Persistent Interneuronopathy in the Prefrontal Cortex of Young Adult Offspring Exposed to Ethanol In Utero

Skorput, A. G. J.; Gupta, V. P.; Yeh, P. W. L.; Yeh, H. H.

doi:10.1523/jneurosci.1462-15.2015

Cited by 92Prenatal Substance Exposure EffectsNeurogenesis and neuroplasticity mechanismsNeuroscience and Neuropharmacology Research

Persistent Interneuronopathy in the Prefrontal Cortex of Young Adult Offspring Exposed to Ethanol In Utero

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Skorput, A. G. J., Gupta, V. P., Yeh, P. W. L., Yeh, H. H.·2015·Journal of Neuroscience

DOI 10.1523/jneurosci.1462-15.2015PMC PMC4524971

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Abstract

Gestational exposure to ethanol has been reported to alter the disposition of tangentially migrating GABAergic cortical interneurons, but much remains to be elucidated. Here we first established the migration of interneurons as a proximal target of ethanol by limiting ethanol exposure in utero to the gestational window when tangential migration is at its height. We then asked whether the aberrant tangential migration of GABAergic interneurons persisted as an enduring interneuronopathy in the medial prefrontal cortex (mPFC) later in the life of offspring prenatally exposed to ethanol. Time pregnant mice with Nkx2.1Cre/Ai14 embryos harboring tdTomato-fluorescent medial ganglionic eminence (MGE)-derived cortical GABAergic interneurons were subjected to a 3 day binge-type 5% w/w ethanol consumption regimen from embryonic day (E) 13.5-16.5, spanning the peak of corticopetal interneuron migration in the fetal brain. Our binge-type regimen increased the density of MGE-derived interneurons in the E16.5 mPFC. In young adult offspring exposed to ethanol in utero, this effect persisted as an increase in the number of mPFC layer V parvalbumin-immunopositive interneurons. Commensurately, patch-clamp recording in mPFC layer V pyramidal neurons uncovered enhanced GABA-mediated spontaneous and evoked synaptic transmission, shifting the inhibitory/excitatory balance toward favoring inhibition. Furthermore, young adult offspring exposed to the 3 day binge-type ethanol regimen exhibited impaired reversal learning in a modified Barnes maze, indicative of decreased PFC-dependent behavioral flexibility, and heightened locomotor activity in an open field arena. Our findings underscore that aberrant neuronal migration, inhibitory/excitatory imbalance, and thus interneuronopathy contribute to indelible abnormal cortical circuit form and function in fetal alcohol spectrum disorders. SIGNIFICANCE STATEMENT: The significance of this study is twofold. First, we demonstrate that a time-delimited binge-type ethanol exposure in utero during early gestation alters corticopetal tangential migration of GABAergic interneurons in the fetal brain. Second, our study is the first to integrate neuroanatomical, electrophysiological, and behavioral evidence that this "interneuronopathy" persists in the young adult offspring and contributes to enduring changes in (1) the distribution of parvalbumin-expressing GABAergic cortical interneurons in the medial prefrontal cortex, (2) GABA-mediated synaptic transmission that resulted in an inhibitory/excitatory synaptic imbalance, and (3) behavioral flexibility. These findings alert women of child-bearing age that fetal alcohol spectrum disorders can be rooted very early in fetal brain development, and reinforce evidence-based counseling against binge drinking even at the earliest stages of pregnancy.

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Structurally, the prefrontal cortical thickness is affected after prenatal alcohol exposure and it matures with a smaller number of excitatory neurons and more GABAergic ones, disrupting the excitatory/inhibitory balance severely.
“Structurally, the prefrontal cortical thickness is affected after prenatal alcohol exposure and it matures with a smaller number of excitatory neurons and more GABAergic ones disrupting the excitatory/inhibitory balance severely [319–321].”
From Development of prefrontal cortex (2022) · cites this paper as [319]
The Results section on GABAergic interneurons reports more PV-positive interneurons in the medial prefrontal cortex of young adult mice exposed to ethanol in utero. The section on inhibitory/excitatory imbalance reports enhanced inhibitory synaptic drive onto layer V pyramidal neurons. The passages do not establish altered prefrontal cortical thickness or a smaller number of excitatory neurons; those parts of the citing sentence are unsupported by this paper. (LLM, conf=0.88)
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The open field as a paradigm to measure the effects of drugs on anxiety-like behaviors: a review.
Prut, L., & Belzung, C. (2003) · European Journal of Pharmacology · doi:10.1016/s0014-2999(03)01272-x · Cited by 3,190 · see citing works
Globally optimal stitching of tiled 3D microscopic image acquisitions
Preibisch, S., Saalfeld, S., & Tomancak, P. (2009) · Bioinformatics · doi:10.1093/bioinformatics/btp184 · Cited by 2,452 · see citing works
Interneuron Migration from Basal Forebrain to Neocortex: Dependence on <i>Dlx</i> Genes
Anderson, S. A., Eisenstat, D. D., Shi, L., & Rubenstein, J. L. R. (1997) · Science · doi:10.1126/science.278.5337.474 · Cited by 1,462 · see citing works
Three groups of interneurons account for nearly 100% of neocortical GABAergic neurons
Rudy, B., Fishell, G., Lee, S., & Hjerling‐Leffler, J. (2011) · Developmental Neurobiology · doi:10.1002/dneu.20853 · Cited by 1,420 · see citing works
Translating developmental time across mammalian species
Clancy, B., Darlington, R. B., & Finlay, B. L. (2001) · Neuroscience · doi:10.1016/s0306-4522(01)00171-3 · Cited by 1,221 · see citing works
Inhibitory Interneuron Deficit Links Altered Network Activity and Cognitive Dysfunction in Alzheimer Model
Verret, L., Mann, E. O., Hang, G. B., Barth, A. M. I., Cobos, I., Ho, K., Devidze, N., Masliah, E., Kreitzer, A. C., Mody, I., et al. (2012) · Cell · doi:10.1016/j.cell.2012.02.046 · Cited by 1,216 · see citing works
Cortical parvalbumin interneurons and cognitive dysfunction in schizophrenia
Lewis, D. A., Curley, A. A., Glausier, J. R., & Volk, D. W. (2012) · Trends in Neurosciences · doi:10.1016/j.tins.2011.10.004 · Cited by 1,071 · see citing works
A long, remarkable journey: Tangential migration in the telencephalon
Marín, Ó., & Rubenstein, J. L. R. (2001) · Nature reviews. Neuroscience · doi:10.1038/35097509 · Cited by 1,050 · see citing works
The medial ganglionic eminence gives rise to a population of early neurons in the developing cerebral cortex
Lavdas, A. A., Grigoriou, M., Pachnis, V., & Parnavelas, J. G. (1999) · The Journal of Neuroscience · doi:10.1523/jneurosci.19-18-07881.1999 · Cited by 765 · see citing works
Origin of GABAergic neurons in the human neocortex
Letinić, K., Zoncu, R., & RAKIC, P. T. (2002) · Nature · doi:10.1038/nature00779 · Cited by 718 · see citing works
Fetal Alcohol Spectrum Disorders: An Overview
Riley, E. P., Infante, M. A., & Warren, K. R. (2011) · Neuropsychology Review · doi:10.1007/s11065-011-9166-x · Cited by 707 · see citing works
Synaptic integration in tuft dendrites of layer 5 pyramidal neurons: a new unifying principle
Larkum, M. E., Nevian, T., Sandler, M., Polsky, A., & Schiller, J. (2009) · Science · doi:10.1126/science.1171958 · Cited by 677 · see citing works
Inhibitory Postsynaptic Potentials Carry Synchronized Frequency Information in Active Cortical Networks
Hasenstaub, A. R., Shu, Y., Haider, B., Kraushaar, U., Duque, A., & McCormick, D. A. (2005) · Neuron · doi:10.1016/j.neuron.2005.06.016 · Cited by 654 · see citing works
Distinct cortical migrations from the medial and lateral ganglionic eminences
Anderson, S. A., Marín, Ó., Horn, C., Jennings, K., & Rubenstein, J. L. R. (2001) · Development · doi:10.1242/dev.128.3.353 · Cited by 651 · see citing works
Origins of Cortical Interneuron Subtypes
Xu, Q., Cobos, I., De La Cruz, E., Rubenstein, J. L., & Anderson, S. A. (2004) · The Journal of Neuroscience · doi:10.1523/jneurosci.5667-03.2004 · Cited by 639 · see citing works
Origin and Molecular Specification of Striatal Interneurons
Marín, Ó., Anderson, S. A., & Rubenstein, J. L. R. (2000) · Journal of Neuroscience · doi:10.1523/jneurosci.20-16-06063.2000 · Cited by 627 · see citing works
Fetal Alcohol Spectrum Disorders: An Overview with Emphasis on Changes in Brain and Behavior
Riley, E. P., & Petrenko, C. L. M. (2005) · Experimental Biology and Medicine · doi:10.1177/15353702-0323006-03 · Cited by 627 · see citing works
Common circuit defect of excitatory-inhibitory balance in mouse models of autism
Gogolla, N., LeBlanc, J. J., Quast, K. B., Südhof, T. C., Fagiolini, M., & Hensch, T. K. (2009) · Journal of Neurodevelopmental Disorders · doi:10.1007/s11689-009-9023-x · Cited by 610 · see citing works
Prevalence and Characteristics of Fetal Alcohol Spectrum Disorders
May, P. A., Baete, A., Russo, J., Elliott, A. J., Blankenship, J., Kalberg, W. O., Buckley, D. G., Brooks, M., Hasken, J. M., Abdul-Rahman, O. A., et al. (2014) · PEDIATRICS · doi:10.1542/peds.2013-3319 · Cited by 564 · see citing works
Fate mapping Nkx2.1‐lineage cells in the mouse telencephalon
Xu, Q., Tam, M., & Anderson, S. A. (2007) · The Journal of Comparative Neurology · doi:10.1002/cne.21529 · Cited by 560 · see citing works
The Contribution of the Medial Prefrontal Cortex, Orbitofrontal Cortex, and Dorsomedial Striatum to Behavioral Flexibility
RAGOZZINO, M. E. (2007) · Annals of the New York Academy of Sciences · doi:10.1196/annals.1401.013 · Cited by 482 · see citing works
Rapid Neocortical Dynamics: Cellular and Network Mechanisms
Haider, B., & McCormick, D. A. (2009) · Neuron · doi:10.1016/j.neuron.2009.04.008 · Cited by 441 · see citing works
Parvalbumin, somatostatin and cholecystokinin as chemical markers for specific GABAergic interneuron types in the rat frontal cortex
Kawaguchi, Y., & Kondo, S. (2002) · Journal of Neurocytology · doi:10.1023/a:1024126110356 · Cited by 395 · see citing works
The origin and migration of cortical neurones: new vistas
Parnavelas, J. G. (2000) · Trends in Neurosciences · doi:10.1016/s0166-2236(00)01553-8 · Cited by 393 · see citing works
Alcohol use and binge drinking among women of childbearing age — United States, 2011–2013
Tan, C. H., Denny, C. H., Cheal, N. E., Sniezek, J. E., & Kanny, D. (2015) · MMWR Morbidity and Mortality Weekly Report · doi:10.15585/mmwr.mm6437a3 · Cited by 378 · see citing works
Executive Functioning in Children With Heavy Prenatal Alcohol Exposure
Mattson, S. N., Goodman, A. M., Caine, C., Delis, D. C., & Riley, E. P. (1999) · Alcoholism Clinical and Experimental Research · doi:10.1111/j.1530-0277.1999.tb04077.x · Cited by 374 · see citing works
Executive Functioning and Working Memory in Fetal Alcohol Spectrum Disorder
Rasmussen, C. (2005) · Alcoholism Clinical and Experimental Research · doi:10.1097/01.alc.0000175040.91007.d0 · Cited by 374 · see citing works
Gamma rhythms link prefrontal interneuron dysfunction with cognitive inflexibility in Dlx5/6(+/-) mice
Cho, K. K. A., Hoch, R., Lee, A. T., Patel, T., Rubenstein, J. L. R., & Sohal, V. S. (2015) · Neuron · doi:10.1016/j.neuron.2015.02.019 · Cited by 329 · see citing works
Drinking patterns and alcohol-related birth defects.
Maier, S. E., & West, J. R. (2001) · PubMed Central · Cited by 326 · see citing works
Sensory Integration in Mouse Insular Cortex Reflects GABA Circuit Maturation
Gogolla, N., Takesian, A. E., Feng, G., Fagiolini, M., & Hensch, T. K. (2014) · Neuron · doi:10.1016/j.neuron.2014.06.033 · Cited by 310 · see citing works
The embryonic preoptic area is a novel source of cortical GABAergic interneurons
Gelman, D. M., Martini, F. J., Nóbrega-Pereira, S., Pierani, A., Kessaris, N., & Marín, O. (2009) · The Journal of Neuroscience · doi:10.1523/jneurosci.0604-09.2009 · Cited by 280 · see citing works
Postmitotic Nkx2-1 controls the migration of telencephalic interneurons by direct repression of guidance receptors
Nóbrega-Pereira, S., Kessaris, N., Du, T., Kimura, S., Anderson, S. A., & Marín, O. (2008) · Neuron · doi:10.1016/j.neuron.2008.07.024 · Cited by 256 · see citing works
Executive function deficits in children with fetal alcohol spectrum disorders (FASD) measured using the Cambridge Neuropsychological Tests Automated Battery (CANTAB)
Green, C. R., Mihic, A., Nikkel, S. M., Stade, B. C., Rasmussen, C., Munoz, D. P., & Reynolds, J. N. (2009) · Journal of Child Psychology and Psychiatry · doi:10.1111/j.1469-7610.2008.01990.x · Cited by 236 · see citing works
GABAergic Interneuron Lineages Selectively Sort into Specific Cortical Layers during Early Postnatal Development
Miyoshi, G., & Fishell, G. (2011) · Cerebral Cortex · doi:10.1093/cercor/bhq155 · Cited by 230 · see citing works
Chapter 3 The Developmental Integration of Cortical Interneurons into a Functional Network
Batista‐Brito, R., & Fishell, G. (2009) · Current Topics in Developmental Biology · doi:10.1016/s0070-2153(09)01203-4 · Cited by 223 · see citing works
Maturation of Layer V Pyramidal Neurons in the Rat Prefrontal Cortex: Intrinsic Properties and Synaptic Function
Zhang, Z. (2004) · Journal of Neurophysiology · doi:10.1152/jn.00855.2003 · Cited by 210 · see citing works
Distinct molecular pathways for development of telencephalic interneuron subtypes revealed through analysis of Lhx6 mutants
Zhao, Y., Flandin, P., Long, J. E., Cuesta, M. D., Westphal, H., & Rubenstein, J. L. R. (2008) · Journal of Comparative Neurology · doi:10.1002/cne.21772 · Cited by 207 · see citing works
Alcohol and the prefrontal cortex
Abernathy, K., Chandler, L. J., & Woodward, J. J. (2010) · International Review of Neurobiology · doi:10.1016/s0074-7742(10)91009-x · Cited by 196 · see citing works
A Triplet Repeat Expansion Genetic Mouse Model of Infantile Spasms Syndrome, Arx(GCG)10+7, with Interneuronopathy, Spasms in Infancy, Persistent Seizures, and Adult Cognitive and Behavioral Impairment
Price, M. G., Yoo, J. W., Burgess, D. L., Deng, F. M., Hrachovy, R. A., Frost, J. D., & Noebels, J. L. (2009) · Journal of Neuroscience · doi:10.1523/jneurosci.0915-09.2009 · Cited by 191 · see citing works
The effects of prenatal alcohol exposure on executive functioning.
Kodituwakku, P. W., Kalberg, W. O., & May, P. A. (2001) · PubMed Central · Cited by 183 · see citing works
Adolescent binge drinking increases expression of the danger signal receptor agonist HMGB1 and toll-like receptors in the adult prefrontal cortex
Vetreno, R. P., & Crews, F. T. (2012) · Neuroscience · doi:10.1016/j.neuroscience.2012.08.046 · Cited by 183 · see citing works
Lack of response inhibition in rats prenatally exposed to alcohol
Riley, E. P., Lochry, E. A., & Shapiro, N. R. (1979) · Psychopharmacology · doi:10.1007/bf00426034 · Cited by 179 · see citing works
Dlx1&2 and Mash1 Transcription Factors Control MGE and CGE Patterning and Differentiation through Parallel and Overlapping Pathways
Long, J. E., Cobos, I., Potter, G. B., & Rubenstein, J. L. R. (2009) · Cerebral Cortex · doi:10.1093/cercor/bhp045 · Cited by 178 · see citing works
Prenatal Alcohol Exposure Affects Frontal–Striatal BOLD Response During Inhibitory Control
Fryer, S. L., Tapert, S. F., Mattson, S. N., Paulus, M. P., Spadoni, A. D., & Riley, E. P. (2007) · Alcoholism Clinical and Experimental Research · doi:10.1111/j.1530-0277.2007.00443.x · Cited by 174 · see citing works
Development and specification of GABAergic cortical interneurons
Kelsom, C., & Lu, W. (2013) · Cell & Bioscience · doi:10.1186/2045-3701-3-19 · Cited by 171 · see citing works
X-Linked Lissencephaly With Abnormal Genitalia as a Tangential Migration Disorder Causing Intractable Epilepsy: Proposal for a New Term, “Interneuronopathy”
Kato, M., & Dobyns, W. B. (2005) · Journal of Child Neurology · doi:10.1177/08830738050200042001 · Cited by 159 · see citing works
Executive Functioning Predicts Social Skills Following Prenatal Alcohol Exposure
Schonfeld, A. M., Paley, B., Frankel, F., & O’Connor, M. J. (2006) · Child Neuropsychology · doi:10.1080/09297040600611338 · Cited by 159 · see citing works
Lhx6 and Lhx8 Coordinately Induce Neuronal Expression of Shh that Controls the Generation of Interneuron Progenitors
Flandin, P., Zhao, Y., Vogt, D., Jeong, J., Long, J., Potter, G., Westphal, H., & Rubenstein, J. L. R. (2011) · Neuron · doi:10.1016/j.neuron.2011.04.020 · Cited by 155 · see citing works
Ethanol Consumption during Early Pregnancy Alters the Disposition of Tangentially Migrating GABAergic Interneurons in the Fetal Cortex
Carlson, V. C. C., Yeh, P. W. L., Yanagawa, Y., Obata, K., & Yeh, H. H. (2008) · Journal of Neuroscience · doi:10.1523/jneurosci.5110-07.2008 · Cited by 140 · see citing works
Self-citation
The Effects of Prenatal Alcohol Exposure on Behavior: Rodent and Primate Studies
Schneider, M. L., Moore, C. F., & Adkins, M. M. (2011) · Neuropsychology Review · doi:10.1007/s11065-011-9168-8 · Cited by 139 · see citing works
Association of Attention Deficit Hyperactivity Disorder and Gestational Alcohol Exposure
Bhatara, V. S., Loudenberg, R., & Ellis, R. B. (2006) · Journal of Attention Disorders · doi:10.1177/1087054705283880 · Cited by 120 · see citing works
Tangential Migration in Neocortical Development
Jiménez, D., López‐Mascaraque, L., Valverde, F., & Carlos, J. (2002) · Developmental Biology · doi:10.1006/dbio.2002.0586 · Cited by 119 · see citing works
Assessment of spatial learning abilities of mice in a new circular maze
Koopmans, G. C., Blokland, A., VANNIEUWENHUIJZEN, P., & Prickaerts, J. (2003) · Physiology & Behavior · doi:10.1016/s0031-9384(03)00171-9 · Cited by 105 · see citing works
Validation of the fetal alcohol spectrum disorder (FASD) 4-Digit Diagnostic Code.
Astley, S. J. (2013) · PubMed · Cited by 105 · see citing works
Cortical Inhibitory Cell Types Differentially Form Intralaminar and Interlaminar Subnetworks withExcitatory Neurons
Otsuka, T., & Kawaguchi, Y. (2009) · Journal of Neuroscience · doi:10.1523/jneurosci.2219-09.2009 · Cited by 99 · see citing works
Optimization of apparatus design and behavioral measures for the assessment of visuo-spatial learning and memory of mice on the Barnes mazePreprint
O’Leary, T. P., & Brown, R. E. (2013) · Learning & Memory · doi:10.1101/lm.028076.112 · Cited by 81 · see citing works
Alcohol use and binge drinking among women of childbearing age--United States, 2006-2010.
(2012) · PubMed · Cited by 81 · see citing works
Spatio-temporal extension in site of origin for cortical calretinin neurons in primates
Hladnik, A., DÅ¾aja, D., Darmopil, S., Jovanov-MiloÅ¡eviÄ‡, N., & Petanjek, Z. (2014) · Frontiers in Neuroanatomy · doi:10.3389/fnana.2014.00050 · Cited by 72 · see citing works
Parvalbumin-Containing Chandelier and Basket Cell Boutons Have Distinctive Modes of Maturation in Monkey Prefrontal Cortex
Fish, K. N., Hoftman, G. D., Sheikh, W., Kitchens, M., & Lewis, D. A. (2013) · Journal of Neuroscience · doi:10.1523/jneurosci.0306-13.2013 · Cited by 72 · see citing works
Interneurons Are Necessary for Coordinated Activity During Reversal Learning in Orbitofrontal Cortex
Bissonette, G. B., Schoenbaum, G. M., Roesch, M. R., & Powell, E. M. (2014) · Biological Psychiatry · doi:10.1016/j.biopsych.2014.07.023 · Cited by 71 · see citing works
Prefrontal cognitive deficits in mice with altered cerebral cortical GABAergic interneurons
Bissonette, G. B., Bae, M. H., Suresh, T., Jaffe, D. E., & Powell, E. M. (2013) · Behavioural Brain Research · doi:10.1016/j.bbr.2013.10.051 · Cited by 61 · see citing works
Prenatal Ethanol Exposure Impairs Executive Function in Mice into Adulthood
Marquardt, K., Sigdel, R., Caldwell, K. K., & Brigman, J. L. (2014) · Alcoholism Clinical and Experimental Research · doi:10.1111/acer.12577 · Cited by 56 · see citing works
Effects of a metabotropic glutamate receptor 5 positive allosteric modulator, CDPPB, on spatial learning task performance in rodents
Fowler, S., Walker, J. M., Klakotskaia, D., Will, M. J., Serfözö, P. D., Simonyi, Á., & Schachtman, T. R. (2012) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2012.10.010 · Cited by 55 · see citing works
Prenatal ethanol exposure stimulates neurogenesis in hypothalamic and limbic peptide systems: Possible mechanism for offspring ethanol overconsumption
Chang, G., Karatayev, O., Liang, S., Barson, J. R., & LEIBOWITZ, S. F. (2012) · Neuroscience · doi:10.1016/j.neuroscience.2012.05.066 · Cited by 53 · see citing works
An fMRI study of behavioral response inhibition in adolescents with and without histories of heavy prenatal alcohol exposure
Ware, A. L., Infante, M. A., O’Brien, J. W., Tapert, S. F., Jones, K. L., Riley, E. P., & Mattson, S. N. (2014) · Behavioural Brain Research · doi:10.1016/j.bbr.2014.09.037 · Cited by 50 · see citing works
The role of the medial prefrontal cortex in the acquisition, retention, and reversal of a tactile visuospatial conditional discrimination task
Shaw, C. L., Watson, G. D. R., Hallock, H. L., Cline, K. M., & Griffin, A. L. (2012) · Behavioural Brain Research · doi:10.1016/j.bbr.2012.08.024 · Cited by 48 · see citing works
A developmental cell-type switch in cortical interneurons leads to a selective defect in cortical oscillations
Takada, N., Pi, H. J., Sousa, V. H., Waters, J., Fishell, G., Kepecs, Á., & Osten, P. (2014) · Nature Communications · doi:10.1038/ncomms6333 · Cited by 41 · see citing works
Long-Lasting Neural Circuit Dysfunction Following Developmental Ethanol Exposure
Sadrian, B., Wilson, D. A., & Saito, M. (2013) · Brain Sciences · doi:10.3390/brainsci3020704 · Cited by 39 · see citing works
Chronic Prenatal Ethanol Exposure and Increased Concentration of Fatty Acid Ethyl Esters in Meconium of Term Fetal Guinea Pig
Brien, J. F., Chan, D., Green, C. R., Iqbal, U. H., Gareri, J., Kobus, S. M., McLaughlin, B. E., Klein, J., Rao, C., Reynolds, J. N., et al. (2006) · Therapeutic Drug Monitoring · doi:10.1097/01.ftd.0000211819.35182.82 · Cited by 35 · see citing works
Late recognition of pregnancy as a predictor of adverse birth outcomes
Ayoola, A. B., Stommel, M., & Nettleman, M. D. (2009) · American Journal of Obstetrics and Gynecology · doi:10.1016/j.ajog.2009.05.011 · Cited by 35 · see citing works
The Effects of Physostigmine on Open‐Field Behavior in Rats Exposed to Alcohol Prenatally
Riley, E. P., Barron, S., Driscoll, C. D., & Hamlin, R. T. (1986) · Alcoholism Clinical and Experimental Research · doi:10.1111/j.1530-0277.1986.tb05613.x · Cited by 31 · see citing works
Mothers' Alcohol Consumption During Pregnancy: Effects on Spatial-Visual Reasoning in 14-Year-Old Children
Hunt, E. B., Streissguth, A. P., Kerr, B., & Olson, H. C. (1995) · Psychological Science · doi:10.1111/j.1467-9280.1995.tb00523.x · Cited by 16 · see citing works

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Harvey, R. E., Berkowitz, L. E., Hamilton, D. A., & Clark, B. J. (2019) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2019.09.018 · Cited by 37 · see citing works
Prenatal sevoflurane exposure causes neuronal excitatory/inhibitory imbalance in the prefrontal cortex and neurofunctional abnormality in rats
Zhao, T., Chen, Y., Sun, Z., Shi, Z., Qin, J., Lu, J., Li, C., Ma, D., Zhou, L., & Song, X. (2020) · Neurobiology of Disease · doi:10.1016/j.nbd.2020.105121 · Cited by 38 · see citing works
Prenatal alcohol exposure is a leading cause of interneuronopathy in humans
Marguet, F., Friocourt, G., Brosolo, M., Sauvestre, F., Marcorelles, P., Lesueur, C., Marret, S., Gonzalez, B. J., & Laquerrière, A. (2020) · Acta Neuropathologica Communications · doi:10.1186/s40478-020-01089-z · Cited by 36 · see citing works
Prenatal Environment That Affects Neuronal Migration
Hwang, H. M., Ku, R. Y., & Hashimoto‐Torii, K. (2019) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2019.00138 · Cited by 35 · see citing works
Alcohol, flexible behavior, and the prefrontal cortex: Functional changes underlying impaired cognitive flexibility
Nippert, K. E., Rowland, C. P., Vazey, E. M., & Moorman, D. E. (2024) · Neuropharmacology · doi:10.1016/j.neuropharm.2024.110114 · Cited by 34 · see citing works
GABAergic Transmission during Brain Development: Multiple Effects at Multiple Stages
Kirmse, K., Hübner, C. A., Isbrandt, D., Witte, O. W., & Holthoff, K. (2017) · The Neuroscientist · doi:10.1177/1073858417701382 · Cited by 35 · see citing works
Early-life exposure to caffeine affects the construction and activity of cortical networks in mice
Fazeli, W., Zappettini, S., Marguet, S. L., Grendel, J., Esclapez, M., Bernard, C., & Isbrandt, D. (2017) · Experimental Neurology · doi:10.1016/j.expneurol.2017.05.013 · Cited by 32 · see citing works
Ethanol Exposure In Utero Disrupts Radial Migration and Pyramidal Cell Development in the Somatosensory Cortex
Delatour, L. C., Yeh, P. W. L., & Yeh, H. H. (2018) · Cerebral Cortex · doi:10.1093/cercor/bhy094 · Cited by 34 · see citing works
Self-citation
Cell-type and fetal-sex-specific targets of prenatal alcohol exposure in developing mouse cerebral cortex
Salem, N. A., Mahnke, A. H., Konganti, K., Hillhouse, A., & Miranda, R. C. (2021) · iScience · doi:10.1016/j.isci.2021.102439 · Cited by 33 · see citing works
Developmental ethanol exposure-induced sleep fragmentation predicts adult cognitive impairment
Wilson, D. A., Masiello, K., Lewin, M. P., Hui, M., Smiley, J. F., & Saito, M. (2016) · Neuroscience · doi:10.1016/j.neuroscience.2016.02.020 · Cited by 34 · see citing works
DNA Methylation program in normal and alcohol-induced thinning cortex
Öztürk, N. C., Resendiz, M., Öztürk, H., & Zhou, F. (2017) · Alcohol · doi:10.1016/j.alcohol.2017.01.006 · Cited by 32 · see citing works
Pre-implantation alcohol exposure induces lasting sex-specific DNA methylation programming errors in the developing forebrain
Legault, L., Doiron, K., Breton‐Larrivée, M., Langford‐Avelar, A., Lemieux, A., Caron, M., Jerome‐Majewska, L. A., Sinnett, D., & McGraw, S. (2021) · Clinical Epigenetics · doi:10.1186/s13148-021-01151-0 · Cited by 29 · see citing works
Interneuron odyssey: molecular mechanisms of tangential migration
Toudji, I., Toumi, A., Chamberland, É., & Rossignol, E. (2023) · Frontiers in Neural Circuits · doi:10.3389/fncir.2023.1256455 · Cited by 29 · see citing works
NADPH Oxidase Isoform 2 (NOX2) Is Involved in Drug Addiction Vulnerability in Progeny Developmentally Exposed to Ethanol
Contreras, M. L., de la Fuente-Ortega, E., Vargas-Robert, S., Muñoz, D. C., Goic, C. A., & Haeger, P. A. (2017) · Frontiers in Neuroscience · doi:10.3389/fnins.2017.00338 · Cited by 29 · see citing works
Developmental ethanol exposure alters the morphology of mouse prefrontal neurons in a layer-specific manner
Louth, E. L., Luctkar, H. D., Heney, K. A., & Bailey, C. D. C. (2017) · Brain Research · doi:10.1016/j.brainres.2017.10.005 · Cited by 29 · see citing works
An Overview of the Mechanisms of Abnormal GABAergic Interneuronal Cortical Migration Associated with Prenatal Ethanol Exposure
Shenoda, B. B. (2017) · Neurochemical Research · doi:10.1007/s11064-016-2169-5 · Cited by 28 · see citing works
Chromatin architecture in addiction circuitry identifies risk genes and potential biological mechanisms underlying cigarette smoking and alcohol use traits
Sey, N. Y. A., Hu, B., Iskhakova, M., Lee, S., Sun, H., Shokrian, N., Hutta, G. B., Marks, J. A., Quach, B. C., Johnson, E. O., et al. (2022) · Molecular Psychiatry · doi:10.1038/s41380-022-01558-y · Cited by 27 · see citing works
Moderate prenatal alcohol exposure reduces parvalbumin expressing GABAergic interneurons in the dorsal hippocampus of adult male and female rat offspring
Madden, J. T., Thompson, S. M., Magcalas, C. M., Wagner, J. L., Hamilton, D. A., Savage, D. D., Clark, B. J., & Pentkowski, N. S. (2019) · Neuroscience Letters · doi:10.1016/j.neulet.2019.134700 · Cited by 26 · see citing works
An overview of current advances in perinatal alcohol exposure and pathogenesis of fetal alcohol spectrum disorders
Zeng, X., Cai, Y., Wu, M., Chen, H., Sun, M., & Yang, H. (2024) · Journal of Neurodevelopmental Disorders · doi:10.1186/s11689-024-09537-w · Cited by 25 · see citing works
Activation of the anterior cingulate cortex ameliorates anxiety in a preclinical model of fetal alcohol spectrum disorders
Hwang, H. M., & Hashimoto‐Torii, K. (2022) · Translational Psychiatry · doi:10.1038/s41398-022-01789-1 · Cited by 22 · see citing works
Caffeine Consumption During Pregnancy Accelerates the Development of Cognitive Deficits in Offspring in a Model of Tauopathy
Zappettini, S., Faivre, É., Ghestem, A., Carrier, S., Buée, L., Blum, D. L., Esclapez, M., & Bernard, C. (2019) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2019.00438 · Cited by 23 · see citing works
Functional Connectivity and Metabolic Alterations in Medial Prefrontal Cortex in a Rat Model of Fetal Alcohol Spectrum Disorder: A Resting-State Functional Magnetic Resonance Imaging and in vivo Proton Magnetic Resonance Spectroscopy Study
Tang, S., Xu, S., Waddell, J., Zhu, W., Gullapalli, R. P., & Mooney, S. M. (2019) · Developmental Neuroscience · doi:10.1159/000499183 · Cited by 22 · see citing works
GABA system as the cause and effect in early development
Topchiy, I., Mohbat, J., Folorunso, O. O., Wang, Z., Lazcano-Etchebarne, C., & Engin, E. (2024) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2024.105651 · Cited by 23 · see citing works
Prenatal Exposure to Ethanol Alters Synaptic Activity in Layer V/VI Pyramidal Neurons of the Somatosensory Cortex
Delatour, L. C., Yeh, P. W. L., & Yeh, H. H. (2019) · Cerebral Cortex · doi:10.1093/cercor/bhz199 · Cited by 23 · see citing works
Self-citation
Gene-environment interactions in cortical interneuron development and dysfunction: A review of preclinical studies
Ansen-Wilson, L. J., & Lipinski, R. J. (2016) · NeuroToxicology · doi:10.1016/j.neuro.2016.12.002 · Cited by 22 · see citing works
Neonatal ethanol exposure triggers apoptosis in the murine retrosplenial cortex: Role of inhibition of NMDA receptor-driven action potential firing
Bird, C. W., Barber, M. J., Post, H. R., Jacquez, B. J., Chavez, G. J., Faturos, N., & Valenzuela, C. F. (2019) · Neuropharmacology · doi:10.1016/j.neuropharm.2019.107837 · Cited by 21 · see citing works
In utero alcohol exposure exacerbates endothelial protease activity from pial microvessels and impairs GABA interneuron positioning
Léger, C., Dupré, N., Laquerrière, A., Lecointre, M., Dumanoir, M., Janin, F., Hauchecorne, M., Fabre, M., Jégou, S., Frébourg, T., et al. (2020) · Neurobiology of Disease · doi:10.1016/j.nbd.2020.105074 · Cited by 21 · see citing works
Executive functioning-specific behavioral impairments in a rat model of human third trimester binge drinking implicate prefrontal-thalamo-hippocampal circuitry in Fetal Alcohol Spectrum Disorders
Gursky, Z. H., Savage, L. M., & Klintsova, A. Y. (2021) · Behavioural Brain Research · doi:10.1016/j.bbr.2021.113208 · Cited by 21 · see citing works
Effects of Ethanol on Cellular Composition and Network Excitability of Human Pluripotent Stem Cell‐Derived Neurons
Larsen, Z. H., Chander, P. N., Joyner, J. A., Floruta, C. M., Demeter, T. L., & Weick, J. P. (2016) · Alcoholism Clinical and Experimental Research · doi:10.1111/acer.13218 · Cited by 20 · see citing works
Synaptic and mitochondrial mechanisms behind alcohol-induced imbalance of excitatory/inhibitory synaptic activity and associated cognitive and behavioral abnormalities
Arzua, T., Yan, Y., Liu, X., Dash, R. K., Liu, Q.-S., & Bai, X. (2024) · Translational Psychiatry · doi:10.1038/s41398-024-02748-8 · Cited by 19 · see citing works
The NKCC1 antagonist bumetanide mitigates interneuronopathy associated with ethanol exposure in utero
Skorput, A. G. J., Lee, S. M., Yeh, P. W. L., & Yeh, H. H. (2019) · eLife · doi:10.7554/elife.48648 · Cited by 19 · see citing works
Self-citation
Corticostriatal Circuit Models of Cognitive Impairments Induced by Fetal Exposure to Alcohol
Bariselli, S., & Lovinger, D. M. (2021) · Biological Psychiatry · doi:10.1016/j.biopsych.2021.05.014 · Cited by 18 · see citing works
Ifenprodil infusion in agranular insular cortex alters social behavior and vocalizations in rats exposed to moderate levels of ethanol during prenatal development
Bird, C. W., Barto, D. R., Magcalas, C. M., Rodriguez, C. I., Donaldson, T. N., Davies, S., Savage, D. D., & Hamilton, D. A. (2016) · Behavioural Brain Research · doi:10.1016/j.bbr.2016.11.036 · Cited by 16 · see citing works
Enhancement of parvalbumin interneuron-mediated neurotransmission in the retrosplenial cortex of adolescent mice following third trimester-equivalent ethanol exposure
Bird, C. W., Chavez, G. J., Barber, M. J., & Valenzuela, C. F. (2021) · Scientific Reports · doi:10.1038/s41598-021-81173-z · Cited by 16 · see citing works
Transcriptomic changes due to early, chronic intermittent alcohol exposure during forebrain development implicate WNT signaling, cell‐type specification, and cortical regionalization as primary determinants of fetal alcohol syndrome
Fischer, M., Chander, P. N., Kang, H., Mellios, N., & Weick, J. P. (2021) · Alcoholism Clinical and Experimental Research · doi:10.1111/acer.14590 · Cited by 16 · see citing works
Synaptic Plasticity Abnormalities in Fetal Alcohol Spectrum Disorders
Basavarajappa, B. S., & Subbanna, S. (2023) · Cells · doi:10.3390/cells12030442 · Cited by 16 · see citing works
Hypersynchrony in MEG spectral amplitude in prospectively-identified 6-month-old infants prenatally exposed to alcohol
Stephen, J. M., Flynn, L., Kabella, D. M., Schendel, M. E., Cano, S., Savage, D. D., Rayburn, W. F., Leeman, L. M., Lowe, J. R., & Bakhireva, L. N. (2017) · NeuroImage Clinical · doi:10.1016/j.nicl.2017.12.012 · Cited by 16 · see citing works
Common basis for orofacial clefting and cortical interneuronopathy
Ansen-Wilson, L. J., Everson, J. L., Fink, D. M., Kietzman, H. W., Sullivan, R., & Lipinski, R. J. (2018) · Translational Psychiatry · doi:10.1038/s41398-017-0057-7 · Cited by 16 · see citing works
Prenatal Ethanol Exposure Misregulates Genes Involved in Iron Homeostasis Promoting a Maladaptation of Iron Dependent Hippocampal Synaptic Transmission and Plasticity
de la Fuente-Ortega, E., Plaza-Briceño, W., Vargas-Robert, S., & Haeger, P. A. (2019) · Frontiers in Pharmacology · doi:10.3389/fphar.2019.01312 · Cited by 15 · see citing works
L-Type Calcium Channels Contribute to Ethanol-Induced Aberrant Tangential Migration of Primordial Cortical GABAergic Interneurons in the Embryonic Medial Prefrontal Cortex
Lee, S. M., Yeh, P. W. L., & Yeh, H. H. (2021) · eNeuro · doi:10.1523/eneuro.0359-21.2021 · Cited by 15 · see citing works
Self-citation
Divergent and overlapping hippocampal and cerebellar transcriptome responses following developmental ethanol exposure during the secondary neurogenic period
Pinson, M. R., Holloway, K. N., Douglas, J. C., Kane, C. J. M., Miranda, R. C., & Drew, P. D. (2021) · Alcoholism Clinical and Experimental Research · doi:10.1111/acer.14633 · Cited by 12 · see citing works
Precocious emergence of cognitive and synaptic dysfunction in 3xTg-AD mice exposed prenatally to ethanol
Tousley, A. R., Yeh, P. W. L., & Yeh, H. H. (2022) · Alcohol · doi:10.1016/j.alcohol.2022.08.003 · Cited by 13 · see citing works
Self-citation
Subpopulations of hypocretin/orexin neurons differ in measures of their cell proliferation, dynorphin co-expression, projections, and response to embryonic ethanol exposure
Yasmin, N., Collier, A. D., Karatayev, O., Abdulai, A. R., Yu, B., Fam, M., Khalizova, N., & LEIBOWITZ, S. F. (2023) · Scientific Reports · doi:10.1038/s41598-023-35432-w · Cited by 12 · see citing works
Long‐term effects of low prenatal alcohol exposure on GABAergic interneurons of the murine posterior parietal cortex
Licheri, V., Jacquez, B. J., Castillo, V. K., Sainz, D. B., Valenzuela, C. F., & Brigman, J. L. (2023) · Alcoholism Clinical and Experimental Research · doi:10.1111/acer.15210 · Cited by 11 · see citing works
Moderate prenatal alcohol exposure produces sex‐specific social impairments and attenuates prelimbic excitability and amygdala‐cortex modulation of adult social behaviour
Przybysz, K. R., Spodnick, M. B., Johnson, J. M., Varlinskaya, E. I., & Diaz, M. R. (2022) · Addiction Biology · doi:10.1111/adb.13252 · Cited by 10 · see citing works
Asymptomatic neonatal herpes simplex virus infection in mice leads to persistent CNS infection and long-term cognitive impairment
Dutton, A. J., Patel, C., Taylor, S., Garland, C. R., Turnbaugh, E. M., Alers-Velazquez, R., Mehrbach, J., Nautiyal, K. M., & Leib, D. A. (2025) · PLoS Pathogens · doi:10.1371/journal.ppat.1012935 · Cited by 10 · see citing works
Prenatal exposure to alcohol impairs social play behavior in adolescent male mice
de Ávila, M. A. P., Gonçalves, R. M., Nascimento, E. C. C., Cabral, L. D. M., Vilela, F. C., & Giusti‐Paiva, A. (2020) · NeuroToxicology · doi:10.1016/j.neuro.2020.05.007 · Cited by 9 · see citing works
Dysfunctions of cellular context-sensitivity in neurodevelopmental learning disabilities
Granato, A., Phillips, W. A., Schulz, J. M., Mototaka Suzuki, A., & Larkum, M. E. (2024) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2024.105688 · Cited by 8 · see citing works
In relentless pursuit of the white whale: A role for the ventral midline thalamus in behavioral flexibility and adaption?
Panzer, É., Olmo, I. G., de Vasconcelos, A. P., Stéphan, A., & Cassel, J. (2024) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2024.105762 · Cited by 8 · see citing works
Somatostatin neuron contributions to cortical slow wave dysfunction in adult mice exposed to developmental ethanol
Wilson, D. A., Fleming, G., Williams, C. R. O., Teixeira, C. M., Smiley, J. F., & Saito, M. (2023) · Frontiers in Neuroscience · doi:10.3389/fnins.2023.1127711 · Cited by 7 · see citing works
Preclinical methodological approaches investigating of the effects of alcohol on perinatal and adolescent neurodevelopment
Bailey, C. D. C., Gerlai, R. T., Cameron, N. M., Marcolin, M. L., & McCormick, C. M. (2020) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2020.07.011 · Cited by 7 · see citing works
Exploring behavioral phenotypes in a mouse model of fetal alcohol spectrum disorders
Chaudoin, T. R., Bonasera, S. J., Dunaevsky, A., & Padmashri, R. (2023) · Developmental Neurobiology · doi:10.1002/dneu.22922 · Cited by 6 · see citing works
The mouse-equivalent of the human BDNF VAL66MET polymorphism increases dorsal hippocampal volume and does not interact with developmental ethanol exposure
Bird, C. W., Barber, M. J., Martin, J. L., Mayfield, J. J., & Valenzuela, C. F. (2020) · Alcohol · doi:10.1016/j.alcohol.2020.03.005 · Cited by 6 · see citing works
Effects of ethanol and varenicline on female Sprague-Dawley rats in a third trimester model of fetal alcohol syndrome
Montgomery, K. S., Bancroft, E. A., Fincher, A. S., Migut, E. A., Provasek, V. E., Murchison, D. A., & DuBois, D. W. (2018) · Alcohol · doi:10.1016/j.alcohol.2018.02.006 · Cited by 6 · see citing works
Neurobiology of Neuronal Network Alteration in Intellectual Disability Related to Fetal Alcohol Spectrum Disorders
Bâ, A. (2022) · Journal of Behavioral and Brain Science · doi:10.4236/jbbs.2022.123004 · Cited by 4 · see citing works
Changes to the somatosensory barrel cortex in C57BL/6J mice at early adulthood (56 days post-natal) following prenatal alcohol exposure
Olateju, O. I., Ihunwo, A. O., & Manger, P. R. (2018) · Journal of Chemical Neuroanatomy · doi:10.1016/j.jchemneu.2018.12.006 · Cited by 3 · see citing works
Impact of Prenatal Alcohol Exposure on Cerebral Cortex Development
Oskera, L., Charlet‐Briart, M., Tielens, S., Nguyen, L., & Laguesse, S. (2026) · Advances in experimental medicine and biology · doi:10.1007/978-3-032-12741-9_6 · Cited by 2 · see citing works
Transcriptomic changes due to early, chronic alcohol exposure during cortical development implicate regionalization, cell-type specification, synaptogenesis and WNT signaling as primary determinants of fetal alcohol Spectrum DisordersPreprint
Fischer, M., Chander, P., Kang, H., & Weick, J. P. (2019) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/784793 · Cited by 2 · see citing works
Asymptomatic neonatal herpes simplex virus infection in mice leads to long-term cognitive impairmentPreprint
Dutton, A. J., Cd, P., Taylor, S., Garland, C. R., Turnbaugh, E. M., Alers-Velazquez, R., Mehrbach, J., Nautiyal, K., & Leib, D. A. (2024) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2024.04.22.590596 · Cited by 2 · see citing works
Prenatal Ethanol Exposure Results in Cell Type, Age, and Sex-Dependent Differences in the Neonatal Striatum That Coincide with Early Motor Deficits
Tousley, A. R., Deykin, I., Koc, B., Yeh, P. W. L., & Yeh, H. H. (2025) · eNeuro · doi:10.1523/eneuro.0448-24.2025 · Cited by 1 · see citing works
Self-citation
Defects of Cortical Microcircuits Following Early Exposure to Alcohol
Granato, A. (2025) · Advances in experimental medicine and biology · doi:10.1007/978-3-031-81908-7_1 · Cited by 1 · see citing works
Paternal ethanol exposure alters offspring motor skills and behavior in a sex-dependent manner and modifies early growth response 1 expression in the medial prefrontal cortex
Gotfryd, L., Fesser, E. A., Cambiasso, M. Y., Stinson, M. G., Birolo, S., Nemirovsky, S. I., Cánepa, E. T., Calvo, J. C., & Fontana, V. A. (2025) · Journal of Affective Disorders · doi:10.1016/j.jad.2025.04.031 · Cited by 1 · see citing works
Comparative study of the effects of prenatal sevoflurane exposure at different cortical stages on forebrain development and maturation in offspring
Wang, T., Weng, H., & Li, Y. (2025) · Frontiers in Neuroscience · doi:10.3389/fnins.2025.1556703 · Cited by 1 · see citing works
FASD and Brain Development: Perspectives on Where We are and Where We Need to Go
Delatour, L. C., & Yeh, H. H. (2017) · OBM Neurobiology · doi:10.21926/obm.neurobiol.1701002 · Cited by 1 · see citing works
Self-citation
Chromatin architecture in addiction circuitry elucidates biological mechanisms underlying cigarette smoking and alcohol use traitsPreprint
Sey, N. Y. A., Hu, B., Iskhakova, M., Sun, H., Shokrian, N., Hutta, G. B., Marks, J. A., Quach, B. C., Johnson, E. O., Hancock, D. B., et al. (2021) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2021.03.18.436046 · Cited by 1 · see citing works
The regulatory role and environmental sensitivity of DNA methylation in neurodevelopment
Resendiz, M. (2017) · IUScholarWorks (Indiana University) · doi:10.7912/c2/2069
Corticostriatal deficits underlying cognitive impairments induced by fetal exposure to alcoholPreprint
Bariselli, S., & Lovinger, D. M. (2020) · doi:10.31234/osf.io/6t2y3
Alcohol
(2021) · Elsevier eBooks · doi:10.1016/b978-0-12-816793-9.00001-3
Gestational day 12 moderate prenatal alcohol exposure produces sex-specific social impairments and attenuates prelimbic excitability and amygdala-cortex modulation of adult social behaviorPreprint
Przybysz, K. R., Spodnick, M. B., Johnson, J. M., Varlinskaya, E. I., & Diaz, M. R. (2022) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2022.05.02.490324
New insights in Foetal Alcohol Syndrome: A Literature Review
Calleja, R., & Calleja‐Agius, J. (2022) · The International Journal of Prenatal & Life Sciences · doi:10.24946/ijpls/20.22.00.00.231122
The use of human iPSC-derived neuronal cultures for the study of persistent neurotoxic effects
Tukker, A. M., & Bowman, A. B. (2024) · Advances in neurotoxicology · doi:10.1016/bs.ant.2024.07.003
The Development of the Central Nervous System and Human Neural Stem Cells
Ávila, A., Ascenzi, B. M., & Vidal, P. M. (2024) · Elsevier eBooks · doi:10.1016/b978-0-12-822404-5.00001-2
Additional file 4 of Prenatal alcohol exposure is a leading cause of interneuronopathy in humans
Marguet, F., Friocourt, G., Brosolo, M., Sauvestre, F., Marcorelles, P., Lesueur, C., Marret, S., Gonzalez, B. J., & Laquerrière, A. (2020) · Figshare · doi:10.6084/m9.figshare.13310404
Additional file 2 of Prenatal alcohol exposure is a leading cause of interneuronopathy in humans
Marguet, F., Friocourt, G., Brosolo, M., Sauvestre, F., Marcorelles, P., Lesueur, C., Marret, S., Gonzalez, B. J., & Laquerrière, A. (2020) · Figshare · doi:10.6084/m9.figshare.13310392
Additional file 1 of Pre-implantation alcohol exposure induces lasting sex-specific DNA methylation programming errors in the developing forebrain
Legault, L. M., Doiron, K., Breton-Larrivée, M., Langford‐Avelar, A., Lemieux, A., Caron, M., Jerome‐Majewska, L. A., Sinnett, D., & McGraw, S. (2021) · Figshare · doi:10.6084/m9.figshare.16417618
Additional file 3 of Prenatal alcohol exposure is a leading cause of interneuronopathy in humans
Marguet, F., Friocourt, G., Brosolo, M., Sauvestre, F., Marcorelles, P., Lesueur, C., Marret, S., Gonzalez, B. J., & Laquerrière, A. (2020) · Figshare · doi:10.6084/m9.figshare.13310398
Additional file 1 of Prenatal alcohol exposure is a leading cause of interneuronopathy in humans
Marguet, F., Friocourt, G., Brosolo, M., Sauvestre, F., Marcorelles, P., Lesueur, C., Marret, S., Gonzalez, B. J., & Laquerrière, A. (2020) · Figshare · doi:10.6084/m9.figshare.13310389
Effets de l'alcoolisation prénatale sur le développement du système GABAergique et de la myélinisation chez l'humain
Marguet, F. (2020) · doi:10.70675/7590e822z0aa7z4868z972bz90e8061311fb
Rôle des microARNs dérégulés par l'alcool dans l'établissement des réseaux neuronaux murins
Altounian, M. (2021) · theses.fr (ABES) · doi:10.70675/a0e0a626zc6c5z4276z9eefz3417c53aea21
Impact d'une exposition prénatale à l'alcool sur le développement de la rétine.
Dumanoir, M. (2021) · doi:10.70675/8e4b1cfdzd2c7z4197zbda8z76e7ad8f87f5
Prenatal alcohol exposure differently affects seizure susceptibility and severity depending on its mechanism of induction: role of excitatory synapses and parvalbumin-positive interneurons
Heringer, L. D. S., de Azevedo, T. B., Pontes, T. M. P., Ciriaco, P. S., Martinez, A. M. B., & Mendonça, H. R. (2026) · Neuroscience Letters · doi:10.1016/j.neulet.2026.138648
Developmental Neurotoxicity of Alcohol from Neuronal Basis to Behavioural Outcomes: A Comprehensive Review
Smimih, K., Azzouhri, C., El‐Mansoury, B., Draoui, A., Lahouaoui, H., Bitar, A., Merzouki, M., & Hiba, O. E. (2026) · Neurology International · doi:10.3390/neurolint18070123
The NKCC1 Antagonist Bumetanide, Administered After Prenatal Alcohol Exposure, Mitigates Ethanol‐Induced Aberrance in Tangential Migration of GABAergic Interneurons in Mouse Medial Prefrontal Cortex
Koc, B., Skorput, A. G. J., Yeh, P. W. L., & Yeh, H. H. (2026) · Alcoholism Clinical and Experimental Research · doi:10.1111/acer.70375
Self-citation
Developmental alcohol exposure: Impacts on medial prefrontal cortex morphology and the excitatory-inhibitory balance
Cirafesi, C. K., Karkhanis, A. N., & Diaz, M. R. (2026) · Progress in Neuro-Psychopharmacology and Biological Psychiatry · doi:10.1016/j.pnpbp.2026.111887

Chronic Gestational Exposure to Ethanol Leads to Enduring Aberrances in Cortical Form and Function in the Medial Prefrontal Cortex
Skorput, A. G. J., & Yeh, H. H. (2016) · Alcoholism: Clinical and Experimental Research · doi:10.1111/acer.13107 · Cited by 50 · see citing works
Self-citation
Ethanol Consumption during Early Pregnancy Alters the Disposition of Tangentially Migrating GABAergic Interneurons in the Fetal Cortex
Carlson, V. C. C., Yeh, P. W. L., Yanagawa, Y., Obata, K., & Yeh, H. H. (2008) · Journal of Neuroscience · doi:10.1523/jneurosci.5110-07.2008 · Cited by 140 · see citing works
Self-citation
Migration of Cortical Neurons Is Altered by Gestational Exposure to Ethanol
Miller, M. W. (1993) · Alcoholism Clinical and Experimental Research · doi:10.1111/j.1530-0277.1993.tb00768.x · Cited by 220 · see citing works
The NKCC1 antagonist bumetanide mitigates interneuronopathy associated with ethanol exposure in utero
Skorput, A. G. J., Lee, S. M., Yeh, P. W. L., & Yeh, H. H. (2019) · eLife · doi:10.7554/elife.48648 · Cited by 19 · see citing works
Self-citation
L-Type Calcium Channels Contribute to Ethanol-Induced Aberrant Tangential Migration of Primordial Cortical GABAergic Interneurons in the Embryonic Medial Prefrontal Cortex
Lee, S. M., Yeh, P. W. L., & Yeh, H. H. (2021) · eNeuro · doi:10.1523/eneuro.0359-21.2021 · Cited by 15 · see citing works
Self-citation

Authors: Skorput, A. G. J., Gupta, V. P., Yeh, P. W. L., & Yeh, H. H.
Affiliations: Dartmouth–Hitchcock Medical Center (US)
ORCID: Gupta, V. P.
Yeh, H. H.
Venue: Journal of Neuroscience
Publisher: Society for Neuroscience
Published: 2015-08-05
Volume: 35
Issue: 31
Pages: 10977-10988
ISSN: 0270-6474 (ISSN-L)
1529-2401
DOI: 10.1523/jneurosci.1462-15.2015
PMC: PMC4524971
OpenAlex: W1727961109
Cited by: 92
References: 72
Citations by year: 2026: 5 · 2025: 5 · 2024: 9 · 2023: 6 · 2022: 7 · 2021: 14 · 2020: 12 · 2019: 11 · 2018: 5 · 2017: 12 · 2016: 6
FWCI: 7.64
Type: journal article
Language: en
Open access: bronze
doi.org
Locations: Journal of Neuroscience (publishedVersion)
PubMed Central (publishedVersion)
PubMed (publishedVersion)
Funders: National Institute on Alcohol Abuse and Alcoholism (R21AA024036, R01AA023410)
National Institute of Mental Health (R01MH069826)
Topics: Health Sciences › Medicine › Pediatrics, Perinatology and Child Health › Prenatal Substance Exposure Effects
Life Sciences › Neuroscience › Developmental Neuroscience › Neurogenesis and neuroplasticity mechanisms
Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
Keywords: prenatal alcohol exposure, fetal alcohol spectrum disorders, GABAergic interneurons, medial prefrontal cortex, parvalbumin interneurons, excitation-inhibition balance, GABAergic neurotransmission, reversal learning, behavioral flexibility, locomotor activity, binge ethanol exposure, medial ganglionic eminence
MeSH terms: Ethanol, Animals, Female, Interneurons, Parvalbumins, Pregnancy, Prenatal Exposure Delayed Effects, Prefrontal Cortex, Mice, GABAergic Neurons

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Persistent Interneuronopathy in the Prefrontal Cortex of Young Adult Offspring Exposed to Ethanol In Utero

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