{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,6,4]],"date-time":"2026-06-04T04:37:37Z","timestamp":1780547857900,"version":"3.54.1"},"reference-count":81,"publisher":"Public Library of Science (PLoS)","issue":"5","license":[{"start":{"date-parts":[[2025,5,29]],"date-time":"2025-05-29T00:00:00Z","timestamp":1748476800000},"content-version":"vor","delay-in-days":0,"URL":"http:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"DOI":"10.13039\/100006781","name":"Giovanni Armenise-Harvard Foundation","doi-asserted-by":"publisher","award":["Career Development Award"],"award-info":[{"award-number":["Career Development Award"]}],"id":[{"id":"10.13039\/100006781","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/100000002","name":"National Institutes of Health","doi-asserted-by":"publisher","award":["AA017447"],"award-info":[{"award-number":["AA017447"]}],"id":[{"id":"10.13039\/100000002","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/100000002","name":"National Institutes of Health","doi-asserted-by":"publisher","award":["AA017447"],"award-info":[{"award-number":["AA017447"]}],"id":[{"id":"10.13039\/100000002","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":["www.plosone.org"],"crossmark-restriction":false},"short-container-title":["PLoS One"],"abstract":"<jats:p>Alcohol use disorders (AUD) are bidirectionally associated with significant sleep disturbances, yet the underlying neural mechanisms remain poorly understood. The Marchigian Sardinian alcohol Preferring (msP) rat is a validated preclinical model that mirrors several genetic and behavioral traits of patients with AUD. This study aimed to characterize the sleep-wake architecture and EEG spectral activity in na\u00efve msP rats compared to Wistar controls. We performed 24-hour polysomnography recordings, revealing that male msP rats (n\u2009=\u20099) spent 7.5% more time awake and less time in NREM sleep relative to Wistar rats (n\u2009=\u20099). This was accompanied by a more fragmented sleep-wake pattern, with a higher number of waking and sleep episodes, state transitions, and sleep fragmentation index. Spectral analysis demonstrated lower high-frequency power, with significant reductions in sigma and beta power during NREM sleep and increased theta\/beta ratios during wakefulness. Slow-wave activity, an indicator of sleep pressure, showed a blunted rise and fall across the sleep cycle in msP rats, with reduced amplitude and slope of slow waves during early sleep. Moreover, msP rats exhibited decreased spindle activity, with significantly lower spindle incidence, amplitude, and duration. These findings suggest that msP rats display significant sleep disturbances, including disrupted NREM sleep and altered spectral characteristics in brain activity that partially resemble changes reported in individuals with AUD. This altered sleep profile may reflect neural circuit dysfunctions linked to substance use vulnerability, offering potential insights into the neurobiological basis of sleep disturbances in these complex neuropsychiatric disorders.<\/jats:p>","DOI":"10.1371\/journal.pone.0324459","type":"journal-article","created":{"date-parts":[[2025,5,29]],"date-time":"2025-05-29T17:36:38Z","timestamp":1748540198000},"page":"e0324459","update-policy":"https:\/\/doi.org\/10.1371\/journal.pone.corrections_policy","source":"Crossref","is-referenced-by-count":1,"title":["Sleep phenotyping in a rat model of susceptibility to substance use disorders"],"prefix":"10.1371","volume":"20","author":[{"given":"Eleonora","family":"Ficiar\u00e0","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Oluwatomisin O.","family":"Faniyan","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Reyila","family":"Simayi","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-0248-2456","authenticated-orcid":true,"given":"Federico","family":"Del Gallo","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Marisa","family":"Roberto","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Roberto","family":"Ciccocioppo","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Michele","family":"Bellesi","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-5676-9279","authenticated-orcid":true,"given":"Luisa","family":"de Vivo","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"340","published-online":{"date-parts":[[2025,5,29]]},"reference":[{"issue":"4","key":"pone.0324459.ref001","doi-asserted-by":"crossref","first-page":"507","DOI":"10.1016\/j.addbeh.2012.01.006","article-title":"Global sleep quality as a moderator of alcohol consumption and consequences in college students","volume":"37","author":"SR Kenney","year":"2012","journal-title":"Addict Behav"},{"issue":"1","key":"pone.0324459.ref002","doi-asserted-by":"crossref","first-page":"89","DOI":"10.1111\/j.1365-2869.2012.01043.x","article-title":"Bidirectional associations between insomnia symptoms and unhealthy behaviours","volume":"22","author":"P Haario","year":"2013","journal-title":"J Sleep Res"},{"issue":"8","key":"pone.0324459.ref003","article-title":"Association between sleep patterns and alcohol use disorders in workers","volume":"19","author":"CR Kim","year":"2024","journal-title":"PLoS One"},{"key":"pone.0324459.ref004","doi-asserted-by":"crossref","first-page":"107913","DOI":"10.1016\/j.neuropharm.2019.107913","article-title":"Dose-dependent alcohol effects on electroencephalogram: sedation\/anesthesia is qualitatively distinct from sleep","volume":"164","author":"KP Abrahao","year":"2020","journal-title":"Neuropharmacol"},{"key":"pone.0324459.ref005","doi-asserted-by":"crossref","first-page":"415","DOI":"10.1016\/B978-0-444-62619-6.00024-0","article-title":"Alcohol and the sleeping brain","volume":"125","author":"IM Colrain","year":"2014","journal-title":"Handb Clin Neurol"},{"issue":"10","key":"pone.0324459.ref006","doi-asserted-by":"crossref","first-page":"1720","DOI":"10.1111\/acer.12141","article-title":"The acute effects of alcohol on sleep architecture in late adolescence","volume":"37","author":"J Chan","year":"2013","journal-title":"Alcohol Clin Exp Res"},{"issue":"4","key":"pone.0324459.ref007","doi-asserted-by":"crossref","first-page":"299","DOI":"10.1016\/j.alcohol.2014.07.019","article-title":"Alcohol disrupts sleep homeostasis","volume":"49","author":"MM Thakkar","year":"2015","journal-title":"Alcohol"},{"issue":"2","key":"pone.0324459.ref008","first-page":"110","article-title":"Alcohol\u2019s effects on sleep in alcoholics","volume":"25","author":"KJ Brower","year":"2001","journal-title":"Alcohol Res Health"},{"issue":"1","key":"pone.0324459.ref009","doi-asserted-by":"crossref","first-page":"50","DOI":"10.1016\/j.beth.2018.03.010","article-title":"The links between social anxiety disorder, insomnia symptoms, and alcohol use disorders: findings from a large sample of adolescents in the United States","volume":"50","author":"H Blumenthal","year":"2019","journal-title":"Behav Ther"},{"issue":"6","key":"pone.0324459.ref010","doi-asserted-by":"crossref","first-page":"523","DOI":"10.1016\/S1087-0792(03)90005-0","article-title":"Insomnia, alcoholism and relapse","volume":"7","author":"KJ Brower","year":"2003","journal-title":"Sleep Med Rev"},{"issue":"3","key":"pone.0324459.ref011","doi-asserted-by":"crossref","first-page":"287","DOI":"10.1093\/alcalc\/agz029","article-title":"The relationship between alcohol craving and insomnia symptoms in alcohol-dependent individuals","volume":"54","author":"S He","year":"2019","journal-title":"Alcohol Alcohol Oxf Oxfs"},{"key":"pone.0324459.ref012","doi-asserted-by":"crossref","first-page":"101435","DOI":"10.1016\/j.smrv.2021.101435","article-title":"Contribution of sleep disturbances to the heterogeneity of cognitive and brain alterations in alcohol use disorder","volume":"58","author":"A Laniepce","year":"2021","journal-title":"Sleep Med Rev"},{"issue":"2","key":"pone.0324459.ref013","doi-asserted-by":"crossref","first-page":"100231","DOI":"10.1016\/j.ejpsy.2023.100231","article-title":"Sleep features in alcohol use disorder: a systematic review and meta-analysis of polysomnographic findings in case-control studies","volume":"38","author":"P Yang","year":"2024","journal-title":"Eur J Psych"},{"issue":"5","key":"pone.0324459.ref014","doi-asserted-by":"crossref","first-page":"848","DOI":"10.1111\/acer.14808","article-title":"Self-reported sleep and circadian characteristics predict alcohol and cannabis use: a longitudinal analysis of the National consortium on alcohol and neurodevelopment in adolescence study","volume":"46","author":"BP Hasler","year":"2022","journal-title":"Alcohol Clin Exp Res"},{"issue":"6","key":"pone.0324459.ref015","doi-asserted-by":"crossref","first-page":"1154","DOI":"10.1111\/acer.13401","article-title":"Eveningness and later sleep timing are associated with greater risk for alcohol and marijuana use in adolescence: initial findings from the national consortium on alcohol and neurodevelopment in adolescence study","volume":"41","author":"BP Hasler","year":"2017","journal-title":"Alcohol Clin Exp Res"},{"issue":"4","key":"pone.0324459.ref016","doi-asserted-by":"crossref","first-page":"377","DOI":"10.1016\/j.alcohol.2014.06.010","article-title":"Sleep and circadian contributions to adolescent alcohol use disorder","volume":"49","author":"BP Hasler","year":"2015","journal-title":"Alcohol"},{"key":"pone.0324459.ref017","doi-asserted-by":"crossref","first-page":"108446","DOI":"10.1016\/j.neuropharm.2020.108446","article-title":"Genetically selected alcohol-preferring msP rats to study alcohol use disorder: anything lost in translation?","volume":"186","author":"AM Borruto","year":"2021","journal-title":"Neuropharmacology"},{"key":"pone.0324459.ref018","doi-asserted-by":"crossref","first-page":"3","DOI":"10.3389\/fnbeh.2019.00003","article-title":"Sub-dimensions of alcohol use disorder in alcohol preferring and non-preferring rats, a comparative study","volume":"13","author":"A Domi","year":"2019","journal-title":"Front Behav Neurosci"},{"issue":"2","key":"pone.0324459.ref019","doi-asserted-by":"crossref","first-page":"151","DOI":"10.1007\/s002130050988","article-title":"Antidepressant-like effect of ethanol revealed in the forced swimming test in Sardinian alcohol-preferring rats","volume":"144","author":"R Ciccocioppo","year":"1999","journal-title":"Psychopharmacology (Berl)"},{"issue":"6","key":"pone.0324459.ref020","doi-asserted-by":"crossref","first-page":"1083","DOI":"10.1007\/s00213-014-3743-7","article-title":"Polymorphism in the corticotropin-releasing factor receptor 1 (CRF1-R) gene plays a role in shaping the high anxious phenotype of Marchigian Sardinian alcohol-preferring (msP) rats","volume":"232","author":"A Cippitelli","year":"2015","journal-title":"Psychopharmacology (Berl)"},{"key":"pone.0324459.ref021","doi-asserted-by":"crossref","first-page":"339","DOI":"10.1111\/j.1369-1600.2006.00032.x","article-title":"Genetically selected Marchigian Sardinian alcohol-preferring (msP) rats: an animal model to study the neurobiology of alcoholism","volume":"11","author":"R Ciccocioppo","year":"2006","journal-title":"Addict Biol"},{"issue":"1","key":"pone.0324459.ref022","doi-asserted-by":"crossref","first-page":"30","DOI":"10.1111\/j.1369-1600.2007.00050.x","article-title":"Region-specific down-regulation of Crhr1 gene expression in alcohol-preferring msP rats following ad lib access to alcohol","volume":"12","author":"AC Hansson","year":"2007","journal-title":"Addict Biol"},{"issue":"6","key":"pone.0324459.ref023","doi-asserted-by":"crossref","first-page":"3095","DOI":"10.3390\/ijms22063095","article-title":"Glucocorticoid receptor antagonist mifepristone does not alter innate anxiety-like behavior in genetically-selected Marchigian Sardinian (msP) rats","volume":"22","author":"V Vozella","year":"2021","journal-title":"Int J Mol Sci"},{"issue":"41","key":"pone.0324459.ref024","doi-asserted-by":"crossref","first-page":"15236","DOI":"10.1073\/pnas.0604419103","article-title":"Variation at the rat Crhr1 locus and sensitivity to relapse into alcohol seeking induced by environmental stress","volume":"103","author":"AC Hansson","year":"2006","journal-title":"Proc Natl Acad Sci U S A"},{"key":"pone.0324459.ref025","doi-asserted-by":"crossref","first-page":"100038","DOI":"10.1016\/j.addicn.2022.100038","article-title":"Corticotropin releasing factor and drug seeking in substance use disorders: preclinical evidence and translational limitations","volume":"4","author":"JR Mantsch","year":"2022","journal-title":"Addict Neurosci"},{"issue":"6","key":"pone.0324459.ref026","doi-asserted-by":"crossref","first-page":"594","DOI":"10.1038\/sj.mp.4001813","article-title":"Genetic association of the human corticotropin releasing hormone receptor 1 (CRHR1) with binge drinking and alcohol intake patterns in two independent samples","volume":"11","author":"J Treutlein","year":"2006","journal-title":"Mol Psychiatry"},{"key":"pone.0324459.ref027","doi-asserted-by":"crossref","first-page":"112","DOI":"10.1016\/j.neuroimage.2012.12.015","article-title":"Reduced limbic metabolism and fronto-cortical volume in rats vulnerable to alcohol addiction","volume":"69","author":"A Gozzi","year":"2013","journal-title":"Neuroimage"},{"issue":"12","key":"pone.0324459.ref028","doi-asserted-by":"crossref","first-page":"2431","DOI":"10.1038\/npp.2011.129","article-title":"Neuroimaging evidence of altered fronto-cortical and striatal function after prolonged cocaine self-administration in the rat","volume":"36","author":"A Gozzi","year":"2011","journal-title":"Neuropsychopharmacology"},{"key":"pone.0324459.ref029","doi-asserted-by":"crossref","first-page":"324","DOI":"10.1111\/j.1369-1600.2006.00031.x","article-title":"Phenotypic characterization of genetically selected Sardinian alcohol-preferring (sP) and -non-preferring (sNP) rats","volume":"11","author":"G Colombo","year":"2006","journal-title":"Addict Biol"},{"issue":"4","key":"pone.0324459.ref030","doi-asserted-by":"crossref","first-page":"045003","DOI":"10.1088\/1741-2552\/aa5eea","article-title":"Open Ephys: an open-source, plugin-based platform for multichannel electrophysiology","volume":"14","author":"JH Siegle","year":"2017","journal-title":"J Neural Eng"},{"key":"pone.0324459.ref031","volume-title":"The AASM manual for the scoring of sleep and associated events: rules, terminology and technical specifications","author":"C Iber","year":"2007"},{"issue":"36","key":"pone.0324459.ref032","doi-asserted-by":"crossref","first-page":"15939","DOI":"10.1073\/pnas.1002570107","article-title":"Sleep homeostasis in the rat is preserved during chronic sleep restriction","volume":"107","author":"S Leemburg","year":"2010","journal-title":"Proc Natl Acad Sci U S A"},{"issue":"7","key":"pone.0324459.ref033","doi-asserted-by":"crossref","first-page":"909","DOI":"10.5665\/sleep.1950","article-title":"Extracellular levels of lactate, but not oxygen, reflect sleep homeostasis in the rat cerebral cortex","volume":"35","author":"MB Dash","year":"2012","journal-title":"Sleep"},{"key":"pone.0324459.ref034","doi-asserted-by":"crossref","DOI":"10.7554\/eLife.70092","article-title":"An open-source, high-performance tool for automated sleep staging","volume":"10","author":"R Vallat","year":"2021","journal-title":"eLife"},{"key":"pone.0324459.ref035","doi-asserted-by":"crossref","first-page":"123","DOI":"10.1186\/1471-2105-7-123","article-title":"Detecting outliers when fitting data with nonlinear regression - a new method based on robust nonlinear regression and the false discovery rate","volume":"7","author":"HJ Motulsky","year":"2006","journal-title":"BMC Bioinform"},{"issue":"4","key":"pone.0324459.ref036","doi-asserted-by":"crossref","DOI":"10.1111\/jsr.13598","article-title":"The two-process model of sleep regulation: beginnings and outlook","volume":"31","author":"A Borb\u00e9ly","year":"2022","journal-title":"J Sleep Res"},{"issue":"12","key":"pone.0324459.ref037","doi-asserted-by":"crossref","first-page":"1631","DOI":"10.1093\/sleep\/30.12.1631","article-title":"Sleep homeostasis and cortical synchronization: II. A local field potential study of sleep slow waves in the rat","volume":"30","author":"VV Vyazovskiy","year":"2007","journal-title":"Sleep"},{"issue":"2","key":"pone.0324459.ref038","doi-asserted-by":"crossref","first-page":"805","DOI":"10.1152\/physrev.00042.2018","article-title":"Sleep spindles: mechanisms and functions","volume":"100","author":"LMJ Fernandez","year":"2020","journal-title":"Physiol Rev"},{"key":"pone.0324459.ref039","doi-asserted-by":"crossref","first-page":"337","DOI":"10.1016\/j.neuropharm.2012.11.026","article-title":"Enhanced GABAergic transmission in the central nucleus of the amygdala of genetically selected Marchigian Sardinian rats: alcohol and CRF effects","volume":"67","author":"MA Herman","year":"2013","journal-title":"Neuropharmacology"},{"issue":"2","key":"pone.0324459.ref040","doi-asserted-by":"crossref","first-page":"111","DOI":"10.1016\/0960-5428(95)00003-K","article-title":"The hypothalamic-pituitary-adrenocortical system and sleep in man","volume":"5","author":"E Friess","year":"1995","journal-title":"Adv Neuroimmunol"},{"issue":"1","key":"pone.0324459.ref041","doi-asserted-by":"crossref","first-page":"67","DOI":"10.1016\/S0031-9384(97)00390-9","article-title":"Rat strain differences suggest a role for corticotropin-releasing hormone in modulating sleep","volume":"63","author":"MR Opp","year":"1997","journal-title":"Physiol Behav"},{"issue":"5","key":"pone.0324459.ref042","doi-asserted-by":"crossref","first-page":"445","DOI":"10.1016\/S0149-7634(01)00024-0","article-title":"Corticotropin-releasing hormone (CRH) as a regulator of waking","volume":"25","author":"F Chang","year":"2001","journal-title":"Neurosci Biobehav Rev"},{"key":"pone.0324459.ref043","doi-asserted-by":"crossref","first-page":"41","DOI":"10.1016\/j.bbr.2014.11.006","article-title":"The crf\u2081 receptor antagonist ssr125543 prevents stress-induced long-lasting sleep disturbances in a mouse model of ptsd: comparison with paroxetine and d-cycloserine","volume":"279","author":"J Philbert","year":"2015","journal-title":"Behav Brain Res"},{"issue":"2","key":"pone.0324459.ref044","doi-asserted-by":"crossref","first-page":"154","DOI":"10.1038\/mp.2009.46","article-title":"Conditional corticotropin-releasing hormone overexpression in the mouse forebrain enhances rapid eye movement sleep","volume":"15","author":"M Kimura","year":"2010","journal-title":"Mol Psychiatry"},{"key":"pone.0324459.ref045","doi-asserted-by":"crossref","first-page":"251","DOI":"10.1007\/978-3-642-28720-6_199","article-title":"Genetically selected alcohol preferring rats to model human alcoholism","volume":"13","author":"R Ciccocioppo","year":"2013","journal-title":"Curr Top Behav Neurosci"},{"key":"pone.0324459.ref046","doi-asserted-by":"crossref","first-page":"18950","DOI":"10.1038\/s41598-019-55427-w","article-title":"Effect of aldh2 on sleep disturbances in patients with Parkinson\u2019s disease","volume":"9","author":"CY Lin","year":"2019","journal-title":"Sci Rep"},{"issue":"6","key":"pone.0324459.ref047","doi-asserted-by":"crossref","DOI":"10.1093\/sleep\/zsz046","article-title":"Genome-wide association meta-analysis and Mendelian randomization analysis confirm the influence of ALDH2 on sleep duration in the Japanese population","volume":"42","author":"T Nishiyama","year":"2019","journal-title":"Sleep"},{"issue":"1","key":"pone.0324459.ref048","doi-asserted-by":"crossref","first-page":"30424","DOI":"10.1038\/srep30424","article-title":"Aldehyde dehydrogenase 2 is associated with cognitive functions in patients with Parkinson\u2019s disease","volume":"6","author":"RL Yu","year":"2016","journal-title":"Sci Rep"},{"issue":"15","key":"pone.0324459.ref049","doi-asserted-by":"crossref","first-page":"3533","DOI":"10.1016\/S0021-9258(18)99864-9","article-title":"Brain aldehyde dehydrogenase: localization, purification, and properties","volume":"241","author":"VG Erwin","year":"1966","journal-title":"J Biol Chem"},{"issue":"2","key":"pone.0324459.ref050","doi-asserted-by":"crossref","first-page":"125","DOI":"10.1124\/pr.59.2.1","article-title":"Neurotoxicity and metabolism of the catecholamine-derived 3,4-dihydroxyphenylacetaldehyde and 3,4-dihydroxyphenylglycolaldehyde: the role of aldehyde dehydrogenase","volume":"59","author":"SA Marchitti","year":"2007","journal-title":"Pharmacol Rev"},{"key":"pone.0324459.ref051","doi-asserted-by":"crossref","first-page":"16","DOI":"10.1016\/j.cotox.2018.12.002","article-title":"Biogenic aldehyde-mediated mechanisms of toxicity in neurodegenerative disease","volume":"13","author":"BS Cagle","year":"2019","journal-title":"Curr Opin Toxicol"},{"issue":"5","key":"pone.0324459.ref052","doi-asserted-by":"crossref","first-page":"374","DOI":"10.1177\/1087054712460087","article-title":"A decade of EEG Theta\/Beta ratio research in ADHD: a meta-analysis","volume":"17","author":"M Arns","year":"2013","journal-title":"J Atten Disord"},{"key":"pone.0324459.ref053","doi-asserted-by":"crossref","first-page":"49","DOI":"10.1016\/j.biopsycho.2016.09.008","article-title":"Frontal EEG theta\/beta ratio as an electrophysiological marker for attentional control and its test-retest reliability","volume":"121","author":"A Angelidis","year":"2016","journal-title":"Biol Psychol"},{"issue":"3","key":"pone.0324459.ref054","doi-asserted-by":"crossref","first-page":"598","DOI":"10.3758\/s13415-015-0351-x","article-title":"Spontaneous EEG theta\/beta ratio and delta-beta coupling in relation to attentional network functioning and self-reported attentional control","volume":"15","author":"A Morillas-Romero","year":"2015","journal-title":"Cogn Affect Behav Neurosci"},{"issue":"3","key":"pone.0324459.ref055","doi-asserted-by":"crossref","first-page":"365","DOI":"10.1016\/j.ijpsycho.2014.09.003","article-title":"Spontaneous eeg activity and spontaneous emotion regulation","volume":"94","author":"M Tortella-Feliu","year":"2014","journal-title":"Int J Psychophysiol"},{"issue":"2","key":"pone.0324459.ref056","doi-asserted-by":"crossref","first-page":"73","DOI":"10.1016\/j.biopsycho.2009.10.008","article-title":"Eeg theta\/beta ratio in relation to fear-modulated response-inhibition, attentional control, and affective traits","volume":"83","author":"P Putman","year":"2010","journal-title":"Biol Psychol"},{"issue":"7","key":"pone.0324459.ref057","doi-asserted-by":"crossref","first-page":"500","DOI":"10.1016\/j.biopsych.2017.01.005","article-title":"Constitutive increases in amygdalar corticotropin-releasing factor and fatty acid amide hydrolase drive an anxious phenotype","volume":"82","author":"LA Natividad","year":"2017","journal-title":"Biol Psychiatry"},{"key":"pone.0324459.ref058","doi-asserted-by":"crossref","DOI":"10.3389\/fpsyt.2013.00023","article-title":"Role of a genetic polymorphism in the corticotropin-releasing factor receptor 1 gene in alcohol drinking and seeking behaviors of Marchigian Sardinian alcohol-preferring rats","volume":"4","author":"L Ayanwuyi","year":"2013","journal-title":"Front Psychiatry"},{"issue":"1","key":"pone.0324459.ref059","doi-asserted-by":"crossref","first-page":"5","DOI":"10.3390\/ctn8010005","article-title":"The two-process model: origin of its concepts and their implications","volume":"8","author":"A Borb\u00e9ly","year":"2024","journal-title":"Clin Transl Neurosci"},{"issue":"1","key":"pone.0324459.ref060","doi-asserted-by":"crossref","first-page":"49","DOI":"10.1016\/j.smrv.2005.05.002","article-title":"Sleep function and synaptic homeostasis","volume":"10","author":"G Tononi","year":"2006","journal-title":"Sleep Med Rev"},{"key":"pone.0324459.ref061","doi-asserted-by":"crossref","first-page":"47","DOI":"10.1016\/j.jpsychires.2016.12.018","article-title":"Widespread reduction in sleep spindle activity in socially anxious children and adolescents","volume":"88","author":"I Wilhelm","year":"2017","journal-title":"J Psychiatr Res"},{"issue":"5","key":"pone.0324459.ref062","doi-asserted-by":"crossref","first-page":"30","DOI":"10.1007\/s11920-019-1013-4","article-title":"An integrated model of slow-wave activity and neuroplasticity impairments in major depressive disorder","volume":"21","author":"JR Goldschmied","year":"2019","journal-title":"Curr Psychiatry Rep"},{"issue":"433","key":"pone.0324459.ref063","doi-asserted-by":"crossref","first-page":"104","DOI":"10.1111\/j.1600-0447.2007.00968.x","article-title":"Sleep and circadian rhythms in mood disorders","author":"R Armitage","year":"2007","journal-title":"Acta Psychiatr Scand Suppl"},{"issue":"9","key":"pone.0324459.ref064","doi-asserted-by":"crossref","first-page":"1530","DOI":"10.1111\/j.1530-0277.2012.01756.x","article-title":"Adolescence and parental history of alcoholism: insights from the sleep EEG","volume":"36","author":"L Tarokh","year":"2012","journal-title":"Alcohol Clin Exp Res"},{"key":"pone.0324459.ref065","doi-asserted-by":"crossref","first-page":"165","DOI":"10.1111\/j.1365-2869.2009.00763.x","article-title":"Sleep electroencephalogram in children with a parental history of alcohol abuse\/dependence","volume":"19","author":"L Tarokh","year":"2010","journal-title":"J Sleep Res"},{"key":"pone.0324459.ref066","doi-asserted-by":"crossref","first-page":"110114","DOI":"10.1016\/j.neuropharm.2024.110114","article-title":"Alcohol, flexible behavior, and the prefrontal cortex: functional changes underlying impaired cognitive flexibility","volume":"260","author":"KE Nippert","year":"2024","journal-title":"Neuropharmacol"},{"issue":"5","key":"pone.0324459.ref067","doi-asserted-by":"crossref","DOI":"10.1111\/adb.13004","article-title":"Impaired cognitive flexibility and heightened urgency are associated with increased alcohol consumption in rodent models of excessive drinking","volume":"26","author":"E De Falco","year":"2021","journal-title":"Addict Biol"},{"key":"pone.0324459.ref068","doi-asserted-by":"crossref","first-page":"95","DOI":"10.1016\/j.alcohol.2018.04.007","article-title":"Low cognitive flexibility as a risk for heavy alcohol drinking in non-human primates","volume":"74","author":"TA Shnitko","year":"2019","journal-title":"Alcohol"},{"issue":"3","key":"pone.0324459.ref069","article-title":"Reward-related attentional bias and adolescent substance use: a prognostic relationship?","volume":"10","author":"Me Hemel-Ruiter","year":"2015","journal-title":"PLoS One"},{"issue":"10","key":"pone.0324459.ref070","doi-asserted-by":"crossref","first-page":"980","DOI":"10.1016\/j.biopsych.2021.01.009","article-title":"Model-based and model-free control predicts alcohol consumption developmental trajectory in young adults: a 3-year prospective study","volume":"89","author":"H Chen","year":"2021","journal-title":"Biol Psychiatry"},{"issue":"5","key":"pone.0324459.ref071","doi-asserted-by":"crossref","first-page":"685","DOI":"10.15288\/jsad.2010.71.685","article-title":"Do premorbid predictors of alcohol dependence also predict the failure to recover from alcoholism?","volume":"71","author":"E Penick","year":"2010","journal-title":"J Stud Alcohol Drugs"},{"issue":"9","key":"pone.0324459.ref072","doi-asserted-by":"crossref","DOI":"10.1136\/bmjopen-2019-028997","article-title":"Intelligence in young adulthood and alcohol use disorders in a prospective cohort study of Danish men: the role of psychiatric disorders and parental psychiatric history","volume":"9","author":"E Just-\u00d8stergaard","year":"2019","journal-title":"BMJ Open"},{"key":"pone.0324459.ref073","doi-asserted-by":"crossref","first-page":"105295","DOI":"10.1016\/j.neubiorev.2023.105295","article-title":"Neurocognitive predictors of addiction-related outcomes: a systematic review of longitudinal studies","volume":"152","author":"E Christensen","year":"2023","journal-title":"Neurosci Biobehav Rev"},{"key":"pone.0324459.ref074","doi-asserted-by":"crossref","first-page":"78","DOI":"10.1016\/j.jpsychires.2016.03.014","article-title":"Executive functioning before and after onset of alcohol use disorder in adolescence. A TRAILS study","volume":"78","author":"SR Boelema","year":"2016","journal-title":"J Psychiatr Res"},{"issue":"4","key":"pone.0324459.ref075","doi-asserted-by":"crossref","first-page":"344","DOI":"10.1177\/15500594221076347","article-title":"Resting-state EEG, substance use and abstinence after chronic use: a systematic review","volume":"53","author":"Y Liu","year":"2022","journal-title":"Clin EEG Neurosci"},{"key":"pone.0324459.ref076","doi-asserted-by":"crossref","first-page":"153","DOI":"10.1016\/j.brainres.2008.06.053","article-title":"Uncovering genes for cognitive (dys)function and predisposition for alcoholism spectrum disorders: a review of human brain oscillations as effective endophenotypes","volume":"1235","author":"M Rangaswamy","year":"2008","journal-title":"Brain Res"},{"issue":"8","key":"pone.0324459.ref077","doi-asserted-by":"crossref","first-page":"831","DOI":"10.1016\/S0006-3223(02)01362-8","article-title":"Beta power in the EEG of alcoholics","volume":"52","author":"M Rangaswamy","year":"2002","journal-title":"Biol Psychiatry"},{"issue":"2","key":"pone.0324459.ref078","doi-asserted-by":"crossref","first-page":"347","DOI":"10.1016\/j.neuroimage.2005.02.008","article-title":"On the human sensorimotor-cortex beta rhythm: sources and modeling","volume":"26","author":"O Jensen","year":"2005","journal-title":"Neuroimage"},{"issue":"4","key":"pone.0324459.ref079","doi-asserted-by":"crossref","first-page":"705","DOI":"10.1086\/383283","article-title":"Variations in GABRA2, encoding the alpha 2 subunit of the GABA(A) receptor, are associated with alcohol dependence and with brain oscillations","volume":"74","author":"HJ Edenberg","year":"2004","journal-title":"Am J Hum Genet"},{"key":"pone.0324459.ref080","doi-asserted-by":"crossref","first-page":"21","DOI":"10.1016\/j.neuropharm.2015.10.027","article-title":"Glutamatergic transmission in the central nucleus of the amygdala is selectively altered in Marchigian Sardinian alcohol-preferring rats: alcohol and CRF effects","volume":"102","author":"MA Herman","year":"2016","journal-title":"Neuropharmacology"},{"issue":"1","key":"pone.0324459.ref081","doi-asserted-by":"crossref","first-page":"22","DOI":"10.1016\/j.neuroscience.2010.07.005","article-title":"Sleep-wakefulness in alcohol preferring (P) and non-preferring (NP) rats following binge alcohol administration","volume":"170","author":"M Thakkar","year":"2010","journal-title":"Neurosci"}],"container-title":["PLOS One"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/dx.plos.org\/10.1371\/journal.pone.0324459","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,5,29]],"date-time":"2025-05-29T17:37:02Z","timestamp":1748540222000},"score":1,"resource":{"primary":{"URL":"https:\/\/dx.plos.org\/10.1371\/journal.pone.0324459"}},"subtitle":[],"editor":[{"given":"Alessandro","family":"Silvani","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"editor"}]}],"short-title":[],"issued":{"date-parts":[[2025,5,29]]},"references-count":81,"journal-issue":{"issue":"5","published-online":{"date-parts":[[2025,5,29]]}},"URL":"https:\/\/doi.org\/10.1371\/journal.pone.0324459","relation":{},"ISSN":["1932-6203"],"issn-type":[{"value":"1932-6203","type":"electronic"}],"subject":[],"published":{"date-parts":[[2025,5,29]]}}}