{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,7,1]],"date-time":"2026-07-01T23:49:03Z","timestamp":1782949743340,"version":"3.54.5"},"reference-count":79,"publisher":"Frontiers Media SA","license":[{"start":{"date-parts":[[2025,4,15]],"date-time":"2025-04-15T00:00:00Z","timestamp":1744675200000},"content-version":"vor","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."],"abstract":"<jats:sec><jats:title>Introduction<\/jats:title><jats:p>A result of the ongoing opioid epidemic has been a significant rise in the rates of opioid use during pregnancy. This includes use of maintenance medications for opioid use disorder (MOUDs), such as methadone, which are the standard of care for pregnant people with an opioid use disorder (OUD). Although the use of MOUDs leads to better neonatal outcomes in exposed offspring compared to those born from individuals with untreated OUD, the pharmacology of MOUDs is similar to misused opioids. Despite the high prevalence of prenatal exposure to opioids, including MOUDs, our understanding of the long-term consequences of these exposures in offspring is limited. Prenatal drug exposure is known to be a risk factor for future substance use disorder and mood disorders, yet, how prenatal opioid exposure influences ethanol intake in adult offspring and associated affective behaviors has not been examined.<\/jats:p><\/jats:sec><jats:sec><jats:title>Methods<\/jats:title><jats:p>Using a rat model of prenatal methadone exposure (PME), which included twice daily methadone injections from gestational day 3-20, this study assessed ethanol intake in adult offspring and how exposure to forced swim stress (FSS) altered ethanol intake, in addition to examination of depressive-like behavior during the FSS. Given the role of the basolateral amygdala (BLA) in emotion and reward processing, we also conducted patch clamp electrophysiology experiments from BLA neurons to investigate changes in synaptic transmission and gene expression of neuromodulatory systems that are known to influence emotion and reward processing.<\/jats:p><\/jats:sec><jats:sec><jats:title>Results<\/jats:title><jats:p>Females with a history of PME consumed less ethanol than control females, with no effects of PME on ethanol intake evident in males. While PME increased immobility during FSS in both males and females, FSS had no effects on ethanol intake. PME increased glutamate transmission and altered dopamine D1, D2, and D3 receptor and mu opioid receptor mRNA in the BLA of females, but not in males.<\/jats:p><\/jats:sec><jats:sec><jats:title>Discussion<\/jats:title><jats:p>Collectively, this study identified impairments in emotion and reward processing, in addition to alterations in synaptic function and gene expression in the BLA of females with a history of PME, supporting previous findings from our lab demonstrating that female offspring are more sensitive to the long-term effects of PME.<\/jats:p><\/jats:sec>","DOI":"10.3389\/fnbeh.2025.1570951","type":"journal-article","created":{"date-parts":[[2025,4,15]],"date-time":"2025-04-15T05:21:06Z","timestamp":1744694466000},"update-policy":"https:\/\/doi.org\/10.3389\/crossmark-policy","source":"Crossref","is-referenced-by-count":4,"title":["Prenatal methadone exposure produces functional and molecular alterations in the basolateral amygdala and decreased voluntary ethanol intake in female, but not male offspring"],"prefix":"10.3389","volume":"19","author":[{"given":"Meredith E.","family":"Gamble","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Michelle","family":"Montero","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Dana N.","family":"Silberstein","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Terrence","family":"Deak","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Elena I.","family":"Varlinskaya","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Marvin R.","family":"Diaz","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1965","published-online":{"date-parts":[[2025,4,15]]},"reference":[{"key":"ref1","doi-asserted-by":"publisher","first-page":"113621","DOI":"10.1016\/j.expneurol.2021.113621","article-title":"Prenatal opioid exposure and vulnerability to future substance use disorders in offspring","volume":"339","author":"Abu","year":"2021","journal-title":"Exp. 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Biobehav. Rev."},{"key":"ref6","doi-asserted-by":"publisher","first-page":"564","DOI":"10.1177\/0269881111405556","article-title":"D1 and D2 dopaminergic systems in the rat basolateral amygdala are involved in anxiogenic-like effects induced by histamine","volume":"26","author":"Bananej","year":"2012","journal-title":"J. Psychopharmacol."},{"key":"ref7","doi-asserted-by":"publisher","first-page":"131","DOI":"10.1007\/s00213-011-2443-9","article-title":"Effects of stress on alcohol drinking: a review of animal studies","volume":"218","author":"Becker","year":"2011","journal-title":"Psychopharmacology"},{"key":"ref8","doi-asserted-by":"publisher","first-page":"1478","DOI":"10.1016\/j.lfs.2005.07.023","article-title":"Effects of prenatal cocaine, morphine, or both on postnatal opioid (mu) receptor development","volume":"78","author":"Bhat","year":"2006","journal-title":"Life Sci."},{"key":"ref9","doi-asserted-by":"publisher","first-page":"325","DOI":"10.1515\/revneuro-2018-0023","article-title":"Understanding the role of dopamine in conditioned and unconditioned fear","volume":"30","author":"Brandao","year":"2019","journal-title":"Rev. Neurosci."},{"key":"ref10","doi-asserted-by":"publisher","first-page":"1048","DOI":"10.1111\/acer.12049","article-title":"Effects of voluntary access to sweetened ethanol during adolescence on intake in adulthood","volume":"37","author":"Broadwater","year":"2013","journal-title":"Alcohol. Clin. Exp. Res."},{"key":"ref11","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1016\/j.yfrne.2017.09.001","article-title":"Modeling prenatal opioid exposure in animals: current findings and future directions","volume":"51","author":"Byrnes","year":"2018","journal-title":"Front. Neuroendocrinol."},{"key":"ref12","doi-asserted-by":"publisher","first-page":"602","DOI":"10.1016\/j.ajog.2019.07.022","article-title":"Opioids affect the fetal brain: reframing the detoxification debate","volume":"221","author":"Caritis","year":"2019","journal-title":"Am. J. Obstet. Gynecol."},{"key":"ref13","doi-asserted-by":"publisher","first-page":"Unit 8 10A","DOI":"10.1002\/0471142301.ns0810as55","article-title":"Rodent models of depression: forced swim and tail suspension behavioral despair tests in rats and mice","author":"Castagne","year":"2011","journal-title":"Curr. Protoc. Neurosci."},{"key":"ref14","doi-asserted-by":"publisher","first-page":"609","DOI":"10.2147\/NDT.S70585","article-title":"Buprenorphine, methadone, and morphine treatment during pregnancy: behavioral effects on the offspring in rats","volume":"11","author":"Chen","year":"2015","journal-title":"Neuropsychiatr. Dis. Treat."},{"key":"ref15","doi-asserted-by":"publisher","first-page":"381","DOI":"10.1016\/j.pbb.2012.05.010","article-title":"Subsequent anxiety-related behavior in rats exposed to low-dose methadone during gestation, lactation or both periods consecutively","volume":"102","author":"Daly","year":"2012","journal-title":"Pharmacol. Biochem. 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Rep."},{"key":"ref35","doi-asserted-by":"publisher","first-page":"770","DOI":"10.1002\/phar.4616","article-title":"Neurodevelopmental outcomes in children prenatally exposed to opioid maintenance treatment: a population-based study","volume":"44","author":"Hasan","year":"2024","journal-title":"Pharmacotherapy"},{"key":"ref36","doi-asserted-by":"publisher","first-page":"149","DOI":"10.1016\/j.devbrainres.2004.05.002","article-title":"Differential effects of gestational buprenorphine, naloxone, and methadone on mesolimbic mu opioid and ORL1 receptor G protein coupling","volume":"151","author":"Hou","year":"2004","journal-title":"Brain Res. Dev. Brain Res."},{"key":"ref37","doi-asserted-by":"publisher","first-page":"443","DOI":"10.1007\/s10802-020-00766-w","article-title":"Emotional and behavioral trajectories of 2 to 9 years old children born to opioid-dependent mothers","volume":"49","author":"Jaekel","year":"2021","journal-title":"Res. Child Adolesc. Psychopathol."},{"key":"ref38","doi-asserted-by":"publisher","first-page":"284","DOI":"10.1038\/nature14188","article-title":"From circuits to behaviour in the amygdala","volume":"517","author":"Janak","year":"2015","journal-title":"Nature"},{"key":"ref39","doi-asserted-by":"publisher","first-page":"73","DOI":"10.1016\/j.ejphar.2014.11.044","article-title":"The dark side of emotion: the addiction perspective","volume":"753","author":"Koob","year":"2015","journal-title":"Eur. J. Pharmacol."},{"key":"ref40","doi-asserted-by":"publisher","first-page":"147","DOI":"10.1007\/7854_2021_288","article-title":"Anhedonia, Hyperkatifeia, and negative reinforcement in substance use disorders","volume":"58","author":"Koob","year":"2022","journal-title":"Curr. Top. Behav. Neurosci."},{"key":"ref41","doi-asserted-by":"publisher","first-page":"245","DOI":"10.1016\/j.neubiorev.2018.09.008","article-title":"Addiction and stress: an allostatic view","volume":"106","author":"Koob","year":"2019","journal-title":"Neurosci. Biobehav. Rev."},{"key":"ref42","doi-asserted-by":"publisher","first-page":"760","DOI":"10.1016\/S2215-0366(16)00104-8","article-title":"Neurobiology of addiction: a neurocircuitry analysis","volume":"3","author":"Koob","year":"2016","journal-title":"Lancet Psychiatry"},{"key":"ref43","doi-asserted-by":"publisher","first-page":"1598","DOI":"10.1152\/jn.00843.2004","article-title":"Dopamine modulates excitability of basolateral amygdala neurons in vitro","volume":"93","author":"Kroner","year":"2005","journal-title":"J. Neurophysiol."},{"key":"ref44","doi-asserted-by":"publisher","first-page":"3185","DOI":"10.1152\/jn.00189.2007","article-title":"Chronic ethanol and withdrawal differentially modulate pre- and postsynaptic function at glutamatergic synapses in rat basolateral amygdala","volume":"98","author":"Lack","year":"2007","journal-title":"J. Neurophysiol."},{"key":"ref45","doi-asserted-by":"publisher","first-page":"1114","DOI":"10.1111\/dmcn.14808","article-title":"Prenatal methadone exposure and child developmental outcomes in 2-year-old children","volume":"63","author":"Levine","year":"2021","journal-title":"Dev. Med. Child Neurol."},{"key":"ref46","doi-asserted-by":"publisher","first-page":"e26065","DOI":"10.1371\/journal.pone.0026065","article-title":"Synergistic activation of dopamine D1 and TrkB receptors mediate gain control of synaptic plasticity in the basolateral amygdala","volume":"6","author":"Li","year":"2011","journal-title":"PLoS One"},{"key":"ref47","doi-asserted-by":"publisher","first-page":"381","DOI":"10.1111\/ejn.13477","article-title":"Amygdala mu-opioid receptors mediate the motivating influence of cue-triggered reward expectations","volume":"45","author":"Lichtenberg","year":"2017","journal-title":"Eur. J. Neurosci."},{"key":"ref48","doi-asserted-by":"publisher","first-page":"224","DOI":"10.1159\/000112395","article-title":"Effects of prenatal methadone on rat brain catecholamines","volume":"3","author":"McGinty","year":"1980","journal-title":"Dev. Neurosci."},{"key":"ref49","doi-asserted-by":"publisher","first-page":"2041","DOI":"10.1007\/s00213-022-06120-w","article-title":"Sex differences in stress-induced alcohol intake: a review of preclinical studies focused on amygdala and inflammatory pathways","volume":"239","author":"Mineur","year":"2022","journal-title":"Psychopharmacology"},{"key":"ref50","doi-asserted-by":"publisher","first-page":"750","DOI":"10.1111\/dmcn.14117","article-title":"Childhood neurodevelopment after prescription of maintenance methadone for opioid dependency in pregnancy: a systematic review and meta-analysis","volume":"61","author":"Monnelly","year":"2019","journal-title":"Dev. Med. Child Neurol."},{"key":"ref51","doi-asserted-by":"publisher","first-page":"173756","DOI":"10.1016\/j.pbb.2024.173756","article-title":"Limited bedding and nesting increases ethanol drinking in female rats","volume":"239","author":"Parks","year":"2024","journal-title":"Pharmacol. Biochem. Behav."},{"key":"ref52","doi-asserted-by":"publisher","first-page":"124","DOI":"10.1016\/j.neuropharm.2017.01.036","article-title":"Age-dependent regulation of GABA transmission by kappa opioid receptors in the basolateral amygdala of Sprague-Dawley rats","volume":"117","author":"Przybysz","year":"2017","journal-title":"Neuropharmacology"},{"key":"ref53","doi-asserted-by":"publisher","first-page":"119959","DOI":"10.1016\/j.lfs.2021.119959","article-title":"Early life stress induces anxiety-like behavior during adulthood through dysregulation of neuronal plasticity in the basolateral amygdala","volume":"285","author":"Qin","year":"2021","journal-title":"Life Sci."},{"key":"ref54","doi-asserted-by":"publisher","first-page":"585","DOI":"10.1007\/s00234-020-02552-3","article-title":"Resting state functional MRI in infants with prenatal opioid exposure-a pilot study","volume":"63","author":"Radhakrishnan","year":"2020","journal-title":"Neuroradiology"},{"key":"ref55","doi-asserted-by":"publisher","first-page":"3788","DOI":"10.3390\/ijms22073788","article-title":"Recent perspectives on sex differences in compulsion-like and binge alcohol drinking","volume":"22","author":"Radke","year":"2021","journal-title":"Int. J. Mol. Sci."},{"key":"ref56","doi-asserted-by":"publisher","first-page":"295","DOI":"10.1016\/S0892-0362(97)00018-4","article-title":"Perinatal methadone exposure affects dopamine, norepinephrine, and serotonin in the weanling rat","volume":"19","author":"Robinson","year":"1997","journal-title":"Neurotoxicol. Teratol."},{"key":"ref57","doi-asserted-by":"publisher","first-page":"141","DOI":"10.1053\/j.semperi.2019.01.003","article-title":"Pharmacological treatment of opioid use disorder in pregnancy","volume":"43","author":"Rodriguez","year":"2019","journal-title":"Semin. Perinatol."},{"key":"ref58","doi-asserted-by":"publisher","first-page":"59","DOI":"10.1016\/j.pnpbp.2017.06.009","article-title":"Opiate exposure state controls dopamine D3 receptor and cdk5\/calcineurin signaling in the basolateral amygdala during reward and withdrawal aversion memory formation","volume":"79","author":"Rosen","year":"2017","journal-title":"Prog. Neuro-Psychopharmacol. Biol. 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Neurosci."},{"key":"ref62","volume-title":"Drug overdose deaths in the united sates, 2002\u20132022","author":"Spencer","year":"2024"},{"key":"ref63","doi-asserted-by":"publisher","first-page":"1118634","DOI":"10.3389\/fped.2023.1118634","article-title":"Executive functioning, behavioural, emotional, and cognitive difficulties in school-aged children prenatally exposed to methadone","volume":"11","author":"Spowart","year":"2023","journal-title":"Front. Pediatr."},{"key":"ref64","doi-asserted-by":"publisher","first-page":"3810","DOI":"10.1007\/s11606-021-06904-4","article-title":"Integrating harm reduction into outpatient opioid use disorder treatment settings: harm reduction in outpatient addiction treatment","volume":"36","author":"Taylor","year":"2021","journal-title":"J. Gen. Intern. Med."},{"key":"ref65","doi-asserted-by":"publisher","first-page":"381","DOI":"10.1016\/S0278-5846(02)00355-X","article-title":"Autoradiographic evidence that prenatal morphine exposure sex-dependently alters mu-opioid receptor densities in brain regions that are involved in the control of drug abuse and other motivated behaviors","volume":"27","author":"Vathy","year":"2003","journal-title":"Prog. Neuro-Psychopharmacol. Biol. Psychiatry"},{"key":"ref66","doi-asserted-by":"publisher","first-page":"e12476","DOI":"10.1111\/gbb.12476","article-title":"Epigenetic variation in OPRM1 gene in opioid-exposed mother-infant dyads","volume":"17","author":"Wachman","year":"2018","journal-title":"Genes Brain Behav."},{"key":"ref67","doi-asserted-by":"publisher","first-page":"83","DOI":"10.1016\/j.alcohol.2007.12.001","article-title":"Dissociable effects of ethanol consumption during the light and dark phase in adolescent and adult Wistar rats","volume":"42","author":"Walker","year":"2008","journal-title":"Alcohol"},{"key":"ref68","first-page":"399","article-title":"Effect of perinatal exposure to methadone on brain opioid and alpha 2-adrenergic receptors","volume":"8","author":"Wang","year":"1986","journal-title":"Neurobehav. Toxicol. Teratol."},{"key":"ref69","doi-asserted-by":"publisher","first-page":"e18739","DOI":"10.1371\/journal.pone.0018739","article-title":"Neurons in the amygdala with response-selectivity for anxiety in two ethologically based tests","volume":"6","author":"Wang","year":"2011","journal-title":"PLoS One"},{"key":"ref70","doi-asserted-by":"publisher","first-page":"1591","DOI":"10.1523\/JNEUROSCI.3102-10.2011","article-title":"Micro-opioid receptor activation in the basolateral amygdala mediates the learning of increases but not decreases in the incentive value of a food reward","volume":"31","author":"Wassum","year":"2011","journal-title":"J. Neurosci."},{"key":"ref71","doi-asserted-by":"publisher","first-page":"271","DOI":"10.1016\/j.neubiorev.2015.08.017","article-title":"The basolateral amygdala in reward learning and addiction","volume":"57","author":"Wassum","year":"2015","journal-title":"Neurosci. Biobehav. 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Physiol."},{"key":"ref73","doi-asserted-by":"publisher","first-page":"353","DOI":"10.1016\/j.neuropharm.2014.08.021","article-title":"Morphine and DAMGO produce an opposite effect on presynaptic glutamate release via different downstream pathways of mu opioid receptors in the basolateral amygdala","volume":"86","author":"Yang","year":"2014","journal-title":"Neuropharmacology"},{"key":"ref74","doi-asserted-by":"publisher","first-page":"98","DOI":"10.1016\/j.brainresbull.2021.02.005","article-title":"Enriched environment and social isolation differentially modulate addiction-related behaviors in male offspring of morphine-addicted dams: the possible role of mu-opioid receptors and DeltaFosB in the brain reward pathway","volume":"170","author":"Yazdanfar","year":"2021","journal-title":"Brain Res. Bull."},{"key":"ref75","doi-asserted-by":"publisher","first-page":"106","DOI":"10.1016\/j.ejphar.2011.09.168","article-title":"Involvement of the dopaminergic receptors of the rat basolateral amygdala in anxiolytic-like effects of the cholinergic system","volume":"672","author":"Zarrindast","year":"2011","journal-title":"Eur. J. Pharmacol."},{"key":"ref76","doi-asserted-by":"publisher","first-page":"247","DOI":"10.3389\/fnmol.2017.00247","article-title":"MPTP-induced dopamine depletion in basolateral amygdala via decrease of D2R activation suppresses GABA(a) receptors expression and LTD induction leading to anxiety-like behaviors","volume":"10","author":"Zhang","year":"2017","journal-title":"Front. Mol. Neurosci."},{"key":"ref77","doi-asserted-by":"publisher","first-page":"189","DOI":"10.1016\/j.biopsych.2018.06.019","article-title":"Chronic stress remodels synapses in an amygdala circuit-specific manner","volume":"85","author":"Zhang","year":"2019","journal-title":"Biol. 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