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Special Issue

Interactions between nicotine and drugs of abuse: a review of preclinical findings

, PhD
Pages 155-170 | Received 27 Feb 2016, Accepted 28 Jun 2016, Published online: 02 Sep 2016

References

  • Center for Behavioral Health Statistics and Quality. Behavioral health trends in the United States: Results from the 2014 National Survey on Drug Use and Health ( HHS Publication No. SMA 15–4927, NSDUH Series H-50), 2015.
  • Weaver SR, Majeed BA, Pechacek TF. Use fo electronic nicotine delivery systems and other tobacco products among USA adults, 2014: results from a national survey. Int J Public Health. 2015, in press.
  • European Monitoring Centre for Drugs and Drug Addiction. Polydrug Use: Patterns and Responses. (2009). Luxembourg: Office for official publications of the European communities.
  • National Center for Chronic Disease Prevention and Health Promotion (US) Office on Smoking and Health (2014): The Health Consequences of Smoking—50 Years of Progress: A Report of the Surgeon General. Atlanta(GA): Centers for Disease Control and Prevention (US).
  • Hurt RD, Offord KP, Croghan IT, Gomez-Dahl L. Mortality following inpatient addictions treatment: Role of tobacco use in a community-based cohort. JAMA 1996;275:1097–1103.
  • Higgins ST, Budney AJ, Hughes JR, Bickel WK. Influence of cocaine use on cigarette smoking. JAMA 1994;14:1724.
  • Henningfield JE, Griffiths RR. Cigarette smoking and subjective response: effects of d-amphetamine. Clin Pharmacol Ther 1981;30:497–505.
  • Mello NK, Mendelson JH, Sellers ML, Kuehnle JC. Effects of heroin self-administration on cigarette smoking. Psychopharmacology 1980;67:45–52.
  • Mello NK, Mendelson JH, Sellers ML. Effect of alcohol and marihuana on tobacco smoking. Clin Pharmacol Ther 1980;27:202–209.
  • Mintz J, Boyd G, Rose JE, Charuvastra VC, Jarvik ME. Alcohol increases cigarette smoking: a laboratory demonstration. Addictive Behav 1985;10:203–207.
  • Bruno A. Cerebrovascular complications of alcohol and sympathomimetic drug abuse. Curr Neurol Neurosci Rep 2003;3:40–45.
  • Moliterno DJ, Willard JE, Lange RA, Negus BH, Boehrer JD, Glamann DB, et al. Coronary-artery vasoconstriction induced by cocaine, cigarette smoking, or both. N Engl J Med 1994;330:454–459.
  • Devlin RJ, Henry JA. Clinical review: Major consequences of illicit drug consumption. Crit Care 2008;12:202.
  • Levine A, Huang Y, Drisaldi B, Griffin EA, Pollak DD, Xu S, et al. Molecular mechanism for a gateway drug: epigenetic changes initiated by nicotine prime gene expression by cocaine. Sci Transl Med. 2011;3 :107ra109–107ra109.
  • Ross EJ, Graham DL, Money KM, Stanwood GD. Developmental consequences of fetal exposure to drugs: what we know and what we still must learn. Neuropsychopharmacology 2015;40:61–87.
  • Lydon DM, Wilson SJ, Child A, Geier CF. Adolescent brain maturation and smoking: what we know and where we’re headed. Neurosci Biobehav Rev 2014;45:323–342.
  • Behnke M, Smith VC. Committee on substance abuse committee on fetus and newborn, prenatal substance abuse: short- and long-term effects on the exposed fetus. Pediatrics 2013;131:e1009–e10024.
  • Slotkin TA. If nicotine is a developmental neurotoxicant in animal studies, dare we recommend nicotine replacement therapy in pregnant women and adolescents? Neurotoxicol Teratol 2008;30:1–19.
  • Shea AK, Steiner M. Cigarette smoking during pregnancy. Nicotine Tobacco Res 2008;10:267–278.
  • Buu A, Dabrowska A, Heinze JE, Hsieh H-F, Zimmerman MA. Gender differences in the developmental trajectories of multiple substance use and the effect of nicotine and marijuana use on heavy drinking in a high-risk sample. Addictive Behaviors 2015;50:6–12.
  • Broome MV, Hurley RA. Substance use disorders: do males and females have differential vulnerability? J Neuropsychiatry Clin Neurosci 2010;22:3:249–255.
  • Darville A, Hahn EJ. Hardcore smokers: what do we know? Addictive Behaviors 2014;39:1706–1712.
  • Fattore L, Melis M, Fadda P, Fratta W. Sex differences in addictive disorders. Front Neuroendocrinology 2014;35:272–284.
  • Bobzean SAM. DeNobrega AK, Perrotti LI. Sex differences in the neurobiology of drug addiction. Exp Neurol 2014;259:64–74.
  • Kuhn C. Emergence of sex differences in the development of substance use and abuse during adolescence. Pharmacol Ther 2015;153:55–78.
  • Kloos A, Weller R, Chan RA, Weller EB. Gender differences in adolescent substance abuse. Curr Psychiatry Rep 2009;11:120–126.
  • Marks MJ, Whiteaker P, Collins AC. Deletion of the alpha7, beta2, or beta4 nicotinic receptor subunit genes identifies highly expressed subtypes with relatively low affinity for [3H]epibatidine. Mol Pharmacol 2006;70:947–959.
  • Buccafusco JJ. Neuronal nicotinic receptor subtypes: defining therapeutic targets. Mol Interv 2004;4:285–295.
  • Rose JE. Multiple brain pathways and receptors underlying tobacco addiction. Biochem Pharmacol 2007;74:1263–1270.
  • Picciotto MR, Kenny PJ. Molecular mechanisms underlying behaviors related to nicotine addiction. Cold Spring Harb Perspect Med 2013;3:a012112–a012112.
  • Pontieri FE, Tanda G, Orzi F, Chiara GD. Effects of nicotine on the nucleus accumbens and similarity to those of addictive drugs. Nature 1996;382:255–257.
  • Di Chiara G. Role of dopamine in the behavioural actions of nicotine related to addiction. Eur. J Pharmacol 2000;393:295–314.
  • Schuster CR, Thompson T. Self administration of and behavioral dependence on drugs. Annu Rev Pharmacol 1969;9:483–502.
  • Griffiths RR, Bigelow GE, Henningfield JE. Similarities in animal and human drug-taking behavior. Adv Subst Abuse 1980;1:1–90.
  • Schuster CR, Johanson CE. Relationship between the discriminative stimulus properties and subjective effects of drugs. Psychopharmacol Ser 1988;4:161–175.
  • Preston KL, Bigelow GE. Subjective and discriminative effects of drugs. Behav Pharmacol 1991;2:293–313.
  • Solinas M, Panlilio LV, Justinova Z. Yasar S, Goldberg SR. Using drug-discrimination techniques to study the abuse-related effects of psychoactive drugs in rats. Nat Protoc 2006;1:1194–1206.
  • Goldberg SR. Stolerman IP Behavioral Analysis of Drug Dependence, 1986.
  • Olmstead MC. Animal models of drug addiction. New York: Humana Press; 2010.
  • Burling TA, Ziff DC. Tobacco smoking: a comparison between alcohol and drug abuse inpatients. Addictive Behav 1988;13:185–190.
  • Toneatto A, Sobell LC, Sobell MB, Kozlowski LT. Effect of cigarette smoking on alcohol treatment outcome. J Subst Abuse 1995;7:245–252.
  • DiFranza JR, Guerrera MP. Alcoholism and smoking. J Stud Alcohol 1990;51:130–135.
  • Potthoff AD, Ellison G, Nelson L. Ethanol intake increases during continuous administration of amphetamine and nicotine, but not several other drugs, Pharmacology. Biochem Behav 1983;18:489–493.
  • Blomqvist O, Ericson M, Johnson DH, Engel JA, Söderpalm B. Voluntary ethanol intake in the rat: effects of nicotinic acetylcholine receptor blockade or subchronic nicotine treatment. Eur J Pharmacol 1996;314:257–267.
  • Lê AD Corrigall WA, Watchus J. Involvement of Nicotinic Receptors in Alcohol Self‐Administration. Alcoholism: Clin Exp Pharm 2000;24: 155–163.
  • 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.
  • Lê AD, Wang A, Harding S, Juzytsch W, Shaham Y. Nicotine increases alcohol self-administration and reinstates alcohol seeking in rats. Psychopharmacology 2003;168:216–221.
  • 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. Addiction Biol 2011;16:440–449.
  • Smith BR Horan JT Gaskin S, Amit Z. Exposure to nicotine enhances acquisition of ethanol drinking by laboratory rats in a limited access paradigm. Psychopharmacology 1999;142: 408–412.
  • 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.
  • Hauser SR, Katner SN, Deehan GA, Ding Z-M, Toalston JE, Scott BJ, et al. Development of an oral operant nicotine/ethanol co-use model in alcohol-preferring (p) rats. Alcohol: Clin Exp Res 2012;36:1963–1972.
  • Lê AD, Lo S, Harding S, Juzytsch W, Marinelli PW. Coadministration of intravenous nicotine and oral alcohol in rats. Psychopharmacol 2010;208:475–486.
  • Lê AD, Funk D, Lo S, Coen K. Operant self-administration of alcohol and nicotine in a preclinical model of co-abuse. Psychopharmacology 2014;231:4019–4029.
  • Kozlowski LT, Skinner W, Kent C, Pope MA. Prospects for smoking treatment in individuals seeking treatment for alcohol and other drug problems. Addictive Behav 1989;14:273–278.
  • Stuyt EB. Recovery rates after treatment for alcohol/drug dependence: Tobacco users vs. non-tobacco users. Am J Addict 1997;6:169–167.
  • De Soto CB, O’Donnell WE, De Soto JL. Long‐term recovery in alcoholics. Alcoholism: Clin Exp Res 1989;13:693–697.
  • Karam-Hage M, Pomerleau CS, Pomerleau OF, Brower KJ. Unaided smoking cessation among smokers in treatment for alcohol dependence. Addictive Behav 2005;30:1247–1253.
  • Alén F, Gómez R, González-Cuevas G, Navarro M, López-Moreno JA. Nicotine causes opposite effects on alcohol intake: Evidence in an animal experimental model of abstinence and relapse from alcohol. Nicotine Tobacco Res 2009;11:1304–1311.
  • 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. Neuropsychopharmacol 2015;40:2327–2336.
  • Ford MM, McCracken AD, Davis NL, Ryabinin AE, Grant KA. Discrimination of ethanol-nicotine drug mixtures in mice: dual interactive mechanisms of overshadowing and potentiation. Psychopharmacology 2012;224:537–548.
  • Troisi JR, Dooley TF, Craig EM. The discriminative stimulus effects of a nicotine-ethanol compound in rats: Extinction with the parts differs from the whole. Behav Neurosci 2013;127:899–912.
  • Le Foll B, Goldberg SR. Ethanol does not affect discriminative-stimulus effects of nicotine in rats. Eur J Pharmacol 2005;519:96–102.
  • Bienkowski P, Kostowski W. Discrimination of ethanol in rats: effects of nicotine, diazepam, CGP 40116, and 1-(m-chlorophenyl)-biguanide, Pharmacology. Biochem Behav 1998;60:61–69.
  • 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.
  • Signs SA, Schechter MD. Nicotine-induced potentiation of ethanol discrimination, Pharmacology. Biochem Behav 1986;24:769–771.
  • Korkosz A, Taracha E, Plaznik A, Wrobel E, Kostowski W, Bienkowski P. Extended blockade of the discriminative stimulus effects of nicotine with low doses of ethanol. Eur J Pharmacol 2005;512:165–172.
  • Korkosz A, Zatorski P, Taracha E, Plaznik A, Kostowski W, Bienkowski P. Effects of ethanol on nicotine-induced conditioned place preference in C57BL/6J mice, Progress in Neuro-Psychopharmacol Biol Psychiatry 2006;30: 1283–1290.
  • Rinker JA, Busse GD, Roma PG, Chen SA, Barr CS, Riley AL. The effects of nicotine on ethanol-induced conditioned taste aversions in Long-Evans rats. Psychopharmacology 2008;197:409–419.
  • Biala G, Budzynska B, Staniak N. Effects of rimonabant on the reinstatement of nicotine-conditioned place preference by drug priming in rats. Behav Brain Res 2009;202:260–265.
  • Taslim N, Al-Rejaie S, Dar MS. Attenuation of ethanol-induced ataxia by α 4 β 2 nicotinic acetylcholine receptor subtype in mouse cerebellum: A functional interaction. Neuroscience 2008;157:204–213.
  • Al-Rejaie S, Dar MS. Behavioral interaction between nicotine and ethanol: possible modulation by mouse cerebellar glutamate. Alcohol: Clin Exp Res 2006;30:1223–1233.
  • Gubner NR, Cunningham CL. Nicotine enhances the locomotor stimulating but not the conditioned rewarding effect of ethanol in DBA/2J mice. Alcohol: Clin Exp Res 2015;39:64–72.
  • Gubner NR, Phillips TJ. Effects of nicotine on ethanol-induced locomotor sensitization: A model of neuroadaptation. Behav Brain Res 2015;288:26–32.
  • Saellstroem Baum S, Huebner A, Krimphove M, Morgenstern R, Badawy AAB, Spies CD. Nicotine stimulation on extracellular glutamate levels in the nucleus accumbens of ethanol-withdrawn rats in vivo. Alcohol: Clin Exp Res 2006;30:1414–1421.
  • 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 2014;231:3745–3755.
  • Chatterjee S, Bartlett SE. Neuronal nicotinic acetylcholine receptors as pharmacotherapeutic targets for the treatment of alcohol use disorders. CNS Neurol Disord Drug - Drug Targets 2010;9:60–76.
  • Wu J, Gao M, Taylor DH. Neuronal nicotinic acetylcholine receptors are important targets for alcohol reward and dependence. Acta Pharmacologica Sinica 2014;35:311–315.
  • Blomqvist O, Engel JA, Nissbrandt H, Söderpalm B. The mesolimbic dopamine-activating properties of ethanol are antagonized by mecamylamine. Eur J Pharmacol 1993;249:207–213.
  • 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 2009;203:99–108.
  • Söderpalm B, Ericson M, Olausson P, Blomqvist O, Engel JA. Nicotinic mechanisms involved in the dopamine activating and reinforcing properties of ethanol. Behav Brain Res 2000;113:85–96.
  • Farook JM, Lewis B, Gaddis JG, Littleton JM, Barron S. Effects of mecamylamine on alcohol consumption and preference in male C57BL/6J mice. Pharmacology 2009;83:379–384.
  • 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 2009;204:563–572.
  • Steensland P, Simms JA, Holgate J. Richards J.K, Bartlett SE Varenicline, an alpha4beta2 nicotinic acetylcholine receptor partial agonist, selectively decreases ethanol consumption and seeking. Proc Natl Acad Sci USA 2007;104: 12518–12523.
  • Erwin BL, Slaton RM. Varenicline in the treatment of alcohol use disorders. Ann Pharmacother 2014;48:1445–1455.
  • Nocente R, Vitali M, Balducci G, Enea D, Kranzler HR, Ceccanti M. Varenicline and neuronal nicotinic acetylcholine receptors: A new approach to the treatment of co-occurring alcohol and nicotine addiction? Am J Addict 2013;22:453–459.
  • Randall PA, Jaramillo AA, Frisbee S, Besheer J. The role of varenicline on alcohol-primed self-administration and seeking behavior in rats. Psychopharmacology 2015;232:2443–2454.
  • Feduccia AA, Simms JA, Mill D, Yi HY. Varenicline decreases ethanol intake and increases dopamine release via neuronal nicotinic acetylcholine receptors in the nucleus accumbens. Br J Pharmacol 2014;171:3420–3431.
  • Kaminski BJ, Weerts EM. The Effects of varenicline on alcohol seeking and self‐administration in baboons. Alcohol: Clin Exp Res 2013;38:376–383.
  • 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.
  • Ginsburg BC, Lamb RJ. Effects of varenicline on ethanol‐and food‐maintained responding in a concurrent access procedure. Alcohol: Clin Exp Res 2013;37:1228–1233.
  • Gubner NR, McKinnon CS. Effects of varenicline on ethanol‐induced conditioned place preference, locomotor stimulation, and sensitization. Alcohol: Clin Res 2014;38:3033–3042.
  • Leão RM, Cruz FC, Vendruscolo LF, de Guglielmo G, Logrip ML, Planeta CS, et al. Chronic nicotine activates stress/reward-related brain regions and facilitates the transition to compulsive alcohol drinking. J Neurosci 2015;35:6241–6253.
  • Truitt WA, Hauser SR, Deehan Jr GA, Toalston JE. 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 2015;232:639–649.
  • Ericson M, Molander A, Löf E, Engel JA, Söderpalm B. Ethanol elevates accumbal dopamine levels via indirect activation of ventral tegmental nicotinic acetylcholine receptors. Eur J Pharmacol 2003;467:85–93.
  • Sharma R, Sahota P, Thakkar MM. Nicotine administration in the cholinergic basal forebrain increases alcohol consumption in C57BL/6J mice. Alcohol: Clin Exp Res 2014;38:1315–1320.
  • 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.
  • Schlaepfer IR, Hoft NR, Ehringer MA. The genetic components of alcohol and nicotine co-addiction: from genes to behavior. Curr Drug Abuse Rev 2008;1:124–134.
  • Li T-K, Volkow ND, Baler RD, Egli M. The biological bases of nicotine and alcohol co-addiction. Biol Psychiatry 2007;61:1–3.
  • Gubner NR McKinnon CS Reed C, Phillips TJ. Accentuating effects of nicotine on ethanol response in mice with high genetic predisposition to ethanol-induced locomotor stimulation. Drug Alcohol Depend 2013;127: 108–114.
  • Budney AJ, Higgins ST, Hughes JR, Bickel WK. Nicotine and caffeine use in cocaine-dependent individuals. J Subst Abuse 1993;5:117–130.
  • Brecht M-L, O’Brien A, von Mayrhauser C, Anglin MD. Methamphetamine use behaviors and gender differences. Addictive Behav 2004;29:89–106.
  • Brecht M-L, Greenwell L, Anglin MD. Substance use pathways to methamphetamine use among treated users. Addictive Behav 2007;32:24–38.
  • Wiseman EJ, McMillan DE. Combined use of cocaine with alcohol or cigarettes. Am J Drug Alcohol Abuse 1996;22:577–587.
  • Roll JM, Higgins ST, Tidey J. Cocaine use can increase cigarette smoking: evidence from laboratory and naturalistic settings. Exp Clin Psychopharmacol 1997;5:263–268.
  • Wiseman EJ, McMillan DE. Rationale for cigarette smoking and for mentholation preference in cocaine- and nicotine-dependent outpatients. Compr Psychiatry 1998;39:358–363.
  • Horger BA, Giles MK, Schenk S. Preexposure to amphetamine and nicotine predisposes rats to self-administer a low dose of cocaine. Psychopharmacology 1992;107:271–276.
  • Bechtholt A, Mark G. Enhancement of cocaine-seeking behavior by repeated nicotine exposure in rats. Psychopharmacology 2002;162:78–185.
  • Cortright JJ, Sampedro GR, Neugebauer NM. Previous exposure to nicotine enhances the incentive motivational effects of amphetamine via nicotine-associated contextual stimuli. Neuropsychopharmacology 2012;37:2277–2284.
  • Freeman KB, Woolverton WL. Self-administration of cocaine and nicotine mixtures by rhesus monkeys. Psychopharmacology 2009;207:99–106.
  • 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.
  • Neugebauer NM, Harrod SB, Bardo MT. Nicotine elicits methamphetamine-seeking in rats previously administered nicotine. Drug Alcohol Depend 2010;106:72–78.
  • Rauhut AS, Neugebauer N, Dwoskin LP, Bardo MT. Effect of bupropion on nicotine self-administration in rats. Psychopharmacology 2003;169:1–9.
  • Schenk S, Partridge B. Cocaine-seeking produced by experimenter-administered drug injections: dose-effect relationships in rats. Psychopharmacology 1999;147:285–290.
  • Hiranita T, Nawata Y, Sakimura K, Yamamoto T. Methamphetamine-seeking behavior is due to inhibition of nicotinic cholinergic transmission by activation of cannabinoid CB1 receptors. Neuropharmacology 2008;55:1300–1306.
  • Hiranita T, Anggadiredja K, Fujisaki C, Watanabe S, Yamamoto T. Nicotine attenuates relapse to methamphetamine‐seeking behavior (craving) in rats. Ann. N.Y. Acad. Sci. 2004;1025:504–507.
  • 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.
  • Desai RI, Barber DJ, Terry P. Asymmetric generalization between the discriminative stimulus effects of nicotine and cocaine. Behav Pharmacol 1999;10:647–656.
  • Desai RI, Barber DJ, Terry P. Dopaminergic and cholinergic involvement in the discriminative stimulus effects of nicotine and cocaine in rats. Psychopharmacol 2003;167:335–343.
  • Gatch MB, Flores E, Forster MJ. Nicotine and methamphetamine share discriminative stimulus effects. Drug Alcohol Depend 2008;93:63–71.
  • Desai RI, Bergman J. Methamphetamine-like discriminative-stimulus effects of nicotinic agonists. J Pharmacol Exp Ther 2014;348:478–488.
  • Brewer III AJ, Mahoney III, Nerumalla CS, Newton TF, De La Garza II R. The influence of smoking cigarettes on the high and desire for cocaine among active cocaine users, Pharmacology. Biochem Behav 2013;106:132–136.
  • Mizoguchi H, Ibi D, Takase F, Nagai T, Kamei H, Toth E, et al. Nicotine ameliorates impairment of working memory in methamphetamine-treated rats. Behav Brain Res 2011;220:159–163.
  • Vieira-Brock PL, Mcfadden LM, Nielsen SM, Ellis JD, Walters ET, Stout KA, et al. Chronic nicotine exposure attenuates methamphetamine-induced dopaminergic deficits. J Pharmacol Exp Ther 2015;355:463–472.
  • Vieira-Brock PL, Mcfadden LM, Nielsen SM, Smith MD, Hanson GR, Fleckenstein AE. Nicotine administration attenuates methamphetamine-induced novel object recognition deficits. Int . Neuropsychopharm 2015;18:1–12.
  • Gould RW, Garg PK, Garg S, Nader MA. Effects of nicotinic acetylcholine receptor agonists on cognition in rhesus monkeys with a chronic cocaine self-administration history. Neuropharmacology 2013;64:479–488.
  • Ahmed SH, Koob GF. Long-lasting increase in the set point for cocaine self-administration after escalation in rats. Psychopharmacology 1999;146:303–312.
  • Hansen ST, Mark GP. The nicotinic acetylcholine receptor antagonist mecamylamine prevents escalation of cocaine self-administration in rats with extended daily access. Psychopharmacology 2007;194:53–61.
  • Adinoff B, Devous MD. Williams MJ Best SE Harris TS Minhajuddin A. et al. Altered neural cholinergic receptor systems in cocaine-addicted subjects. Neuropsychopharmacology 2010;35:1485–1499.
  • Vezina P, Lorrain DS, Arnold GM, Austin JD, Suto N. Sensitization of midbrain dopamine neuron reactivity promotes the pursuit of amphetamine. J Neurosci 2002;22:4654–4662.
  • Jutkiewicz EM, Nicolazzo DM, Kim MN, Gnegy ME. Nicotine and amphetamine acutely cross-potentiate their behavioral and neurochemical responses in female Holtzman rats. Psychopharmacology 2008;200:93–103.
  • Wooters TE, Neugebauer NM, Rush CR, Bardo MT. Methylphenidate enhances the abuse-related behavioral effects of nicotine in rats: intravenous self-administration, drug discrimination, and locomotor cross-sensitization. Neuropsychopharmacology 2007;33:1137–1148.
  • Desai RI, Terry P. Evidence of cross-tolerance between behavioural effects of nicotine and cocaine in mice. Psychopharmacology 2003;166:111–119.
  • Suemaru K, Gomita Y, Furuno K, Araki Y. Chronic nicotine treatment potentiates behavioral responses to dopaminergic drugs in rats, Pharmacology. Biochem Behav 1993;46:135–139.
  • Kandel ER, Kandel DB. A molecular basis for nicotine as a gateway drug. New England J Med 2014;371:932–943.
  • Di Chiara G, Imperato A. Drugs abused by humans preferentially increase synaptic dopamine concentrations in the mesolimbic system of freely moving rats. Proc Natl Acad Sci USA 1988;85:5274–5278.
  • Merlo Pich E. Common neural substrates for the addictive properties of nicotine and cocaine. Science 1997;275:83–86.
  • Sziraki I, Sershen H, Benuck M, Lipovac M, Hashim A, Cooper TB, et al. The effect of cotinine on nicotine- and cocaine-induced dopamine release in the nucleus accumbens. Neurochem Res 1999;24:1471–1478.
  • 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.
  • Sziraki I, Sershen H, Benuck M, Hashim AA. Lajtha, differences in receptor system participation between nicotine- and cocaine-induced dopamine overflow in nucleus accumbens. Ann New York Acad Sci 1999;877:800–802.
  • 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.
  • Tsukada H, Miyasato K, Kakiuchi T, Nishiyama S, Harada N, Domino EF. Comparative effects of methamphetamine and nicotine on the striatal [11C]raclopride binding in unanesthetized monkeys. Synapse 2002;45:207–212.
  • Kim SE, Han S-M. Nicotine- and methamphetamine-induced dopamine release evaluated with in-vivo binding of radiolabelled raclopride to dopamine D2 receptors: comparison with in-vivo microdialysis data. Int J Neuropsychopharm 2009;12:833.
  • Kohut SJ, Hiranita T, Hong S-K, Ebbs AL, Tronci V, Green J, et al. Preference for Distinct functional conformations of the dopamine transporter alters the relationship between subjective effects of cocaine and stimulation of mesolimbic dopamine. Biol Psychiatry 2014;76:802–809.
  • Desai RI, Bergman J. Drug discrimination in methamphetamine-trained rats: effects of cholinergic nicotinic compounds. J Pharmacol Exp Ther 2010;335:807–816.
  • Nahvi S, Richter K, Li X, Modali L, Arnsten J. Cigarette smoking and interest in quitting in methadone maintenance patients. Addictive Behav 2006;31:2127–2134.
  • Chisolm MS, Fitzsimons H, Leoutsakos J-MS, Acquavita SP, Heil SH, Wilson-Murphy M, et al. A comparison of cigarette smoking profiles in opioid-dependent pregnant patients receiving methadone or buprenorphine. Nicotine Tobacco Res 2013;15:1297–1304.
  • Zale EL, Dorfman ML, Hooten WM, Warner DO, Zvolensky MJ, Ditre JW. Tobacco smoking, nicotine dependence, and patterns of prescription opioid misuse: results from a nationally representative sample. Nicotine Tobacco Res 2015;17:1096–1103.
  • Chait LD, Griffiths RR. Effects of methadone on human cigarette smoking and subjective ratings. J Pharmacol Exp Ther 1984;229:636–640.
  • Wewers ME, Dhatt R, Tejwani GA. Naltrexone administration affects ad libitum smoking behavior. Psychopharmacology 1998;140:185–190.
  • Spiga R, Schmitz J, Day J. Effects of nicotine on methadone self-administration in humans. Drug Alcohol Depend 1998;50:157–165.
  • Frosch DL, Shoptaw S, Nahom, D. Associations between tobacco smoking and illicit drug use among methadone-maintained opiate-dependent individuals. Exp Clin Psychopharmacol 2000;8:97–103.
  • Clemmey P, Brooner R, Chutuape MA, Kidorf M, Stitzer, M. Smoking habits and attitudes in a methadone maintenance treatment population. Drug Alcohol Depend 1997;44:123–132.
  • Corrigall WA, Herling S, Coen KM. Evidence for opioid mechanisms in the behavioral effects of nicotine. Psychopharmacology 1988;96:29–35.
  • DeNoble VJ, Mele PC. Intravenous nicotine self-administration in rats: effects of mecamylamine, hexamethonium and naloxone. Psychopharmacology 2006;184:266–272.
  • Huston-Lyons D, Sarkar M, Kornetsky C. Nicotine and brain-stimulation reward: interactions with morphine, amphetamine and pimozide. Pharmacol, Biochem Behav 1993;46:453–457.
  • Zarrindast M-R, Faraji N, Rostami P, Sahraei H, Ghoshouni H. Cross-tolerance between morphine- and nicotine-induced conditioned place preference in mice. Pharmacol Biochem Behav 2003;74:363–369.
  • Vihavainen T, Relander TRA, Leiviskä R, Airavaara M, Tuominen RK, Ahtee L, et al. Chronic nicotine modifies the effects of morphine on extracellular striatal dopamine and ventral tegmental GABA. J Neurochem 2008;107:844–854.
  • Rezayof A, Nazari-Serenjeh F, Zarrindast M-R, Sepehri H, Delphi L. Morphine-induced place preference: involvement of cholinergic receptors of the ventral tegmental area. Eur J Pharmacol 2007;562:92–102.
  • Rezayof A, Zatali H, Haeri-Rohani A, Zarrindast M-R. Dorsal hippocampal muscarinic and nicotinic receptors are involved in mediating morphine reward. Behav Brain Res 2006;166:281–290.
  • Zarrindast M-R, Fattahi Z, Rostami P, Rezayof A. Role of the cholinergic system in the rat basolateral amygdala on morphine-induced conditioned place preference. Pharmacol, Biochem Behav 2005;82:1–10.
  • Biala G, Budzynska B. Reinstatement of nicotine-conditioned place preference by drug priming: effects of calcium channel antagonists. Eur J Pharmacol 2006;537:85–93.
  • Shams J, Sahraei H, Gholami A, Haeri-Rohani A, Alaf-Javadi M, Sepehri H, et al. Effects of ultra-low doses of nicotine on the expression of morphine-induced conditioned place preference in mice. Behav Pharmacol 2006;17:629–635.
  • Zarrindast M-R, Nouraei N, Khallilzadeh A, Askari E. Influence of acute and sub-chronic nicotine pretreatment on morphine state-dependent learning. Behav Brain Res 2006;173:268–273.
  • Stolerman IP. Discriminative stimulus effects of nicotine in rats trained under different schedules of reinforcement. Psychopharmacology 1989;97:131–138.
  • Romano C, Goldstein A, Jewell NP. Characterization of the receptor mediating the nicotine discriminative stimulus. Psychopharmacology 1981;74:310–315.
  • Overton DA. Test for a neurochemically specific mechanism mediating drug discriminations and for stimulus masking. Psychopharmacology 1983;81:340–344.
  • Zarrindast MR, Khoshayand MR, Shafaghi B. The development of cross-tolerance between morphine and nicotine in mice. Eur Neuropsychopharmacol 1999;9:227–233.
  • Haghparast A, Khani A, Naderi N, Alizadeh A-M, Motamedi F. Repeated administration of nicotine attenuates the development of morphine tolerance and dependence in mice. Pharmacol, Biochem Behav 2008;88:385–392.
  • Araki H, Kawakami K-Y, Jin C, Suemaru K, Kitamura Y, Nagata M, et al. Nicotine attenuates place aversion induced by naloxone in single-dose, morphine-treated rats. Psychopharmacology 2004;171:398–404.
  • Zarrindast MR, Barghi-Lashkari S, Shafizadeh M. The possible cross-tolerance between morphine- and nicotine-induced hypothermia in mice, Pharmacology. Biochem Behav 2001;68:283–289.
  • Neugebauer NM, Einstein EB, Lopez MB, McClure-Begley TD, Mineur YS, and Picciotto MR. Morphine dependence and withdrawal induced changes in cholinergic signaling, Pharmacology. Biochem Behav 2013;109:77–83.
  • Zarrindast MR, Farzin D. Nicotine attenuates naloxone-induced jumping behaviour in morphine-dependent mice. Eur. J. Pharmacol. 1996;298:1–6.
  • Malin DH, Lake JR, Newlin-Maultsby P. Rodent model of nicotine abstinence syndrome. Pharmacology 1992;43:779–784.
  • Ueno K, Kiguchi N, Kobayashi Y, Saika F. Possible involvement of endogenous opioid system located downstream of α7 nicotinic acetylcholine receptor in mice with physical dependence on nicotine. J Pharmacol Sci 2014;124:47–53.
  • Ise Y, Narita M, Nagase H, Suzuki T. Modulation of opioidergic system on mecamylamine-precipitated nicotine-withdrawal aversion in rats. Psychopharmacology 2000;151:49–54.
  • Malin DH, Lake JR, Payne MC, Short PE, Carter VA, Cunningham JS, et al. Nicotine alleviation of nicotine abstinence syndrome is naloxone-reversible. Pharmacol, Biochem Behav 1996;53:81–85.
  • Plesner K, Jensen HI, Højsted J. Smoking history, nicotine dependence and opioid use in patients with chronic non‐malignant pain. Acta Anaesthesiologica 2016;1–7.
  • Davenport KE, Houdi AA, Van Loon GR. Nicotine protects against μ-opioid receptor antagonism by β-funaltrexamine: evidence for nicotine-induced release of endogenous opioids in brain. Neurosci Lett 1990;113:40–46.
  • Drews E, Zimmer A. Modulation of alcohol and nicotine responses through the endogenous opioid system. Prog Neurobiol 2010;90:1–15.
  • Schmidt BL, Tambeli CH, Gear RW, Levine JD. Nicotine withdrawal hyperalgesia and opioid-mediated analgesia depend on nicotine receptors in nucleus accumbens. Neurosci 2001;106:129–136.
  • Zarrindast MR, Pazouki M, Nassiri-Rad S. Involvement of cholinergic and opioid receptor mechanisms in nicotine‐induced antinociception. Pharmacol Toxicol 1997;81:209–213.
  • Amos A, Wiltshire S, Bostock Y, Haw S, McNeill A. ‘You can‘t go without a fag… you need it for your hash’—a qualitative exploration of smoking, cannabis and young people. Addiction 2004;99:77–81.
  • Penetar DM, Kouri EM, Gross MM, McCarthy EM, Rhee CK, Peters EN, et al. Transdermal nicotine alters some of marihuana’s effects in male and female volunteers. Drug Alcohol Depend 2005;79:211–223.
  • Forget B, Hamon M, Thiébot MH. Cannabinoid CB1 receptors are involved in motivational effects of nicotine in rats. Psychopharmacology 2005;181:722–734.
  • Castañé A, Valjent E, Ledent C, Parmentier M, Maldonado R, Valverde O. Lack of CB1 cannabinoid receptors modifies nicotine behavioural responses, but not nicotine abstinence. Neuropharmacology 2002;43:857–867.
  • Panlilio LV, Zanettini C, Barnes C, Solinas M. Prior exposure to THC increases the addictive effects of nicotine in rats. Neuropsychopharmacology 2013;38:1198–1208.
  • Gamaleddin I, Zvonok A, Makriyannis A, Goldberg SR, Le Foll B. Effects of a selective cannabinoid CB2 agonist and antagonist on intravenous nicotine self administration and reinstatement of nicotine seeking. PLoS ONE 2012;7:e29900.
  • Cohen C, Perrault G, Voltz C, Steinberg R. SR141716, a central cannabinoid (CB1) receptor antagonist, blocks the motivational and dopamine-releasing effects of nicotine in rats. Behav Pharmacol 2002;13:451–463.
  • Zaniewska M, Mccreary AC, Przegaliński E, Filip M. Evaluation of the role of nicotinic acetylcholine receptor subtypes and cannabinoid system in the discriminative stimulus effects of nicotine in rats. Eur J Pharmacol 2006;540:96–106.
  • Gamaleddin I, Zvonok A, Makriyannis A, Goldberg SR, Le Foll B. Effects of a selective cannabinoid CB2 agonist and antagonist on intravenous nicotine self administration and reinstatement of nicotine seeking. PLoS ONE 2012;7:e29900.
  • Valjent E, Mitchell JM, Besson M-J, Caboche J, Maldonado R. Behavioural and biochemical evidence for interactions between Delta 9-tetrahydrocannabinol and nicotine. Br J Pharmacol 2002;135:564–578.
  • Balerio GN, Aso E, Berrendero Murtra P, Maldonado R. Delta9-tetrahydrocannabinol decreases somatic and motivational manifestations of nicotine withdrawal in mice. Eur J Neurosci 2004;20:2737–2748.
  • Solinas M, Scherma M, Tanda G, Wertheim CE, Fratta W, Goldberg SR. Nicotinic facilitation of delta9-tetrahydrocannabinol discrimination involves endogenous anandamide. J Pharmacol Exp Ther 2007;321:1127–1134.
  • Scherma M, Muntoni AL, Melis M, Fattore L. Interactions between the endocannabinoid and nicotinic cholinergic systems: preclinical evidence and therapeutic perspectives, Psychopharmacology 2016; in press.
  • Cheer JF, Wassum KM, Sombers LAM, Heien LAV, Ariansen JL, Aragona BJ, et al. Phasic dopamine release evoked by abused substances requires cannabinoid receptor activation. J Neurosci 2007;27:791–795.
  • Melis M, Pillolla G, Luchicchi AL, Muntoni A, Yasar S, Goldberg SR, et al. Endogenous fatty acid ethanolamides suppress nicotine-induced activation of mesolimbic dopamine neurons through nuclear receptors. J Neurosci 2008;28:13985–13994.
  • Cadet JL, Bisagno V. Neuropsychological consequences of chronic drug use: relevance to treatment approaches. Front. Psychiatry 2015;6:189.
  • Robbins TW. The acquisition of responding with conditioned reinforcement: effects of pipradrol, methylphenidate, d-amphetamine, and nomifensine. Psychopharmacology 1978;58:79–87.
  • Taylor JR, Robbins TW. Enhanced behavioural control by conditioned reinforcers following microinjections of d-amphetamine into the nucleus accumbens. Psychopharmacology 1984;84:405–412.
  • Donny EC, Chaudhri N, Caggiula AR, Evans-Martin FF, Booth S, Gharib MA, et al. Operant responding for a visual reinforcer in rats is enhanced by noncontingent nicotine: implications for nicotine self-administration and reinforcement. Psychopharmacology 2003;169:68–76.
  • Caggiula A, Donny E, Chaudhri N, Perkins K, Evansmartin F, Sved A. Importance of nonpharmacological factors in nicotine self-administration. Physiol Behav 2002;77:683–687.
  • Le Foll B, Wertheim C, Goldberg SR. High reinforcing efficacy of nicotine in non-human primates. PLoS ONE 2007;2:e230.
  • Goodwin AK, Hiranita T, Paule MG. The reinforcing effects of nicotine in humans and nonhuman primates: a review of intravenous self-administration evidence and future directions for research. Nicotine Tobacco Res 2015;1–14.
  • Panlilio LV, Goldberg SR. Self-administration of drugs in animals and humans as a model and an investigative tool. Addiction 2007;102:1863–1870.
  • Desai RI, Sullivan KA, Kohut SJ, Bergman J. Influence of experimental history on nicotine self-administration in squirrel monkeys. Psychopharmacology 2016;233:2253–2263.
  • Kohut SJ, Bergman J. Reinforcing effectiveness of nicotine in nonhuman primates: effects of nicotine dose and history of nicotine self-administration. Psychopharmacology 2016; in press.
  • Broadbear JH, Winger G, Cicero TJ, Woods JH. Effects of response contingent and noncontingent cocaine injection on hypothalamic-pituitary-adrenal activity in rhesus monkeys. J Pharmacol Exp Ther 1999;290:393–402.
  • Williams KL, Broadbear JH, Woods JH. Noncontingent and response-contingent intravenous ethanol attenuates the effect of naltrexone on hypothalamic-pituitary-adrenal activity in rhesus monkeys. Alcohol: Clin Exp Res 2004;28:566–571.
  • Rauhut A, Hawrylak M, Mardekian S. Bupropion differentially alters the aversive, locomotor and rewarding properties of nicotine in CD-1 mice. Pharmacol, Biochem Behav 2008;90:598–607.
  • Rezvani AH, Sexton HG, Johnson J. Effects of Caffeine on alcohol consumption and nicotine self‐administration in rats. Alcohol: Clin Exp Res 2013;37:1609–1617.
  • Manzardo AM, Stein L, Belluzzi JD. Rats prefer cocaine over nicotine in a two-lever self-administration choice test. Brain Res 2002;924:10–19.
  • Fowler CD, Kenny PJ. Nicotine aversion: Neurobiological mechanisms and relevance to tobacco dependence vulnerability. Neuropharmacol 2014;76:533–544.
  • 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.
  • Mello NK, Fivel PA, Kohut SJ. Effects of chronic buspirone treatment on nicotine and concurrent Nicotine + cocaine self-administration. Neuropsychopharmacology 2013;38:1264–1275.
  • Mello NK, Fivel PA, Kohut SJ, Bergman J. Effects of chronic buspirone treatment on cocaine self-administration. Neuropsychopharmacology 2012;38:455–467.
  • Mello NK, Fivel PA, Kohut SJ, Carroll FI. Effects of chronic varenicline treatment on nicotine, cocaine, and concurrent nicotine + cocaine self-administration. Neuropsychopharmacology 2013;39:1222–1231.
  • Funk DLO, 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 2016;296:157–162.
  • Mello N.K, Negus SS. Effects of d-Amphetamine and buprenorphine combinations on speedball (Cocaine + Heroin) self-administration by rhesus monkeys. Neuropsychopharmacology 2007;32:1985–1994.

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