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Cannabinoid-Nicotine Interactions

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Cannabinoid Modulation of Emotion, Memory, and Motivation

Abstract

Although nicotine and delta-9-tetrahydrocannabinol (THC), the main psychoactive ingredients in tobacco and cannabis, bind to different receptors in the brain, they have several features in common. Each of these drugs is typically self-administered by smoking, and this behavior is maintained by rewarding effects that are mediated by brain circuitry that at least partially overlaps between the drugs. Each tends to be used chronically, leading to dependence and addiction in many users. Perhaps most importantly, the nicotinic and cannabinergic systems appear to interact in such a way that modulating one system can enhance or counteract effects of the other system. Therefore, studying cannabinoid-nicotine interactions could potentially lead to new treatments for addiction. This chapter considers such interactions, focusing on recent preclinical work that suggests manipulating the cannabinoid system can counteract the addictive effects of nicotine that manipulating the nicotinic system can counteract the addictive effects of cannabis, and that prior or concurrent use of cannabis has the detrimental effect of increasing the addictive effects of nicotine. Interactive effects of these systems on anxiety and memory are also considered, although these have been studied less than addiction-related effects.

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References

  1. World Health Organization. Global health risks: mortality and burden of disease attributable to selected major risks. Geneva:World Health Organization; 2004.

    Google Scholar 

  2. U.S. Department of Health and Human Services. How Tobacco Smoke Causes Disease: The Biology and Behavioral Basis for Smoking-Attributable Disease: A Report of the Surgeon General. Atlanta (GA): U.S. Department of Health and Human Services, Centers for Disease Control and Prevention, National Center for Chronic Disease Prevention and Health Promotion, Office on Smoking and Health; 2010.

    Google Scholar 

  3. Abrams DB. Nicotine addiction: paradigms for research in the 21st century. Nicotine Tob Res. 1999;1(Suppl 2):S211–S5.

    Article  PubMed  Google Scholar 

  4. Stolerman IP, Jarvis MJ. The scientific case that nicotine is addictive. Psychopharmacology (Berl). 1995;117(1):2–10.

    Article  CAS  Google Scholar 

  5. Rose JE. Nicotine and nonnicotine factors in cigarette addiction. Psychopharmacology (Berl). 2006;184(3–4):274–85.

    Article  CAS  Google Scholar 

  6. DeNoble VJ, Mele PC. Intravenous nicotine self-administration in rats: effects of mecamylamine, hexamethonium and naloxone. Psychopharmacology (Berl). 2006;184(3–4):266–72.

    Article  CAS  Google Scholar 

  7. Goldberg SR, Henningfield JE. Reinforcing effects of nicotine in humans and experimental animals responding under intermittent schedules of i.v. drug injection. Pharmacol Biochem Behav. 1988;30(1):227–34.

    Article  CAS  PubMed  Google Scholar 

  8. Goldberg SR, Spealman RD, Goldberg DM. Persistent behavior at high rates maintained by intravenous self-administration of nicotine. Science. 1981;214(4520):573–5.

    Article  CAS  PubMed  Google Scholar 

  9. Le Foll B, Goldberg SR. Effects of nicotine in experimental animals and humans: an update on addictive properties. Handb Exp Pharmacol. 2009;(192):335–67. doi:10.1007/978-3-540-69248-5_12.

    Google Scholar 

  10. Chaudhri N, Caggiula AR, Donny EC, Palmatier MI, Liu X, Sved AF. Complex interactions between nicotine and nonpharmacological stimuli reveal multiple roles for nicotine in reinforcement. Psychopharmacology (Berl). 2006;184(3–4):353–66.

    Article  CAS  Google Scholar 

  11. Soria R, Stapleton JM, Gilson SF, Sampson-Cone A, Henningfield JE, London ED. Subjective and cardiovascular effects of intravenous nicotine in smokers and non-smokers. Psychopharmacology (Berl). 1996;128(3):221–6.

    Article  CAS  Google Scholar 

  12. De Biasi M, Salas R. Influence of neuronal nicotinic receptors over nicotine addiction and withdrawal. Exp Biol Med (Maywood). 2008;233(8):917–29.

    Article  CAS  Google Scholar 

  13. Benowitz NL. Drug therapy. Pharmacologic aspects of cigarette smoking and nicotine addiction. N Engl J Med. 1988;319(20):1318–30.

    Article  CAS  PubMed  Google Scholar 

  14. Hughes JR, Hatsukami DK, Pickens RW, Krahn D, Malin S, Luknic A. Effect of nicotine on the tobacco withdrawal syndrome. Psychopharmacology (Berl). 1984;83(1):82–7.

    Article  CAS  Google Scholar 

  15. Hughes JR. Tobacco withdrawal in self-quitters. J Consult Clin Psychol. 1992;60(5):689–97.

    Article  CAS  PubMed  Google Scholar 

  16. Hughes JR, Gust SW, Skoog K, Keenan RM, Fenwick JW. Symptoms of tobacco withdrawal. A replication and extension. Arch Gen Psychiatry. 1991;48(1):52–9.

    Article  CAS  PubMed  Google Scholar 

  17. Hukkanen J, Jacob P III, Benowitz NL. Metabolism and disposition kinetics of nicotine. Pharmacol Rev. 2005;57(1):79–115.

    Article  CAS  PubMed  Google Scholar 

  18. Albuquerque EX, Pereira EF, Alkondon M, Rogers SW. Mammalian nicotinic acetylcholine receptors: from structure to function. Physiol Rev. 2009;89(1):73–120.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  19. Picciotto MR, Zoli M, Rimondini R, Lena C, Marubio LM, Pich EM, et al. Acetylcholine receptors containing the beta2 subunit are involved in the reinforcing properties of nicotine. Nature. 1998;391(6663):173–7.

    Article  CAS  PubMed  Google Scholar 

  20. Dani JA, Bertrand D. Nicotinic acetylcholine receptors and nicotinic cholinergic mechanisms of the central nervous system. Annu Rev Pharmacol Toxicol. 2007;47:699–729.

    Article  CAS  PubMed  Google Scholar 

  21. Buisson B, Bertrand D. Chronic exposure to nicotine upregulates the human (alpha)4(beta)2 nicotinic acetylcholine receptor function. J Neurosci. 2001;21(6):1819–29.

    CAS  PubMed  Google Scholar 

  22. Bousman CA, Rivard C, Haese JD, Ambrosone C, Hyland A. Alpha-5 and -3 nicotinic receptor gene variants predict nicotine dependence but not cessation: findings from the COMMIT cohort. Am J Med Genet B Neuropsychiatr Genet. 2012;159B(2):227–35.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  23. Exley R, Maubourguet N, David V, Eddine R, Evrard A, Pons S, et al. Distinct contributions of nicotinic acetylcholine receptor subunit alpha4 and subunit alpha6 to the reinforcing effects of nicotine. Proc Natl Acad Sci U S A. 2011;108(18):7577–82.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  24. Fowler CD, Tuesta L, Kenny PJ. Role of alpha5* nicotinic acetylcholine receptors in the effects of acute and chronic nicotine treatment on brain reward function in mice. Psychopharmacology (Berl). 2013;229(3):503–13.

    Article  CAS  Google Scholar 

  25. Gold AB, Lerman C. Pharmacogenetics of smoking cessation: role of nicotine target and metabolism genes. Hum Genet. 2012;131(6):857–76.

    Article  CAS  Google Scholar 

  26. Gotti C, Guiducci S, Tedesco V, Corbioli S, Zanetti L, Moretti M, et al. Nicotinic acetylcholine receptors in the mesolimbic pathway: primary role of ventral tegmental area alpha6beta2* receptors in mediating systemic nicotine effects on dopamine release, locomotion, and reinforcement. J Neurosci. 2010;30(15):5311–25.

    Article  CAS  PubMed  Google Scholar 

  27. Jackson KJ, McIntosh JM, Brunzell DH, Sanjakdar SS, Damaj MI. The role of alpha6-containing nicotinic acetylcholine receptors in nicotine reward and withdrawal. J Pharmacol Exp Ther. 2009;331(2):547–54.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  28. Liu L, Zhao-Shea R, McIntosh JM, Gardner PD, Tapper AR. Nicotine persistently activates ventral tegmental area dopaminergic neurons via nicotinic acetylcholine receptors containing alpha4 and alpha6 subunits. Mol Pharmacol. 2012;81(4):541–8.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  29. Morel C, Fattore L, Pons S, Hay YA, Marti F, Lambolez B, et al. Nicotine consumption is regulated by a human polymorphism in dopamine neurons. Mol Psychiatry. 2013. doi:10.1038/mp.2013.158.

    Google Scholar 

  30. Picciotto MR, Kenny PJ. Molecular mechanisms underlying behaviors related to nicotine addiction. Cold Spring Harb Perspect Med. 2013;3(1):a012112.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  31. Yang K, Buhlman L, Khan GM, Nichols RA, Jin G, McIntosh JM, et al. Functional nicotinic acetylcholine receptors containing alpha6 subunits are on GABAergic neuronal boutons adherent to ventral tegmental area dopamine neurons. J Neurosci. 2011;31(7):2537–48.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  32. Balfour DJ. Neural mechanisms underlying nicotine dependence. Addiction. 1994;89(11):1419–23.

    Article  CAS  PubMed  Google Scholar 

  33. Dani JA, Heinemann S. Molecular and cellular aspects of nicotine abuse. Neuron. 1996;16(5):905–8.

    Article  CAS  PubMed  Google Scholar 

  34. 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 U S A. 1988;85(14):5274–8.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  35. Mereu G, Yoon KW, Boi V, Gessa GL, Naes L, Westfall TC. Preferential stimulation of ventral tegmental area dopaminergic neurons by nicotine. Eur J Pharmacol. 1987;141(3):395–9.

    Article  CAS  PubMed  Google Scholar 

  36. Pidoplichko VI, DeBiasi M, Williams JT, Dani JA. Nicotine activates and desensitizes midbrain dopamine neurons. Nature. 1997;390(6658):401–4.

    Article  CAS  PubMed  Google Scholar 

  37. Albuquerque EX, Pereira EF, Alkondon M, Schrattenholz A, Maelicke A. Nicotinic acetylcholine receptors on hippocampal neurons: distribution on the neuronal surface and modulation of receptor activity. J Recept Signal Transduct Res. 1997;17(1–3):243–66.

    Article  CAS  PubMed  Google Scholar 

  38. Alkondon M, Pereira EF, Barbosa CT, Albuquerque EX. Neuronal nicotinic acetylcholine receptor activation modulates gamma-aminobutyric acid release from CA1 neurons of rat hippocampal slices. J Pharmacol Exp Ther. 1997;283(3):1396–411.

    CAS  PubMed  Google Scholar 

  39. Gray R, Rajan AS, Radcliffe KA, Yakehiro M, Dani JA. Hippocampal synaptic transmission enhanced by low concentrations of nicotine. Nature. 1996;383(6602):713–6.

    Article  CAS  PubMed  Google Scholar 

  40. Guo JZ, Tredway TL, Chiappinelli VA. Glutamate and GABA release are enhanced by different subtypes of presynaptic nicotinic receptors in the lateral geniculate nucleus. J Neurosci. 1998;18(6):1963–9.

    CAS  PubMed  Google Scholar 

  41. Jones IW, Wonnacott S. Precise localization of alpha7 nicotinic acetylcholine receptors on glutamatergic axon terminals in the rat ventral tegmental area. J Neurosci. 2004;24(50):11244–52.

    Article  CAS  PubMed  Google Scholar 

  42. Li X, Rainnie DG, McCarley RW, Greene RW. Presynaptic nicotinic receptors facilitate monoaminergic transmission. J Neurosci. 1998;18(5):1904–12.

    CAS  PubMed  Google Scholar 

  43. Mansvelder HD, McGehee DS. Long-term potentiation of excitatory inputs to brain reward areas by nicotine. Neuron. 2000;27(2):349–57.

    Article  CAS  PubMed  Google Scholar 

  44. McGehee DS, Heath MJ, Gelber S, Devay P, Role LW. Nicotine enhancement of fast excitatory synaptic transmission in CNS by presynaptic receptors. Science. 1995;269(5231):1692–6.

    Article  CAS  PubMed  Google Scholar 

  45. McGehee DS, Role LW. Physiological diversity of nicotinic acetylcholine receptors expressed by vertebrate neurons. Annu Rev Physiol. 1995;57:521–46.

    Article  CAS  PubMed  Google Scholar 

  46. Radcliffe KA, Dani JA. Nicotinic stimulation produces multiple forms of increased glutamatergic synaptic transmission. J Neurosci. 1998;18(18):7075–83.

    CAS  PubMed  Google Scholar 

  47. Radcliffe KA, Fisher JL, Gray R, Dani JA. Nicotinic modulation of glutamate and GABA synaptic transmission of hippocampal neurons. Ann N Y Acad Sci. 1999;868:591–610.

    Article  CAS  PubMed  Google Scholar 

  48. Role LW, Berg DK. Nicotinic receptors in the development and modulation of CNS synapses. Neuron. 1996;16(6):1077–85.

    Article  CAS  PubMed  Google Scholar 

  49. Wonnacott S. Presynaptic nicotinic ACh receptors. Trends Neurosci. 1997;20(2):92–8.

    Article  CAS  PubMed  Google Scholar 

  50. Yin R, French ED. A comparison of the effects of nicotine on dopamine and non-dopamine neurons in the rat ventral tegmental area: an in vitro electrophysiological study. Brain Res Bull. 2000;51(6):507–14.

    Article  CAS  PubMed  Google Scholar 

  51. Mansvelder HD, Keath JR, McGehee DS. Synaptic mechanisms underlie nicotine-induced excitability of brain reward areas. Neuron. 2002;33(6):905–19.

    Article  CAS  PubMed  Google Scholar 

  52. Mansvelder HD, McGehee DS. Cellular and synaptic mechanisms of nicotine addiction. J Neurobiol. 2002;53(4):606–17.

    Article  CAS  PubMed  Google Scholar 

  53. Benwell ME, Balfour DJ. Effects of nicotine administration and its withdrawal on plasma corticosterone and brain 5-hydroxyindoles. Psychopharmacology (Berl). 1979;63(1):7–11.

    Article  CAS  Google Scholar 

  54. Schwartz RD, Lehmann J, Kellar KJ. Presynaptic nicotinic cholinergic receptors labeled by [3H]acetylcholine on catecholamine and serotonin axons in brain. J Neurochem. 1984;42(5):1495–8.

    Article  CAS  PubMed  Google Scholar 

  55. Cesselin F. Opioid and anti-opioid peptides. Fundam Clin Pharmacol. 1995;9(5):409–33.

    Article  CAS  PubMed  Google Scholar 

  56. Kesner RP, Hopkins RO. Mnemonic functions of the hippocampus: a comparison between animals and humans. Biol Psychol. 2006;73(1):3–18.

    Article  PubMed  Google Scholar 

  57. Martin BR, Aceto MD. Nicotine binding sites and their localization in the central nervous system. Neurosci Biobehav Rev. 1981;5(4):473–8.

    Article  CAS  PubMed  Google Scholar 

  58. Herkenham M, Lynn AB, Johnson MR, Melvin LS, de Costa BR, Rice KC. Characterization and localization of cannabinoid receptors in rat brain: a quantitative in vitro autoradiographic study. J Neurosci. 1991;11(2):563–83.

    CAS  PubMed  Google Scholar 

  59. Gotti C, Zoli M, Clementi F. Brain nicotinic acetylcholine receptors: native subtypes and their relevance. Trends Pharmacol Sci. 2006;27(9):482–91.

    Article  CAS  PubMed  Google Scholar 

  60. Moldrich G, Wenger T. Localization of the CB1 cannabinoid receptor in the rat brain. An immunohistochemical study. Peptides. 2000;21(11):1735–42.

    Article  CAS  PubMed  Google Scholar 

  61. Levey AI, Kitt CA, Simonds WF, Price DL, Brann MR. Identification and localization of muscarinic acetylcholine receptor proteins in brain with subtype-specific antibodies. J Neurosci. 1991;11(10):3218–26.

    CAS  PubMed  Google Scholar 

  62. Degroot A, Kofalvi A, Wade MR, Davis RJ, Rodrigues RJ, Rebola N, et al. CB1 receptor antagonism increases hippocampal acetylcholine release: site and mechanism of action. Mol Pharmacol. 2006;70(4):1236–45.

    Article  CAS  PubMed  Google Scholar 

  63. Gerdeman G, Lovinger DM. CB1 cannabinoid receptor inhibits synaptic release of glutamate in rat dorsolateral striatum. J Neurophysiol. 2001;85(1):468–71.

    CAS  PubMed  Google Scholar 

  64. Kano M, Ohno-Shosaku T, Hashimotodani Y, Uchigashima M, Watanabe M. Endocannabinoid-mediated control of synaptic transmission. Physiol Rev. 2009;89(1):309–80.

    Article  CAS  PubMed  Google Scholar 

  65. Melis M, Pistis M, Perra S, Muntoni AL, Pillolla G, Gessa GL. Endocannabinoids mediate presynaptic inhibition of glutamatergic transmission in rat ventral tegmental area dopamine neurons through activation of CB1 receptors. J Neurosci. 2004;24(1):53–62.

    Article  CAS  PubMed  Google Scholar 

  66. Marsicano G, Lutz B. Expression of the cannabinoid receptor CB1 in distinct neuronal subpopulations in the adult mouse forebrain. Eur J Neurosci. 1999;11(12):4213–25.

    Article  CAS  PubMed  Google Scholar 

  67. Endo T, Yanagawa Y, Obata K, Isa T. Nicotinic acetylcholine receptor subtypes involved in facilitation of GABAergic inhibition in mouse superficial superior colliculus. J Neurophysiol. 2005;94(6):3893–902.

    Article  CAS  PubMed  Google Scholar 

  68. Pidoplichko VI, Prager EM, Aroniadou-Anderjaska V, Braga MF. alpha7-Containing nicotinic acetylcholine receptors on interneurons of the basolateral amygdala and their role in the regulation of the network excitability. J Neurophysiol. 2013;110(10):2358–69.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  69. Szabo B, Siemes S, Wallmichrath I. Inhibition of GABAergic neurotransmission in the ventral tegmental area by cannabinoids. Eur J Neurosci. 2002;15(12):2057–61.

    Article  PubMed  Google Scholar 

  70. Gong JP, Onaivi ES, Ishiguro H, Liu QR, Tagliaferro PA, Brusco A, et al. Cannabinoid CB2 receptors: immunohistochemical localization in rat brain. Brain Res. 2006;1071(1):10–23.

    Article  CAS  PubMed  Google Scholar 

  71. Onaivi ES, Ishiguro H, Gong JP, Patel S, Perchuk A, Meozzi PA, et al. Discovery of the presence and functional expression of cannabinoid CB2 receptors in brain. Ann N Y Acad Sci. 2006;1074:514–36.

    Article  CAS  PubMed  Google Scholar 

  72. Navarrete F, Rodriguez-Arias M, Martin-Garcia E, Navarro D, Garcia-Gutierrez MS, Aguilar MA, et al. Role of CB2 cannabinoid receptors in the rewarding, reinforcing, and physical effects of nicotine. Neuropsychopharmacology. 2013;38(12):2515–24.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  73. Valjent E, Mitchell JM, Besson MJ, Caboche J, Maldonado R. Behavioural and biochemical evidence for interactions between Delta9-tetrahydrocannabinol and nicotine. Br J Pharmacol. 2002;135(2):564–78.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  74. Scherma M, Justinova Z, Zanettini C, Panlilio LV, Mascia P, Fadda P, et al. The anandamide transport inhibitor AM404 reduces the rewarding effects of nicotine and nicotine-induced dopamine elevations in the nucleus accumbens shell in rats. Br J Pharmacol. 2012;165(8):2539–48.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  75. 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(1):77–81.

    Article  PubMed  Google Scholar 

  76. Lee JP, Battle RS, Lipton R, Soller B. ‘Smoking’: use of cigarettes, cigars and blunts among Southeast Asian American youth and young adults. Health Educ Res. 2010;25(1):83–96.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  77. Gonzalez S, Cascio MG, Fernandez-Ruiz J, Fezza F, Di Marzo V, Ramos JA. Changes in endocannabinoid contents in the brain of rats chronically exposed to nicotine, ethanol or cocaine. Brain Res. 2002;954(1):73–81.

    Article  CAS  PubMed  Google Scholar 

  78. Di Marzo V, Berrendero F, Bisogno T, Gonzalez S, Cavaliere P, Romero J, et al. Enhancement of anandamide formation in the limbic forebrain and reduction of endocannabinoid contents in the striatum of delta9-tetrahydrocannabinol-tolerant rats. J Neurochem. 2000;74(4):1627–35.

    Article  CAS  PubMed  Google Scholar 

  79. Panlilio LV, Goldberg SR. Self-administration of drugs in animals and humans as a model and an investigative tool. Addiction. 2007;102(12):1863–70.

    Article  PubMed  PubMed Central  Google Scholar 

  80. Castane 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(5):857–67.

    Article  CAS  PubMed  Google Scholar 

  81. Le Foll B, Goldberg SR. Rimonabant, a CB1 antagonist, blocks nicotine-conditioned place preferences. Neuroreport. 2004;15(13):2139–43.

    Article  CAS  PubMed  Google Scholar 

  82. Forget B, Hamon M, Thiebot MH. Cannabinoid CB1 receptors are involved in motivational effects of nicotine in rats. Psychopharmacology (Berl). 2005;181(4):722–34.

    Article  CAS  Google Scholar 

  83. Forget B, Barthelemy S, Saurini F, Hamon M, Thiebot MH. Differential involvement of the endocannabinoid system in short- and long-term expression of incentive learning supported by nicotine in rats. Psychopharmacology (Berl). 2006;189(1):59–69.

    Article  CAS  Google Scholar 

  84. 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(2):260–5.

    Article  CAS  PubMed  Google Scholar 

  85. Fang Q, Li FQ, Li YQ, Xue YX, He YY, Liu JF, et al. Cannabinoid CB1 receptor antagonist rimonabant disrupts nicotine reward-associated memory in rats. Pharmacol Biochem Behav. 2011;99(4):738–42.

    Article  CAS  PubMed  Google Scholar 

  86. Cossu G, Ledent C, Fattore L, Imperato A, Bohme GA, Parmentier M, et al. Cannabinoid CB1 receptor knockout mice fail to self-administer morphine but not other drugs of abuse. Behav Brain Res. 2001;118(1):61–5.

    Article  CAS  PubMed  Google Scholar 

  87. Cohen C, Perrault G, Voltz C, Steinberg R, Soubrie P. SR141716, a central cannabinoid (CB(1)) receptor antagonist, blocks the motivational and dopamine-releasing effects of nicotine in rats. Behav Pharmacol. 2002;13(5–6):451–63.

    Article  CAS  PubMed  Google Scholar 

  88. Shoaib M. The cannabinoid antagonist AM251 attenuates nicotine self-administration and nicotine-seeking behaviour in rats. Neuropharmacology. 2008;54(2):438–44.

    Article  CAS  PubMed  Google Scholar 

  89. Wing VC, Shoaib M. Second-order schedules of nicotine reinforcement in rats: effect of AM251. Addict Biol. 2010;15(4):393–402.

    Article  CAS  PubMed  Google Scholar 

  90. Gamaleddin I, Wertheim C, Zhu AZ, Coen KM, Vemuri K, Makryannis A, et al. Cannabinoid receptor stimulation increases motivation for nicotine and nicotine seeking. Addict Biol. 2012;17(1):47–61.

    Article  CAS  PubMed  Google Scholar 

  91. Simonnet A, Cador M, Caille S. Nicotine reinforcement is reduced by cannabinoid CB1 receptor blockade in the ventral tegmental area. Addict Biol. 2013;18(6):930–6.

    Article  CAS  PubMed  Google Scholar 

  92. Exley R, Clements MA, Hartung H, McIntosh JM, Cragg SJ. Alpha6-containing nicotinic acetylcholine receptors dominate the nicotine control of dopamine neurotransmission in nucleus accumbens. Neuropsychopharmacology. 2008;33(9):2158–66.

    Article  CAS  PubMed  Google Scholar 

  93. Lupica CR, Riegel AC. Endocannabinoid release from midbrain dopamine neurons: a potential substrate for cannabinoid receptor antagonist treatment of addiction. Neuropharmacology. 2005;48(8):1105–16.

    Article  CAS  PubMed  Google Scholar 

  94. Riegel AC, Lupica CR. Independent presynaptic and postsynaptic mechanisms regulate endocannabinoid signaling at multiple synapses in the ventral tegmental area. J Neurosci. 2004;24(49):11070–8.

    Article  CAS  PubMed  Google Scholar 

  95. Melis M, Pillolla G, Luchicchi A, Muntoni AL, 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(51):13985–94.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  96. Caggiula AR, Donny EC, White AR, Chaudhri N, Booth S, Gharib MA, et al. Environmental stimuli promote the acquisition of nicotine self-administration in rats. Psychopharmacology (Berl). 2002;163(2):230–7.

    Article  CAS  Google Scholar 

  97. Caggiula AR, Donny EC, Chaudhri N, Perkins KA, Evans-Martin FF, Sved AF. Importance of nonpharmacological factors in nicotine self-administration. Physiol Behav. 2002;77(4–5):683–7.

    Article  CAS  PubMed  Google Scholar 

  98. 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 (Berl). 2003;169(1):68–76.

    Article  CAS  Google Scholar 

  99. Cohen C, Perrault G, Griebel G, Soubrie P. Nicotine-associated cues maintain nicotine-seeking behavior in rats several weeks after nicotine withdrawal: reversal by the cannabinoid (CB1) receptor antagonist, rimonabant (SR141716). Neuropsychopharmacology. 2005;30(1):145–55.

    Article  CAS  PubMed  Google Scholar 

  100. Kodas E, Cohen C, Louis C, Griebel G. Cortico-limbic circuitry for conditioned nicotine-seeking behavior in rats involves endocannabinoid signaling. Psychopharmacology (Berl). 2007;194(2):161–71.

    Article  CAS  Google Scholar 

  101. De Vries TJ, Schoffelmeer AN. Cannabinoid CB1 receptors control conditioned drug seeking. Trends Pharmacol Sci. 2005;26(8):420–6.

    Article  CAS  PubMed  Google Scholar 

  102. Diergaarde L, de Vries W, Raaso H, Schoffelmeer AN, De Vries TJ. Contextual renewal of nicotine seeking in rats and its suppression by the cannabinoid-1 receptor antagonist Rimonabant (SR141716A). Neuropharmacology. 2008;55(5):712–6.

    Article  CAS  PubMed  Google Scholar 

  103. Wing VC, Shoaib M. A second-order schedule of food reinforcement in rats to examine the role of CB1 receptors in the reinforcement-enhancing effects of nicotine. Addict Biol. 2010;15(4):380–92.

    Article  CAS  PubMed  Google Scholar 

  104. Zaniewska M, McCreary AC, Przegalinski 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(1–3):96–106.

    Article  CAS  PubMed  Google Scholar 

  105. Murray JE, Wells NR, Lyford GD, Bevins RA. Investigation of endocannabinoid modulation of conditioned responding evoked by a nicotine CS and the Pavlovian stimulus effects of CP 55,940 in adult male rats. Psychopharmacology (Berl). 2009;205(4):655–65.

    Article  CAS  Google Scholar 

  106. Cahill K, Ussher M. Cannabinoid type 1 receptor antagonists (rimonabant) for smoking cessation. Cochrane Database Syst Rev. 2007(3):CD005353.

    Google Scholar 

  107. Salamone JD, McLaughlin PJ, Sink K, Makriyannis A, Parker LA. Cannabinoid CB1 receptor inverse agonists and neutral antagonists: effects on food intake, food-reinforced behavior and food aversions. Physiol Behav. 2007;91(4):383–8.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  108. Sink KS, McLaughlin PJ, Wood JA, Brown C, Fan P, Vemuri VK, et al. The novel cannabinoid CB1 receptor neutral antagonist AM4113 suppresses food intake and food-reinforced behavior but does not induce signs of nausea in rats. Neuropsychopharmacology. 2008;33(4):946–55.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  109. Morgan CJ, Das RK, Joye A, Curran HV, Kamboj SK. Cannabidiol reduces cigarette consumption in tobacco smokers: preliminary findings. Addict Behav. 2013;38(9):2433–6.

    Article  PubMed  Google Scholar 

  110. Leweke FM, Piomelli D, Pahlisch F, Muhl D, Gerth CW, Hoyer C, et al. Cannabidiol enhances anandamide signaling and alleviates psychotic symptoms of schizophrenia. Transl Psychiatry. 2012;2:e94.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  111. Mahgoub M, Keun-Hang SY, Sydorenko V, Ashoor A, Kabbani N, Al KL, et al. Effects of cannabidiol on the function of alpha7-nicotinic acetylcholine receptors. Eur J Pharmacol. 2013;720(1–3):310–9.

    Article  CAS  PubMed  Google Scholar 

  112. Ishiguro H, Iwasaki S, Teasenfitz L, Higuchi S, Horiuchi Y, Saito T, et al. Involvement of cannabinoid CB2 receptor in alcohol preference in mice and alcoholism in humans. Pharmacogenomics J. 2007;7(6):380–5.

    Article  CAS  PubMed  Google Scholar 

  113. Ishiguro H, Carpio O, Horiuchi Y, Shu A, Higuchi S, Schanz N, et al. A nonsynonymous polymorphism in cannabinoid CB2 receptor gene is associated with eating disorders in humans and food intake is modified in mice by its ligands. Synapse. 2010;64(1):92–6.

    Article  CAS  PubMed  Google Scholar 

  114. Onaivi ES, Ishiguro H, Gong JP, Patel S, Meozzi PA, Myers L, et al. Brain neuronal CB2 cannabinoid receptors in drug abuse and depression: from mice to human subjects. PLoS One. 2008;3(2):e1640.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  115. Xi ZX, Peng XQ, Li X, Song R, Zhang HY, Liu QR, et al. Brain cannabinoid CB(2) receptors modulate cocaine’s actions in mice. Nat Neurosci. 2011;14(9):1160–6.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  116. Adamczyk P, Miszkiel J, McCreary AC, Filip M, Papp M, Przegalinski E. The effects of cannabinoid CB1, CB2 and vanilloid TRPV1 receptor antagonists on cocaine addictive behavior in rats. Brain Res. 2012;1444:45–54.

    Article  CAS  PubMed  Google Scholar 

  117. Aracil-Fernandez A, Trigo JM, Garcia-Gutierrez MS, Ortega-Alvaro A, Ternianov A, Navarro D, et al. Decreased cocaine motor sensitization and self-administration in mice overexpressing cannabinoid CB(2) receptors. Neuropsychopharmacology. 2012;37(7):1749–63.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  118. 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(1):e29900.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  119. Ignatowska-Jankowska BM, Muldoon PP, Lichtman AH, Damaj MI. The cannabinoid CB2 receptor is necessary for nicotine-conditioned place preference, but not other behavioral effects of nicotine in mice. Psychopharmacology (Berl). 2013;229(4):591–601.

    Article  CAS  Google Scholar 

  120. Pons S, Fattore L, Cossu G, Tolu S, Porcu E, McIntosh JM, et al. Crucial role of alpha4 and alpha6 nicotinic acetylcholine receptor subunits from ventral tegmental area in systemic nicotine self-administration. J Neurosci. 2008;28(47):12318–27.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  121. Glick SD, Sell EM, McCallum SE, Maisonneuve IM. Brain regions mediating alpha3beta4 nicotinic antagonist effects of 18-MC on nicotine self-administration. Eur J Pharmacol. 2011;669(1–3):71–5.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  122. Hall W, Degenhardt L. Adverse health effects of non-medical cannabis use. Lancet. 2009;374(9698):1383–91.

    Article  CAS  PubMed  Google Scholar 

  123. O’Sullivan SE. Cannabinoids go nuclear: evidence for activation of peroxisome proliferator-activated receptors. Br J Pharmacol. 2007;152(5):576–82.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  124. Pistis M, Melis M. From surface to nuclear receptors: the endocannabinoid family extends its assets. Curr Med Chem. 2010;17(14):1450–67.

    Article  CAS  PubMed  Google Scholar 

  125. Merritt LL, Martin BR, Walters C, Lichtman AH, Damaj MI. The endogenous cannabinoid system modulates nicotine reward and dependence. J Pharmacol Exp Ther. 2008;326(2):483–92.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  126. Muldoon PP, Lichtman AH, Parsons LH, Damaj MI. The role of fatty acid amide hydrolase inhibition in nicotine reward and dependence. Life Sci. 2013;92(8–9):458–62.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  127. Scherma M, Panlilio LV, Fadda P, Fattore L, Gamaleddin I, Le Foll B, et al. Inhibition of anandamide hydrolysis by cyclohexyl carbamic acid 3’-carbamoyl-3-yl ester (URB597) reverses abuse-related behavioral and neurochemical effects of nicotine in rats. J Pharmacol Exp Ther. 2008;327(2):482–90.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  128. Forget B, Coen KM, Le Foll B. Inhibition of fatty acid amide hydrolase reduces reinstatement of nicotine seeking but not break point for nicotine self-administration-comparison with CB(1) receptor blockade. Psychopharmacology (Berl). 2009;205(4):613–24.

    Article  CAS  Google Scholar 

  129. Luchicchi A, Lecca S, Carta S, Pillolla G, Muntoni AL, Yasar S, et al. Effects of fatty acid amide hydrolase inhibition on neuronal responses to nicotine, cocaine and morphine in the nucleus accumbens shell and ventral tegmental area: involvement of PPAR-alpha nuclear receptors. Addict Biol. 2010;15(3):277–88.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  130. Moreno S, Farioli-Vecchioli S, Ceru MP. Immunolocalization of peroxisome proliferator-activated receptors and retinoid X receptors in the adult rat CNS. Neuroscience. 2004;123(1):131–45.

    Article  CAS  PubMed  Google Scholar 

  131. Mascia P, Pistis M, Justinova Z, Panlilio LV, Luchicchi A, Lecca S, et al. Blockade of nicotine reward and reinstatement by activation of alpha-type peroxisome proliferator-activated receptors. Biol Psychiatry. 2011;69(7):633–41.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  132. Panlilio LV, Justinova Z, Mascia P, Pistis M, Luchicchi A, Lecca S, et al. Novel use of a lipid-lowering fibrate medication to prevent nicotine reward and relapse: preclinical findings. Neuropsychopharmacology. 2012;37(8):1838–47.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  133. Melis M, Carta S, Fattore L, Tolu S, Yasar S, Goldberg SR, et al. Peroxisome proliferator-activated receptors-alpha modulate dopamine cell activity through nicotinic receptors. Biol Psychiatry. 2010;68(3):256–64.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  134. Charpantier E, Wiesner A, Huh KH, Ogier R, Hoda JC, Allaman G, et al. Alpha7 neuronal nicotinic acetylcholine receptors are negatively regulated by tyrosine phosphorylation and Src-family kinases. J Neurosci. 2005;25(43):9836–49.

    Article  CAS  PubMed  Google Scholar 

  135. Jackevicius CA, Tu JV, Ross JS, Ko DT, Carreon D, Krumholz HM. Use of fibrates in the United States and Canada. JAMA. 2011;305(12):1217–24.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  136. Hata Y, Nakajima K. Life-style and serum lipids and lipoproteins. J Atheroscler Thromb. 2000;7(4):177–97.

    Article  CAS  PubMed  Google Scholar 

  137. Gamaleddin I, Guranda M, Scherma M, Fratta W, Makriyannis A, Vadivel SK, et al. AM404 attenuates reinstatement of nicotine seeking induced by nicotine-associated cues and nicotine priming but does not affect nicotine- and food-taking. J Psychopharmacol. 2013;27(6):564–71.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  138. Gamaleddin I, Guranda M, Goldberg SR, Le Foll B. The selective anandamide transport inhibitor VDM11 attenuates reinstatement of nicotine seeking behaviour, but does not affect nicotine intake. Br J Pharmacol. 2011;164(6):1652–60.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  139. Everitt BJ, Robbins TW. From the ventral to the dorsal striatum: devolving views of their roles in drug addiction. Neurosci Biobehav Rev. 2013;37(9 Pt A):1946–54.

    Article  PubMed  Google Scholar 

  140. Everitt BJ, Robbins TW. Neural systems of reinforcement for drug addiction: from actions to habits to compulsion. Nat Neurosci. 2005;8(11):1481–9.

    Article  CAS  PubMed  Google Scholar 

  141. Bura SA, Burokas A, Martin-Garcia E, Maldonado R. Effects of chronic nicotine on food intake and anxiety-like behaviour in CB(1) knockout mice. Eur Neuropsychopharmacol. 2010;20(6):369–78.

    Article  CAS  PubMed  Google Scholar 

  142. Cippitelli A, Astarita G, Duranti A, Caprioli G, Ubaldi M, Stopponi S, et al. Endocannabinoid regulation of acute and protracted nicotine withdrawal: effect of FAAH inhibition. PLoS One. 2011;6(11):e28142.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  143. Balerio GN, Aso E, Berrendero F, Murtra P, Maldonado R. Delta9-tetrahydrocannabinol decreases somatic and motivational manifestations of nicotine withdrawal in mice. Eur J Neurosci. 2004;20(10):2737–48.

    Article  PubMed  Google Scholar 

  144. Kandel D. Stages in adolescent involvement in drug use. Science. 1975;190(4217):912–4.

    Article  CAS  PubMed  Google Scholar 

  145. Kandel DB, Yamaguchi K, Klein LC. Testing the Gateway Hypothesis. Addiction. 2006;101(4):470–2.

    Article  PubMed  Google Scholar 

  146. Vaughn M, Wallace J, Perron B, Copeland V, Howard M. Does marijuana use serve as a gateway to cigarette use for high-risk African-American youth? Am J Drug Alcohol Abuse. 2008;34(6):782–91.

    Article  PubMed  PubMed Central  Google Scholar 

  147. Ellgren M, Artmann A, Tkalych O, Gupta A, Hansen HS, Hansen SH, et al. Dynamic changes of the endogenous cannabinoid and opioid mesocorticolimbic systems during adolescence: THC effects. Eur Neuropsychopharmacol. 2008;18(11):826–34.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  148. Ellgren M, Spano SM, Hurd YL. Adolescent cannabis exposure alters opiate intake and opioid limbic neuronal populations in adult rats. Neuropsychopharmacology. 2007;32(3):607–15.

    Article  CAS  PubMed  Google Scholar 

  149. Maldonado R. Study of cannabinoid dependence in animals. Pharmacol Ther. 2002;95(2):153–64.

    Article  CAS  PubMed  Google Scholar 

  150. Panlilio LV, Zanettini C, Barnes C, Solinas M, Goldberg SR. Prior exposure to THC increases the addictive effects of nicotine in rats. Neuropsychopharmacology. 2013;38(7):1198–208.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  151. Solinas M, Panlilio LV, Goldberg SR. Exposure to delta-9-tetrahydrocannabinol (THC) increases subsequent heroin taking but not heroin’s reinforcing efficacy: a self-administration study in rats. Neuropsychopharmacology. 2004;29(7):1301–11.

    Article  CAS  PubMed  Google Scholar 

  152. Panlilio LV, Solinas M, Matthews SA, Goldberg SR. Previous exposure to THC alters the reinforcing efficacy and anxiety-related effects of cocaine in rats. Neuropsychopharmacology. 2007;32(3):646–57.

    Article  CAS  PubMed  Google Scholar 

  153. Levine A, Huang Y, Drisaldi B, Griffin EA Jr, 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(107):107ra109.

    Article  CAS  Google Scholar 

  154. Le Foll B, Wiggins M, Goldberg SR. Nicotine pre-exposure does not potentiate the locomotor or rewarding effects of Delta-9-tetrahydrocannabinol in rats. Behav Pharmacol. 2006;17(2):195–9.

    Article  CAS  PubMed  Google Scholar 

  155. Chen JP, Paredes W, Li J, Smith D, Lowinson J, Gardner EL. Delta9-tetrahydrocannabinol produces naloxone-blockable enhancement of presynaptic basal dopamine efflux in nucleus accumbens of conscious, freely-moving rats as measured by intracerebral microdialysis. Psychopharmacology (Berl). 1990;102(2):156–62.

    Article  CAS  Google Scholar 

  156. Tanda G, Pontieri FE, Di Chiara G. Cannabinoid and heroin activation of mesolimbic dopamine transmission by a common mu1 opioid receptor mechanism. Science. 1997;276(5321):2048–50.

    Article  CAS  PubMed  Google Scholar 

  157. Gardner EL. Endocannabinoid signaling system and brain reward: emphasis on dopamine. Pharmacol Biochem Behav. 2005;81(2):263–84.

    Article  CAS  PubMed  Google Scholar 

  158. Schlicker E, Kathmann M. Modulation of transmitter release via presynaptic cannabinoid receptors. Trends Pharmacol Sci. 2001;22(11):565–72.

    Article  CAS  PubMed  Google Scholar 

  159. French ED. delta9-Tetrahydrocannabinol excites rat VTA dopamine neurons through activation of cannabinoid CB1 but not opioid receptors. Neurosci Lett. 1997;226(3):159–62.

    Article  CAS  PubMed  Google Scholar 

  160. French ED, Dillon K, Wu X. Cannabinoids excite dopamine neurons in the ventral tegmentum and substantia nigra. Neuroreport. 1997;8(3):649–52.

    Article  CAS  PubMed  Google Scholar 

  161. Gessa GL, Melis M, Muntoni AL, Diana M. Cannabinoids activate mesolimbic dopamine neurons by an action on cannabinoid CB1 receptors. Eur J Pharmacol. 1998;341(1):39–44.

    Article  CAS  PubMed  Google Scholar 

  162. Wu X, French ED. Effects of chronic delta9-tetrahydrocannabinol on rat midbrain dopamine neurons: an electrophysiological assessment. Neuropharmacology. 2000;39(3):391–8.

    Article  CAS  PubMed  Google Scholar 

  163. Ng Cheong Ton JM, Gerhardt GA, Friedemann M, Etgen AM, Rose GM, Sharpless NS, et al. The effects of delta9-tetrahydrocannabinol on potassium-evoked release of dopamine in the rat caudate nucleus: an in vivo electrochemical and in vivo microdialysis study. Brain Res. 1988;451(1–2):59–68.

    CAS  PubMed  Google Scholar 

  164. Collins RJ, Weeks JR, Cooper MM, Good PI, Russell RR. Prediction of abuse liability of drugs using IV self-administration by rats. Psychopharmacology (Berl). 1984;82(1–2):6–13.

    CAS  Google Scholar 

  165. Koob GF, Weiss F. Pharmacology of drug self-administration. Alcohol. 1990;7(3):193–7.

    Article  CAS  PubMed  Google Scholar 

  166. Yokel RA. Intravenous self-administration: response rates, the effects of pharmacological challenges, and drug preference. In: Bozarth MA, editor. Methods of assessing the reinforcing properties of abused drugs. New York: Springer-Verlag; 1987. pp. 1–33.

    Chapter  Google Scholar 

  167. Young AM, Herling S. Drugs as reinforcers: Studies in laboratory animals. In: Goldberg SR, Stolerman IP, editors. Behavioral analysis of drug dependence. Orlando: Academic; 1986. pp. 9–67.

    Google Scholar 

  168. Justinova Z, Tanda G, Redhi GH, Goldberg SR. Self-administration of Delta(9)-tetrahydrocannabinol (THC) by drug naive squirrel monkeys. Psychopharmacology (Berl). 2003;169(2):135–40.

    Article  CAS  Google Scholar 

  169. Justinova Z, Goldberg SR, Heishman SJ, Tanda G. Self-administration of cannabinoids by experimental animals and human marijuana smokers. Pharmacol Biochem Behav. 2005;81(2):285–99.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  170. Justinova Z, Mangieri RA, Bortolato M, Chefer SI, Mukhin AG, Clapper JR, et al. Fatty acid amide hydrolase inhibition heightens anandamide signaling without producing reinforcing effects in primates. Biol Psychiatry. 2008;64(11):930–7.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  171. Justinova Z, Munzar P, Panlilio LV, Yasar S, Redhi GH, Tanda G, et al. Blockade of THC-seeking behavior and relapse in monkeys by the cannabinoid CB(1)-receptor antagonist rimonabant. Neuropsychopharmacology. 2008;33(12):2870–7.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  172. Justinova Z, Ferre S, Redhi GH, Mascia P, Stroik J, Quarta D, et al. Reinforcing and neurochemical effects of cannabinoid CB1 receptor agonists, but not cocaine, are altered by an adenosine A2A receptor antagonist. Addict Biol. 2011;16(3):405–15.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  173. Justinova Z, Mascia P, Wu HQ, Secci ME, Redhi GH, Panlilio LV, et al. Reducing cannabinoid abuse and preventing relapse by enhancing endogenous brain levels of kynurenic acid. Nat Neurosci. 2013;16(11):1652–61.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  174. Fattore L, Cossu G, Martellotta CM, Fratta W. Intravenous self-administration of the cannabinoid CB1 receptor agonist WIN 55,212-2 in rats. Psychopharmacology (Berl). 2001;156(4):410–6.

    Article  CAS  Google Scholar 

  175. Martellotta MC, Cossu G, Fattore L, Gessa GL, Fratta W. Self-administration of the cannabinoid receptor agonist WIN 55,212-2 in drug-naive mice. Neuroscience. 1998;85(2):327–30.

    Article  CAS  PubMed  Google Scholar 

  176. Spano MS, Fattore L, Cossu G, Deiana S, Fadda P, Fratta W. CB1 receptor agonist and heroin, but not cocaine, reinstate cannabinoid-seeking behaviour in the rat. Br J Pharmacol. 2004;143(3):343–50.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  177. 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(3):1127–34.

    Article  CAS  PubMed  Google Scholar 

  178. Solinas M, Scherma M, Fattore L, Stroik J, Wertheim C, Tanda G, et al. Nicotinic alpha 7 receptors as a new target for treatment of cannabis abuse. J Neurosci. 2007;27(21):5615–20.

    Article  CAS  PubMed  Google Scholar 

  179. Pomerleau OF. Nicotine as a psychoactive drug: anxiety and pain reduction. Psychopharmacol Bull. 1986;22(3):865–9.

    CAS  PubMed  Google Scholar 

  180. Gilbert DG, Robinson JH, Chamberlin CL, Spielberger CD. Effects of smoking/nicotine on anxiety, heart rate, and lateralization of EEG during a stressful movie. Psychophysiology 1989;26(3):311–20.

    Article  CAS  PubMed  Google Scholar 

  181. Picciotto MR, Brunzell DH, Caldarone BJ. Effect of nicotine and nicotinic receptors on anxiety and depression. Neuroreport. 2002;13(9):1097–106.

    Article  CAS  PubMed  Google Scholar 

  182. Balerio GN, Aso E, Maldonado R. Role of the cannabinoid system in the effects induced by nicotine on anxiety-like behaviour in mice. Psychopharmacology (Berl). 2006;184(3–4):504–13.

    Article  CAS  Google Scholar 

  183. Hayase T. Working memory- and anxiety-related behavioral effects of repeated nicotine as a stressor: the role of cannabinoid receptors. BMC Neurosci. 2013;14:20.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  184. Aydin C, Oztan O, Isgor C. Nicotine-induced anxiety-like behavior in a rat model of the novelty-seeking phenotype is associated with long-lasting neuropeptidergic and neuroplastic adaptations in the amygdala: effects of the cannabinoid receptor 1 antagonist AM251. Neuropharmacology. 2012;63(8):1335–45.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  185. Heishman SJ. Behavioral and cognitive effects of smoking: relationship to nicotine addiction. Nicotine Tob Res. 1999;1(Suppl 2):S143–S7.

    Article  PubMed  Google Scholar 

  186. Heishman SJ, Kleykamp BA, Singleton EG. Meta-analysis of the acute effects of nicotine and smoking on human performance. Psychopharmacology (Berl). 2010;210(4):453–69.

    Article  CAS  Google Scholar 

  187. Biala G, Kruk M. Cannabinoid receptor ligands suppress memory-related effects of nicotine in the elevated plus maze test in mice. Behav Brain Res. 2008;192(2):198–202.

    Article  CAS  PubMed  Google Scholar 

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The research activity of the authors is supported by the Intramural Research Program, National Institute on Drug Abuse, National Institutes of Health, Department of Health and Human Services.

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Auber, A., Justinova, Z., Scherma, M., Goldberg, S., Panlilio, L. (2015). Cannabinoid-Nicotine Interactions. In: Campolongo, P., Fattore, L. (eds) Cannabinoid Modulation of Emotion, Memory, and Motivation. Springer, New York, NY. https://doi.org/10.1007/978-1-4939-2294-9_13

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