{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,8,16]],"date-time":"2026-08-16T09:16:41Z","timestamp":1786871801114,"version":"build-2736575974"},"reference-count":87,"publisher":"MDPI AG","issue":"19","license":[{"start":{"date-parts":[[2022,10,2]],"date-time":"2022-10-02T00:00:00Z","timestamp":1664668800000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"DOI":"10.13039\/100000738","name":"Veterans Affairs Career Development Award","doi-asserted-by":"publisher","award":["BX002505"],"award-info":[{"award-number":["BX002505"]}],"id":[{"id":"10.13039\/100000738","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/100000738","name":"Veterans Affairs Career Development Award","doi-asserted-by":"publisher","award":["BX005403"],"award-info":[{"award-number":["BX005403"]}],"id":[{"id":"10.13039\/100000738","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/100000738","name":"Veterans Affairs Career Development Award","doi-asserted-by":"publisher","award":["NNX15AI01H"],"award-info":[{"award-number":["NNX15AI01H"]}],"id":[{"id":"10.13039\/100000738","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/100000738","name":"Veterans Affairs Career Development Award","doi-asserted-by":"publisher","award":["P20GM103434"],"award-info":[{"award-number":["P20GM103434"]}],"id":[{"id":"10.13039\/100000738","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/100000738","name":"Veterans Affairs Career Development Award","doi-asserted-by":"publisher","award":["1P20GM121299"],"award-info":[{"award-number":["1P20GM121299"]}],"id":[{"id":"10.13039\/100000738","id-type":"DOI","asserted-by":"publisher"}]},{"name":"MLR and the Veterans Affairs Merit Award","award":["BX002505"],"award-info":[{"award-number":["BX002505"]}]},{"name":"MLR and the Veterans Affairs Merit Award","award":["BX005403"],"award-info":[{"award-number":["BX005403"]}]},{"name":"MLR and the Veterans Affairs Merit Award","award":["NNX15AI01H"],"award-info":[{"award-number":["NNX15AI01H"]}]},{"name":"MLR and the Veterans Affairs Merit Award","award":["P20GM103434"],"award-info":[{"award-number":["P20GM103434"]}]},{"name":"MLR and the Veterans Affairs Merit Award","award":["1P20GM121299"],"award-info":[{"award-number":["1P20GM121299"]}]},{"name":"United States (U.S.) Department of Veterans Affairs Biomedical Laboratory Research and Development and the NASA West Virginia Space Grant Consortium Training Grant","award":["BX002505"],"award-info":[{"award-number":["BX002505"]}]},{"name":"United States (U.S.) Department of Veterans Affairs Biomedical Laboratory Research and Development and the NASA West Virginia Space Grant Consortium Training Grant","award":["BX005403"],"award-info":[{"award-number":["BX005403"]}]},{"name":"United States (U.S.) Department of Veterans Affairs Biomedical Laboratory Research and Development and the NASA West Virginia Space Grant Consortium Training Grant","award":["NNX15AI01H"],"award-info":[{"award-number":["NNX15AI01H"]}]},{"name":"United States (U.S.) Department of Veterans Affairs Biomedical Laboratory Research and Development and the NASA West Virginia Space Grant Consortium Training Grant","award":["P20GM103434"],"award-info":[{"award-number":["P20GM103434"]}]},{"name":"United States (U.S.) Department of Veterans Affairs Biomedical Laboratory Research and Development and the NASA West Virginia Space Grant Consortium Training Grant","award":["1P20GM121299"],"award-info":[{"award-number":["1P20GM121299"]}]},{"name":"CDW. Additional resources and facilities were provided through the Genomics Core, Bioinformatics Core, the WV-INBRE grant","award":["BX002505"],"award-info":[{"award-number":["BX002505"]}]},{"name":"CDW. Additional resources and facilities were provided through the Genomics Core, Bioinformatics Core, the WV-INBRE grant","award":["BX005403"],"award-info":[{"award-number":["BX005403"]}]},{"name":"CDW. Additional resources and facilities were provided through the Genomics Core, Bioinformatics Core, the WV-INBRE grant","award":["NNX15AI01H"],"award-info":[{"award-number":["NNX15AI01H"]}]},{"name":"CDW. Additional resources and facilities were provided through the Genomics Core, Bioinformatics Core, the WV-INBRE grant","award":["P20GM103434"],"award-info":[{"award-number":["P20GM103434"]}]},{"name":"CDW. Additional resources and facilities were provided through the Genomics Core, Bioinformatics Core, the WV-INBRE grant","award":["1P20GM121299"],"award-info":[{"award-number":["1P20GM121299"]}]},{"name":"COBRE ACCORD","award":["BX002505"],"award-info":[{"award-number":["BX002505"]}]},{"name":"COBRE ACCORD","award":["BX005403"],"award-info":[{"award-number":["BX005403"]}]},{"name":"COBRE ACCORD","award":["NNX15AI01H"],"award-info":[{"award-number":["NNX15AI01H"]}]},{"name":"COBRE ACCORD","award":["P20GM103434"],"award-info":[{"award-number":["P20GM103434"]}]},{"name":"COBRE ACCORD","award":["1P20GM121299"],"award-info":[{"award-number":["1P20GM121299"]}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Cells"],"abstract":"<jats:p>Adolescence is a developmental period that encompasses, but is not limited to, puberty and continues into early adulthood. During this period, maturation and refinement are observed across brain regions such as the prefrontal cortex (PFC), which is critical for cognitive function. Adolescence is also a time when excessive alcohol consumption in the form of binge drinking peaks, increasing the risk of long-term cognitive deficits and the risk of developing an alcohol use disorder later in life. Animal models have revealed that adolescent ethanol (EtOH) exposure results in protracted disruption of neuronal function and performance on PFC-dependent tasks that require higher-order decision-making. However, the role of astrocytes in EtOH-induced disruption of prefrontal cortex-dependent function has yet to be elucidated. Astrocytes have complex morphologies with an extensive network of peripheral astrocyte processes (PAPs) that ensheathe pre- and postsynaptic terminals to form the \u2018tripartite synapse.\u2019 At the tripartite synapse, astrocytes play several critical roles, including synaptic maintenance, dendritic spine maturation, and neurotransmitter clearance through proximity-dependent interactions. Here, we investigate the effects of adolescent binge EtOH exposure on astrocyte morphology, PAP-synaptic proximity, synaptic stabilization proteins, and dendritic spine morphology in subregions of the PFC that are important in the emergence of higher cognitive function. We found that adolescent binge EtOH exposure resulted in subregion specific changes in astrocyte morphology and astrocyte-neuronal interactions. While this did not correspond to a loss of astrocytes, synapses, or dendritic spines, there was a corresponding region-specific and EtOH-dependent shift in dendritic spine phenotype. Lastly, we found that changes in astrocyte-neuronal interactions were not a consequence of changes in the expression of key synaptic structural proteins neurexin, neuroligin 1, or neuroligin 3. These data demonstrate that adolescent EtOH exposure results in enduring effects on neuron-glia interactions that persist into adulthood in a subregion-specific PFC manner, suggesting selective vulnerability. Further work is necessary to understand the functional and behavioral implications.<\/jats:p>","DOI":"10.3390\/cells11193111","type":"journal-article","created":{"date-parts":[[2022,10,8]],"date-time":"2022-10-08T01:52:21Z","timestamp":1665193941000},"page":"3111","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":16,"title":["Diverging Effects of Adolescent Ethanol Exposure on Tripartite Synaptic Development across Prefrontal Cortex Subregions"],"prefix":"10.3390","volume":"11","author":[{"given":"Christopher Douglas","family":"Walker","sequence":"first","affiliation":[{"name":"Department of Biomedical Research, Joan C. Edwards School of Medicine, Marshall University, Huntington, WV 25701, USA"},{"name":"Neurobiology Research Laboratory, Hershel \u2018Woody\u2019 Williams Veterans Affairs Medical Center, Huntington, WV 25704, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-1844-086X","authenticated-orcid":false,"given":"Hannah Gray","family":"Sexton","sequence":"additional","affiliation":[{"name":"Department of Biomedical Research, Joan C. Edwards School of Medicine, Marshall University, Huntington, WV 25701, USA"},{"name":"Neurobiology Research Laboratory, Hershel \u2018Woody\u2019 Williams Veterans Affairs Medical Center, Huntington, WV 25704, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Jentre","family":"Hyde","sequence":"additional","affiliation":[{"name":"Department of Biomedical Research, Joan C. Edwards School of Medicine, Marshall University, Huntington, WV 25701, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-9407-135X","authenticated-orcid":false,"given":"Brittani","family":"Greene","sequence":"additional","affiliation":[{"name":"Department of Biomedical Research, Joan C. Edwards School of Medicine, Marshall University, Huntington, WV 25701, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-3139-4378","authenticated-orcid":false,"given":"Mary-Louise","family":"Risher","sequence":"additional","affiliation":[{"name":"Department of Biomedical Research, Joan C. Edwards School of Medicine, Marshall University, Huntington, WV 25701, USA"},{"name":"Neurobiology Research Laboratory, Hershel \u2018Woody\u2019 Williams Veterans Affairs Medical Center, Huntington, WV 25704, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1968","published-online":{"date-parts":[[2022,10,2]]},"reference":[{"key":"ref_1","first-page":"193","article-title":"Prevalence and predictors of adolescent alcohol use and binge drinking in the United States","volume":"35","author":"Patrick","year":"2013","journal-title":"Alcohol Res."},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"1704","DOI":"10.1001\/jama.2022.4308","article-title":"Alcohol-Related Deaths During the COVID-19 Pandemic","volume":"327","author":"White","year":"2022","journal-title":"JAMA"},{"key":"ref_3","unstructured":"WHO (2018). Global Status Report on Alcohol and Health 2018, World Health Organization."},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"178","DOI":"10.1111\/acer.14239","article-title":"Using Death Certificates to Explore Changes in Alcohol-Related Mortality in the United States, 1999 to 2017","volume":"44","author":"White","year":"2020","journal-title":"Alcohol. Clin. Exp. Res."},{"key":"ref_5","first-page":"5","article-title":"Adolescent Binge Drinking: Developmental context and opportunities for prevention","volume":"39","author":"Chung","year":"2018","journal-title":"Alcohol Res. Curr. Rev."},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"158","DOI":"10.15288\/jsad.2014.75.158","article-title":"New research findings since the 2007 Surgeon General\u2019s Call to Action to Prevent and Reduce Underage Drinking: A review","volume":"75","author":"Hingson","year":"2014","journal-title":"J. Stud. Alcohol Drugs"},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"19","DOI":"10.1159\/000495210","article-title":"Characterization of the Hippocampal Neuroimmune Response to Binge-Like Ethanol Consumption in the Drinking in the Dark Model","volume":"26","author":"Grifasi","year":"2019","journal-title":"Neuroimmunomodulation"},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"121","DOI":"10.1023\/A:1025779412167","article-title":"Psychiatric disorders associated with substance use among children and adolescents: Findings from the Methods for the Epidemiology of Child and Adolescent Mental Disorders (MECA) Study","volume":"25","author":"Kandel","year":"1997","journal-title":"J. Abnorm. Child Psychol."},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"976","DOI":"10.1080\/08870446.2017.1325889","article-title":"Binge drinking: Health impact, prevalence, correlates and interventions","volume":"32","author":"Kuntsche","year":"2017","journal-title":"Psychol. Health"},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"76","DOI":"10.1542\/peds.2006-1517","article-title":"Binge drinking and associated health risk behaviors among high school students","volume":"119","author":"Miller","year":"2007","journal-title":"Pediatrics"},{"key":"ref_11","doi-asserted-by":"crossref","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":"ref_12","doi-asserted-by":"crossref","first-page":"139","DOI":"10.1038\/nrn1033","article-title":"Human prefrontal cortex: Processing and representational perspectives","volume":"4","author":"Wood","year":"2003","journal-title":"Nat. Rev. Neurosci."},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"215","DOI":"10.1016\/S1364-6613(00)01483-2","article-title":"Cognitive and emotional influences in anterior cingulate cortex","volume":"4","author":"Bush","year":"2000","journal-title":"Trends Cogn. Sci."},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"121","DOI":"10.1176\/jnp.23.2.jnp121","article-title":"Anterior cingulate cortex: Unique role in cognition and emotion","volume":"23","author":"Stevens","year":"2011","journal-title":"J. Neuropsychiatry Clin. Neurosci."},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"fcab125","DOI":"10.1093\/braincomms\/fcab125","article-title":"The role of the medial prefrontal cortex in cognition, ageing and dementia","volume":"3","author":"Jobson","year":"2021","journal-title":"Brain Commun."},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"6691","DOI":"10.1523\/JNEUROSCI.0140-16.2016","article-title":"Distinct Fos-Expressing Neuronal Ensembles in the Ventromedial Prefrontal Cortex Mediate Food Reward and Extinction Memories","volume":"36","author":"Warren","year":"2016","journal-title":"J. Neurosci."},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"520","DOI":"10.1101\/lm.1474609","article-title":"Inactivation of the infralimbic but not the prelimbic cortex impairs consolidation and retrieval of fear extinction","volume":"16","author":"Laurent","year":"2009","journal-title":"Learn. Mem."},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"231","DOI":"10.1016\/j.conb.2010.02.005","article-title":"Prefrontal control of fear: More than just extinction","volume":"20","author":"Quirk","year":"2010","journal-title":"Curr. Opin. Neurobiol."},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"fcaa196","DOI":"10.1093\/braincomms\/fcaa196","article-title":"The orbitofrontal cortex: Reward, emotion and depression","volume":"2","author":"Rolls","year":"2020","journal-title":"Brain Commun."},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"120","DOI":"10.1503\/jpn.180032","article-title":"Lateral orbitofrontal dysfunction in the Sapap3 knockout mouse model of obsessive-compulsive disorder","volume":"44","author":"Lei","year":"2019","journal-title":"J. Psychiatry Neurosci."},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"14823","DOI":"10.1038\/ncomms14823","article-title":"Lateral orbitofrontal cortex anticipates choices and integrates prior with current information","volume":"8","author":"Nogueira","year":"2017","journal-title":"Nat. Commun."},{"key":"ref_22","doi-asserted-by":"crossref","first-page":"195","DOI":"10.3389\/fnbeh.2017.00195","article-title":"Neurobehavioral Abnormalities Associated with Executive Dysfunction after Traumatic Brain Injury","volume":"11","author":"Wood","year":"2017","journal-title":"Front. Behav. Neurosci."},{"key":"ref_23","doi-asserted-by":"crossref","first-page":"2086","DOI":"10.1093\/cercor\/bhs190","article-title":"Resting-state synchrony during early alcohol abstinence can predict subsequent relapse","volume":"23","author":"Camchong","year":"2013","journal-title":"Cereb. Cortex"},{"key":"ref_24","doi-asserted-by":"crossref","first-page":"771","DOI":"10.1111\/j.1530-0277.2010.01149.x","article-title":"Increased activation of the ACC during a spatial working memory task in alcohol-dependence versus heavy social drinking","volume":"34","author":"Hermann","year":"2010","journal-title":"Alcohol. Clin. Exp. Res."},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"12","DOI":"10.1111\/j.1749-6632.2012.06768.x","article-title":"Associative learning mechanisms underpinning the transition from recreational drug use to addiction","volume":"1282","author":"Hogarth","year":"2013","journal-title":"Ann. N. Y. Acad. Sci."},{"key":"ref_26","doi-asserted-by":"crossref","first-page":"561","DOI":"10.1038\/nrn2515","article-title":"The glutamate homeostasis hypothesis of addiction","volume":"10","author":"Kalivas","year":"2009","journal-title":"Nat. Rev. Neurosci."},{"key":"ref_27","doi-asserted-by":"crossref","first-page":"276","DOI":"10.1016\/j.neubiorev.2009.11.016","article-title":"Prefrontal cortex plasticity mechanisms in drug seeking and relapse","volume":"35","author":"Spijker","year":"2010","journal-title":"Neurosci. Biobehav. Rev."},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"14383","DOI":"10.1523\/JNEUROSCI.2551-07.2007","article-title":"Immediate reward bias in humans: Fronto-parietal networks and a role for the catechol-O-methyltransferase 158(Val\/Val) genotype","volume":"27","author":"Boettiger","year":"2007","journal-title":"J. Neurosci."},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"1845","DOI":"10.1111\/j.1530-0277.2006.00221.x","article-title":"Reduced glial and neuronal packing density in the orbitofrontal cortex in alcohol dependence and its relationship with suicide and duration of alcohol dependence","volume":"30","author":"Overholser","year":"2006","journal-title":"Alcohol. Clin. Exp. Res."},{"key":"ref_30","doi-asserted-by":"crossref","first-page":"1712","DOI":"10.1111\/j.1530-0277.2000.tb01973.x","article-title":"Binge ethanol consumption causes differential brain damage in young adolescent rats compared with adult rats","volume":"24","author":"Crews","year":"2000","journal-title":"Alcohol. Clin. Exp. Res."},{"key":"ref_31","doi-asserted-by":"crossref","first-page":"745","DOI":"10.1176\/appi.ajp.157.5.745","article-title":"Age at first alcohol use: A risk factor for the development of alcohol disorders","volume":"157","author":"DeWit","year":"2000","journal-title":"Am. J. Psychiatry"},{"key":"ref_32","doi-asserted-by":"crossref","first-page":"786293","DOI":"10.3389\/fncir.2021.786293","article-title":"From Synapses to Circuits, Astrocytes Regulate Behavior","volume":"15","author":"Lyon","year":"2021","journal-title":"Front. Neural Circuits"},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"658343","DOI":"10.3389\/fncir.2021.658343","article-title":"Transient Astrocytic Gq Signaling Underlies Remote Memory Enhancement","volume":"15","author":"Iwai","year":"2021","journal-title":"Front. Neural Circuits"},{"key":"ref_34","doi-asserted-by":"crossref","first-page":"1229","DOI":"10.1038\/s41593-020-0679-6","article-title":"Astrocytes contribute to remote memory formation by modulating hippocampal-cortical communication during learning","volume":"23","author":"Kol","year":"2020","journal-title":"Nat. Neurosci."},{"key":"ref_35","doi-asserted-by":"crossref","first-page":"500","DOI":"10.1038\/s41386-020-0721-0","article-title":"Cortical astrocytes regulate ethanol consumption and intoxication in mice","volume":"46","author":"Erickson","year":"2021","journal-title":"Neuropsychopharmacology"},{"key":"ref_36","doi-asserted-by":"crossref","unstructured":"Walker, C.D., Risher, W.C., and Risher, M.L. (2020). Regulation of Synaptic Development by Astrocyte Signaling Factors and Their Emerging Roles in Substance Abuse. Cells, 9.","DOI":"10.3390\/cells9020297"},{"key":"ref_37","doi-asserted-by":"crossref","first-page":"3276","DOI":"10.1523\/JNEUROSCI.4707-08.2009","article-title":"Uniquely hominid features of adult human astrocytes","volume":"29","author":"Oberheim","year":"2009","journal-title":"J. Neurosci."},{"key":"ref_38","doi-asserted-by":"crossref","first-page":"7","DOI":"10.1186\/s13064-018-0104-y","article-title":"Astrocytes, neurons, synapses: A tripartite view on cortical circuit development","volume":"13","author":"Allen","year":"2018","journal-title":"Neural Dev."},{"key":"ref_39","doi-asserted-by":"crossref","first-page":"1719","DOI":"10.1002\/glia.23169","article-title":"Astrocyte-mediated synapse remodeling in the pathological brain","volume":"65","author":"Kim","year":"2017","journal-title":"Glia"},{"key":"ref_40","doi-asserted-by":"crossref","first-page":"331","DOI":"10.1523\/JNEUROSCI.4466-06.2007","article-title":"Direct astrocytic contacts regulate local maturation of dendritic spines","volume":"27","author":"Nishida","year":"2007","journal-title":"J. Neurosci."},{"key":"ref_41","doi-asserted-by":"crossref","first-page":"e04047","DOI":"10.7554\/eLife.04047","article-title":"Astrocytes refine cortical connectivity at dendritic spines","volume":"3","author":"Risher","year":"2014","journal-title":"Elife"},{"key":"ref_42","doi-asserted-by":"crossref","first-page":"13","DOI":"10.1002\/glia.20415","article-title":"Plasticity of perisynaptic astroglia during synaptogenesis in the mature rat hippocampus","volume":"55","author":"Witcher","year":"2007","journal-title":"Glia"},{"key":"ref_43","doi-asserted-by":"crossref","first-page":"192","DOI":"10.1038\/nature24638","article-title":"Astrocytic neuroligins control astrocyte morphogenesis and synaptogenesis","volume":"551","author":"Stogsdill","year":"2017","journal-title":"Nature"},{"key":"ref_44","doi-asserted-by":"crossref","first-page":"3244","DOI":"10.1038\/emboj.2009.249","article-title":"Neuroligin-1 performs neurexin-dependent and neurexin-independent functions in synapse validation","volume":"28","author":"Ko","year":"2009","journal-title":"EMBO J."},{"key":"ref_45","doi-asserted-by":"crossref","first-page":"98","DOI":"10.1016\/j.neuroscience.2018.12.044","article-title":"Region-Specific Differences in Morphometric Features and Synaptic Colocalization of Astrocytes During Development","volume":"400","author":"Testen","year":"2019","journal-title":"Neuroscience"},{"key":"ref_46","doi-asserted-by":"crossref","unstructured":"Carty, N., Nash, K.R., Brownlow, M., Cruite, D., Wilcock, D., Selenica, M.L., Lee, D.C., Gordon, M.N., and Morgan, D. (2013). Intracranial injection of AAV expressing NEP but not IDE reduces amyloid pathology in APP+PS1 transgenic mice. PLoS ONE, 8.","DOI":"10.1371\/journal.pone.0059626"},{"key":"ref_47","doi-asserted-by":"crossref","first-page":"41","DOI":"10.1016\/j.jneumeth.2004.05.013","article-title":"Ballistic labeling and dynamic imaging of astrocytes in organotypic hippocampal slice cultures","volume":"141","author":"Benediktsson","year":"2005","journal-title":"J. Neurosci. Methods"},{"key":"ref_48","doi-asserted-by":"crossref","first-page":"633","DOI":"10.1085\/jgp.201210949","article-title":"Imaging calcium microdomains within entire astrocyte territories and endfeet with GCaMPs expressed using adeno-associated viruses","volume":"141","author":"Shigetomi","year":"2013","journal-title":"J. Gen. Physiol."},{"key":"ref_49","doi-asserted-by":"crossref","first-page":"673","DOI":"10.1242\/jcs.110.5.673","article-title":"Retargeting of cytosolic proteins to the plasma membrane by the Lck protein tyrosine kinase dual acylation motif","volume":"110","author":"Zlatkine","year":"1997","journal-title":"J. Cell Sci."},{"key":"ref_50","doi-asserted-by":"crossref","first-page":"207","DOI":"10.1016\/j.biopsych.2015.12.022","article-title":"Cocaine Self-Administration and Extinction Leads to Reduced Glial Fibrillary Acidic Protein Expression and Morphometric Features of Astrocytes in the Nucleus Accumbens Core","volume":"80","author":"Scofield","year":"2016","journal-title":"Biol. Psychiatry"},{"key":"ref_51","doi-asserted-by":"crossref","first-page":"246","DOI":"10.3389\/fncel.2018.00246","article-title":"Region-Specific Reductions in Morphometric Properties and Synaptic Colocalization of Astrocytes Following Cocaine Self-Administration and Extinction","volume":"12","author":"Testen","year":"2018","journal-title":"Front. Cell. Neurosci."},{"key":"ref_52","doi-asserted-by":"crossref","first-page":"2403","DOI":"10.1111\/acer.12913","article-title":"Adolescent Intermittent Alcohol Exposure: Dysregulation of Thrombospondins and Synapse Formation are Associated with Decreased Neuronal Density in the Adult Hippocampus","volume":"39","author":"Risher","year":"2015","journal-title":"Alcohol. Clin. Exp. Res."},{"key":"ref_53","doi-asserted-by":"crossref","first-page":"e975","DOI":"10.1542\/peds.2008-0027","article-title":"Estimated blood alcohol concentrations for child and adolescent drinking and their implications for screening instruments","volume":"123","author":"Donovan","year":"2009","journal-title":"Pediatrics"},{"key":"ref_54","doi-asserted-by":"crossref","first-page":"149","DOI":"10.1016\/S0165-0270(99)00142-9","article-title":"A simple and sensitive antigen retrieval method for free-floating and slide-mounted tissue sections","volume":"93","author":"Jiao","year":"1999","journal-title":"J. Neurosci. Methods"},{"key":"ref_55","doi-asserted-by":"crossref","unstructured":"Risher, W.C., Ustunkaya, T., Singh Alvarado, J., and Eroglu, C. (2014). Rapid Golgi analysis method for efficient and unbiased classification of dendritic spines. PLoS ONE, 9.","DOI":"10.1371\/journal.pone.0107591"},{"key":"ref_56","doi-asserted-by":"crossref","first-page":"47","DOI":"10.1146\/annurev.neuro.31.060407.125646","article-title":"Balancing structure and function at hippocampal dendritic spines","volume":"31","author":"Bourne","year":"2008","journal-title":"Annu. Rev. Neurosci."},{"key":"ref_57","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1016\/j.neures.2006.09.017","article-title":"Factors critical for the plasticity of dendritic spines and memory storage","volume":"57","author":"Matsuzaki","year":"2007","journal-title":"Neurosci Res."},{"key":"ref_58","doi-asserted-by":"crossref","first-page":"2122","DOI":"10.1093\/cercor\/bhp282","article-title":"White Matter Development in Adolescence: A DTI Study","volume":"20","author":"Asato","year":"2010","journal-title":"Cereb. Cortex"},{"key":"ref_59","doi-asserted-by":"crossref","first-page":"2693","DOI":"10.1002\/cne.22359","article-title":"Prefrontal cortical inputs to the basal amygdala undergo pruning during late adolescence in the rat","volume":"518","author":"Cressman","year":"2010","journal-title":"J. Comp. Neurol."},{"key":"ref_60","doi-asserted-by":"crossref","first-page":"116","DOI":"10.1002\/cne.10376","article-title":"Amygdalo-cortical sprouting continues into early adulthood: Implications for the development of normal and abnormal function during adolescence","volume":"453","author":"Cunningham","year":"2002","journal-title":"J. Comp. Neurol."},{"key":"ref_61","doi-asserted-by":"crossref","first-page":"553","DOI":"10.1093\/cercor\/bhj003","article-title":"Frontostriatal Microstructure Modulates Efficient Recruitment of Cognitive Control","volume":"16","author":"Liston","year":"2005","journal-title":"Cereb. Cortex"},{"key":"ref_62","doi-asserted-by":"crossref","first-page":"961","DOI":"10.1016\/j.neuroscience.2006.10.015","article-title":"Neuron number decreases in the rat ventral, but not dorsal, medial prefrontal cortex between adolescence and adulthood","volume":"144","author":"Markham","year":"2007","journal-title":"Neuroscience"},{"key":"ref_63","doi-asserted-by":"crossref","first-page":"719","DOI":"10.1007\/s00787-012-0291-8","article-title":"Functional brain imaging across development","volume":"22","author":"Rubia","year":"2013","journal-title":"Eur. Child Adolesc. Psychiatry"},{"key":"ref_64","doi-asserted-by":"crossref","first-page":"290","DOI":"10.1016\/j.neuroimage.2010.04.009","article-title":"Development of functional and structural connectivity within the default mode network in young children","volume":"52","author":"Supekar","year":"2010","journal-title":"Neuroimage"},{"key":"ref_65","doi-asserted-by":"crossref","first-page":"810","DOI":"10.1111\/adb.12530","article-title":"Adolescent alcohol exposure decreases frontostriatal resting-state functional connectivity in adulthood","volume":"23","author":"Broadwater","year":"2018","journal-title":"Addict. Biol."},{"key":"ref_66","doi-asserted-by":"crossref","first-page":"671","DOI":"10.1111\/j.1530-0277.2010.01385.x","article-title":"Adolescent binge drinking alters adult brain neurotransmitter gene expression, behavior, brain regional volumes, and neurochemistry in mice","volume":"35","author":"Coleman","year":"2011","journal-title":"Alcohol. Clin. Exp. Res."},{"key":"ref_67","doi-asserted-by":"crossref","first-page":"142","DOI":"10.1016\/j.pbb.2013.11.021","article-title":"Adolescent binge ethanol treatment alters adult brain regional volumes, cortical extracellular matrix protein and behavioral flexibility","volume":"116","author":"Coleman","year":"2014","journal-title":"Pharmacol. Biochem. Behav."},{"key":"ref_68","doi-asserted-by":"crossref","first-page":"2570","DOI":"10.1038\/npp.2014.109","article-title":"Adolescent alcohol exposure reduces behavioral flexibility, promotes disinhibition, and increases resistance to extinction of ethanol self-administration in adulthood","volume":"39","author":"Gass","year":"2014","journal-title":"Neuropsychopharmacology"},{"key":"ref_69","doi-asserted-by":"crossref","first-page":"475","DOI":"10.1016\/j.neuroscience.2012.08.046","article-title":"Adolescent binge drinking increases expression of the danger signal receptor agonist HMGB1 and Toll-like receptors in the adult prefrontal cortex","volume":"226","author":"Vetreno","year":"2012","journal-title":"Neuroscience"},{"key":"ref_70","doi-asserted-by":"crossref","unstructured":"Hwang, S.N., Lee, J.S., Seo, K., and Lee, H. (2021). Astrocytic Regulation of Neural Circuits Underlying Behaviors. Cells, 10.","DOI":"10.3390\/cells10020296"},{"key":"ref_71","doi-asserted-by":"crossref","first-page":"439","DOI":"10.1146\/annurev-cellbio-100913-013053","article-title":"Astrocyte regulation of synaptic behavior","volume":"30","author":"Allen","year":"2014","journal-title":"Annu. Rev. Cell Dev. Biol."},{"key":"ref_72","doi-asserted-by":"crossref","first-page":"1903","DOI":"10.1113\/JP270988","article-title":"Role of astrocyte-synapse interactions in CNS disorders","volume":"595","author":"Caldwell","year":"2017","journal-title":"J. Physiol."},{"key":"ref_73","doi-asserted-by":"crossref","first-page":"21","DOI":"10.1016\/j.alcohol.2014.07.017","article-title":"Withdrawal from chronic intermittent alcohol exposure increases dendritic spine density in the lateral orbitofrontal cortex of mice","volume":"49","author":"McGuier","year":"2015","journal-title":"Alcohol"},{"key":"ref_74","doi-asserted-by":"crossref","first-page":"7495","DOI":"10.1523\/JNEUROSCI.0470-10.2010","article-title":"LRRTMs and neuroligins bind neurexins with a differential code to cooperate in glutamate synapse development","volume":"30","author":"Siddiqui","year":"2010","journal-title":"J. Neurosci."},{"key":"ref_75","doi-asserted-by":"crossref","first-page":"269","DOI":"10.3389\/fnmol.2019.00269","article-title":"Differential Properties of the Synaptogenic Activities of the Neurexin Ligands Neuroligin1 and LRRTM2","volume":"12","author":"Dagar","year":"2019","journal-title":"Front. Mol. Neurosci."},{"key":"ref_76","doi-asserted-by":"crossref","first-page":"799","DOI":"10.1016\/j.neuron.2009.12.019","article-title":"LRRTM2 interacts with Neurexin1 and regulates excitatory synapse formation","volume":"64","author":"Sylwestrak","year":"2009","journal-title":"Neuron"},{"key":"ref_77","doi-asserted-by":"crossref","first-page":"300","DOI":"10.1002\/glia.22930","article-title":"Sequential activation of microglia and astrocyte cytokine expression precedes increased Iba-1 or GFAP immunoreactivity following systemic immune challenge","volume":"64","author":"Norden","year":"2016","journal-title":"Glia"},{"key":"ref_78","doi-asserted-by":"crossref","first-page":"1553","DOI":"10.1089\/neu.2004.21.1553","article-title":"GFAP versus S100B in serum after traumatic brain injury: Relationship to brain damage and outcome","volume":"21","author":"Pelinka","year":"2004","journal-title":"J. Neurotrauma"},{"key":"ref_79","doi-asserted-by":"crossref","first-page":"202","DOI":"10.1002\/(SICI)1098-1136(199802)22:2<202::AID-GLIA11>3.0.CO;2-1","article-title":"Regulation of astrocyte GFAP expression by TGF-beta1 and FGF-2","volume":"22","author":"Reilly","year":"1998","journal-title":"Glia"},{"key":"ref_80","doi-asserted-by":"crossref","first-page":"1957","DOI":"10.1002\/jnr.24841","article-title":"Chemogenetic manipulation of astrocytic signaling in the basolateral amygdala reduces binge-like alcohol consumption in male mice","volume":"99","author":"Nwachukwu","year":"2021","journal-title":"J. Neurosci. Res."},{"key":"ref_81","doi-asserted-by":"crossref","first-page":"31","DOI":"10.1016\/j.alcohol.2022.02.002","article-title":"Sex-specific effects of adolescent intermittent ethanol exposure-induced dysregulation of hippocampal glial cells in adulthood","volume":"100","author":"Nwachukwu","year":"2022","journal-title":"Alcohol"},{"key":"ref_82","doi-asserted-by":"crossref","first-page":"481","DOI":"10.1038\/nature21029","article-title":"Neurotoxic reactive astrocytes are induced by activated microglia","volume":"541","author":"Liddelow","year":"2017","journal-title":"Nature"},{"key":"ref_83","doi-asserted-by":"crossref","first-page":"816","DOI":"10.1016\/0046-8177(95)90001-2","article-title":"Glial cytokines in Alzheimer\u2019s disease: Review and pathogenic implications","volume":"26","author":"Mrak","year":"1995","journal-title":"Hum. Pathol."},{"key":"ref_84","first-page":"1005","article-title":"Inflammation in Alzheimer disease: Driving force, bystander or beneficial response?","volume":"12","year":"2006","journal-title":"Nat. Med."},{"key":"ref_85","doi-asserted-by":"crossref","first-page":"2246","DOI":"10.1038\/s41598-018-20424-y","article-title":"Beneficial effects of low alcohol exposure, but adverse effects of high alcohol intake on glymphatic function","volume":"8","author":"Lundgaard","year":"2018","journal-title":"Sci. Rep."},{"key":"ref_86","doi-asserted-by":"crossref","first-page":"285","DOI":"10.1016\/j.molmed.2019.11.008","article-title":"Glymphatic System Impairment in Alzheimer\u2019s Disease and Idiopathic Normal Pressure Hydrocephalus","volume":"26","author":"Reeves","year":"2020","journal-title":"Trends Mol. Med."},{"key":"ref_87","doi-asserted-by":"crossref","first-page":"43","DOI":"10.1111\/j.1440-1819.2008.01904.x","article-title":"Alcohol consumption and transition of mild cognitive impairment to dementia","volume":"63","author":"Xu","year":"2009","journal-title":"Psychiatry Clin. Neurosci."}],"container-title":["Cells"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/2073-4409\/11\/19\/3111\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,11]],"date-time":"2025-10-11T00:45:42Z","timestamp":1760143542000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/2073-4409\/11\/19\/3111"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2022,10,2]]},"references-count":87,"journal-issue":{"issue":"19","published-online":{"date-parts":[[2022,10]]}},"alternative-id":["cells11193111"],"URL":"https:\/\/doi.org\/10.3390\/cells11193111","relation":{},"ISSN":["2073-4409"],"issn-type":[{"value":"2073-4409","type":"electronic"}],"subject":[],"published":{"date-parts":[[2022,10,2]]}}}