{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,10,29]],"date-time":"2026-10-29T21:03:54Z","timestamp":1793307834637,"version":"4.5.0"},"reference-count":86,"publisher":"Springer Science and Business Media LLC","issue":"4","license":[{"start":{"date-parts":[[2022,1,8]],"date-time":"2022-01-08T00:00:00Z","timestamp":1641600000000},"content-version":"tdm","delay-in-days":0,"URL":"https:\/\/www.springer.com\/tdm"},{"start":{"date-parts":[[2022,1,8]],"date-time":"2022-01-08T00:00:00Z","timestamp":1641600000000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/www.springer.com\/tdm"}],"content-domain":{"domain":["link.springer.com"],"crossmark-restriction":false},"short-container-title":["Psychopharmacology"],"published-print":{"date-parts":[[2022,4]]},"DOI":"10.1007\/s00213-021-06024-1","type":"journal-article","created":{"date-parts":[[2022,1,8]],"date-time":"2022-01-08T09:02:46Z","timestamp":1641632566000},"page":"1081-1095","update-policy":"https:\/\/doi.org\/10.1007\/springer_crossmark_policy","source":"Crossref","is-referenced-by-count":20,"title":["Early social isolation stress increases addiction vulnerability to heroin and alters c-Fos expression in the mesocorticolimbic system"],"prefix":"10.1007","volume":"239","author":[{"given":"Archana","family":"Singh","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Yang","family":"Xie","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Ashton","family":"Davis","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-0036-1901","authenticated-orcid":false,"given":"Zi-Jun","family":"Wang","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"297","published-online":{"date-parts":[[2022,1,8]]},"reference":[{"key":"6024_CR1","doi-asserted-by":"crossref","unstructured":"Anderson EM, Engelhardt A, D\u2019emis S, Porath E, Hearing MC (2020) Sex-specific prefrontal cortex dysfunction underlying opioid-induced cognitive impairment. Bio-rxiv","DOI":"10.1101\/666099"},{"key":"6024_CR2","doi-asserted-by":"publisher","first-page":"59","DOI":"10.3109\/00952998709001500","volume":"13","author":"MD Anglin","year":"1987","unstructured":"Anglin MD, Hser YI, McGlothlin WH (1987) Sex differences in addict careers. 2. Becoming addicted. Am J Drug Alcohol Abuse 13:59\u201371","journal-title":"Am J Drug Alcohol Abuse"},{"key":"6024_CR3","doi-asserted-by":"publisher","first-page":"109","DOI":"10.1111\/j.1360-0443.2005.01296.x","volume":"101","author":"AE Barrett","year":"2006","unstructured":"Barrett AE, Turner RJ (2006) Family structure and substance use problems in adolescence and early adulthood: examining explanations for the relationship. Addiction 101:109\u2013120","journal-title":"Addiction"},{"key":"6024_CR4","doi-asserted-by":"publisher","first-page":"1991","DOI":"10.1007\/s00213-015-4060-5","volume":"233","author":"JM Bossert","year":"2016","unstructured":"Bossert JM, Adhikary S, St Laurent R, Marchant NJ, Wang HL, Morales M, Shaham Y (2016) Role of projections from ventral subiculum to nucleus accumbens shell in context-induced reinstatement of heroin seeking in rats. Psychopharmacology (Berl) 233:1991\u20132004","journal-title":"Psychopharmacology (Berl)"},{"key":"6024_CR5","doi-asserted-by":"publisher","first-page":"10726","DOI":"10.1523\/JNEUROSCI.3207-04.2004","volume":"24","author":"JM Bossert","year":"2004","unstructured":"Bossert JM, Liu SY, Lu L, Shaham Y (2004) A role of ventral tegmental area glutamate in contextual cue-induced relapse to heroin seeking. J Neurosci 24:10726\u201310730","journal-title":"J Neurosci"},{"key":"6024_CR6","doi-asserted-by":"publisher","first-page":"420","DOI":"10.1038\/nn.2758","volume":"14","author":"JM Bossert","year":"2011","unstructured":"Bossert JM, Stern AL, Theberge FR, Cifani C, Koya E, Hope BT, Shaham Y (2011) Ventral medial prefrontal cortex neuronal ensembles mediate context-induced relapse to heroin. Nat Neurosci 14:420\u2013422","journal-title":"Nat Neurosci"},{"key":"6024_CR7","doi-asserted-by":"publisher","first-page":"4982","DOI":"10.1523\/JNEUROSCI.0005-12.2012","volume":"32","author":"JM Bossert","year":"2012","unstructured":"Bossert JM, Stern AL, Theberge FR, Marchant NJ, Wang HL, Morales M, Shaham Y (2012) Role of projections from ventral medial prefrontal cortex to nucleus accumbens shell in context-induced reinstatement of heroin seeking. J Neurosci 32:4982\u20134991","journal-title":"J Neurosci"},{"key":"6024_CR8","doi-asserted-by":"publisher","first-page":"269","DOI":"10.1016\/0091-3057(91)90178-5","volume":"39","author":"AE Boyle","year":"1991","unstructured":"Boyle AE, Gill K, Smith BR, Amit Z (1991) Differential effects of an early housing manipulation on cocaine-induced activity and self-administration in laboratory rats. Pharmacol Biochem Behav 39:269\u2013274","journal-title":"Pharmacol Biochem Behav"},{"key":"6024_CR9","doi-asserted-by":"publisher","first-page":"903","DOI":"10.1016\/0091-3057(89)90490-5","volume":"33","author":"MA Bozarth","year":"1989","unstructured":"Bozarth MA, Murray A, Wise RA (1989) Influence of housing conditions on the acquisition of intravenous heroin and cocaine self-administration in rats. Pharmacol Biochem Behav 33:903\u2013907","journal-title":"Pharmacol Biochem Behav"},{"key":"6024_CR10","doi-asserted-by":"publisher","first-page":"517","DOI":"10.1002\/cne.902960402","volume":"296","author":"E Bullitt","year":"1990","unstructured":"Bullitt E (1990) Expression of c-fos-like protein as a marker for neuronal activity following noxious stimulation in the rat. J Comp Neurol 296:517\u2013530","journal-title":"J Comp Neurol"},{"key":"6024_CR11","doi-asserted-by":"publisher","first-page":"182","DOI":"10.1016\/j.neuroscience.2018.01.006","volume":"373","author":"MJ Caruso","year":"2018","unstructured":"Caruso MJ, Crowley NA, Reiss DE, Caulfield JI, Luscher B, Cavigelli SA, Kamens HM (2018) Adolescent social stress increases anxiety-like behavior and alters synaptic transmission, without influencing nicotine responses, in a sex-dependent manner. Neuroscience 373:182\u2013198","journal-title":"Neuroscience"},{"key":"6024_CR12","doi-asserted-by":"publisher","first-page":"102","DOI":"10.1016\/j.brainres.2018.12.040","volume":"1710","author":"L Chang","year":"2019","unstructured":"Chang L, Kigar SL, Ho JH, Cuarenta A, Gunderson HC, Baldo BA, Bakshi VP, Auger AP (2019) Early life stress alters opioid receptor mRNA levels within the nucleus accumbens in a sex-dependent manner. Brain Res 1710:102\u2013108","journal-title":"Brain Res"},{"key":"6024_CR13","doi-asserted-by":"publisher","first-page":"206","DOI":"10.1037\/0021-843X.97.2.206","volume":"97","author":"L Chassin","year":"1988","unstructured":"Chassin L, Mann LM, Sher KJ (1988) Self-awareness theory, family history of alcoholism, and adolescent alcohol involvement. J Abnorm Psychol 97:206\u2013217","journal-title":"J Abnorm Psychol"},{"key":"6024_CR14","doi-asserted-by":"publisher","first-page":"185","DOI":"10.1097\/FBP.0000000000000213","volume":"27","author":"DM Cortes-Patino","year":"2016","unstructured":"Cortes-Patino DM, Serrano C, Garcia-Mijares M (2016) Early social isolation increases persistence of alcohol-seeking behavior in alcohol-related contexts. Behav Pharmacol 27:185\u2013191","journal-title":"Behav Pharmacol"},{"key":"6024_CR15","doi-asserted-by":"publisher","first-page":"480","DOI":"10.15288\/jsa.1999.60.480","volume":"60","author":"FM Costa","year":"1999","unstructured":"Costa FM, Jessor R, Turbin MS (1999) Transition into adolescent problem drinking: the role of psychosocial risk and protective factors. J Stud Alcohol 60:480\u2013490","journal-title":"J Stud Alcohol"},{"key":"6024_CR16","doi-asserted-by":"publisher","first-page":"157","DOI":"10.1016\/j.brainres.2014.11.005","volume":"1628","author":"FC Cruz","year":"2015","unstructured":"Cruz FC, Javier Rubio F, Hope BT (2015) Using c-fos to study neuronal ensembles in corticostriatal circuitry of addiction. Brain Res 1628:157\u2013173","journal-title":"Brain Res"},{"key":"6024_CR17","doi-asserted-by":"publisher","first-page":"41","DOI":"10.1007\/s00213-020-05657-y","volume":"238","author":"M Engeln","year":"2021","unstructured":"Engeln M, Fox ME, Lobo MK (2021) Housing conditions during self-administration determine motivation for cocaine in mice following chronic social defeat stress. Psychopharmacology (Berl) 238:41\u201354","journal-title":"Psychopharmacology (Berl)"},{"key":"6024_CR18","doi-asserted-by":"publisher","first-page":"11600","DOI":"10.1523\/JNEUROSCI.1914-12.2012","volume":"32","author":"S Fanous","year":"2012","unstructured":"Fanous S, Goldart EM, Theberge FR, Bossert JM, Shaham Y, Hope BT (2012) Role of orbitofrontal cortex neuronal ensembles in the expression of incubation of heroin craving. J Neurosci 32:11600\u201311609","journal-title":"J Neurosci"},{"key":"6024_CR19","doi-asserted-by":"publisher","first-page":"589","DOI":"10.1016\/j.bbr.2018.10.007","volume":"359","author":"AQ Fosnocht","year":"2019","unstructured":"Fosnocht AQ, Lucerne KE, Ellis AS, Olimpo NA, Briand LA (2019) Adolescent social isolation increases cocaine seeking in male and female mice. Behav Brain Res 359:589\u2013596","journal-title":"Behav Brain Res"},{"key":"6024_CR20","doi-asserted-by":"publisher","first-page":"459","DOI":"10.1007\/s00213-004-1895-6","volume":"176","author":"RA Fuchs","year":"2004","unstructured":"Fuchs RA, Evans KA, Parker MC, See RE (2004) Differential involvement of the core and shell subregions of the nucleus accumbens in conditioned cue-induced reinstatement of cocaine seeking in rats. Psychopharmacology (Berl) 176:459\u2013465","journal-title":"Psychopharmacology (Berl)"},{"key":"6024_CR21","doi-asserted-by":"publisher","first-page":"251","DOI":"10.1016\/j.ddmod.2009.03.001","volume":"5","author":"RA Fuchs","year":"2008","unstructured":"Fuchs RA, Lasseter HC, Ramirez DR, Xie X (2008) Relapse to drug seeking following prolonged abstinence: the role of environmental stimuli. Drug Discov Today Dis Models 5:251\u2013258","journal-title":"Drug Discov Today Dis Models"},{"key":"6024_CR22","doi-asserted-by":"publisher","first-page":"215","DOI":"10.1007\/s00213-012-2637-9","volume":"222","author":"AM Gancarz","year":"2012","unstructured":"Gancarz AM, Kausch MA, Lloyd DR, Richards JB (2012) Between-session progressive ratio performance in rats responding for cocaine and water reinforcers. Psychopharmacology (Berl) 222:215\u2013223","journal-title":"Psychopharmacology (Berl)"},{"key":"6024_CR23","doi-asserted-by":"publisher","first-page":"959","DOI":"10.1038\/nn.4036","volume":"18","author":"AM Gancarz","year":"2015","unstructured":"Gancarz AM, Wang ZJ, Schroeder GL, Damez-Werno D, Braunscheidel KM, Mueller LE, Humby MS, Caccamise A, Martin JA, Dietz KC, Neve RL, Dietz DM (2015) Activin receptor signaling regulates cocaine-primed behavioral and morphological plasticity. Nat Neurosci 18:959\u2013961","journal-title":"Nat Neurosci"},{"key":"6024_CR24","doi-asserted-by":"publisher","unstructured":"Goldstein RZ, Volkow ND (2011) Dysfunction of the prefrontal cortex in addiction: neuroimaging findings and clinical implications. Nature Review Neuroscience 12(11):652\u2013669. https:\/\/doi.org\/10.1038\/nrn3119","DOI":"10.1038\/nrn3119"},{"key":"6024_CR25","first-page":"1","volume-title":"Role of prefrontal cortex in stress responsivity","author":"A Gratton","year":"2005","unstructured":"Gratton A, Sullivan RM (2005) Role of prefrontal cortex in stress responsivity. In Handbook of stress and the Brian, Elsevier Dusseldorf, p 1"},{"key":"6024_CR26","doi-asserted-by":"publisher","first-page":"494","DOI":"10.1016\/j.cpr.2006.09.004","volume":"27","author":"L Gregg","year":"2007","unstructured":"Gregg L, Barrowclough C, Haddock G (2007) Reasons for increased substance use in psychosis. Clin Psychol Rev 27:494\u2013510","journal-title":"Clin Psychol Rev"},{"key":"6024_CR27","doi-asserted-by":"publisher","first-page":"9","DOI":"10.1038\/nn0107-9","volume":"10","author":"BK Harvey","year":"2007","unstructured":"Harvey BK, Hope BT, Shaham Y (2007) Tolerance to opiate reward: role of midbrain IRS2-Akt pathway. Nat Neurosci 10:9\u201310","journal-title":"Nat Neurosci"},{"key":"6024_CR28","doi-asserted-by":"publisher","first-page":"354","DOI":"10.1016\/j.physbeh.2010.12.019","volume":"104","author":"G Hermes","year":"2011","unstructured":"Hermes G, Li N, Duman C, Duman R (2011) Post-weaning chronic social isolation produces profound behavioral dysregulation with decreases in prefrontal cortex synaptic-associated protein expression in female rats. Physiol Behav 104:354\u2013359","journal-title":"Physiol Behav"},{"key":"6024_CR29","doi-asserted-by":"publisher","first-page":"16362","DOI":"10.1523\/JNEUROSCI.1392-15.2015","volume":"35","author":"GE Hodes","year":"2015","unstructured":"Hodes GE, Pfau ML, Purushothaman I, Ahn HF, Golden SA, Christoffel DJ, Magida J, Brancato A, Takahashi A, Flanigan ME, Menard C, Aleyasin H, Koo JW, Lorsch ZS, Feng J, Heshmati M, Wang M, Turecki G, Neve R et al (2015) Sex differences in nucleus accumbens transcriptome profiles associated with susceptibility versus resilience to subchronic variable stress. J Neurosci 35:16362\u201316376","journal-title":"J Neurosci"},{"key":"6024_CR30","doi-asserted-by":"publisher","first-page":"943","DOI":"10.1126\/science.134.3483.943","volume":"134","author":"W Hodos","year":"1961","unstructured":"Hodos W (1961) Progressive ratio as a measure of reward strength. Science 134:943\u2013944","journal-title":"Science"},{"key":"6024_CR31","doi-asserted-by":"publisher","first-page":"55","DOI":"10.1007\/s002130000451","volume":"151","author":"SR Howes","year":"2000","unstructured":"Howes SR, Dalley JW, Morrison CH, Robbins TW, Everitt BJ (2000) Leftward shift in the acquisition of cocaine self-administration in isolation-reared rats: relationship to extracellular levels of dopamine, serotonin and glutamate in the nucleus accumbens and amygdala-striatal FOS expression. Psychopharmacology (Berl) 151:55\u201363","journal-title":"Psychopharmacology (Berl)"},{"key":"6024_CR32","doi-asserted-by":"publisher","first-page":"231","DOI":"10.3109\/00952998709001512","volume":"13","author":"YI Hser","year":"1987","unstructured":"Hser YI, Anglin MD, Booth MW (1987) Sex differences in addict careers. 3. Addiction. Am J Drug Alcohol Abuse 13:231\u2013251","journal-title":"Addiction. Am J Drug Alcohol Abuse"},{"key":"6024_CR33","doi-asserted-by":"publisher","first-page":"389","DOI":"10.1038\/nn1217","volume":"7","author":"R Ito","year":"2004","unstructured":"Ito R, Robbins TW, Everitt BJ (2004) Differential control over cocaine-seeking behavior by nucleus accumbens core and shell. Nat Neurosci 7:389\u2013397","journal-title":"Nat Neurosci"},{"key":"6024_CR34","doi-asserted-by":"publisher","first-page":"235","DOI":"10.1007\/BF03033360","volume":"10","author":"JH Krystal","year":"2006","unstructured":"Krystal JH, D'Souza DC, Gallinat J, Driesen N, Abi-Dargham A, Petrakis I, Heinz A, Pearlson G (2006) The vulnerability to alcohol and substance abuse in individuals diagnosed with schizophrenia. Neurotox Res 10:235\u2013252","journal-title":"Neurotox Res"},{"key":"6024_CR35","doi-asserted-by":"publisher","first-page":"1621","DOI":"10.1038\/nn.3263","volume":"15","author":"J Liu","year":"2012","unstructured":"Liu J, Dietz K, DeLoyht JM, Pedre X, Kelkar D, Kaur J, Vialou V, Lobo MK, Dietz DM, Nestler EJ, Dupree J, Casaccia P (2012) Impaired adult myelination in the prefrontal cortex of socially isolated mice. Nat Neurosci 15:1621\u20131623","journal-title":"Nat Neurosci"},{"key":"6024_CR36","doi-asserted-by":"publisher","first-page":"457","DOI":"10.1016\/S0149-7634(03)00073-3","volume":"27","author":"L Lu","year":"2003","unstructured":"Lu L, Shepard JD, Hall FS, Shaham Y (2003) Effect of environmental stressors on opiate and psychostimulant reinforcement, reinstatement and discrimination in rats: a review. Neurosci Biobehav Rev 27:457\u2013491","journal-title":"Neurosci Biobehav Rev"},{"key":"6024_CR37","doi-asserted-by":"publisher","first-page":"434","DOI":"10.1038\/nrn2639","volume":"10","author":"SJ Lupien","year":"2009","unstructured":"Lupien SJ, McEwen BS, Gunnar MR, Heim C (2009) Effects of stress throughout the lifespan on the brain, behaviour and cognition. Nat Rev Neurosci 10:434\u2013445","journal-title":"Nat Rev Neurosci"},{"key":"6024_CR38","doi-asserted-by":"publisher","first-page":"650","DOI":"10.1016\/j.neuron.2011.01.017","volume":"69","author":"C Luscher","year":"2011","unstructured":"Luscher C, Malenka RC (2011) Drug-evoked synaptic plasticity in addiction: from molecular changes to circuit remodeling. Neuron 69:650\u2013663","journal-title":"Neuron"},{"key":"6024_CR39","doi-asserted-by":"publisher","first-page":"235","DOI":"10.1016\/0306-4603(84)90015-7","volume":"9","author":"R Marks-Kaufman","year":"1984","unstructured":"Marks-Kaufman R, Lewis MJ (1984) Early housing experience modifies morphine self-administration and physical dependence in adult rats. Addict Behav 9:235\u2013243","journal-title":"Addict Behav"},{"key":"6024_CR40","doi-asserted-by":"publisher","first-page":"49","DOI":"10.1007\/s00213-010-2110-6","volume":"215","author":"E Martin-Garcia","year":"2011","unstructured":"Martin-Garcia E, Burokas A, Kostrzewa E, Gieryk A, Korostynski M, Ziolkowska B, Przewlocka B, Przewlocki R, Maldonado R (2011) New operant model of reinstatement of food-seeking behavior in mice. Psychopharmacology (Berl) 215:49\u201370","journal-title":"Psychopharmacology (Berl)"},{"key":"6024_CR41","doi-asserted-by":"publisher","first-page":"1385","DOI":"10.1038\/npp.2017.303","volume":"43","author":"JA Martin","year":"2018","unstructured":"Martin JA, Caccamise A, Werner CT, Viswanathan R, Polanco JJ, Stewart AF, Thomas SA, Sim FJ, Dietz DM (2018) A novel role for oligodendrocyte precursor cells (OPCs) and Sox10 in mediating cellular and behavioral responses to heroin. Neuropsychopharmacology 43:1385\u20131394","journal-title":"Neuropsychopharmacology"},{"key":"6024_CR42","doi-asserted-by":"publisher","first-page":"93","DOI":"10.1016\/0376-8716(96)01245-8","volume":"41","author":"TJ Martin","year":"1996","unstructured":"Martin TJ, Walker LE, Sizemore GM, Smith JE, Dworkin SI (1996) Within-session determination of dose-response curves for heroin self-administration in rats: comparison with between-session determination and effects of naltrexone. Drug Alcohol Depend 41:93\u2013100","journal-title":"Drug Alcohol Depend"},{"key":"6024_CR43","doi-asserted-by":"publisher","first-page":"1980","DOI":"10.1038\/sj.npp.1300507","volume":"29","author":"RI Melendez","year":"2004","unstructured":"Melendez RI, Gregory ML, Bardo MT, Kalivas PW (2004) Impoverished rearing environment alters metabotropic glutamate receptor expression and function in the prefrontal cortex. Neuropsychopharmacology 29:1980\u20131987","journal-title":"Neuropsychopharmacology"},{"key":"6024_CR44","doi-asserted-by":"publisher","first-page":"235","DOI":"10.1038\/npp.2017.142","volume":"43","author":"E Mikics","year":"2018","unstructured":"Mikics E, Guirado R, Umemori J, Toth M, Biro L, Miskolczi C, Balazsfi D, Zelena D, Castren E, Haller J, Karpova NN (2018) Social learning requires plasticity enhanced by fluoxetine through prefrontal Bdnf-TrkB signaling to limit aggression induced by post-weaning social isolation. Neuropsychopharmacology 43:235\u2013245","journal-title":"Neuropsychopharmacology"},{"key":"6024_CR45","doi-asserted-by":"publisher","first-page":"798","DOI":"10.1523\/JNEUROSCI.20-02-00798.2000","volume":"20","author":"JL Neisewander","year":"2000","unstructured":"Neisewander JL, Baker DA, Fuchs RA, Tran-Nguyen LT, Palmer A, Marshall JF (2000) Fos protein expression and cocaine-seeking behavior in rats after exposure to a cocaine self-administration environment. J Neurosci 20:798\u2013805","journal-title":"J Neurosci"},{"key":"6024_CR46","doi-asserted-by":"publisher","first-page":"48","DOI":"10.1016\/j.neuron.2019.01.016","volume":"102","author":"EJ Nestler","year":"2019","unstructured":"Nestler EJ, Luscher C (2019) The molecular basis of drug addiction: linking epigenetic to synaptic and circuit mechanisms. Neuron 102:48\u201359","journal-title":"Neuron"},{"key":"6024_CR47","doi-asserted-by":"publisher","first-page":"64","DOI":"10.1037\/0021-843X.97.1.64","volume":"97","author":"MD Newcomb","year":"1988","unstructured":"Newcomb MD, Bentler PM (1988) Impact of adolescent drug use and social support on problems of young adults: a longitudinal study. J Abnorm Psychol 97:64\u201375","journal-title":"J Abnorm Psychol"},{"key":"6024_CR48","doi-asserted-by":"publisher","first-page":"564","DOI":"10.1037\/0022-3514.51.3.564","volume":"51","author":"MD Newcomb","year":"1986","unstructured":"Newcomb MD, Harlow LL (1986) Life events and substance use among adolescents: mediating effects of perceived loss of control and meaninglessness in life. J Pers Soc Psychol 51:564\u2013577","journal-title":"J Pers Soc Psychol"},{"key":"6024_CR49","doi-asserted-by":"crossref","unstructured":"Ordones Sanchez E, Bavley CC, Deutschmann AU, Carpenter R, Peterson DR, Karbalaei R, Flowers J 2nd, Rogers CM, Langrehr MG, Ardekani CS, Famularo ST, Bongiovanni AR, Knouse MC, Floresco SB, Briand LA, Wimmer ME, Bangasser DA (2021) Early life adversity promotes resilience to opioid addiction-related phenotypes in male rats and sex-specific transcriptional changes. Proc Natl Acad Sci U S A:118","DOI":"10.1073\/pnas.2020173118"},{"key":"6024_CR50","doi-asserted-by":"publisher","first-page":"947","DOI":"10.1038\/nrn2513","volume":"9","author":"T Paus","year":"2008","unstructured":"Paus T, Keshavan M, Giedd JN (2008) Why do many psychiatric disorders emerge during adolescence? Nat Rev Neurosci 9:947\u2013957","journal-title":"Nat Rev Neurosci"},{"key":"6024_CR51","doi-asserted-by":"publisher","first-page":"129","DOI":"10.1016\/0165-0270(80)90021-7","volume":"3","author":"G Paxinos","year":"1980","unstructured":"Paxinos G, Watson CR, Emson PC (1980) AChE-stained horizontal sections of the rat brain in stereotaxic coordinates. J Neurosci Methods 3:129\u2013149","journal-title":"J Neurosci Methods"},{"key":"6024_CR52","doi-asserted-by":"publisher","first-page":"5098","DOI":"10.1038\/s41467-019-13085-6","volume":"10","author":"CJ Pena","year":"2019","unstructured":"Pena CJ, Smith M, Ramakrishnan A, Cates HM, Bagot RC, Kronman HG, Patel B, Chang AB, Purushothaman I, Dudley J, Morishita H, Shen L, Nestler EJ (2019) Early life stress alters transcriptomic patterning across reward circuitry in male and female mice. Nat Commun 10:5098","journal-title":"Nat Commun"},{"key":"6024_CR53","doi-asserted-by":"publisher","first-page":"407","DOI":"10.1007\/BF02245084","volume":"115","author":"GD Phillips","year":"1994","unstructured":"Phillips GD, Howes SR, Whitelaw RB, Wilkinson LS, Robbins TW, Everitt BJ (1994) Isolation rearing enhances the locomotor response to cocaine and a novel environment, but impairs the intravenous self-administration of cocaine. Psychopharmacology (Berl) 115:407\u2013418","journal-title":"Psychopharmacology (Berl)"},{"key":"6024_CR54","doi-asserted-by":"publisher","first-page":"4226","DOI":"10.1523\/JNEUROSCI.20-11-04226.2000","volume":"20","author":"PV Piazza","year":"2000","unstructured":"Piazza PV, Deroche-Gamonent V, Rouge-Pont F, Le Moal M (2000) Vertical shifts in self-administration dose-response functions predict a drug-vulnerable phenotype predisposed to addiction. J Neurosci 20:4226\u20134232","journal-title":"J Neurosci"},{"key":"6024_CR55","doi-asserted-by":"publisher","first-page":"411","DOI":"10.1016\/j.tins.2011.06.001","volume":"34","author":"CL Pickens","year":"2011","unstructured":"Pickens CL, Airavaara M, Theberge F, Fanous S, Hope BT, Shaham Y (2011) Neurobiology of the incubation of drug craving. Trends Neurosci 34:411\u2013420","journal-title":"Trends Neurosci"},{"key":"6024_CR56","doi-asserted-by":"publisher","first-page":"465","DOI":"10.1038\/s41386-018-0234-2","volume":"44","author":"DJ Reiner","year":"2019","unstructured":"Reiner DJ, Fredriksson I, Lofaro OM, Bossert JM, Shaham Y (2019) Relapse to opioid seeking in rat models: behavior, pharmacology and circuits. Neuropsychopharmacology 44:465\u2013477","journal-title":"Neuropsychopharmacology"},{"key":"6024_CR57","doi-asserted-by":"publisher","first-page":"14764","DOI":"10.1523\/JNEUROSCI.4291-09.2009","volume":"29","author":"Y Ren","year":"2009","unstructured":"Ren Y, Whittard J, Higuera-Matas A, Morris CV, Hurd YL (2009) Cannabidiol, a nonpsychotropic component of cannabis, inhibits cue-induced heroin seeking and normalizes discrete mesolimbic neuronal disturbances. J Neurosci 29:14764\u201314769","journal-title":"J Neurosci"},{"key":"6024_CR58","doi-asserted-by":"publisher","first-page":"485","DOI":"10.1007\/s00213-009-1678-1","volume":"207","author":"B Ribeiro Do Couto","year":"2009","unstructured":"Ribeiro Do Couto B, Aguilar MA, Lluch J, Rodriguez-Arias M, Minarro J (2009) Social experiences affect reinstatement of cocaine-induced place preference in mice. Psychopharmacology (Berl) 207:485\u2013498","journal-title":"Psychopharmacology (Berl)"},{"key":"6024_CR59","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1016\/0165-0270(95)00153-0","volume":"66","author":"NR Richardson","year":"1996","unstructured":"Richardson NR, Roberts DC (1996) Progressive ratio schedules in drug self-administration studies in rats: a method to evaluate reinforcing efficacy. J Neurosci Methods 66:1\u201311","journal-title":"J Neurosci Methods"},{"key":"6024_CR60","doi-asserted-by":"publisher","first-page":"579","DOI":"10.1016\/j.neuroscience.2007.10.012","volume":"151","author":"JL Rogers","year":"2008","unstructured":"Rogers JL, Ghee S, See RE (2008) The neural circuitry underlying reinstatement of heroin-seeking behavior in an animal model of relapse. Neuroscience 151:579\u2013588","journal-title":"Neuroscience"},{"key":"6024_CR61","doi-asserted-by":"publisher","first-page":"93","DOI":"10.1038\/nn1812","volume":"10","author":"SJ Russo","year":"2007","unstructured":"Russo SJ, Bolanos CA, Theobald DE, DeCarolis NA, Renthal W, Kumar A, Winstanley CA, Renthal NE, Wiley MD, Self DW, Russell DS, Neve RL, Eisch AJ, Nestler EJ (2007) IRS2-Akt pathway in midbrain dopamine neurons regulates behavioral and cellular responses to opiates. Nat Neurosci 10:93\u201399","journal-title":"Nat Neurosci"},{"key":"6024_CR62","doi-asserted-by":"publisher","first-page":"59","DOI":"10.1016\/0091-3057(88)90311-5","volume":"31","author":"S Schenk","year":"1988","unstructured":"Schenk S, Robinson B, Amit Z (1988) Housing conditions fail to affect the intravenous self-administration of amphetamine. Pharmacol Biochem Behav 31:59\u201362","journal-title":"Pharmacol Biochem Behav"},{"key":"6024_CR63","doi-asserted-by":"publisher","first-page":"2347","DOI":"10.1111\/j.1460-9568.2005.04435.x","volume":"22","author":"ED Schmidt","year":"2005","unstructured":"Schmidt ED, Voorn P, Binnekade R, Schoffelmeer AN, De Vries TJ (2005) Differential involvement of the prelimbic cortex and striatum in conditioned heroin and sucrose seeking following long-term extinction. Eur J Neurosci 22:2347\u20132356","journal-title":"Eur J Neurosci"},{"key":"6024_CR64","doi-asserted-by":"publisher","first-page":"3","DOI":"10.1007\/s00213-002-1224-x","volume":"168","author":"Y Shaham","year":"2003","unstructured":"Shaham Y, Shalev U, Lu L, de Wit H, Stewart J (2003) The reinstatement model of drug relapse: history, methodology and major findings. Psychopharmacology (Berl) 168:3\u201320","journal-title":"Psychopharmacology (Berl)"},{"key":"6024_CR65","doi-asserted-by":"publisher","first-page":"98","DOI":"10.1007\/s002130100748","volume":"156","author":"U Shalev","year":"2001","unstructured":"Shalev U, Morales M, Hope B, Yap J, Shaham Y (2001) Time-dependent changes in extinction behavior and stress-induced reinstatement of drug seeking following withdrawal from heroin in rats. Psychopharmacology (Berl) 156:98\u2013107","journal-title":"Psychopharmacology (Berl)"},{"key":"6024_CR66","doi-asserted-by":"publisher","first-page":"588476","DOI":"10.3389\/fcell.2020.588476","volume":"8","author":"RD Shepard","year":"2020","unstructured":"Shepard RD, Nugent FS (2020) Early life stress- and drug-induced histone modifications within the ventral tegmental area. Front Cell Dev Biol 8:588476","journal-title":"Front Cell Dev Biol"},{"key":"6024_CR67","doi-asserted-by":"publisher","first-page":"414","DOI":"10.15288\/jsa.1997.58.414","volume":"58","author":"KJ Sher","year":"1997","unstructured":"Sher KJ, Gershuny BS, Peterson L, Raskin G (1997) The role of childhood stressors in the intergenerational transmission of alcohol use disorders. J Stud Alcohol 58:414\u2013427","journal-title":"J Stud Alcohol"},{"key":"6024_CR68","doi-asserted-by":"publisher","first-page":"105","DOI":"10.1196\/annals.1441.030","volume":"1141","author":"R Sinha","year":"2008","unstructured":"Sinha R (2008) Chronic stress, drug use, and vulnerability to addiction. Ann N Y Acad Sci 1141:105\u2013130","journal-title":"Ann N Y Acad Sci"},{"key":"6024_CR69","first-page":"19","volume":"25","author":"JP Smith","year":"2008","unstructured":"Smith JP, Book SW (2008) Anxiety and substance use disorders: a review. Psychiatr Times 25:19\u201323","journal-title":"Psychiatr Times"},{"key":"6024_CR70","doi-asserted-by":"publisher","first-page":"593","DOI":"10.1007\/s00213-008-1184-x","volume":"199","author":"G Soria","year":"2008","unstructured":"Soria G, Barbano MF, Maldonado R, Valverde O (2008) A reliable method to study cue-, priming-, and stress-induced reinstatement of cocaine self-administration in mice. Psychopharmacology (Berl) 199:593\u2013603","journal-title":"Psychopharmacology (Berl)"},{"key":"6024_CR71","doi-asserted-by":"publisher","first-page":"417","DOI":"10.1016\/S0149-7634(00)00014-2","volume":"24","author":"LP Spear","year":"2000","unstructured":"Spear LP (2000) The adolescent brain and age-related behavioral manifestations. Neurosci Biobehav Rev 24:417\u2013463","journal-title":"Neurosci Biobehav Rev"},{"key":"6024_CR72","doi-asserted-by":"publisher","first-page":"729","DOI":"10.1016\/j.biopsych.2012.12.019","volume":"73","author":"FR Theberge","year":"2013","unstructured":"Theberge FR, Li X, Kambhampati S, Pickens CL, St Laurent R, Bossert JM, Baumann MH, Hutchinson MR, Rice KC, Watkins LR, Shaham Y (2013) Effect of chronic delivery of the Toll-like receptor 4 antagonist (+)-naltrexone on incubation of heroin craving. Biol Psychiatry 73:729\u2013737","journal-title":"Biol Psychiatry"},{"key":"6024_CR73","doi-asserted-by":"publisher","first-page":"559","DOI":"10.1007\/s00213-012-2784-z","volume":"224","author":"FR Theberge","year":"2012","unstructured":"Theberge FR, Pickens CL, Goldart E, Fanous S, Hope BT, Liu QR, Shaham Y (2012) Association of time-dependent changes in mu opioid receptor mRNA, but not BDNF, TrkB, or MeCP2 mRNA and protein expression in the rat nucleus accumbens with incubation of heroin craving. Psychopharmacology (Berl) 224:559\u2013571","journal-title":"Psychopharmacology (Berl)"},{"key":"6024_CR74","doi-asserted-by":"publisher","first-page":"189","DOI":"10.1016\/j.neuropharm.2019.03.019","volume":"151","author":"EB Towers","year":"2019","unstructured":"Towers EB, Tunstall BJ, McCracken ML, Vendruscolo LF, Koob GF (2019) Male and female mice develop escalation of heroin intake and dependence following extended access. Neuropharmacology 151:189\u2013194","journal-title":"Neuropharmacology"},{"key":"6024_CR75","doi-asserted-by":"publisher","first-page":"66","DOI":"10.3389\/fnbeh.2019.00066","volume":"13","author":"DM Walker","year":"2019","unstructured":"Walker DM, Cunningham AM, Gregory JK, Nestler EJ (2019) Long-term behavioral effects of post-weaning social isolation in males and females. Front Behav Neurosci 13:66","journal-title":"Front Behav Neurosci"},{"key":"6024_CR76","doi-asserted-by":"crossref","unstructured":"Walker DM, Zhou X, Cunningham AM, Lipschultz AP, Ramakrishnan A, Cates HM, Bagot RC, Shen L, Zhang B, Nestler EJ (2021) Sex-specific transcriptional changes in response to adolescent social stress in the brain\u2019s reward circuitry. Biol Psychiatry.","DOI":"10.1016\/j.biopsych.2021.02.964"},{"key":"6024_CR77","doi-asserted-by":"publisher","first-page":"43658","DOI":"10.1038\/srep43658","volume":"7","author":"ZJ Wang","year":"2017","unstructured":"Wang ZJ, Martin JA, Gancarz AM, Adank DN, Sim FJ, Dietz DM (2017) Activin A is increased in the nucleus accumbens following a cocaine binge. Sci Rep 7:43658","journal-title":"Sci Rep"},{"key":"6024_CR78","doi-asserted-by":"publisher","first-page":"652","DOI":"10.1016\/j.biopsych.2016.04.020","volume":"80","author":"ZJ Wang","year":"2016","unstructured":"Wang ZJ, Martin JA, Mueller LE, Caccamise A, Werner CT, Neve RL, Gancarz AM, Li JX, Dietz DM (2016) BRG1 in the nucleus accumbens regulates cocaine-seeking behavior. Biol Psychiatry 80:652\u2013660","journal-title":"Biol Psychiatry"},{"key":"6024_CR79","doi-asserted-by":"publisher","first-page":"9442","DOI":"10.1038\/srep09442","volume":"5","author":"ZJ Wang","year":"2015","unstructured":"Wang ZJ, Zhang XQ, Cui XY, Cui SY, Yu B, Sheng ZF, Li SJ, Cao Q, Huang YL, Xu YP, Zhang YH (2015) Glucocorticoid receptors in the locus coeruleus mediate sleep disorders caused by repeated corticosterone treatment. Sci Rep 5:9442","journal-title":"Sci Rep"},{"key":"6024_CR80","doi-asserted-by":"publisher","first-page":"335","DOI":"10.1016\/j.neuron.2012.11.022","volume":"77","author":"LR Whitaker","year":"2013","unstructured":"Whitaker LR, Degoulet M, Morikawa H (2013) Social deprivation enhances VTA synaptic plasticity and drug-induced contextual learning. Neuron 77:335\u2013345","journal-title":"Neuron"},{"key":"6024_CR81","doi-asserted-by":"publisher","first-page":"611","DOI":"10.1001\/archpsyc.1973.01750350005001","volume":"28","author":"A Wikler","year":"1973","unstructured":"Wikler A (1973) Dynamics of drug dependence. Implications of a conditioning theory for research and treatment. Arch Gen Psychiatry 28:611\u2013616","journal-title":"Arch Gen Psychiatry"},{"key":"6024_CR82","doi-asserted-by":"publisher","first-page":"156","DOI":"10.1016\/j.neuropharm.2016.11.015","volume":"114","author":"JL Wilkerson","year":"2017","unstructured":"Wilkerson JL, Ghosh S, Mustafa M, Abdullah RA, Niphakis MJ, Cabrera R, Maldonado RL, Cravatt BF, Lichtman AH (2017) The endocannabinoid hydrolysis inhibitor SA-57: intrinsic antinociceptive effects, augmented morphine-induced antinociception, and attenuated heroin seeking behavior in mice. Neuropharmacology 114:156\u2013167","journal-title":"Neuropharmacology"},{"key":"6024_CR83","doi-asserted-by":"publisher","first-page":"937","DOI":"10.1037\/0022-3514.71.5.937","volume":"71","author":"TA Wills","year":"1996","unstructured":"Wills TA, Cleary SD (1996) How are social support effects mediated? A test with parental support and adolescent substance use. J Pers Soc Psychol 71:937\u2013952","journal-title":"J Pers Soc Psychol"},{"key":"6024_CR84","doi-asserted-by":"publisher","first-page":"349","DOI":"10.1007\/BF00937914","volume":"20","author":"TA Wills","year":"1992","unstructured":"Wills TA, Vaccaro D, McNamara G (1992) The role of life events, family support, and competence in adolescent substance use: a test of vulnerability and protective factors. Am J Community Psychol 20:349\u2013374","journal-title":"Am J Community Psychol"},{"key":"6024_CR85","doi-asserted-by":"publisher","first-page":"673","DOI":"10.1016\/j.pbb.2005.11.007","volume":"82","author":"D Yajie","year":"2005","unstructured":"Yajie D, Lin K, Baoming L, Lan M (2005) Enhanced cocaine self-administration in adult rats with adolescent isolation experience. Pharmacol Biochem Behav 82:673\u2013677","journal-title":"Pharmacol Biochem Behav"},{"key":"6024_CR86","doi-asserted-by":"publisher","first-page":"998","DOI":"10.1093\/cercor\/bhx010","volume":"28","author":"K Yamamuro","year":"2018","unstructured":"Yamamuro K, Yoshino H, Ogawa Y, Makinodan M, Toritsuka M, Yamashita M, Corfas G, Kishimoto T (2018) Social isolation during the critical period reduces synaptic and intrinsic excitability of a subtype of pyramidal cell in mouse prefrontal cortex. Cereb Cortex 28:998\u20131010","journal-title":"Cereb Cortex"}],"container-title":["Psychopharmacology"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/link.springer.com\/content\/pdf\/10.1007\/s00213-021-06024-1.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/link.springer.com\/article\/10.1007\/s00213-021-06024-1\/fulltext.html","content-type":"text\/html","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/link.springer.com\/content\/pdf\/10.1007\/s00213-021-06024-1.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2022,10,25]],"date-time":"2022-10-25T00:04:49Z","timestamp":1666656289000},"score":1,"resource":{"primary":{"URL":"https:\/\/link.springer.com\/10.1007\/s00213-021-06024-1"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2022,1,8]]},"references-count":86,"journal-issue":{"issue":"4","published-print":{"date-parts":[[2022,4]]}},"alternative-id":["6024"],"URL":"https:\/\/doi.org\/10.1007\/s00213-021-06024-1","relation":{},"ISSN":["0033-3158","1432-2072"],"issn-type":[{"value":"0033-3158","type":"print"},{"value":"1432-2072","type":"electronic"}],"subject":[],"published":{"date-parts":[[2022,1,8]]},"assertion":[{"value":"21 June 2021","order":1,"name":"received","label":"Received","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"4 November 2021","order":2,"name":"accepted","label":"Accepted","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"8 January 2022","order":3,"name":"first_online","label":"First Online","group":{"name":"ArticleHistory","label":"Article History"}},{"order":1,"name":"Ethics","group":{"name":"EthicsHeading","label":"Declarations"}},{"value":"The authors declare no competing interests.","order":2,"name":"Ethics","group":{"name":"EthicsHeading","label":"Conflict of interest"}}]}}