011","article-title":"Single alcohol exposure in early life damages hippocampal stem\/progenitor cells and reduces adult neurogenesis","volume":"26","author":"Ieraci","year":"2007","journal-title":"Neurobiol Dis"},{"key":"2020052705595934100_CIT0024","doi-asserted-by":"crossref","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":"2020052705595934100_CIT0025","doi-asserted-by":"crossref","first-page":"514","DOI":"10.1038\/s41386-018-0181-y","article-title":"CB1R regulates CDK5 signaling and epigenetically controls Rac1 expression contributing to neurobehavioral abnormalities in mice postnatally exposed to ethanol","volume":"44","author":"Joshi","year":"2019","journal-title":"Neuropsychopharmacology"},{"key":"2020052705595934100_CIT0026","doi-asserted-by":"crossref","first-page":"215","DOI":"10.1016\/j.vascn.2012.08.001","article-title":"Epigenetic histone acetylation and deacetylation mechanisms in experimental models of neurodegenerative disorders","volume":"66","author":"Konsoula","year":"2012","journal-title":"J Pharmacol Toxicol Methods"},{"key":"2020052705595934100_CIT0027","doi-asserted-by":"crossref","first-page":"e71455","DOI":"10.1371\/journal.pone.0071455","article-title":"Sonic hedgehog-induced histone deacetylase activation is required for cerebellar granule precursor hyperplasia in medulloblastoma","volume":"8","author":"Lee","year":"2013","journal-title":"Plos One"},{"key":"2020052705595934100_CIT0028","doi-asserted-by":"crossref","first-page":"605","DOI":"10.1016\/S0896-6273(02)00828-0","article-title":"Function and regulation of CREB family transcription factors in the nervous system","volume":"35","author":"Lonze","year":"2002","journal-title":"Neuron"},{"key":"2020052705595934100_CIT0029","doi-asserted-by":"crossref","first-page":"1403","DOI":"10.1111\/acer.13114","article-title":"Alcohol-induced developmental origins of adult-onset diseases","volume":"40","author":"Lunde","year":"2016","journal-title":"Alcohol Clin Exp Res"},{"key":"2020052705595934100_CIT0030","doi-asserted-by":"crossref","first-page":"291","DOI":"10.2217\/epi-2016-0163","article-title":"Epigenetics studies of fetal alcohol spectrum disorder: where are we now?","volume":"9","author":"Lussier","year":"2017","journal-title":"Epigenomics"},{"key":"2020052705595934100_CIT0031","doi-asserted-by":"crossref","first-page":"3","DOI":"10.1038\/npp.2012.124","article-title":"Histone regulation in the CNS: basic principles of epigenetic plasticity","volume":"38","author":"Maze","year":"2013","journal-title":"Neuropsychopharmacology"},{"key":"2020052705595934100_CIT0032","doi-asserted-by":"crossref","first-page":"1573","DOI":"10.1111\/j.1476-5381.2010.00873.x","article-title":"Guidelines for reporting experiments involving animals: the ARRIVE guidelines","volume":"160","author":"McGrath","year":"2010","journal-title":"Br J Pharmacol"},{"key":"2020052705595934100_CIT0033","doi-asserted-by":"crossref","first-page":"7876","DOI":"10.1073\/pnas.0902750106","article-title":"Histone deacetylases 1 and 2 control the progression of neural precursors to neurons during brain development","volume":"106","author":"Montgomery","year":"2009","journal-title":"Proc Natl Acad Sci U S A"},{"key":"2020052705595934100_CIT0034","doi-asserted-by":"crossref","first-page":"370","DOI":"10.1016\/j.ijdevneu.2013.02.005","article-title":"Unique functional roles for class I and class II histone deacetylases in central nervous system development and function","volume":"31","author":"Morris","year":"2013","journal-title":"Int J Dev Neurosci"},{"key":"2020052705595934100_CIT0035","doi-asserted-by":"crossref","first-page":"1527","DOI":"10.1387\/ijdb.092971cm","article-title":"Expression of class I histone deacetylases during chick and mouse development","volume":"54","author":"Murko","year":"2010","journal-title":"Int J Dev Biol"},{"key":"2020052705595934100_CIT0036","doi-asserted-by":"crossref","first-page":"429","DOI":"10.1111\/jnc.13006","article-title":"CB1-receptor knockout neonatal mice are protected against ethanol-induced impairments of DNMT1, DNMT3A, and DNA methylation","volume":"132","author":"Nagre","year":"2015","journal-title":"J Neurochem"},{"key":"2020052705595934100_CIT0037","doi-asserted-by":"crossref","first-page":"5069","DOI":"10.1073\/pnas.1017608108","article-title":"Tissue plasminogen activator is required for the development of fetal alcohol syndrome in mice","volume":"108","author":"Noel","year":"2011","journal-title":"Proc Natl Acad Sci U S A"},{"key":"2020052705595934100_CIT0038","doi-asserted-by":"crossref","first-page":"115","DOI":"10.1016\/S0165-3806(02)00279-1","article-title":"Ethanol-induced apoptotic neurodegeneration in the developing C57BL\/6 mouse brain","volume":"133","author":"Olney","year":"2002","journal-title":"Brain Res Dev Brain Res"},{"key":"2020052705595934100_CIT0039","doi-asserted-by":"crossref","first-page":"607","DOI":"10.1016\/j.nbd.2015.03.019","article-title":"Potential role of adolescent alcohol exposure-induced amygdaloid histone modifications in anxiety and alcohol intake during adulthood","volume":"82","author":"Pandey","year":"2015","journal-title":"Neurobiol Dis"},{"key":"2020052705595934100_CIT0040","doi-asserted-by":"crossref","first-page":"3652","DOI":"10.1073\/pnas.96.7.3652","article-title":"Factor-specific modulation of CREB-binding protein acetyltransferase activity","volume":"96","author":"Perissi","year":"1999","journal-title":"Proc Natl Acad Sci U S A"},{"key":"2020052705595934100_CIT0041","doi-asserted-by":"crossref","first-page":"73","DOI":"10.1007\/s11065-011-9166-x","article-title":"Fetal alcohol spectrum disorders: an overview","volume":"21","author":"Riley","year":"2011","journal-title":"Neuropsychol Rev"},{"key":"2020052705595934100_CIT0042","doi-asserted-by":"crossref","first-page":"662","DOI":"10.1021\/acschemneuro.6b00372","article-title":"Expression of HDAC2 but not HDAC1 transcript is reduced in dorsolateral prefrontal cortex of patients with schizophrenia","volume":"8","author":"Schroeder","year":"2017","journal-title":"ACS Chem Neurosci"},{"key":"2020052705595934100_CIT0043","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1007\/s12031-014-0461-x","article-title":"Histone deacetylase inhibitor, trichostatin A, improves learning and memory in high-fat diet-induced cognitive deficits in mice","volume":"56","author":"Sharma","year":"2015","journal-title":"J Mol Neurosci"},{"key":"2020052705595934100_CIT0044","doi-asserted-by":"crossref","first-page":"5786","DOI":"10.1073\/pnas.96.10.5786","article-title":"Altered gene expression in striatal projection neurons in CB1 cannabinoid receptor knockout mice","volume":"96","author":"Steiner","year":"1999","journal-title":"Proc Natl Acad Sci U S A"},{"key":"2020052705595934100_CIT0045","doi-asserted-by":"crossref","first-page":"34","DOI":"10.1016\/j.expneurol.2014.07.003","article-title":"Pre-administration of G9a\/GLP inhibitor during synaptogenesis prevents postnatal ethanol-induced LTP deficits and neurobehavioral abnormalities in adult mice","volume":"261","author":"Subbanna","year":"2014","journal-title":"Exp Neurol"},{"key":"2020052705595934100_CIT0046","doi-asserted-by":"crossref","first-page":"230","DOI":"10.1016\/j.neuroscience.2018.07.011","article-title":"Activity-dependent signaling and epigenetic abnormalities in mice exposed to postnatal ethanol","volume":"392","author":"Subbanna","year":"2018","journal-title":"Neuroscience"},{"key":"2020052705595934100_CIT0047","doi-asserted-by":"crossref","first-page":"45","DOI":"10.3389\/fnmol.2018.00045","article-title":"CB1R-mediated activation of caspase-3 causes epigenetic and neurobehavioral abnormalities in postnatal ethanol-exposed mice","volume":"11","author":"Subbanna","year":"2018","journal-title":"Front Mol Neurosci"},{"key":"2020052705595934100_CIT0048","doi-asserted-by":"crossref","first-page":"422","DOI":"10.1016\/j.neuroscience.2013.11.043","article-title":"Ethanol induced acetylation of histone at G9a exon1 and G9a-mediated histone H3 dimethylation leads to neurodegeneration in neonatal mice","volume":"258","author":"Subbanna","year":"2014","journal-title":"Neuroscience"},{"key":"2020052705595934100_CIT0049","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1093\/ijnp\/pyu028","article-title":"Ethanol exposure induces neonatal neurodegeneration by enhancing CB1R Exon1 histone H4K8 acetylation and up-regulating CB1R function causing neurobehavioral abnormalities in adult mice","volume":"18","author":"Subbanna","year":"2015","journal-title":"Int J Neuropsychopharmacol"},{"key":"2020052705595934100_CIT0050","doi-asserted-by":"crossref","first-page":"6350","DOI":"10.1523\/JNEUROSCI.3786-12.2013","article-title":"Anandamide-CB1 receptor signaling contributes to postnatal ethanol-induced neonatal neurodegeneration, adult synaptic and memory deficits","volume":"33","author":"Subbanna","year":"2013","journal-title":"J Neurosci"},{"key":"2020052705595934100_CIT0051","doi-asserted-by":"crossref","first-page":"475","DOI":"10.1016\/j.nbd.2013.01.022","article-title":"G9a-mediated histone methylation regulates ethanol-induced neurodegeneration in the neonatal mouse brain","volume":"54","author":"Subbanna","year":"2013","journal-title":"Neurobiol Dis"},{"key":"2020052705595934100_CIT0052","first-page":"1501","article-title":"Intraneuronal amyloid beta accumulation disrupts hippocampal CRTC1-dependent gene expression and cognitive function in a rat model of Alzheimer disease","volume":"27","author":"Wilson","year":"2017","journal-title":"Cereb Cortex"},{"key":"2020052705595934100_CIT0053","doi-asserted-by":"crossref","first-page":"457","DOI":"10.1111\/jnc.12210","article-title":"Early life stress-induced histone acetylations correlate with activation of the synaptic plasticity genes Arc and Egr1 in the mouse hippocampus","volume":"125","author":"Xie","year":"2013","journal-title":"J Neurochem"},{"key":"2020052705595934100_CIT0054","doi-asserted-by":"crossref","first-page":"313","DOI":"10.1017\/S1461145713001144","article-title":"Reversal of deficits in dendritic spines, BDNF and Arc expression in the amygdala during alcohol dependence by HDAC inhibitor treatment","volume":"17","author":"You","year":"2014","journal-title":"Int J Neuropsychopharmacol"},{"key":"2020052705595934100_CIT0055","doi-asserted-by":"crossref","first-page":"60","DOI":"10.1016\/j.expneurol.2017.10.020","article-title":"Sulforaphane restores acetyl-histone H3 binding to Bcl-2 promoter and prevents apoptosis in ethanol-exposed neural crest cells and mouse embryos","volume":"300","author":"Yuana","year":"2018","journal-title":"Exp Neurol"},{"key":"2020052705595934100_CIT0056","doi-asserted-by":"crossref","first-page":"24","DOI":"10.1038\/nrn1300","article-title":"Genesis of dendritic spines: insights from ultrastructural and imaging studies","volume":"5","author":"Yuste","year":"2004","journal-title":"Nat Rev Neurosci"},{"key":"2020052705595934100_CIT0057","doi-asserted-by":"crossref","first-page":"40","DOI":"10.1186\/s13072-015-0032-6","article-title":"Prenatal ethanol exposure alters adult hippocampal VGLUT2 expression with concomitant changes in promoter DNA methylation, H3K4 trimethylation and miR-467b-5p levels","volume":"8","author":"Zhang","year":"2015","journal-title":"Epigenetics Chromatin"}],"container-title":["International Journal of Neuropsychopharmacology"],"original-title":[],"language":"en","link":[{"URL":"http:\/\/academic.oup.com\/ijnp\/advance-article-pdf\/doi\/10.1093\/ijnp\/pyaa017\/33014635\/pyaa017.pdf","content-type":"application\/pdf","content-version":"am","intended-application":"syndication"},{"URL":"http:\/\/academic.oup.com\/ijnp\/article-pdf\/23\/5\/324\/33314640\/pyaa017.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"syndication"},{"URL":"http:\/\/academic.oup.com\/ijnp\/article-pdf\/23\/5\/324\/33314640\/pyaa017.pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2020,5,27]],"date-time":"2020-05-27T10:00:32Z","timestamp":1590573632000},"score":1,"resource":{"primary":{"URL":"https:\/\/academic.oup.com\/ijnp\/article\/23\/5\/324\/5805189"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2020,3,14]]},"references-count":57,"journal-issue":{"issue":"5","published-print":{"date-parts":[[2020,5,27]]}},"URL":"https:\/\/doi.org\/10.1093\/ijnp\/pyaa017","relation":{},"ISSN":["1461-1457","1469-5111"],"issn-type":[{"value":"1461-1457","type":"print"},{"value":"1469-5111","type":"electronic"}],"subject":[],"published-other":{"date-parts":[[2020,5]]},"published":{"date-parts":[[2020,3,14]]}}}