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Special Issue

Mechanisms and genetic factors underlying co-use of nicotine and alcohol or other drugs of abuse

, BA ORCID Icon, , PhD & , PhD
Pages 171-185 | Received 27 Jan 2016, Accepted 28 Jun 2016, Published online: 17 Aug 2016

References

  • Batel P, Pessione F, Maître C, Rueff B. Relationship between alcohol and tobacco dependencies among alcoholics who smoke. Addiction 1995;90:977–980.
  • Falk DE, Yi H-y, Hiller-Sturmhöfel S. An epidemiologic analysis of co-occurring alcohol and tobacco use and disorders: findings from the National Epidemiologic Survey on Alcohol and Related Conditions. Alcohol Res Health 2006;29:162–171.
  • Kandel D, Chen K, Warner LA, Kessler RC, Grant B. Prevalence and demographic correlates of symptoms of last year dependence on alcohol, nicotine, marijuana and cocaine in the U.S. population. Drug Alcohol Depend 1997;44:11–29.
  • Budney AJ, Higgins ST, Hughes JR, Bickel WK. Nicotine and caffeine use in cocaine-dependent individuals. J Subst Abuse 1993;5:117–130.
  • Gorelick DA, Simmons MS, Carriero N, Tashkin DP. Characteristics of smoked drug use among cocaine smokers. Am J Addict 1997;6:237–245.
  • Weinberger AH, Sofuoglu M. The impact of cigarette smoking on stimulant addiction. Am J Drug Alcohol Abuse 2009;35:12–17.
  • Humfleet G, Muñoz R, Sees K, Reus V, Hall S. History of alcohol or drug problems, current use of alcohol or marijuana, and success in quitting smoking. Addict Behav 1999;24:149–154.
  • McKee SA, Krishnan-Sarin S, Shi J, Mase T, O’Malley SS. Modeling the effect of alcohol on smoking lapse behavior. Psychopharmacology (Berl) 2006;189:201–210.
  • Kahler CW, Borland R, Hyland A, McKee SA, Thompson ME, Cummings KM. Alcohol consumption and quitting smoking in the International Tobacco Control (ITC) Four Country Survey. Drug Alcohol Depend 2009;100:214–220.
  • Blot WJ, McLaughlin JK, Winn DM, Austin DF, Greenberg RS, Preston-Martin S, Bernstein L, Schoenberg JB, Stemhagen A, Fraumeni JF. Smoking and drinking in relation to oral and pharyngeal cancer. Cancer Res 1988;48:3282–3287.
  • Acott AA, Theus SA, Marchant-Miros KE, Mancino AT. Association of tobacco and alcohol use with earlier development of colorectal cancer: should we modify screening guidelines? Am J Surg 2008;196:915–918.
  • Le Strat Y, Ramoz N, Gorwood P. In alcohol-dependent drinkers, what does the presence of nicotine dependence tell us about psychiatric and addictive disorders comorbidity? Alcohol Alcohol 2010;45:167–172.
  • Rueda M, Robertson Y, Acott A, Rueda S, Keikhoff A, Guerrero W, Mancino AT. Association of tobacco and alcohol use with earlier development of colorectal pathology: should screening guidelines be modified to include these risk factors? Am J Surg 2012;204:963–967.
  • Dal Maso L, Torelli N, Biancotto E, Di Maso M, Gini A, Franchin G, Levi F, La Vecchia C, Serraino D, Polesel J. Combined effect of tobacco smoking and alcohol drinking in the risk of head and neck cancers: a re-analysis of case-control studies using bi-dimensional spline models. Eur J Epidemiol 2015;31:385–393.
  • Kandel DB, Yamaguchi K, Chen K. Stages of progression in drug involvement from adolescence to adulthood: further evidence for the gateway theory. J Stud Alcohol 1992;53:447–457.
  • Lai S, Lai H, Page JB, McCoy CB. The association between cigarette smoking and drug abuse in the United States. J Addict Dis 2000;19:11–24.
  • Degenhardt L, Dierker L, Chiu WT, Medina-Mora ME, Neumark Y, Sampson N, Alonso J, Angermeyer M, Anthony JC, Bruffaerts R, de Girolamo G, de Graaf R, Gureje O, Karam AN, Kostyuchenko S, Lee S, Lépine J-P, Levinson D, Nakamura Y, Posada-Villa J, Stein D, Wells JE, Kessler RC. Evaluating the drug use “gateway” theory using cross-national data: consistency and associations of the order of initiation of drug use among participants in the WHO World Mental Health Surveys. Drug Alcohol Depend 2010;108:84–97.
  • Kandel D, Kandel E. The Gateway Hypothesis of substance abuse: developmental, biological and societal perspectives. Acta Paediatr 2015;104:130–137.
  • McQuown SC, Belluzzi JD, Leslie FM. Low dose nicotine treatment during early adolescence increases subsequent cocaine reward. Neurotoxicol Teratol 2007;29:66–73.
  • McQuown SC, Dao JM, Belluzzi JD, Leslie FM. Age-dependent effects of low-dose nicotine treatment on cocaine-induced behavioral plasticity in rats. Psychopharmacology (Berl) 2009;207:143–152.
  • Dao JM, McQuown SC, Loughlin SE, Belluzzi JD, Leslie FM. Nicotine alters limbic function in adolescent rat by a 5-HT1A receptor mechanism. Neuropsychopharmacology 2011;36:1319–1331.
  • Hanna EZ, Yi HY, Dufour MC, Whitmore CC. The relationship of early-onset regular smoking to alcohol use, depression, illicit drug use, and other risky behaviors during early adolescence: results from the youth supplement to the third national health and nutrition examination survey. J Subst Abuse 2001;13:265–282.
  • Biederman J, Monuteaux MC, Mick E, Wilens TE, Fontanella JA, Poetzl KM, Kirk T, Masse J, Faraone SV. Is cigarette smoking a gateway to alcohol and illicit drug use disorders? A study of youths with and without attention deficit hyperactivity disorder. Biol Psychiatry 2006;59:258–264.
  • Substance Abuse and Mental Health Services Administration. Results from the 2010 National Survey on Drug Use and Health: Summary of National Findings, HHS Publication No. (SMA) 11–4658; Rockville, MD, USA: Substance Abuse & Mental Health Services Administration, 2011
  • Chen P, Jacobson KC. Developmental trajectories of substance use from early adolescence to young adulthood: gender and racial/ethnic differences. J Adolesc Health 2012;50:154–163.
  • Anderson C, Burns DM. Patterns of adolescent smoking initiation rates by ethnicity and sex. Tob Control 2000;9:II4–II8.
  • Perkins KA. Smoking Cessation in Women. CNS Drugs 2001;15:391–411.
  • Spear LP. The adolescent brain and age-related behavioral manifestations. Neurosci Biobehav Rev 2000;24:417–463.
  • O’Donnell P. Adolescent maturation of cortical dopamine. Neurotox Res 2010;18:306–312.
  • Spear LP. Adolescent neurodevelopment. J Adolesc Health 2013;52:S7–13.
  • Yuan M, Cross SJ, Loughlin SE, Leslie FM. Nicotine and the adolescent brain. J Physiol (Lond) 2015;593:3397–3412.
  • Spear LP. Assessment of adolescent neurotoxicity: rationale and methodological considerations. Neurotoxicol Teratol 2007;29:1–9.
  • Laviola G, Macrì S, Morley-Fletcher S, Adriani W. Risk-taking behavior in adolescent mice: psychobiological determinants and early epigenetic influence. Neurosci Biobehav Rev 2003;27:19–31.
  • Sturman DA, Moghaddam B. The neurobiology of adolescence: changes in brain architecture, functional dynamics, and behavioral tendencies. Neurosci Biobehav Rev 2011;35:1704–1712.
  • Hollenstein T, Lougheed JP. Beyond storm and stress: typicality, transactions, timing, and temperament to account for adolescent change. Am Psychol 2013;68:444–454.
  • Burke AR, Miczek KA. Stress in adolescence and drugs of abuse in rodent models: role of dopamine, CRF, and HPA axis. Psychopharmacology (Berl) 2014;231:1557–1580.
  • Koob GF, Volkow ND. Neurocircuitry of addiction. Neuropsychopharmacology 2010;35:217–238.
  • Ikemoto S, Bonci A. Neurocircuitry of drug reward. Neuropharmacology 2014;76:329–341.
  • Dwyer JB, Leslie FM. Adolescent maturation of dopamine D1 and D2 receptor function and interactions in rodents. In PLoS ONE, 2016;11:e0146966.
  • Kota D, Martin BR, Robinson SE, Damaj MI. Nicotine dependence and reward differ between adolescent and adult male mice. J Pharmacol Exp Ther 2007;322:399–407.
  • Doura MB, Gold AB, Keller AB, Perry DC. Adult and periadolescent rats differ in expression of nicotinic cholinergic receptor subtypes and in the response of these subtypes to chronic nicotine exposure. Brain Res 2008;1215:40–52.
  • Dwyer JB, McQuown SC, Leslie FM. The dynamic effects of nicotine on the developing brain. Pharmacol Ther 2009;122:125–139.
  • Azam L, Chen Y, Leslie FM. Developmental regulation of nicotinic acetylcholine receptors within midbrain dopamine neurons. Neuroscience 2007;144:1347–1360.
  • Lárraga A. Age- and sex-dependent behaviors induced by alcohol and nicotine [dissertation]. 2013.
  • Mojica CY, Belluzzi JD, Leslie FM. Age-dependent alterations in reward-seeking behavior after brief nicotine exposure. Psychopharmacology (Berl) 2014;231:1763–1773.
  • Mojica CY, Dao JM, Yuan M, Loughlin SE, Leslie FM. Nicotine modulation of adolescent dopamine receptor signaling and hypothalamic peptide response. Neuropharmacology 2014;77:285–293.
  • National Institute on Drug Abuse. Trends and statistics. Available from: https://www.drugabuse.gov/related-topics/trends-statistics [last accessed 2 Aug 2016].
  • DiFranza JR, Guerrera MP. Alcoholism and smoking. J Stud Alcohol 1990;51:130–135.
  • Weitzman ER, Chen Y-Y. The co-occurrence of smoking and drinking among young adults in college: national survey results from the United States. Drug Alcohol Depend 2005;80:377–386.
  • Campbell ML, Bozec LJ, McGrath D, Barrett SP. Alcohol and tobacco co-use in nondaily smokers: an inevitable phenomenon? Drug Alcohol Rev 2012;31:447–450.
  • Cohn A, Villanti A, Richardson A, Rath JM, Williams V, Stanton C, Mermelstein R. The association between alcohol, marijuana use, and new and emerging tobacco products in a young adult population. Addict Behav 2015;48:79–88.
  • Kristjansson AL, Sigfusdottir ID. E-cigarette use and relations to tobacco and alcohol use among adolescents. BMC Med 2015;13:103.
  • Surís J-C, Berchtold A, Akre C. Reasons to use e-cigarettes and associations with other substances among adolescents in Switzerland. Drug Alcohol Depend 2015;153:140–144.
  • Jiang N, Wang MP, Ho SY, Leung LT, Lam TH. Electronic cigarette use among adolescents: a cross-sectional study in Hong Kong. BMC Public Health 2016;16:202.
  • Camenga DR, Kong G, Cavallo DA, Liss A, Hyland A, Delmerico J, Cummings KM, Krishnan-Sarin S. Alternate tobacco product and drug use among adolescents who use electronic cigarettes, cigarettes only, and never smokers. J Adolesc Health 2014;55:588–591.
  • Weinberger AH, Pilver CE, Hoff RA, Mazure CM, McKee SA. Changes in smoking for adults with and without alcohol and drug use disorders: Longitudinal evaluation in the US population. Am J Drug Alcohol Abuse 2013;39:186–193.
  • McKee SA, Weinberger AH. How can we use our knowledge of alcohol-tobacco interactions to reduce alcohol use? Annu Rev Clin Psychol 2013;9:649–674.
  • Chiappetta V, García-Rodríguez O, Jin CJ, Secades-Villa R, Blanco C. Predictors of quit attempts and successful quit attempts among individuals with alcohol use disorders in a nationally representative sample. Drug Alcohol Depend 2014;141:138–144.
  • Weinberger AH, Platt J, Jiang B, Goodwin RD. Cigarette smoking and risk of alcohol use relapse among adults in recovery from alcohol use disorders. Alcohol Clin Exp Res 2015;39:1989–1996.
  • Hitschfeld MJ, Schneekloth TD, Ebbert JO, Hall-Flavin DK, Karpyak VM, Abulseoud OA, Patten CA, Geske JR, Frye MA. Female smokers have the highest alcohol craving in a residential alcoholism treatment cohort. Drug Alcohol Depend 2015;150:179–182.
  • Kouri EM, McCarthy EM, Faust AH, Lukas SE. Pretreatment with transdermal nicotine enhances some of ethanol’s acute effects in men. Drug Alcohol Depend 2004;75:55–65.
  • Rose JE, Brauer LH, Behm FM, Cramblett M, Calkins K, Lawhon D. Psychopharmacological interactions between nicotine and ethanol. Nicotine Tob Res 2004;6:133–144.
  • Glautier S, Clements K, White JAW, Taylor C, Stolerman IP. Alcohol and the reward value of cigarette smoking. Behav Pharmacol 1996;7:144–154.
  • King AC, Epstein AM. Alcohol dose-dependent increases in smoking urge in light smokers. Alcohol Clin Exp Res 2005;29:547–552.
  • Grant BF. Age at smoking onset and its association with alcohol consumption and DSM-IV alcohol abuse and dependence: results from the National Longitudinal Alcohol Epidemiologic Survey. J Subst Abuse 1998;10:59–73.
  • Riala K, Hakko H, Isohanni M, Järvelin M-R, Räsänen P. Teenage smoking and substance use as predictors of severe alcohol problems in late adolescence and in young adulthood. J Adolesc Health 2004;35:245–254.
  • Daw J, Nowotny KM, Boardman JD. Changing patterns of tobacco and alcohol co-use by gender in the United States, 1976–2010. Demogr Res 2013;28:637–648.
  • Tanner J-A, Chenoweth MJ, Tyndale RF. Pharmacogenetics of nicotine and associated smoking behaviors. Curr Top Behav Neurosci 2015;23:37–86.
  • Noble EP. Addiction and its reward process through polymorphisms of the D2 dopamine receptor gene: a review. Eur Psychiatry 2000;15:79–89.
  • Enoch M-A. Genetic influences on response to alcohol and response to pharmacotherapies for alcoholism. Pharmacol Biochem Behav 2014;123:17–24.
  • Swan GE, Carmelli D, Cardon LR. Heavy consumption of cigarettes, alcohol and coffee in male twins. J Stud Alcohol 1997;58:182–190.
  • True WR, Xian H, Scherrer JF, Madden PA, Bucholz KK, Heath AC, Eisen SA, Lyons MJ, Goldberg J, Tsuang M. Common genetic vulnerability for nicotine and alcohol dependence in men. Arch Gen Psychiatry 1999;56:655–661.
  • Bierut LJ, Rice JP, Goate A, Hinrichs AL, Saccone NL, Foroud T, Edenberg HJ, Cloninger CR, Begleiter H, Conneally PM, Crowe RR, Hesselbrock V, Li T-K, Nurnberger JI, Porjesz B, Schuckit MA, Reich T. A genomic scan for habitual smoking in families of alcoholics: common and specific genetic factors in substance dependence. Am J Med Genet A 2004; 124A, 19–27.
  • Spitz MR, Amos CI, Dong Q, Lin J, Wu X. The CHRNA5-A3 region on chromosome 15q24-25.1 is a risk factor both for nicotine dependence and for lung cancer. J Natl Cancer Inst 2008;100:1552–1556.
  • Bierut LJ. Nicotine dependence and genetic variation in the nicotinic receptors. Drug Alcohol Depend 2009;104:S64–S69.
  • Wang JC, Grucza R, Cruchaga C, Hinrichs AL, Bertelsen S, Budde JP, Fox L, Goldstein E, Reyes O, Saccone N, Saccone S, Xuei X, Bucholz K, Kuperman S, Nurnberger J, Rice JP, Schuckit M, Tischfield J, Hesselbrock V, Porjesz B, Edenberg HJ, Bierut LJ, Goate AM. Genetic variation in the CHRNA5 gene affects mRNA levels and is associated with risk for alcohol dependence. Mol Psychiatry 2009;14:501–510.
  • Li MD, Xu Q, Lou X-Y, Payne TJ, Niu T, Ma JZ. Association and interaction analysis of variants in CHRNA5/CHRNA3/CHRNB4 gene cluster with nicotine dependence in African and European Americans. Am J Med Genet B Neuropsychiatr Genet2010; 153B:745–756.
  • Ehringer MA, Clegg HV, Collins AC, Corley RP, Crowley T, Hewitt JK, Hopfer CJ, Krauter K, Lessem J, Rhee SH, Schlaepfer I, Smolen A, Stallings MC, Young SE, Zeiger JS. Association of the neuronal nicotinic receptor beta2 subunit gene (CHRNB2) with subjective responses to alcohol and nicotine. Am J Med Genet B Neuropsychiatr Genet 2007;144B:596–604.
  • Hoft NR, Corley RP, McQueen MB, Huizinga D, Menard S, Ehringer MA. SNPs in CHRNA6 and CHRNB3 are associated with alcohol consumption in a nationally representative sample. Genes Brain Behav 2009;8:631–637.
  • Hoft NR, Corley RP, McQueen MB, Schlaepfer IR, Huizinga D, Ehringer MA. Genetic association of the CHRNA6 and CHRNB3 genes with tobacco dependence in a nationally representative sample. Neuropsychopharmacology 2009;34:698–706.
  • Schlaepfer IR, Hoft NR, Collins AC, Corley RP, Hewitt JK, Hopfer CJ, Lessem JM, McQueen MB, Rhee SH, Ehringer MA. The CHRNA5/A3/B4 gene cluster variability as an important determinant of early alcohol and tobacco initiation in young adults. Biol Psychiatry 2008;63:1039–1046.
  • Weiss RB, Baker TB, Cannon DS, von Niederhausern A, Dunn DM, Matsunami N, Singh NA, Baird L, Coon H, McMahon WM, Piper ME, Fiore MC, Scholand MB, Connett JE, Kanner RE, Gahring LC, Rogers SW, Hoidal JR, Leppert MF. A candidate gene approach identifies the CHRNA5-A3-B4 region as a risk factor for age-dependent nicotine addiction. PLoS Genet 2008;4:e1000125.
  • Kapoor M, Wang J-C, Bertelsen S, Bucholz K, Budde JP, Hinrichs A, Agrawal A, Brooks A, Chorlian D, Dick D, Hesselbrock V, Foroud T, Kramer J, Kuperman S, Manz N, Nurnberger J, Porjesz B, Rice J, Tischfield J, Xuei X, Schuckit M, Edenberg HJ, Bierut LJ, Goate AM. Variants located upstream of CHRNB4 on chromosome 15q25.1 are associated with age at onset of daily smoking and habitual smoking. PLoS ONE 2012;7:e33513.
  • Lubke GH, Stephens SH, Lessem JM, Hewitt JK, Ehringer MA. The CHRNA5/A3/B4 gene cluster and tobacco, alcohol, cannabis, inhalants and other substance use initiation: replication and new findings using mixture analyses. Behav Genet 2012;42:636–646.
  • Coon H, Piasecki TM, Cook EH, Dunn D, Mermelstein RJ, Weiss RB, Cannon DS. Association of the CHRNA4 neuronal nicotinic receptor subunit gene with frequency of binge drinking in young adults. Alcohol Clin Exp Res 2014;38:930–937.
  • Mihalak KB, Carroll FI, Luetje CW. Varenicline is a partial agonist at alpha4beta2 and a full agonist at alpha7 neuronal nicotinic receptors. Mol Pharmacol 2006;70:801–805.
  • Erwin BL, Slaton RM. Varenicline in the treatment of alcohol use disorders. Ann Pharmacother 2014;48:1445–1455.
  • de Bejczy A, Löf E, Walther L, Guterstam J, Hammarberg A, Asanovska G, Franck J, Isaksson A, Söderpalm B. Varenicline for treatment of alcohol dependence: a randomized, placebo-controlled trial. Alcohol Clin Exp Res 2015;39:2189–2199.
  • Falk DE, Castle IJP, Ryan M, Fertig J, Litten RZ. Moderators of varenicline treatment effects in a double-blind, placebo-controlled trial for alcohol dependence: an exploratory analysis. J Addict Med 2015;9:296–303.
  • de Fiebre CM, Marks MJ, Collins AC. Ethanol-nicotine interactions in long-sleep and short-sleep mice. Alcohol 1990;7:249–257.
  • de Fiebre CM, Romm E, Collins JT, Draski LJ, Deitrich RA, Collins AC. Responses to cholinergic agonists of rats selectively bred for differential sensitivity to ethanol. Alcohol Clin Exp Res 1991;15:270–276.
  • de Fiebre NC, Dawson R, de Fiebre CM. The selectively bred high alcohol sensitivity (HAS) and low alcohol sensitivity (LAS) rats differ in sensitivity to nicotine. Alcohol Clin Exp Res 2002;266:765–772.
  • Bergstrom HC, Palmer AA, Wood RD, Burkhart-Kasch S, McKinnon CS, Phillips TJ. Reverse selection for differential response to the locomotor stimulant effects of ethanol provides evidence for pleiotropic genetic influence on locomotor response to other drugs of abuse. Alcohol Clin Exp Res 2003;27:1535–1547.
  • Lê AD, Li Z, Funk D, Shram M, Li TK, Shaham Y. Increased vulnerability to nicotine self-administration and relapse in alcohol-naive offspring of rats selectively bred for high alcohol intake. J Neurosci 2006;26:1872–1879.
  • Tritto T, Marley RJ, Bastidas D, Stitzel JA, Collins AC. Potential regulation of nicotine and ethanol actions by alpha4-containing nicotinic receptors. Alcohol 2001;24:69–78.
  • Butt CM, Hutton SR, Stitzel JA, Balogh SA, Owens JC, Collins AC. A polymorphism in the alpha4 nicotinic receptor gene (Chrna4) modulates enhancement of nicotinic receptor function by ethanol. Alcohol Clin Exp Res 2003;27:733–742.
  • Butt CM, King NM, Stitzel JA, Collins AC. Interaction of the nicotinic cholinergic system with ethanol withdrawal. J Pharmacol Exp Ther 2004;308:591–599.
  • Dawson A, Miles MF, Damaj MI. The β2 nicotinic acetylcholine receptor subunit differentially influences ethanol behavioral effects in the mouse. Alcohol 2013;47:85–94.
  • Butt CM, King NM, Hutton SR, Collins AC, Stitzel JA. Modulation of nicotine but not ethanol preference by the mouse Chrna4 A529T polymorphism. Behav Neurosci 2005;119:26–37.
  • Kamens HM, Andersen J, Picciotto MR. Modulation of ethanol consumption by genetic and pharmacological manipulation of nicotinic acetylcholine receptors in mice. Psychopharmacology (Berl) 2010;208:613–626.
  • Bowers BJ, McClure-Begley TD, Keller JJ, Paylor R, Collins AC, Wehner JM. Deletion of the alpha7 nicotinic receptor subunit gene results in increased sensitivity to several behavioral effects produced by alcohol. Alcohol Clin Exp Res 2005;29:295–302.
  • Gallego X, Ruiz-Medina J, Valverde O, Molas S, Robles N, Sabrià J, Crabbe JC, Dierssen M. Transgenic over expression of nicotinic receptor alpha 5, alpha 3, and beta 4 subunit genes reduces ethanol intake in mice. Alcohol 2012;46:205–215.
  • Santos N, Chatterjee S, Henry A, Holgate J, Bartlett SE. The α5 neuronal nicotinic acetylcholine receptor subunit plays an important role in the sedative effects of ethanol but does not modulate consumption in mice. Alcohol Clin Exp Res 2013;37:655–662.
  • Azam L, Winzer-Serhan UH, Chen Y, Leslie FM. Expression of neuronal nicotinic acetylcholine receptor subunit mRNAs within midbrain dopamine neurons. J Comp Neurol 2002;444:260–274.
  • Leslie FM, Mojica CY, Reynaga DD. Nicotinic receptors in addiction pathways. Mol Pharmacol 2013;83:753–758.
  • Kamens HM, Hoft NR, Cox RJ, Miyamoto JH, Ehringer MA. The α6 nicotinic acetylcholine receptor subunit influences ethanol-induced sedation. Alcohol 2012;46:463–471.
  • Powers MS, Broderick HJ, Drenan RM, Chester JA. Nicotinic acetylcholine receptors containing α6 subunits contribute to alcohol reward-related behaviours. Genes Brain Behav 2013;12:543–553.
  • Hendrickson LM, Zhao-Shea R, Pang X, Gardner PD, Tapper AR. Activation of alpha4* nAChRs is necessary and sufficient for varenicline-induced reduction of alcohol consumption. J Neurosci 2010;30:10169–10176.
  • Liu L, Hendrickson LM, Guildford MJ, Zhao-Shea R, Gardner PD, Tapper AR. Nicotinic acetylcholine receptors containing the α4 subunit modulate alcohol reward. Biol Psychiatry 2013;73:738–746.
  • Hendrickson LM, Gardner P, Tapper AR. Nicotinic acetylcholine receptors containing the α4 subunit are critical for the nicotine-induced reduction of acute voluntary ethanol consumption. Channels (Austin) 2011;5:124–127.
  • Hendrickson LM, Zhao-Shea R, Tapper AR. Modulation of ethanol drinking-in-the-dark by mecamylamine and nicotinic acetylcholine receptor agonists in C57BL/6J mice. Psychopharmacology (Berl) 2009;204:563–572.
  • Bhutada P, Mundhada Y, Ghodki Y, Dixit P, Umathe S, Jain K. Acquisition, expression, and reinstatement of ethanol-induced conditioned place preference in mice: effects of exposure to stress and modulation by mecamylamine. J Psychopharmacol (Oxford) 2012;26:315–323.
  • Jerlhag E, Grøtli M, Luthman K, Svensson L, Engel JA. Role of the subunit composition of central nicotinic acetylcholine receptors for the stimulatory and dopamine-enhancing effects of ethanol. Alcohol Alcohol 2006;41:486–493.
  • Larsson A, Jerlhag E, Svensson L, Söderpalm B, Engel JA. Is an alpha-conotoxin MII-sensitive mechanism involved in the neurochemical, stimulatory, and rewarding effects of ethanol? Alcohol 2004;34:239–250.
  • Kuzmin A, Jerlhag E, Liljequist S, Engel J. Effects of subunit selective nACh receptors on operant ethanol self-administration and relapse-like ethanol-drinking behavior. Psychopharmacology (Berl) 2009;203:99–108.
  • Chatterjee S, Steensland P, Simms JA, Holgate J, Coe JW, Hurst RS, Shaffer CL, Lowe J, Rollema H, Bartlett SE. Partial agonists of the α3β4* neuronal nicotinic acetylcholine receptor reduce ethanol consumption and seeking in rats. Neuropsychopharmacology 2011;36:603–615.
  • Lê AD, Corrigall WA, Harding JW, Juzytsch W, Li TK. Involvement of nicotinic receptors in alcohol self-administration. Alcohol Clin Exp Res 2000;24:155–163.
  • Lê AD, Wang A, Harding S, Juzytsch W, Shaham Y. Nicotine increases alcohol self-administration and reinstates alcohol seeking in rats. Psychopharmacology (Berl) 2003;168:216–221.
  • Olausson P, Ericson M, Löf E, Engel JA, Söderpalm B. Nicotine-induced behavioral disinhibition and ethanol preference correlate after repeated nicotine treatment. Eur J Pharmacol 2001;417:117–123.
  • Bito-Onon JJ, Simms JA, Chatterjee S, Holgate J, Bartlett SE. Varenicline, a partial agonist at neuronal nicotinic acetylcholine receptors, reduces nicotine-induced increases in 20% ethanol operant self-administration in Sprague-Dawley rats. Addict Biol 2011;16:440–449.
  • Hauser SR, Getachew B, Oster SM, Dhaher R, Ding Z-M, Bell RL, McBride WJ, Rodd ZA. Nicotine modulates alcohol-seeking and relapse by alcohol-preferring (P) rats in a time-dependent manner. Alcohol Clin Exp Res 2012;36:43–54.
  • Doyon WM, Dong Y, Ostroumov A, Thomas AM, Zhang TA, Dani JA. Nicotine decreases ethanol-induced dopamine signaling and increases self-administration via stress hormones. Neuron 2013;79:530–540.
  • Tizabi Y, Copeland RL, Louis VA, Taylor RE. Effects of combined systemic alcohol and central nicotine administration into ventral tegmental area on dopamine release in the nucleus accumbens. Alcohol Clin Exp Res 2002;26:394–399.
  • Tizabi Y, Bai L, Copeland RL, Taylor RE. Combined effects of systemic alcohol and nicotine on dopamine release in the nucleus accumbens shell. Alcohol Alcohol 2007;42:413–416.
  • Deehan GA, Hauser SR, Waeiss RA, Knight CP, Toalston JE, Truitt WA, McBride WJ, Rodd ZA. Co-administration of ethanol and nicotine: the enduring alterations in the rewarding properties of nicotine and glutamate activity within the mesocorticolimbic system of female alcohol-preferring (P) rats. Psychopharmacology (Berl) 2015;232:4293–4302.
  • Lê AD, Lo S, Harding S, Juzytsch W, Marinelli PW, Funk D. Coadministration of intravenous nicotine and oral alcohol in rats. Psychopharmacology (Berl) 2010;208:475–486.
  • Truitt WA, Hauser SR, Deehan GA, Toalston JE, Wilden JA, Bell RL, McBride WJ, Rodd ZA. Ethanol and nicotine interaction within the posterior ventral tegmental area in male and female alcohol-preferring rats: evidence of synergy and differential gene activation in the nucleus accumbens shell. Psychopharmacology (Berl) 2015;232:639–649.
  • Hauser SR, Deehan GA, Toalston JE, Bell RL, McBride WJ, Rodd ZA. Enhanced alcohol-seeking behavior by nicotine in the posterior ventral tegmental area of female alcohol-preferring (P) rats: modulation by serotonin-3 and nicotinic cholinergic receptors. Psychopharmacology (Berl) 2014;231:3745–3755.
  • Cippitelli A, Brunori G, Gaiolini KA, Zaveri NT, Toll L. Pharmacological stress is required for the anti-alcohol effect of the α3β4* nAChR partial agonist AT-1001. Neuropharmacology 2015;93:229–236.
  • Funk D, Lo S, Coen K, Lê AD. Effects of varenicline on operant self-administration of alcohol and/or nicotine in a rat model of co-abuse. Behav Brain Res 2015;296:157–162.
  • Scuppa G, Cippitelli A, Toll L, Ciccocioppo R, Ubaldi M. Varenicline decreases nicotine but not alcohol self-administration in genetically selected Marchigian Sardinian alcohol-preferring (msP) rats. Drug Alcohol Depend 2015;156:126–132.
  • Perez E, Quijano-Cardé N, De Biasi M. Nicotinic mechanisms modulate ethanol withdrawal and modify time course and symptoms severity of simultaneous withdrawal from alcohol and nicotine. Neuropsychopharmacology 2015;40:2327–2336.
  • Kuhn C. Emergence of sex differences in the development of substance use and abuse during adolescence. Pharmacol Ther 2015;153:55–78.
  • Locker AR, Marks MJ, Kamens HM, Klein LC. Exposure to nicotine increases nicotinic acetylcholine receptor density in the reward pathway and binge ethanol consumption in C57BL/6J adolescent female mice. Brain Res Bull 2015;123:13–22.
  • Smith AM, Kelly RB, Chen W-JA. Chronic continuous nicotine exposure during periadolescence does not increase ethanol intake during adulthood in rats. Alcohol Clin Exp Res 2002;26:976–979.
  • O’Dell LE, Bruijnzeel AW, Smith RT, Parsons LH, Merves ML, Goldberger BA, Richardson HN, Koob GF, Markou A. Diminished nicotine withdrawal in adolescent rats: implications for vulnerability to addiction. Psychopharmacology (Berl) 2006;186:612–619.
  • Cao J, Belluzzi JD, Loughlin SE, Keyler DE, Pentel PR, Leslie FM. Acetaldehyde, a major constituent of tobacco smoke, enhances behavioral, endocrine, and neuronal responses to nicotine in adolescent and adult rats. Neuropsychopharmacology 2007;32:2025–2035.
  • Adriani W, Macrì S, Pacifici R, Laviola G. Peculiar vulnerability to nicotine oral self-administration in mice during early adolescence. Neuropsychopharmacology 2002;27:212–224.
  • Hefner K, Holmes A. An investigation of the behavioral actions of ethanol across adolescence in mice. Psychopharmacology (Berl) 2007;191:311–322.
  • Green AS, Grahame NJ. Ethanol drinking in rodents: is free-choice drinking related to the reinforcing effects of ethanol? Alcohol 2008;42:1–11.
  • Philpot RM, Engberg ME, Wecker L. Ethanol conditioned place preference and alterations in ΔFosB following adolescent nicotine administration differ in rats exhibiting high or low behavioral reactivity to a novel environment. Behav Brain Res 2014;262:101–108.
  • Belluzzi JD, Wang R, Leslie FM. Acetaldehyde enhances acquisition of nicotine self-administration in adolescent rats. Neuropsychopharmacology 2005;30:705–712.
  • Park MK, Belluzzi JD, Han S-H, Cao J, Leslie FM. Age, sex and early environment contribute to individual differences in nicotine/acetaldehyde-induced behavioral and endocrine responses in rats. Pharmacol Biochem Behav 2007;86:297–305.
  • Bachmanov AA, Kiefer SW, Molina JC, Tordoff MG, Duffy VB, Bartoshuk LM, Mennella JA. Chemosensory factors influencing alcohol perception, preferences, and consumption. Alcohol Clin Exp Res 2003;27:220–231.
  • Pritchard WS, Robinson JH, Guy TD, Davis RA, Stiles MF. Assessing the sensory role of nicotine in cigarette smoking. Psychopharmacology (Berl) 1996;127:55–62.
  • Mantella NM, Youngentob SL. Prenatal alcohol exposure increases postnatal acceptability of nicotine odor and taste in adolescent rats. PLoS ONE 2014;9:e102255.
  • Youngentob SL, Glendinning JI. Fetal ethanol exposure increases ethanol intake by making it smell and taste better. Proc Natl Acad Sci U S A 2009;106:5359–5364.
  • Glendinning JI, Simons YM, Youngentob L, Youngentob SL. Fetal ethanol exposure attenuates aversive oral effects of TrpV1, but not TrpA1 agonists in rats. Exp Biol Med (Maywood) 2012;237:236–240.
  • Ribeiro-Carvalho A, Lima CS, Filgueiras CC, Manhães AC, Abreu-Villaça Y. Nicotine and ethanol interact during adolescence: effects on the central cholinergic systems. Brain Res 2008;1232:48–60.
  • Trauth JA, McCook EC, Seidler FJ, Slotkin TA. Modeling adolescent nicotine exposure: effects on cholinergic systems in rat brain regions. Brain Res 2000;873:18–25.
  • Brewer AJ, Mahoney JJ, Nerumalla CS, Newton TF, De La Garza R. The influence of smoking cigarettes on the high and desire for cocaine among active cocaine users. Pharmacol Biochem Behav 2013;106:132–136.
  • O’Neill J. Interaction of methamphetamine abuse, tobacco abuse, and gender in the brain. Am J Drug Alcohol Abuse 2015;41:269–271.
  • National Institute on Drug Abuse. DrugFacts: Nationwide trends. Available from: https://www.drugabuse.gov/publications/drugfacts/nationwide-trends [last accessed 2 Aug 2016].
  • Grant KM, Kelley SS, Agrawal S, Meza JL, Meyer JR, Romberger DJ. Methamphetamine use in rural Midwesterners. Am J Addict 2007;16:79–84.
  • Russell K, Dryden DM, Liang Y, Friesen C, O’Gorman K, Durec T, Wild TC, Klassen TP. Risk factors for methamphetamine use in youth: a systematic review. BMC Pediatr 2008;8:48.
  • Tidey JW, O’Neill SC, Higgins ST. d-amphetamine increases choice of cigarette smoking over monetary reinforcement. Psychopharmacology (Berl) 2000;153:85–92.
  • Winhusen TM, Kropp F, Theobald J, Lewis DF. Achieving smoking abstinence is associated with decreased cocaine use in cocaine-dependent patients receiving smoking-cessation treatment. Drug Alcohol Depend 2014;134:391–395.
  • Grucza RA, Wang JC, Stitzel JA, Hinrichs AL, Saccone SF, Saccone NL, Bucholz KK, Cloninger CR, Neuman RJ, Budde JP, Fox L, Bertelsen S, Kramer J, Hesselbrock V, Tischfield J, Nurnberger JI, Almasy L, Porjesz B, Kuperman S, Schuckit MA, Edenberg HJ, Rice JP, Goate AM, Bierut LJ. A risk allele for nicotine dependence in CHRNA5 is a protective allele for cocaine dependence. Biol Psychiatry 2008;64:922–929.
  • Sherva R, Kranzler HR, Yu Y, Logue MW, Poling J, Arias AJ, Anton RF, Oslin D, Farrer LA, Gelernter J. Variation in nicotinic acetylcholine receptor genes is associated with multiple substance dependence phenotypes. Neuropsychopharmacology 2010;35:1921–1931.
  • Yang J, Li MD. Association and interaction analyses of 5-HT3 receptor and serotonin transporter genes with alcohol, cocaine, and nicotine dependence using the SAGE data. Hum Genet 2014;133:905–918.
  • Palmer RHC, Button TM, Rhee SH, Corley RP, Young SE, Stallings MC, Hopfer CJ, Hewitt JK. Genetic etiology of the common liability to drug dependence: evidence of common and specific mechanisms for DSM-IV dependence symptoms. Drug Alcohol Depend 2012;123:S24–S32.
  • Vanyukov MM, Tarter RE, Kirillova GP, Kirisci L, Reynolds MD, Kreek MJ, Conway KP, Maher BS, Iacono WG, Bierut L, Neale MC, Clark DB, Ridenour TA. Common liability to addiction and “gateway hypothesis”: theoretical, empirical and evolutionary perspective. Drug Alcohol Depend 2012;123:S3–17.
  • Lewinsohn PM, Rohde P, Brown RA. Level of current and past adolescent cigarette smoking as predictors of future substance use disorders in young adulthood. Addiction 1999;94:913–921.
  • Brook JS, Balka EB, Ning Y, Brook DW. Trajectories of cigarette smoking among African Americans and Puerto Ricans from adolescence to young adulthood: associations with dependence on alcohol and illegal drugs. Am J Addict 2007;16:195–201.
  • Wilens TE, Adamson J, Monuteaux MC, Faraone SV, Schillinger M, Westerberg D, Biederman J. Effect of prior stimulant treatment for attention-deficit/hyperactivity disorder on subsequent risk for cigarette smoking and alcohol and drug use disorders in adolescents. Arch Pediatr Adolesc Med 2008;162:916–921.
  • Lambert NM, McLeod M, Schenk S. Subjective responses to initial experience with cocaine: an exploration of the incentive-sensitization theory of drug abuse. Addiction 2006;101:713–725.
  • Horger BA, Giles MK, Schenk S. Preexposure to amphetamine and nicotine predisposes rats to self-administer a low dose of cocaine. Psychopharmacology (Berl) 1992;107:271–276.
  • Levine A, Huang Y, Drisaldi B, Griffin EA, Pollak DD, Xu S, Yin D, Schaffran C, Kandel DB, Kandel ER. Molecular mechanism for a gateway drug: epigenetic changes initiated by nicotine prime gene expression by cocaine. Sci Transl Med 2011;3:107ra109.
  • Mello NK, Newman JL. Discriminative and reinforcing stimulus effects of nicotine, cocaine, and cocaine + nicotine combinations in rhesus monkeys. Exp Clin Psychopharmacol 2011;19:203–214.
  • Buffalari DM, Marfo NYA, Smith TT, Levin ME, Weaver MT, Thiels E, Sved AF, Donny EC. Nicotine enhances the expression of a sucrose or cocaine conditioned place preference in adult male rats. Pharmacol Biochem Behav 2014;124:320–325.
  • Li H, Bu Q, Chen B, Shao X, Hu Z, Deng P, Lv L, Deng Y, Zhu R, Li Y, Zhang B, Hou J, Du C, Zhao Q, Fu D, Zhao Y, Cen X. Mechanisms of metabonomic for a gateway drug: nicotine priming enhances behavioral response to cocaine with modification in energy metabolism and neurotransmitter level. PLoS ONE 2014;9:e87040.
  • Hiranita T, Nawata Y, Sakimura K, Anggadiredja K, Yamamoto T. Suppression of methamphetamine-seeking behavior by nicotinic agonists. Proc Natl Acad Sci U S A 2006;103:8523–8527.
  • Neugebauer NM, Harrod SB, Bardo MT. Nicotine elicits methamphetamine-seeking in rats previously administered nicotine. Drug Alcohol Depend 2010;106:72–78.
  • Zernig G, O’Laughlin IA, Fibiger HC. Nicotine and heroin augment cocaine-induced dopamine overflow in nucleus accumbens. Eur J Pharmacol 1997;337:1–10.
  • Gerasimov MR, Franceschi M, Volkow ND, Rice O, Schiffer WK, Dewey SL. Synergistic interactions between nicotine and cocaine or methylphenidate depend on the dose of dopamine transporter inhibitor. Synapse 2000;38:432–437.
  • Kim MN, Jutkiewicz EM, Zhang M, Gnegy ME. The sensitizing effect of acute nicotine on amphetamine-stimulated behavior and dopamine efflux requires activation of β2 subunit-containing nicotinic acetylcholine receptors and glutamate N-methyl-D-aspartate receptors. Neuropharmacology 2011;60:1126–1134.
  • Mark GP, Hajnal A, Kinney AE, Keys AS. Self-administration of cocaine increases the release of acetylcholine to a greater extent than response-independent cocaine in the nucleus accumbens of rats. Psychopharmacology (Berl) 1999;143:47–53.
  • Shinohara F, Kihara Y, Ide S, Minami M, Kaneda K. Critical role of cholinergic transmission from the laterodorsal tegmental nucleus to the ventral tegmental area in cocaine-induced place preference. Neuropharmacology 2014;79:573–579.
  • Levin ED, Mead T, Rezvani AH, Rose JE, Gallivan C, Gross R. The nicotinic antagonist mecamylamine preferentially inhibits cocaine vs. food self-administration in rats. Physiol Behav 2000;71:565–570.
  • Zachariou V, Caldarone BJ, Weathers-Lowin A, George TP, Elsworth JD, Roth RH, Changeux JP, Picciotto MR. Nicotine receptor inactivation decreases sensitivity to cocaine. Neuropsychopharmacology 2001;24:576–589.
  • McGranahan TM, Patzlaff NE, Grady SR, Heinemann SF, Booker TK. α4β2 nicotinic acetylcholine receptors on dopaminergic neurons mediate nicotine reward and anxiety relief. J Neurosci 2011;31:10891–10902.
  • Sanjakdar SS, Maldoon PP, Marks MJ, Brunzell DH, Maskos U, McIntosh JM, Bowers MS, Damaj MI. Differential roles of α6β2* and α4β2* neuronal nicotinic receptors in nicotine- and cocaine-conditioned reward in mice. Neuropsychopharmacology 2015;40:350–360.
  • Khroyan TV, Yasuda D, Toll L, Polgar WE, Zaveri NT. High affinity α3β4 nicotinic acetylcholine receptor ligands AT-1001 and AT-1012 attenuate cocaine-induced conditioned place preference and behavioral sensitization in mice. Biochem Pharmacol 2015;97:531–541.
  • Glick SD, Kuehne ME, Raucci J, Wilson TE, Larson D, Keller RW, Carlson JN. Effects of iboga alkaloids on morphine and cocaine self-administration in rats: relationship to tremorigenic effects and to effects on dopamine release in nucleus accumbens and striatum. Brain Res 1994;657:14–22.
  • Glick SD, Maisonneuve IM, Szumlinski KK. 18-Methoxycoronaridine (18-MC) and ibogaine: comparison of antiaddictive efficacy, toxicity, and mechanisms of action. Ann N Y Acad Sci 2000;914:369–386.
  • Alajaji M, Lazenka MF, Kota D, Wise LE, Younis RM, Carroll FI, Levine A, Selley DE, Sim- Selley LJ, Damaj MI. Early adolescent nicotine exposure affects later-life cocaine reward in mice. In Neuropharmacology, 2016;105:308–317.
  • Dickson PE, Miller MM, Rogers TD, Blaha CD, Mittleman G. Effects of adolescent nicotine exposure and withdrawal on intravenous cocaine self-administration during adulthood in male C57BL/6J mice. Addict Biol 2014;19:37–48.
  • Pomfrey RL, Bostwick TA, Wetzell BB, Riley AL. Adolescent nicotine exposure fails to impact cocaine reward, aversion and self-administration in adult male rats. Pharmacol Biochem Behav 2015;137:30–37.
  • Kelley BM, Rowan JD. Long-term, low-level adolescent nicotine exposure produces dose-dependent changes in cocaine sensitivity and reward in adult mice. Int J Dev Neurosci 2004;22:339–348.
  • Santos GC, Marin MT, Cruz FC, Delucia R, Planeta CS. Amphetamine- and nicotine-induced cross-sensitization in adolescent rats persists until adulthood. Addict Biol 2009;14:270–275.
  • Pipkin JA, Kaplan GJ, Plant CP, Eaton SE, Gil SM, Zavala AR, Crawford CA. Nicotine exposure beginning in adolescence enhances the acquisition of methamphetamine self-administration, but not methamphetamine-primed reinstatement in male rats. Drug Alcohol Depend 2014;142:341–344.
  • Mathers M, Toumbourou JW, Catalano RF, Williams J, Patton GC. Consequences of youth tobacco use: a review of prospective behavioural studies. Addiction 2006;101:948–958.
  • Dutra LM, Glantz SA. Electronic cigarettes and conventional cigarette use among U.S. adolescents: a cross-sectional study. JAMA Pediatr 2014;168:610–617.
  • Bunnell RE, Agaku IT, Arrazola RA, Apelberg BJ, Caraballo RS, Corey CG, Coleman BN, Dube SR, King BA. Intentions to smoke cigarettes among never-smoking US middle and high school electronic cigarette users: National Youth Tobacco Survey, 2011–2013. Nicotine Tob Res 2015;17:228–235.
  • Wills TA, Knight R, Williams RJ, Pagano I, Sargent JD. Risk factors for exclusive e-cigarette use and dual e-cigarette use and tobacco use in adolescents. Pediatrics 2015;135:e43–e51.
  • Farrelly MC, Loomis BR, Han B, Gfroerer J, Kuiper N, Couzens GL, Dube S, Caraballo RS. A comprehensive examination of the influence of state tobacco control programs and policies on youth smoking. Am J Public Health 2013;103:549–555.
  • Miech RA, O’Malley PM, Johnston LD, Patrick ME. E-Cigarettes and the drug use patterns of adolescents. Nicotine Tob Res 2015.
  • Hughes K, Bellis MA, Hardcastle KA, McHale P, Bennett A, Ireland R, Pike K. Associations between e-cigarette access and smoking and drinking behaviours in teenagers. BMC Public Health 2015;15:244.
  • Azagba S, Sharaf MF. Binge drinking and marijuana use among menthol and non-menthol adolescent smokers: findings from the youth smoking survey. Addict Behav 2014;39:740–743.
  • Perkins KA, Donny E, Caggiula AR. Sex differences in nicotine effects and self-administration: review of human and animal evidence. Nicotine Tob Res 1999;1:301–315.
  • Randall CL, Roberts JS, Del Boca FK, Carroll KM, Connors GJ, Mattson ME. Telescoping of landmark events associated with drinking: a gender comparison. J Stud Alcohol 1999;60:252–260.
  • Zilberman M, Tavares H, el-Guebaly N. Gender similarities and differences: the prevalence and course of alcohol- and other substance-related disorders. J Addict Dis 2003;22:61–74.
  • Mann K, Ackermann K, Croissant B, Mundle G, Nakovics H, Diehl A. Neuroimaging of gender differences in alcohol dependence: are women more vulnerable? Alcohol Clin Exp Res 2005;29:896–901.
  • Back SE, Brady KT, Jackson JL, Salstrom S, Zinzow H. Gender differences in stress reactivity among cocaine-dependent individuals. Psychopharmacology (Berl) 2005;180:169–176.
  • Becker JB, Hu M. Sex differences in drug abuse. Front Neuroendocrinol 2008;29:36–47.
  • O’Dell LE, Torres OV. A mechanistic hypothesis of the factors that enhance vulnerability to nicotine use in females. Neuropharmacology 2014;76:566–580.
  • Almeida OF, Shoaib M, Deicke J, Fischer D, Darwish MH, Patchev VK. Gender differences in ethanol preference and ingestion in rats. The role of the gonadal steroid environment. J Clin Invest 1998;101:2677–2685.
  • McMurray MS, Williams SK, Jarrett TM, Cox ET, Fay EE, Overstreet DH, Walker CH, Johns JM. Gestational ethanol and nicotine exposure: effects on maternal behavior, oxytocin, and offspring ethanol intake in the rat. Neurotoxicol Teratol 2008;30:475–486.
  • Lynch WJ. Sex differences in vulnerability to drug self-administration. Exp Clin Psychopharmacol 2006;14:34–41.
  • Roberts DC, Bennett SA, Vickers GJ. The estrous cycle affects cocaine self-administration on a progressive ratio schedule in rats. Psychopharmacology (Berl) 1989;98:408–411.

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