{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,11,10]],"date-time":"2026-11-10T18:25:57Z","timestamp":1794335157077,"version":"4.9.0"},"reference-count":43,"publisher":"Springer Science and Business Media LLC","issue":"7","license":[{"start":{"date-parts":[[2022,12,31]],"date-time":"2022-12-31T00:00:00Z","timestamp":1672444800000},"content-version":"tdm","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0"},{"start":{"date-parts":[[2022,12,31]],"date-time":"2022-12-31T00:00:00Z","timestamp":1672444800000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0"}],"funder":[{"DOI":"10.13039\/501100004359","name":"Vetenskapsr\u00e5det","doi-asserted-by":"publisher","award":["2018-02320"],"award-info":[{"award-number":["2018-02320"]}],"id":[{"id":"10.13039\/501100004359","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":["link.springer.com"],"crossmark-restriction":false},"short-container-title":["Neuropsychopharmacol."],"published-print":{"date-parts":[[2023,6]]},"abstract":"<jats:title>Abstract<\/jats:title>\n                  <jats:p>Animal models of substance use disorders have been criticized for their limited translation. One important factor behind seeking and taking that has so far been largely overlooked is the availability of alternative non-drug rewards. We recently reported that only about 15% of outbred Wistar rats will choose alcohol over a sweet solution of saccharin. It was also shown using a novel operant model of choice of drugs over social rewards that social interaction consistently attenuates self-administration and incubation of craving for stimulants and opioids. Whether this is also true for alcohol and choice of alcohol over a sweet reward translates to social rewards is currently unknown. We therefore evaluated choice between alcohol and a social reward in different experimental settings in both male and female Wistar rats. We found, in contrast to prior work that employed discrete choice of drugs vs. social reward, that rats almost exclusively prefer alcohol over social interaction, irrespective of the nature of the social partner (cagemate vs. novel rat), the length of interaction, housing conditions and sex. Alcohol choice was reduced when the response requirement for alcohol was increased. However, rats persisted in choosing alcohol, even when the effort required to obtain it was 10\u201316 times higher (for females and males respectively) than the one for the social reward. Altogether, these results indicate that the social choice model may not generalize to alcohol, pointing to the possibility that specific interactions between alcohol and social reward, not seen when a sweet solution is used as an alternative to the drug, may play a crucial role in alcohol vs. social choice experiments.<\/jats:p>","DOI":"10.1038\/s41386-022-01526-8","type":"journal-article","created":{"date-parts":[[2022,12,31]],"date-time":"2022-12-31T04:07:38Z","timestamp":1672459658000},"page":"1098-1107","update-policy":"https:\/\/doi.org\/10.1007\/springer_crossmark_policy","source":"Crossref","is-referenced-by-count":31,"title":["Wistar rats choose alcohol over social interaction in a discrete-choice model"],"prefix":"10.1038","volume":"48","author":[{"given":"Ga\u00eblle","family":"Augier","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Veronika","family":"Schwabl","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Asmae","family":"Lguensat","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Mihai","family":"Atudorei","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Osamudiamen Consoler","family":"Iyere","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Sandra Eriksson","family":"Solander","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-5615-2973","authenticated-orcid":false,"given":"Eric","family":"Augier","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"297","published-online":{"date-parts":[[2022,12,31]]},"reference":[{"key":"1526_CR1","doi-asserted-by":"publisher","first-page":"1053","DOI":"10.1038\/npp.2014.306","volume":"40","author":"LE Kwako","year":"2015","unstructured":"Kwako LE, et al. The corticotropin releasing hormone-1 (CRH1) receptor antagonist pexacerfont in alcohol dependence: a randomized controlled experimental medicine study. Neuropsychopharmacology. 2015;40:1053\u201363.","journal-title":"Neuropsychopharmacology"},{"key":"1526_CR2","doi-asserted-by":"publisher","first-page":"2795","DOI":"10.1038\/npp.2016.94","volume":"41","author":"Y Shaham","year":"2016","unstructured":"Shaham Y, de Wit H. Lost in Translation: CRF1 Receptor Antagonists and Addiction Treatment. Neuropsychopharmacology. 2016;41:2795\u20137.","journal-title":"Neuropsychopharmacology"},{"key":"1526_CR3","doi-asserted-by":"publisher","first-page":"2818","DOI":"10.1038\/npp.2016.61","volume":"41","author":"ML Schwandt","year":"2016","unstructured":"Schwandt ML, et al. The CRF1 Antagonist Verucerfont in Anxious Alcohol-Dependent Women: Translation of Neuroendocrine, But not of Anti-Craving Effects. Neuropsychopharmacology. 2016;41:2818\u201329.","journal-title":"Neuropsychopharmacology"},{"key":"1526_CR4","doi-asserted-by":"publisher","first-page":"6","DOI":"10.1111\/add.14764","volume":"115","author":"M Field","year":"2020","unstructured":"Field M, Kersbergen I. Are animal models of addiction useful? Addiction. 2020;115:6\u201312.","journal-title":"Addiction"},{"key":"1526_CR5","doi-asserted-by":"publisher","first-page":"592","DOI":"10.1038\/nrn.2016.67","volume":"17","author":"M Heilig","year":"2016","unstructured":"Heilig M, et al. Time to connect: bringing social context into addiction neuroscience. Nat Rev Neurosci. 2016;17:592\u20139.","journal-title":"Nat Rev Neurosci"},{"key":"1526_CR6","doi-asserted-by":"publisher","first-page":"172","DOI":"10.1016\/j.neubiorev.2010.04.005","volume":"35","author":"SH Ahmed","year":"2010","unstructured":"Ahmed SH. Validation crisis in animal models of drug addiction: beyond non-disordered drug use toward drug addiction. Neurosci Biobehav Rev. 2010;35:172\u201384.","journal-title":"Neurosci Biobehav Rev"},{"key":"1526_CR7","doi-asserted-by":"publisher","first-page":"201","DOI":"10.1016\/0376-8716(93)90061-T","volume":"33","author":"ME Carroll","year":"1993","unstructured":"Carroll ME. The economic context of drug and non-drug reinforcers affects acquisition and maintenance of drug-reinforced behavior and withdrawal effects. Drug Alcohol Depend. 1993;33:201\u201310.","journal-title":"Drug Alcohol Depend"},{"key":"1526_CR8","first-page":"6","volume":"169","author":"ME Carroll","year":"1998","unstructured":"Carroll ME. Acquisition and reacquisition (relapse) of drug abuse: modulation by alternative reinforcers. NIDA Res Monogr. 1998;169:6\u201325.","journal-title":"NIDA Res Monogr"},{"key":"1526_CR9","doi-asserted-by":"publisher","first-page":"8","DOI":"10.1080\/15265160601063969","volume":"7","author":"SE Hyman","year":"2007","unstructured":"Hyman SE. The neurobiology of addiction: implications for voluntary control of behavior. Am J Bioeth. 2007;7:8\u201311.","journal-title":"Am J Bioeth"},{"key":"1526_CR10","doi-asserted-by":"crossref","unstructured":"Heyman GM. Addiction: a disorder of choice. Cambridge, MA: Harvard University Press; 2009.","DOI":"10.4159\/9780674053991"},{"key":"1526_CR11","doi-asserted-by":"publisher","first-page":"1403","DOI":"10.1176\/appi.ajp.162.8.1403","volume":"162","author":"PW Kalivas","year":"2005","unstructured":"Kalivas PW, Volkow ND. The neural basis of addiction: a pathology of motivation and choice. Am J Psychiatry. 2005;162:1403\u201313.","journal-title":"Am J Psychiatry"},{"key":"1526_CR12","unstructured":"Berkman LF and Kawachi I. Social epidemiology. 2000, New York: Oxford University Press; 2000. xxii, p. 391."},{"key":"1526_CR13","doi-asserted-by":"publisher","first-page":"181","DOI":"10.1016\/j.tips.2016.11.002","volume":"38","author":"ML Banks","year":"2017","unstructured":"Banks ML, Negus SS. Insights from Preclinical Choice Models on Treating Drug Addiction. Trends Pharm Sci. 2017;38:181\u201394.","journal-title":"Trends Pharm Sci"},{"key":"1526_CR14","doi-asserted-by":"publisher","first-page":"3","DOI":"10.1016\/j.pnpbp.2017.09.027","volume":"87","author":"SH Ahmed","year":"2018","unstructured":"Ahmed SH. Trying to make sense of rodents\u2019 drug choice behavior. Prog Neuropsychopharmacol Biol Psychiatry. 2018;87:3\u201310.","journal-title":"Prog Neuropsychopharmacol Biol Psychiatry"},{"key":"1526_CR15","doi-asserted-by":"publisher","first-page":"1321","DOI":"10.1126\/science.aao1157","volume":"360","author":"E Augier","year":"2018","unstructured":"Augier E, et al. A molecular mechanism for choosing alcohol over an alternative reward. Science. 2018;360:1321\u20136.","journal-title":"Science"},{"key":"1526_CR16","doi-asserted-by":"publisher","first-page":"1520","DOI":"10.1038\/s41593-018-0246-6","volume":"21","author":"M Venniro","year":"2018","unstructured":"Venniro M, et al. Volitional social interaction prevents drug addiction in rat models. Nat Neurosci. 2018;21:1520\u20139.","journal-title":"Nat Neurosci"},{"key":"1526_CR17","doi-asserted-by":"crossref","unstructured":"Augier E, et al. A Method for Evaluating the Reinforcing Properties of Ethanol in Rats without Water Deprivation, Saccharin Fading or Extended Access Training. J Vis Exp. 2017;53305.","DOI":"10.3791\/53305"},{"key":"1526_CR18","doi-asserted-by":"publisher","first-page":"4561","DOI":"10.1007\/s00213-014-3605-3","volume":"231","author":"E Augier","year":"2014","unstructured":"Augier E, et al. Wistar rats acquire and maintain self-administration of 20 % ethanol without water deprivation, saccharin\/sucrose fading, or extended access training. Psychopharmacol (Berl). 2014;231:4561\u20138.","journal-title":"Psychopharmacol (Berl)"},{"key":"1526_CR19","doi-asserted-by":"publisher","first-page":"1542","DOI":"10.1038\/s41596-020-0296-6","volume":"15","author":"M Venniro","year":"2020","unstructured":"Venniro M, Shaham Y. An operant social self-administration and choice model in rats. Nat Protoc. 2020;15:1542\u201359.","journal-title":"Nat Protoc"},{"key":"1526_CR20","doi-asserted-by":"publisher","unstructured":"Lenoir M, et al. A choice-based screening method for compulsive drug users in rats. Curr Protoc Neurosci. 2013. Chapter 9: p. Unit 9 44. https:\/\/doi.org\/10.1002\/0471142301.ns0944s64.","DOI":"10.1002\/0471142301.ns0944s64"},{"key":"1526_CR21","doi-asserted-by":"publisher","first-page":"848","DOI":"10.1016\/j.biopsych.2019.05.018","volume":"86","author":"M Venniro","year":"2019","unstructured":"Venniro M, et al. Operant Social Reward Decreases Incubation of Heroin Craving in Male and Female Rats. Biol Psychiatry. 2019;86:848\u201356.","journal-title":"Biol Psychiatry"},{"key":"1526_CR22","doi-asserted-by":"crossref","unstructured":"Chow JJ, et al. Characterization of operant social interaction in rats: effects of access duration, effort, peer familiarity, housing conditions, and choice between social interaction vs. food or remifentanil. Psychopharmacology (Berl). 2022;239:2093\u20132108.","DOI":"10.1007\/s00213-022-06064-1"},{"key":"1526_CR23","doi-asserted-by":"publisher","first-page":"2350","DOI":"10.1038\/s41386-021-01148-6","volume":"46","author":"M Venniro","year":"2021","unstructured":"Venniro M, et al. The protective effect of operant social reward on cocaine self-administration, choice, and relapse is dependent on delay and effort for the social reward. Neuropsychopharmacology. 2021;46:2350\u20137.","journal-title":"Neuropsychopharmacology"},{"key":"1526_CR24","doi-asserted-by":"publisher","first-page":"173462","DOI":"10.1016\/j.pbb.2022.173462","volume":"220","author":"MM Marcus","year":"2022","unstructured":"Marcus MM, Negus SS, Banks ML. Effects of environmental manipulations on cocaine-vs-social choice in male and female rats. Pharm Biochem Behav. 2022;220:173462.","journal-title":"Pharm Biochem Behav"},{"key":"1526_CR25","doi-asserted-by":"publisher","unstructured":"Marchant NJ, et al. Rats choose alcohol over social reward in an operant choice procedure. Neuropsychopharmacology. 2022 https:\/\/doi.org\/10.1038\/s41386-022-01447-6. (Epub ahead of print).","DOI":"10.1038\/s41386-022-01447-6"},{"key":"1526_CR26","doi-asserted-by":"publisher","first-page":"e11592","DOI":"10.1371\/journal.pone.0011592","volume":"5","author":"L Cantin","year":"2010","unstructured":"Cantin L, et al. Cocaine is low on the value ladder of rats: possible evidence for resilience to addiction. PLoS ONE. 2010;5:e11592. p","journal-title":"PLoS ONE"},{"key":"1526_CR27","doi-asserted-by":"publisher","first-page":"1209","DOI":"10.1038\/npp.2013.17","volume":"38","author":"M Lenoir","year":"2013","unstructured":"Lenoir M, et al. Extended heroin access increases heroin choices over a potent nondrug alternative. Neuropsychopharmacology. 2013;38:1209\u201320.","journal-title":"Neuropsychopharmacology"},{"key":"1526_CR28","doi-asserted-by":"publisher","first-page":"142","DOI":"10.1111\/adb.12306","volume":"22","author":"C Huynh","year":"2017","unstructured":"Huynh C, et al. Rats quit nicotine for a sweet reward following an extensive history of nicotine use. Addict Biol. 2017;22:142\u201351.","journal-title":"Addict Biol"},{"key":"1526_CR29","doi-asserted-by":"publisher","first-page":"463","DOI":"10.1016\/j.biopsych.2015.02.018","volume":"78","author":"D Caprioli","year":"2015","unstructured":"Caprioli D, et al. Effect of the Novel Positive Allosteric Modulator of Metabotropic Glutamate Receptor 2 AZD8529 on Incubation of Methamphetamine Craving After Prolonged Voluntary Abstinence in a Rat Model. Biol Psychiatry. 2015;78:463\u201373.","journal-title":"Biol Psychiatry"},{"key":"1526_CR30","doi-asserted-by":"publisher","first-page":"757","DOI":"10.1001\/jamapsychiatry.2015.0584","volume":"72","author":"BF Grant","year":"2015","unstructured":"Grant BF, et al. Epidemiology of DSM-5 Alcohol Use Disorder: Results From the National Epidemiologic Survey on Alcohol and Related Conditions III. JAMA Psychiatry. 2015;72:757\u201366.","journal-title":"JAMA Psychiatry"},{"key":"1526_CR31","doi-asserted-by":"publisher","first-page":"1089","DOI":"10.1016\/j.pnpbp.2004.05.044","volume":"28","author":"A Tomie","year":"2004","unstructured":"Tomie A, et al. Social opportunity and ethanol drinking in rats. Prog Neuropsychopharmacol Biol Psychiatry. 2004;28:1089\u201397.","journal-title":"Prog Neuropsychopharmacol Biol Psychiatry"},{"key":"1526_CR32","doi-asserted-by":"publisher","first-page":"197","DOI":"10.1093\/alcalc\/agh055","volume":"39","author":"A Tomie","year":"2004","unstructured":"Tomie A, et al. Effects of ethanol sipper and social opportunity on ethanol drinking in rats. Alcohol Alcohol. 2004;39:197\u2013202.","journal-title":"Alcohol Alcohol"},{"key":"1526_CR33","doi-asserted-by":"publisher","first-page":"23","DOI":"10.1037\/a0034669","volume":"22","author":"JC Strickland","year":"2014","unstructured":"Strickland JC, Smith MA. The effects of social contact on drug use: behavioral mechanisms controlling drug intake. Exp Clin Psychopharmacol. 2014;22:23\u201334.","journal-title":"Exp Clin Psychopharmacol"},{"key":"1526_CR34","doi-asserted-by":"publisher","first-page":"1097","DOI":"10.1007\/s00213-021-06033-0","volume":"239","author":"E Giorla","year":"2022","unstructured":"Giorla E, et al. Peer presence and familiarity as key factors to reduce cocaine intake in both rats and humans: an effect mediated by the subthalamic nucleus. Psychopharmacol (Berl). 2022;239:1097\u2013113.","journal-title":"Psychopharmacol (Berl)"},{"key":"1526_CR35","doi-asserted-by":"publisher","first-page":"1772","DOI":"10.1111\/acer.14924","volume":"46","author":"CE Ardinger","year":"2022","unstructured":"Ardinger CE, et al. A critical review of front-loading: A maladaptive drinking pattern driven by alcohol\u2019s rewarding effects. Alcohol: Clin Exp Res. 2022;46:1772\u201382.","journal-title":"Alcohol: Clin Exp Res"},{"key":"1526_CR36","doi-asserted-by":"publisher","first-page":"398","DOI":"10.1016\/j.bbr.2007.11.024","volume":"188","author":"EI Varlinskaya","year":"2008","unstructured":"Varlinskaya EI, Spear LP. Social interactions in adolescent and adult Sprague-Dawley rats: impact of social deprivation and test context familiarity. Behav Brain Res. 2008;188:398\u2013405.","journal-title":"Behav Brain Res"},{"key":"1526_CR37","doi-asserted-by":"publisher","unstructured":"Olaniran A, et al. Operant social seeking to a novel peer after social isolation is associated with activation of nucleus accumbens shell in rats. Psychopharmacology (Berl). 2022 https:\/\/doi.org\/10.1007\/s00213-022-06280-9. (Epub ahead of print).","DOI":"10.1007\/s00213-022-06280-9"},{"key":"1526_CR38","doi-asserted-by":"publisher","first-page":"377","DOI":"10.1016\/j.pbb.2009.01.016","volume":"92","author":"DJ Stairs","year":"2009","unstructured":"Stairs DJ, Bardo MT. Neurobehavioral effects of environmental enrichment and drug abuse vulnerability. Pharm Biochem Behav. 2009;92:377\u201382.","journal-title":"Pharm Biochem Behav"},{"key":"1526_CR39","doi-asserted-by":"publisher","first-page":"1692","DOI":"10.1111\/j.1530-0277.2007.00466.x","volume":"31","author":"GA Deehan Jr","year":"2007","unstructured":"Deehan GA Jr, Cain ME, Kiefer SW. Differential rearing conditions alter operant responding for ethanol in outbred rats. Alcohol Clin Exp Res. 2007;31:1692\u20138.","journal-title":"Alcohol Clin Exp Res"},{"key":"1526_CR40","doi-asserted-by":"publisher","first-page":"273","DOI":"10.1111\/j.1530-0277.2008.00830.x","volume":"33","author":"BA McCool","year":"2009","unstructured":"McCool BA, Chappell AM. Early social isolation in male Long-Evans rats alters both appetitive and consummatory behaviors expressed during operant ethanol self-administration. Alcohol Clin Exp Res. 2009;33:273\u201382.","journal-title":"Alcohol Clin Exp Res"},{"key":"1526_CR41","doi-asserted-by":"publisher","first-page":"149","DOI":"10.1016\/j.neuropharm.2015.05.025","volume":"97","author":"MJ Skelly","year":"2015","unstructured":"Skelly MJ, et al. Adolescent social isolation increases anxiety-like behavior and ethanol intake and impairs fear extinction in adulthood: Possible role of disrupted noradrenergic signaling. Neuropharmacology. 2015;97:149\u201359.","journal-title":"Neuropharmacology"},{"key":"1526_CR42","doi-asserted-by":"publisher","first-page":"771114","DOI":"10.3389\/fnbeh.2021.771114","volume":"15","author":"MA Smith","year":"2021","unstructured":"Smith MA, et al. Social Contact Reinforces Cocaine Self-Administration in Young Adult Male Rats: The Role of Social Reinforcement in Vulnerability to Drug Use. Front Behav Neurosci. 2021;15:771114.","journal-title":"Front Behav Neurosci"},{"key":"1526_CR43","doi-asserted-by":"publisher","first-page":"480","DOI":"10.1111\/acer.14540","volume":"45","author":"KM Moench","year":"2021","unstructured":"Moench KM, Logrip ML. Housing Condition Differentially Impacts Escalation of Alcohol Intake, Relapse-Like Drinking, Anxiety-Like Behavior, and Stress History Effects by Sex. Alcohol Clin Exp Res. 2021;45:480\u20139.","journal-title":"Alcohol Clin Exp Res"}],"container-title":["Neuropsychopharmacology"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.nature.com\/articles\/s41386-022-01526-8.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/www.nature.com\/articles\/s41386-022-01526-8","content-type":"text\/html","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/www.nature.com\/articles\/s41386-022-01526-8.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2023,5,24]],"date-time":"2023-05-24T09:03:04Z","timestamp":1684918984000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.nature.com\/articles\/s41386-022-01526-8"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2022,12,31]]},"references-count":43,"journal-issue":{"issue":"7","published-print":{"date-parts":[[2023,6]]}},"alternative-id":["1526"],"URL":"https:\/\/doi.org\/10.1038\/s41386-022-01526-8","relation":{},"ISSN":["0893-133X","1740-634X"],"issn-type":[{"value":"0893-133X","type":"print"},{"value":"1740-634X","type":"electronic"}],"subject":[],"published":{"date-parts":[[2022,12,31]]},"assertion":[{"value":"25 April 2022","order":1,"name":"received","label":"Received","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"19 December 2022","order":2,"name":"revised","label":"Revised","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"21 December 2022","order":3,"name":"accepted","label":"Accepted","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"31 December 2022","order":4,"name":"first_online","label":"First Online","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"EA is PI of a research contract with Indivior Inc to evaluate novel candidates for AUD, which is not related to the present work. Other than that, the authors report no biomedical financial interests or potential competing interests.","order":1,"name":"Ethics","group":{"name":"EthicsHeading","label":"Competing interests"}}]}}