Advertisement

Neurobiological Bases of Cue- and Nicotine-induced Reinstatement of Nicotine Seeking: Implications for the Development of Smoking Cessation Medications

Chapter
Part of the Current Topics in Behavioral Neurosciences book series (CTBN, volume 24)

Abstract

A better understanding of the neurobiological factors that contribute to relapse to smoking is needed for the development of efficacious smoking cessation medications. Reinstatement procedures allow the preclinical assessment of several factors that contribute to relapse in humans, including re-exposure to nicotine via tobacco smoking and the presentation of stimuli that were previously associated with nicotine administration (i.e., conditioned stimuli). This review provides an integrated discussion of the results of animal studies that used reinstatement procedures to assess the efficacy of pharmacologically targeting various neurotransmitter systems in attenuating the cue- and nicotine-induced reinstatement of nicotine seeking. The results of these animal studies have increased our understanding of the neurobiological processes that mediate the conditioned effects of stimuli that trigger reinstatement to nicotine seeking. Thus, these findings provide important insights into the neurobiological substrates that modulate relapse to tobacco smoking in humans and the ongoing search for novel efficacious smoking cessation medications.

Keywords

Animal models Nicotine Cue-induced reinstatement Nicotine-induced reinstatement Drug seeking Medication development 

Notes

Acknowledgements

This work was supported by Postdoctoral Fellowship 21FT-0022 from the Tobacco-Related Disease Research Program to AKS and research grant R56 DA011946 from the National Institute on Drug Abuse to AM. The authors would like to thank Ms. Janet Hightower for assistance with preparation of the figure and Mr. Michael Arends for editorial assistance.

References

  1. Abdolahi A, Acosta G, Breslin FJ, Hemby SE, Lynch WJ (2010) Incubation of nicotine seeking is associated with enhanced protein kinase A-regulated signaling of dopamine- and cAMP-regulated phosphoprotein of 32 kDa in the insular cortex. Eur J Neurosci 31:733–741PubMedCentralPubMedGoogle Scholar
  2. Alberg AJ, Shopland DR, Cummings KM (2014) The 2014 Surgeon general’s report: commemorating the 50th anniversary of the 1964 report of the advisory committee to the us surgeon general and updating the evidence on the health consequences of cigarette smoking. Am J Epidemiol 179:403Google Scholar
  3. Andreoli M, Tessari M, Pilla M, Valerio E, Hagan JJ, Heidbreder CA (2003) Selective antagonism at dopamine D3 receptors prevents nicotine-triggered relapse to nicotine-seeking behavior. Neuropsychopharmacology 28:1272–1280PubMedGoogle Scholar
  4. Bedi G, Preston KL, Epstein DH, Heishman SJ, Marrone GF, Shaham Y, de Wit H (2011) Incubation of cue-induced cigarette craving during abstinence in human smokers. Biol Psychiatry 69:708–711PubMedCentralPubMedGoogle Scholar
  5. Beltramo M, Stella N, Calignano A, Lin SY, Makriyannis A, Piomelli D (1997) Functional role of high-affinity Anandamide transport, as revealed by selective inhibition. Science 277:1094–1097PubMedGoogle Scholar
  6. Berlin I, Said S, Spreux-Varoquaux O, Launay JM, Olivares R, Millet V, Lecrubier Y, Puech AJ (1995) A reversible monoamine oxidase A inhibitor (moclobemide) facilitates smoking cessation and abstinence in heavy, dependent smokers. Clin Pharmacol Ther 58:444–452PubMedGoogle Scholar
  7. Bespalov AY, Dravolina OA, Sukhanov I, Zakharova E, Blokhina E, Zvartau E, Danysz W, van Heeke G, Markou A (2005) Metabotropic glutamate receptor (mGluR5) antagonist MPEP attenuated cue- and schedule-induced reinstatement of nicotine self-administration behavior in rats. Neuropharmacology 49:167–178PubMedGoogle Scholar
  8. Biggs JT, Spiker DG, Petit JM, Ziegler VE (1977) Tricyclic antidepressant overdose: incidence of symptoms. JAMA 238:135–138PubMedGoogle Scholar
  9. Bormann J (1986) Electrophysiology of single GABA receptor chloride channels. Clin Neuropharmacol 9:386–388PubMedGoogle Scholar
  10. Bruijnzeel AW, Prado M, Isaac S (2009) Corticotropin-releasing factor-1 receptor activation mediates nicotine withdrawal-induced deficit in brain reward function and stress-induced relapse. Biol Psychiatry 66:110–117PubMedCentralPubMedGoogle Scholar
  11. Cahill K, Ussher MH (2011) Cannabinoid type 1 receptor antagonists for smoking cessation. Cochrane Database Syst Rev 3:CD005353Google Scholar
  12. Centers for Disease Control and Prevention (2000) Cigarette smoking among adults - United States, 1998. Morb Mortal Wkly Rep 49:881–884Google Scholar
  13. Centers for Disease Control and Prevention (2010) Quitting smoking among adults—United States 2001–2010. Morb Mortal Wkly Rep 60:1513–1519Google Scholar
  14. Chiamulera C, Tedesco V, Zangrandi L, Giuliano C, Fumagalli G (2010) Propranolol transiently inhibits reinstatement of nicotine-seeking behaviour in rats. J Psychopharmacol 24:389–395PubMedGoogle Scholar
  15. Clinicaltrials.gov (2007) Effects of AFQ056 and nicotine in reducing cigarette smoking. http://clinicaltrials.gov/ct2/show/NCT00414752?term=Effects+of+AFQ056+and+Nicotine+in+Reducing+Cigarette+Smoking&rank=1. Accessed 23 Mar 2014
  16. Coe JW, Brooks PR, Vetelino MG, Wirtz MC, Arnold EP, Huang J, Sands SB, Davis TI, Lebel LA, Fox CB, Shrikhande A, Heym JH, Schaeffer E, Rollema H, Lu Y, Mansbach RS, Chambers LK, Rovetti CC, Schulz DW, Tingley FD 3rd, O’Neill BT (2005) Varenicline: an alpha4beta2 nicotinic receptor partial agonist for smoking cessation. J Med Chem 48:3474–3477PubMedGoogle Scholar
  17. Cohen C, Perrault G, Griebel G, Soubrie P (2005) Nicotine-associated cues maintain nicotine-seeking behavior in rats several weeks after nicotine withdrawal: reversal by the cannabinoid (CB1) receptor antagonist, rimonabant (SR141716). Neuropsychopharmacology 30:145–155PubMedGoogle Scholar
  18. Contreras M, Billeke P, Vicencio S, Madrid C, Perdomo G, Gonzalez M, Torrealba F (2012) A role for the insular cortex in long-term memory for context-evoked drug craving in rats. Neuropsychopharmacology 37:2101–2108PubMedCentralPubMedGoogle Scholar
  19. Contreras M, Ceric F, Torrealba F (2007) Inactivation of the interoceptive insula disrupts drug craving and malaise induced by lithium. Science 318:655–658PubMedGoogle Scholar
  20. Cousins MS, Stamat HM, de Wit H (2001) Effects of a single dose of baclofen on self-reported subjective effects and tobacco smoking. Nicotine Tob Res 3:123–129PubMedGoogle Scholar
  21. Cravatt BF, Giang DK, Mayfield SP, Boger DL, Lerner RA, Gilula NB (1996) Molecular characterization of an enzyme that degrades neuromodulatory fatty-acid amides. Nature 384:83–87PubMedGoogle Scholar
  22. Cryan JF, Bruijnzeel AW, Skjei KL, Markou A (2003) Bupropion enhances brain reward function and reverses the affective and somatic aspects of nicotine withdrawal in the rat. Psychopharmacology 168:347–358PubMedGoogle Scholar
  23. De Biasi M, Salas R (2008) Influence of neuronal nicotinic receptors over nicotine addiction and withdrawal. Exp Biol Med (Maywood) 233:917–929Google Scholar
  24. De Vries TJ, de Vries W, Janssen MC, Schoffelmeer AN (2005) Suppression of conditioned nicotine and sucrose seeking by the cannabinoid-1 receptor antagonist SR141716A. Behav Brain Res 161:164–168PubMedGoogle Scholar
  25. Diergaarde L, de Vries W, Raaso H, Schoffelmeer AN, De Vries TJ (2008) Contextual renewal of nicotine seeking in rats and its suppression by the cannabinoid-1 receptor antagonist Rimonabant (SR141716A). Neuropharmacology 55:712–716PubMedGoogle Scholar
  26. Doherty K, Kinnunen T, Militello FS, Garvey AJ (1995) Urges to smoke during the first month of abstinence: relationship to relapse and predictors. Psychopharmacology 119:171–178PubMedGoogle Scholar
  27. Dravolina OA, Zakharova ES, Shekunova EV, Zvartau EE, Danysz W, Bespalov AY (2007) mGlu1 receptor blockade attenuates cue- and nicotine-induced reinstatement of extinguished nicotine self-administration behavior in rats. Neuropharmacology 52:263–269PubMedGoogle Scholar
  28. Edwards NB, Murphy JK, Downs AD, Ackerman BJ, Rosenthal TL (1989) Doxepin as an adjunct to smoking cessation: a double-blind pilot study. Am J Psychiatry 146:373–376PubMedGoogle Scholar
  29. Epstein AM, King AC (2004) Naltrexone attenuates acute cigarette smoking behavior. Pharmacol Biochem Behav 77:29–37PubMedGoogle Scholar
  30. Everitt BJ, Belin D, Economidou D, Pelloux Y, Dalley JW, Robbins TW (2008) Review neural mechanisms underlying the vulnerability to develop compulsive drug-seeking habits and addiction. Philos Trans R Soc Lond B Biol Sci 363:3125–3135PubMedCentralPubMedGoogle Scholar
  31. Falvella FS, Galvan A, Frullanti E, Spinola M, Calabro E, Carbone A, Incarbone M, Santambrogio L, Pastorino U, Dragani TA (2009) Transcription deregulation at the 15q25 locus in association with lung adenocarcinoma risk. Clin Cancer Res 15:1837–1842PubMedGoogle Scholar
  32. Fattore L, Spano MS, Cossu G, Scherma M, Fratta W, Fadda P (2009) Baclofen prevents drug-induced reinstatement of extinguished nicotine-seeking behaviour and nicotine place preference in rodents. Eur Neuropsychopharmacol 19:487–498PubMedGoogle Scholar
  33. Fegley D, Gaetani S, Duranti A, Tontini A, Mor M, Tarzia G, Piomelli D (2005) Characterization of the fatty acid amide hydrolase inhibitor cyclohexyl carbamic acid 3’-carbamoyl-biphenyl-3-yl ester (URB597): effects on anandamide and oleoylethanolamide deactivation. J Pharmacol Exp Ther 313:352–358PubMedGoogle Scholar
  34. Feltenstein MW, Ghee SM, See RE (2012) Nicotine self-administration and reinstatement of nicotine-seeking in male and female rats. Drug Alcohol Depend 121:240–246PubMedCentralPubMedGoogle Scholar
  35. Fletcher PJ, Le AD, Higgins GA (2008) Serotonin receptors as potential targets for modulation of nicotine use and dependence. Prog Brain Res 172:361–383PubMedGoogle Scholar
  36. Fletcher PJ, Rizos Z, Noble K, Soko AD, Silenieks LB, Le AD, Higgins GA (2012) Effects of the 5-HT2C receptor agonist Ro60-0175 and the 5-HT2A receptor antagonist M100907 on nicotine self-administration and reinstatement. Neuropharmacology 62:2288–2298PubMedGoogle Scholar
  37. Forget B, Coen KM, Le Foll B (2009) 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 205:613–624PubMedGoogle Scholar
  38. Forget B, Pushparaj A, Le Foll B (2010a) Granular insular cortex inactivation as a novel therapeutic strategy for nicotine addiction. Biol Psychiatry 68:265–271PubMedGoogle Scholar
  39. Forget B, Wertheim C, Mascia P, Pushparaj A, Goldberg SR, Le Foll B (2010b) Noradrenergic alpha1 receptors as a novel target for the treatment of nicotine addiction. Neuropsychopharmacology 35:1751–1760PubMedCentralPubMedGoogle Scholar
  40. Fowler CD, Lu Q, Johnson PM, Marks MJ, Kenny PJ (2011) Habenular alpha5 nicotinic receptor subunit signalling controls nicotine intake. Nature 471:597–601PubMedCentralPubMedGoogle Scholar
  41. Fowler CD, Tuesta L, Kenny PJ (2013) Role of alpha5* nicotinic acetylcholine receptors in the effects of acute and chronic nicotine treatment on brain reward function in mice. Psychopharmacology 229:503–513Google Scholar
  42. Frahm S, Slimak MA, Ferrarese L, Santos-Torres J, Antolin-Fontes B, Auer S, Filkin S, Pons S, Fontaine JF, Tsetlin V, Maskos U, Ibanez-Tallon I (2011) Aversion to nicotine is regulated by the balanced activity of beta4 and alpha5 nicotinic receptor subunits in the medial habenula. Neuron 70:522–535PubMedGoogle Scholar
  43. French ED (1997) delta9-Tetrahydrocannabinol excites rat VTA dopamine neurons through activation of cannabinoid CB1 but not opioid receptors. Neurosci Lett 226:159–162PubMedGoogle Scholar
  44. French ED, Dillon K, Wu X (1997) Cannabinoids excite dopamine neurons in the ventral tegmentum and substantia nigra. NeuroReport 8:649–652PubMedGoogle Scholar
  45. Fuchs RA, Branham RK, See RE (2006) Different neural substrates mediate cocaine seeking after abstinence versus extinction training: a critical role for the dorsolateral caudate-putamen. J Neurosci 26:3584–3588PubMedCentralPubMedGoogle Scholar
  46. Fucile S, Barabino B, Palma E, Grassi F, Limatola C, Mileo AM, Alema S, Ballivet M, Eusebi F (1997) Alpha 5 subunit forms functional alpha 3 beta 4 alpha 5 nAChRs in transfected human cells. NeuroReport 8:2433–2436PubMedGoogle Scholar
  47. Fung YK, Richard LA (1994) Behavioural consequences of cocaine withdrawal in rats. J Pharm Pharmacol 46:150–152PubMedGoogle Scholar
  48. Gabriele A, See RE (2011) Lesions and reversible inactivation of the dorsolateral caudate-putamen impair cocaine-primed reinstatement to cocaine-seeking in rats. Brain Res 1417:27–35PubMedCentralPubMedGoogle Scholar
  49. Gamaleddin I, Guranda M, Goldberg SR, Le Foll B (2011) The selective Anandamide transport inhibitor VDM11 attenuates reinstatement of nicotine seeking behaviour, but does not affect nicotine intake. Br J Pharmacol 164:1652–1660PubMedCentralPubMedGoogle Scholar
  50. Gamaleddin I, Guranda M, Scherma M, Fratta W, Makriyannis A, Vadivel SK, Goldberg SR, Le Foll B (2013) AM404 attenuates reinstatement of nicotine seeking induced by nicotine-associated cues and nicotine priming but does not affect nicotine- and food-taking. J Psychopharmacol 27:564–571PubMedCentralPubMedGoogle Scholar
  51. Gamaleddin I, Wertheim C, Zhu AZ, Coen KM, Vemuri K, Makryannis A, Goldberg SR, Le Foll B (2012a) Cannabinoid receptor stimulation increases motivation for nicotine and nicotine seeking. Addict Biol 17:47–61PubMedGoogle Scholar
  52. Gamaleddin I, Zvonok A, Makriyannis A, Goldberg SR, Le Foll B (2012b) Effects of a selective cannabinoid CB2 agonist and antagonist on intravenous nicotine self administration and reinstatement of nicotine seeking. PLoS ONE 7:e29900PubMedCentralPubMedGoogle Scholar
  53. Gardner EL (2005) Endocannabinoid signaling system and brain reward: emphasis on dopamine. Pharmacol Biochem Behav 81:263–284PubMedGoogle Scholar
  54. Gardner EL, Vorel SR (1998) Cannabinoid transmission and reward-related events. Neurobiol Dis 5:502–533PubMedGoogle Scholar
  55. Gass JT, Olive MF (2008) Glutamatergic substrates of drug addiction and alcoholism. Biochem Pharmacol 75:218–265PubMedCentralPubMedGoogle Scholar
  56. Gerasimov MR, Franceschi M, Volkow ND, Rice O, Schiffer WK, Dewey SL (2000) Synergistic interactions between nicotine and cocaine or methylphenidate depend on the dose of dopamine transporter inhibitor. Synapse 38:432–437PubMedGoogle Scholar
  57. Geyer MA, Markou A (1995) Animal models of psychiatric disorders. In: Bloom FE, Kupfer DJ (eds) Psychopharmacology: the fourth generation of progress. Raven Press, New York, pp 787–798Google Scholar
  58. Giang DK, Cravatt BF (1997) Molecular characterization of human and mouse fatty acid amide hydrolases. Proc Natl Acad Sci USA 94:2238–2242PubMedCentralPubMedGoogle Scholar
  59. Gipson CD, Reissner KJ, Kupchik YM, Smith AC, Stankeviciute N, Hensley-Simon ME, Kalivas PW (2013) Reinstatement of nicotine seeking is mediated by glutamatergic plasticity. Proc Natl Acad Sci USA 110:9124–9129PubMedCentralPubMedGoogle Scholar
  60. Gonzales D, Rennard SI, Nides M, Oncken C, Azoulay S, Billing CB, Watsky EJ, Gong J, Williams KE, Reeves KR (2006) Varenicline, an alpha4beta2 nicotinic acetylcholine receptor partial agonist, versus sustained-release bupropion and placebo for smoking cessation: a randomized controlled trial. JAMA 296:47–55PubMedGoogle Scholar
  61. Guery S, Floersheim P, Kaupmann K, Froestl W (2007) Syntheses and optimization of new GS39783 analogues as positive allosteric modulators of GABA B receptors. Bioorg Med Chem Lett 17:6206–6211PubMedCentralPubMedGoogle Scholar
  62. Hall SM, Reus VI, Munoz RF, Sees KL, Humfleet G, Hartz DT, Frederick S, Triffleman E (1998) Nortriptyline and cognitive-behavioral therapy in the treatment of cigarette smoking. Arch Gen Psychiatry 55:683–690PubMedGoogle Scholar
  63. Higgins GA, Silenieks LB, Rossmann A, Rizos Z, Noble K, Soko AD, Fletcher PJ (2012) The 5-HT2C receptor agonist lorcaserin reduces nicotine self-administration, discrimination, and reinstatement: relationship to feeding behavior and impulse control. Neuropsychopharmacology 37:1177–1191PubMedCentralPubMedGoogle Scholar
  64. Hollander JA, Lu Q, Cameron MD, Kamenecka TM, Kenny PJ (2008) Insular hypocretin transmission regulates nicotine reward. Proc Natl Acad Sci USA 105:19480–19485PubMedCentralPubMedGoogle Scholar
  65. Hopkins TJ, Rupprecht LE, Hayes MR, Blendy JA, Schmidt HD (2012) Galantamine, an acetylcholinesterase inhibitor and positive allosteric modulator of nicotinic acetylcholine receptors, attenuates nicotine taking and seeking in rats. Neuropsychopharmacology 37:2310–2321PubMedCentralPubMedGoogle Scholar
  66. Howlett AC (2002) The cannabinoid receptors. Prostaglandins Other Lipid Mediat 68–69:619–631PubMedGoogle Scholar
  67. Howlett AC, Breivogel CS, Childers SR, Deadwyler SA, Hampson RE, Porrino LJ (2004) Cannabinoid physiology and pharmacology: 30 years of progress. Neuropharmacology 47:345–358PubMedGoogle Scholar
  68. Hughes JR, Keely J, Naud S (2004) Shape of the relapse curve and long-term abstinence among untreated smokers. Addiction 99:29–38PubMedGoogle Scholar
  69. Hughes JR, Shiffman S, Callas P, Zhang J (2003) A meta-analysis of the efficacy of over-the-counter nicotine replacement. Tob Control 12:21–27PubMedCentralPubMedGoogle Scholar
  70. Hung RJ, McKay JD, Gaborieau V, Boffetta P, Hashibe M, Zaridze D, Mukeria A, Szeszenia-Dabrowska N, Lissowska J, Rudnai P, Fabianova E, Mates D, Bencko V, Foretova L, Janout V, Chen C, Goodman G, Field JK, Liloglou T, Xinarianos G, Cassidy A, McLaughlin J, Liu G, Narod S, Krokan HE, Skorpen F, Elvestad MB, Hveem K, Vatten L, Linseisen J, Clavel-Chapelon F, Vineis P, Bueno-de-Mesquita HB, Lund E, Martinez C, Bingham S, Rasmuson T, Hainaut P, Riboli E, Ahrens W, Benhamou S, Lagiou P, Trichopoulos D, Holcatova I, Merletti F, Kjaerheim K, Agudo A, Macfarlane G, Talamini R, Simonato L, Lowry R, Conway DI, Znaor A, Healy C, Zelenika D, Boland A, Delepine M, Foglio M, Lechner D, Matsuda F, Blanche H, Gut I, Heath S, Lathrop M, Brennan P (2008) A susceptibility locus for lung cancer maps to nicotinic acetylcholine receptor subunit genes on 15q25. Nature 452:633–637PubMedGoogle Scholar
  71. Hurt RD, Sachs DP, Glover ED, Offord KP, Johnston JA, Dale LC, Khayrallah MA, Schroeder DR, Glover PN, Sullivan CR, Croghan IT, Sullivan PM (1997) A comparison of sustained-release bupropion and placebo for smoking cessation. N Engl J Med 337:1195–1202PubMedGoogle Scholar
  72. Ito R, Dalley JW, Robbins TW, Everitt BJ (2002) Dopamine release in the dorsal striatum during cocaine-seeking behavior under the control of a drug-associated cue. J Neurosci 22:6247–6253PubMedGoogle Scholar
  73. Jackson KJ, Martin BR, Changeux JP, Damaj MI (2008) Differential role of nicotinic acetylcholine receptor subunits in physical and affective nicotine withdrawal signs. J Pharmacol Exp Ther 325:302–312PubMedGoogle Scholar
  74. Jorenby DE, Hays JT, Rigotti NA, Azoulay S, Watsky EJ, Williams KE, Billing CB, Gong J, Reeves KR (2006) Efficacy of varenicline, an alpha4beta2 nicotinic acetylcholine receptor partial agonist, vs placebo or sustained-release bupropion for smoking cessation: a randomized controlled trial. JAMA 296:56–63PubMedGoogle Scholar
  75. Kalivas PW (2004) Glutamate systems in cocaine addiction. Curr Opin Pharmacol 4:23–29PubMedGoogle Scholar
  76. Kalivas PW, McFarland K (2003) Brain circuitry and the reinstatement of cocaine-seeking behavior. Psychopharmacology 168:44–56PubMedGoogle Scholar
  77. Katz JL, Higgins ST (2003) The validity of the reinstatement model of craving and relapse to drug use. Psychopharmacology 168:21–30PubMedGoogle Scholar
  78. Khaled MA, Farid Araki K, Li B, Coen KM, Marinelli PW, Varga J, Gaal J, Le Foll B (2010) The selective dopamine D3 receptor antagonist SB 277011-A, but not the partial agonist BP 897, blocks cue-induced reinstatement of nicotine-seeking. Int J Neuropsychopharmacol 13:181–190PubMedGoogle Scholar
  79. Kimmey BA, Rupprecht LE, Hayes MR, Schmidt HD (2012) Donepezil, an acetylcholinesterase inhibitor, attenuates nicotine self-administration and reinstatement of nicotine seeking in rats. Addict Biol 19:539–51Google Scholar
  80. King AC (2002) Role of naltrexone in initial smoking cessation: preliminary findings. Alcohol Clin Exp Res 26:1942–1944PubMedGoogle Scholar
  81. King AC, Cao D, O’Malley SS, Kranzler HR, Cai X, deWit H, Matthews AK, Stachoviak RJ (2012) Effects of naltrexone on smoking cessation outcomes and weight gain in nicotine-dependent men and women. J Clin Psychopharmacol 32:630–636PubMedGoogle Scholar
  82. King AC, Cao D, Zhang L, O’Malley SS (2013) Naltrexone reduction of long-term smoking cessation weight gain in women but not men: a randomized controlled trial. Biol Psychiatry 73:924–930PubMedCentralPubMedGoogle Scholar
  83. King AC, Meyer PJ (2000) Naltrexone alteration of acute smoking response in nicotine-dependent subjects. Pharmacol Biochem Behav 66:563–572PubMedGoogle Scholar
  84. Klitenick MA, DeWitte P, Kalivas PW (1992) Regulation of somatodendritic dopamine release in the ventral tegmental area by opioids and GABA: an in vivo microdialysis study. J Neurosci 12:2623–2632PubMedGoogle Scholar
  85. Knackstedt LA, LaRowe S, Mardikian P, Malcolm R, Upadhyaya H, Hedden S, Markou A, Kalivas PW (2009) The role of cystine-glutamate exchange in nicotine dependence in rats and humans. Biol Psychiatry 65:841–845PubMedCentralPubMedGoogle Scholar
  86. Kupchik YM, Moussawi K, Tang XC, Wang X, Kalivas BC, Kolokithas R, Ogburn KB, Kalivas PW (2012) The effect of N-acetylcysteine in the nucleus accumbens on neurotransmission and relapse to cocaine. Biol Psychiatry 71:978–986PubMedCentralPubMedGoogle Scholar
  87. Laviolette SR, van der Kooy D (2004) The neurobiology of nicotine addiction: bridging the gap from molecules to behaviour. Nat Rev Neurosci 5:55–65PubMedGoogle Scholar
  88. Le Foll B, Chakraborty-Chatterjee M, Lev-Ran S, Barnes C, Pushparaj A, Gamaleddin I, Yan Y, Khaled M, Goldberg SR (2012) Varenicline decreases nicotine self-administration and cue-induced reinstatement of nicotine-seeking behaviour in rats when a long pretreatment time is used. Int J Neuropsychopharmacol 15:1265–1274PubMedCentralPubMedGoogle Scholar
  89. Li S, Li Z, Pei L, Le AD, Liu F (2012) The alpha7nACh-NMDA receptor complex is involved in cue-induced reinstatement of nicotine seeking. J Exp Med 209:2141–2147PubMedCentralPubMedGoogle Scholar
  90. Li X, Semenova S, D’Souza MS, Stoker AK, Markou A (2014) Involvement of glutamatergic and GABAergic systems in nicotine dependence: Implications for novel pharmacotherapies for smoking cessation. Neuropharmacology Part B 76:554–565Google Scholar
  91. Liechti ME, Lhuillier L, Kaupmann K, Markou A (2007) Metabotropic glutamate 2/3 receptors in the ventral tegmental area and the nucleus accumbens shell are involved in behaviors relating to nicotine dependence. J Neurosci 27:9077–9085PubMedGoogle Scholar
  92. Liechti ME, Markou A (2008) Role of the glutamatergic system in nicotine dependence : implications for the discovery and development of new pharmacological smoking cessation therapies. CNS Drugs 22:705–724PubMedGoogle Scholar
  93. Liu X (2014) Effects of blockade of alpha4beta2 and alpha7 nicotinic acetylcholine receptors on cue-induced reinstatement of nicotine-seeking behaviour in rats. Int J Neuropsychopharmacol 17:105–116PubMedGoogle Scholar
  94. Liu X, Caggiula AR, Palmatier MI, Donny EC, Sved AF (2008) Cue-induced reinstatement of nicotine-seeking behavior in rats: effect of bupropion, persistence over repeated tests, and its dependence on training dose. Psychopharmacology 196:365–375PubMedCentralPubMedGoogle Scholar
  95. Liu X, Caggiula AR, Yee SK, Nobuta H, Sved AF, Pechnick RN, Poland RE (2007) Mecamylamine attenuates cue-induced reinstatement of nicotine-seeking behavior in rats. Neuropsychopharmacology 32:710–718PubMedCentralPubMedGoogle Scholar
  96. Liu X, Jernigen C, Gharib M, Booth S, Caggiula AR, Sved AF (2010) Effects of dopamine antagonists on drug cue-induced reinstatement of nicotine-seeking behavior in rats. Behav Pharmacol 21:153–160PubMedCentralPubMedGoogle Scholar
  97. Liu X, Palmatier MI, Caggiula AR, Sved AF, Donny EC, Gharib M, Booth S (2009) Naltrexone attenuation of conditioned but not primary reinforcement of nicotine in rats. Psychopharmacology 202:589–598PubMedCentralPubMedGoogle Scholar
  98. Mameli-Engvall M, Evrard A, Pons S, Maskos U, Svensson TH, Changeux JP, Faure P (2006) Hierarchical control of dopamine neuron-firing patterns by nicotinic receptors. Neuron 50:911–921PubMedGoogle Scholar
  99. Mansvelder HD, McGehee DS (2000) Long-term potentiation of excitatory inputs to brain reward areas by nicotine. Neuron 27:349–357PubMedGoogle Scholar
  100. Markou A (2007) Metabotropic glutamate receptor antagonists: novel therapeutics for nicotine dependence and depression? Biol Psychiatry 61:17–22PubMedGoogle Scholar
  101. Mascia P, Pistis M, Justinova Z, Panlilio LV, Luchicchi A, Lecca S, Scherma M, Fratta W, Fadda P, Barnes C, Redhi GH, Yasar S, Le Foll B, Tanda G, Piomelli D, Goldberg SR (2011) Blockade of nicotine reward and reinstatement by activation of alpha-type peroxisome proliferator-activated receptors. Biol Psychiatry 69:633–641PubMedCentralPubMedGoogle Scholar
  102. Maskos U, Molles BE, Pons S, Besson M, Guiard BP, Guilloux JP, Evrard A, Cazala P, Cormier A, Mameli-Engvall M, Dufour N, Cloez-Tayarani I, Bemelmans AP, Mallet J, Gardier AM, David V, Faure P, Granon S, Changeux JP (2005) Nicotine reinforcement and cognition restored by targeted expression of nicotinic receptors. Nature 436:103–107PubMedGoogle Scholar
  103. Mihalak KB, Carroll FI, Luetje CW (2006) Varenicline is a partial agonist at alpha4beta2 and a full agonist at alpha7 neuronal nicotinic receptors. Mol Pharmacol 70:801–805PubMedGoogle Scholar
  104. Moreira FA, Crippa JA (2009) The psychiatric side-effects of rimonabant. Rev Bras Psiquiatr 31:145–153PubMedGoogle Scholar
  105. Muskens JB, Schellekens AF, de Leeuw FE, Tendolkar I, Hepark S (2012) Damage in the dorsal striatum alleviates addictive behavior. Gen Hosp Psychiatry 34: 702 e9-702 e11Google Scholar
  106. Naqvi NH, Bechara A (2009) The hidden island of addiction: the insula. Trends Neurosci 32:56–67PubMedCentralPubMedGoogle Scholar
  107. Naqvi NH, Rudrauf D, Damasio H, Bechara A (2007) Damage to the insula disrupts addiction to cigarette smoking. Science 315:531–534PubMedCentralPubMedGoogle Scholar
  108. Ng M, Freeman MK, Fleming TD, Robinson M, Dwyer-Lindgren L, Thomson B, Wollum A, Sanman E, Wulf S, Lopez AD, Murray CJ, Gakidou E (2014) Smoking prevalence and cigarette consumption in 187 countries, 1980-2012. JAMA 311:183–192PubMedGoogle Scholar
  109. O’Connor EC, Parker D, Rollema H, Mead AN (2010) The alpha4beta2 nicotinic acetylcholine-receptor partial agonist varenicline inhibits both nicotine self-administration following repeated dosing and reinstatement of nicotine seeking in rats. Psychopharmacology 208:365–376PubMedGoogle Scholar
  110. Panlilio LV, Justinova Z, Mascia P, Pistis M, Luchicchi A, Lecca S, Barnes C, Redhi GH, Adair J, Heishman SJ, Yasar S, Aliczki M, Haller J, Goldberg SR (2012) Novel use of a lipid-lowering fibrate medication to prevent nicotine reward and relapse: preclinical findings. Neuropsychopharmacology 37:1838–1847PubMedCentralPubMedGoogle Scholar
  111. Paterson NE, Balfour DJ, Markou A (2007) Chronic bupropion attenuated the anhedonic component of nicotine withdrawal in rats via inhibition of dopamine reuptake in the nucleus accumbens shell. Eur J Neurosci 25:3099–3108PubMedGoogle Scholar
  112. Paterson NE, Froestl W, Markou A (2005) Repeated administration of the GABAB receptor agonist CGP44532 decreased nicotine self-administration, and acute administration decreased cue-induced reinstatement of nicotine-seeking in rats. Neuropsychopharmacology 30:119–128PubMedGoogle Scholar
  113. Pechnick RN, Manalo CM, Lacayo LM, Vit JP, Bholat Y, Spivak I, Reyes KC, Farrokhi C (2011) Acamprosate attenuates cue-induced reinstatement of nicotine-seeking behavior in rats. Behav Pharmacol 22:222–227PubMedGoogle Scholar
  114. Picciotto MR (1998) Common aspects of the action of nicotine and other drugs of abuse. Drug Alcohol Depend 51:165–172PubMedGoogle Scholar
  115. Plaza-Zabala A, Flores Á, Martín-García E, Saravia R, Maldonado R, Berrendero F (2013) A role for hypocretin/orexin receptor-1 in cue-induced reinstatement of nicotine-seeking behavior. Neuropsychopharmacology 38:1724–36Google Scholar
  116. Prochazka AV, Weaver MJ, Keller RT, Fryer GE, Licari PA, Lofaso D (1998) A randomized trial of nortriptyline for smoking cessation. Arch Intern Med 158:2035–2039PubMedGoogle Scholar
  117. Pushparaj A, Hamani C, Yu W, Shin DS, Kang B, Nobrega JN, Le Foll B (2013) Electrical stimulation of the insular region attenuates nicotine-taking and nicotine-seeking behaviors. Neuropsychopharmacology 38:690–698PubMedCentralPubMedGoogle Scholar
  118. Ramirez-Nino AM, D’Souza MS, Markou A (2013) N-acetylcysteine decreased nicotine self-administration and cue-induced reinstatement of nicotine seeking in rats: comparison with the effects of N-acetylcysteine on food responding and food seeking. Psychopharmacology 225:473–482PubMedCentralPubMedGoogle Scholar
  119. Roose SP, Dalack GW, Glassman AH, Woodring S, Walsh BT, Giardina EG (1991) Is doxepin a safer tricyclic for the heart? J Clin Psychiatry 52:338–341PubMedGoogle Scholar
  120. Saccone NL, Culverhouse RC, Schwantes-An TH, Cannon DS, Chen X, Cichon S, Giegling I, Han S, Han Y, Keskitalo-Vuokko K, Kong X, Landi MT, Ma JZ, Short SE, Stephens SH, Stevens VL, Sun L, Wang Y, Wenzlaff AS, Aggen SH, Breslau N, Broderick P, Chatterjee N, Chen J, Heath AC, Heliovaara M, Hoft NR, Hunter DJ, Jensen MK, Martin NG, Montgomery GW, Niu T, Payne TJ, Peltonen L, Pergadia ML, Rice JP, Sherva R, Spitz MR, Sun J, Wang JC, Weiss RB, Wheeler W, Witt SH, Yang BZ, Caporaso NE, Ehringer MA, Eisen T, Gapstur SM, Gelernter J, Houlston R, Kaprio J, Kendler KS, Kraft P, Leppert MF, Li MD, Madden PA, Nothen MM, Pillai S, Rietschel M, Rujescu D, Schwartz A, Amos CI, Bierut LJ (2010) Multiple independent loci at chromosome 15q25.1 affect smoking quantity: a meta-analysis and comparison with lung cancer and COPD. PLoS Genet 6:e1001053Google Scholar
  121. Saccone SF, Hinrichs AL, Saccone NL, Chase GA, Konvicka K, Madden PA, Breslau N, Johnson EO, Hatsukami D, Pomerleau O, Swan GE, Goate AM, Rutter J, Bertelsen S, Fox L, Fugman D, Martin NG, Montgomery GW, Wang JC, Ballinger DG, Rice JP, Bierut LJ (2007) Cholinergic nicotinic receptor genes implicated in a nicotine dependence association study targeting 348 candidate genes with 3713 SNPs. Hum Mol Genet 16:36–49PubMedCentralPubMedGoogle Scholar
  122. Salas R, Main A, Gangitano D, De Biasi M (2007) Decreased withdrawal symptoms but normal tolerance to nicotine in mice null for the alpha7 nicotinic acetylcholine receptor subunit. Neuropharmacology 53:863–869PubMedCentralPubMedGoogle Scholar
  123. Scherma M, Panlilio LV, Fadda P, Fattore L, Gamaleddin I, Le Foll B, Justinova Z, Mikics E, Haller J, Medalie J, Stroik J, Barnes C, Yasar S, Tanda G, Piomelli D, Fratta W, Goldberg SR (2008) 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 327:482–490PubMedCentralPubMedGoogle Scholar
  124. Schlicker E, Kathmann M (2001) Modulation of transmitter release via presynaptic cannabinoid receptors. Trends Pharmacol Sci 22:565–572PubMedGoogle Scholar
  125. Scott D, Hiroi N (2011) Deconstructing craving: dissociable cortical control of cue reactivity in nicotine addiction. Biol Psychiatry 69:1052–1059PubMedCentralPubMedGoogle Scholar
  126. See RE, Fuchs RA, Ledford CC, McLaughlin J (2003) Drug addiction, relapse, and the amygdala. Ann N Y Acad Sci 985:294–307PubMedGoogle Scholar
  127. Shaham Y, Shalev U, Lu L, De Wit H, Stewart J (2003) The reinstatement model of drug relapse: history, methodology and major findings. Psychopharmacology 168:3–20PubMedGoogle Scholar
  128. Shoaib M (2008) The cannabinoid antagonist AM251 attenuates nicotine self-administration and nicotine-seeking behaviour in rats. Neuropharmacology 54:438–44Google Scholar
  129. Slemmer JE, Martin BR, Damaj MI (2000) Bupropion is a nicotinic antagonist. J Pharmacol Exp Ther 295:321–327PubMedGoogle Scholar
  130. Stabl M, Biziere K, Schmid-Burgk W, Amrein R (1989) Review of comparative clinical trials. Moclobemide vs tricyclic antidepressants and vs placebo in depressive states. J Neural Transm 28:77–89Google Scholar
  131. Stoker AK, Olivier B, Markou A (2012) Role of alpha7- and beta4-containing nicotinic acetylcholine receptors in the affective and somatic aspects of nicotine withdrawal: studies in knockout mice. Behav Genet 42:423–436PubMedCentralPubMedGoogle Scholar
  132. Stolerman IP, Jarvis MJ (1995) The scientific case that nicotine is addictive. Psychopharmacology 117: 2–10:14–20Google Scholar
  133. Tanda G, Pontieri FE, Di Chiara G (1997) Cannabinoid and heroin activation of mesolimbic dopamine transmission by a common mu1 opioid receptor mechanism. Science 276:2048–2050PubMedGoogle Scholar
  134. Thompson GH, Hunter DA (1998) Nicotine replacement therapy. Ann Pharmacother 32:1067–1075PubMedGoogle Scholar
  135. Uslaner JM, Smith SM, Huszar SL, Pachmerhiwala R, Hinchliffe RM, Vardigan JD, Nguyen SJ, Surles NO, Yao L, Barrow JC, Uebele VN, Renger JJ, Clark J, Hutson PH (2012) T-type calcium channel antagonism produces antipsychotic-like effects and reduces stimulant-induced glutamate release in the nucleus accumbens of rats. Neuropharmacology 62:1413–1421PubMedGoogle Scholar
  136. Uslaner JM, Vardigan JD, Drott JM, Uebele VN, Renger JJ, Lee A, Li Z, Le AD, Hutson PH (2010) T-type calcium channel antagonism decreases motivation for nicotine and blocks nicotine- and cue-induced reinstatement for a response previously reinforced with nicotine. Biol Psychiatry 68:712–718PubMedGoogle Scholar
  137. Uslaner JM, Winrow CJ, Gotter AL, Roecker AJ, Coleman PJ, Hutson PH, Le AD, Renger JJ (2014) Selective orexin 2 receptor antagonism blocks cue-induced reinstatement, but not nicotine self-administration or nicotine-induced reinstatement. Behav Brain Res 269:61–5Google Scholar
  138. Vlachou S, Guery S, Froestl W, Banerjee D, Benedict J, Finn MG, Markou A (2011) Repeated administration of the GABAB receptor positive modulator BHF177 decreased nicotine self-administration, and acute administration decreased cue-induced reinstatement of nicotine seeking in rats. Psychopharmacology 215:117–128PubMedCentralPubMedGoogle Scholar
  139. Vlachou S, Markou A (2010) GABAB receptors in reward processes. Adv Pharmacol 58:315–371PubMedGoogle Scholar
  140. Volkow ND, Wang GJ, Telang F, Fowler JS, Logan J, Childress AR, Jayne M, Ma Y, Wong C (2006) Cocaine cues and dopamine in dorsal striatum: mechanism of craving in cocaine addiction. J Neurosci 26:6583–6588PubMedGoogle Scholar
  141. Wang JC, Cruchaga C, Saccone NL, Bertelsen S, Liu P, Budde JP, Duan W, Fox L, Grucza RA, Kern J, Mayo K, Reyes O, Rice J, Saccone SF, Spiegel N, Steinbach JH, Stitzel JA, Anderson MW, You M, Stevens VL, Bierut LJ, Goate AM (2009) Risk for nicotine dependence and lung cancer is conferred by mRNA expression levels and amino acid change in CHRNA5. Hum Mol Genet 18:3125–3135PubMedCentralPubMedGoogle Scholar
  142. West R, Baker CL, Cappelleri JC, Bushmakin AG (2008) Effect of varenicline and bupropion SR on craving, nicotine withdrawal symptoms, and rewarding effects of smoking during a quit attempt. Psychopharmacology 197:371–377PubMedGoogle Scholar
  143. Wise RA (2009) Ventral tegmental glutamate: a role in stress-, cue-, and cocaine-induced reinstatement of cocaine-seeking. Neuropharmacology 56:174–176PubMedCentralPubMedGoogle Scholar
  144. Wouda JA, Riga D, De Vries W, Stegeman M, van Mourik Y, Schetters D, Schoffelmeer AN, Pattij T, De Vries TJ (2011) Varenicline attenuates cue-induced relapse to alcohol, but not nicotine seeking, while reducing inhibitory response control. Psychopharmacology 216:267–277PubMedCentralPubMedGoogle Scholar
  145. Yan Y, Pushparaj A, Le Strat Y, Gamaleddin I, Barnes C, Justinova Z, Goldberg SR, Le Foll B (2013) Blockade of dopamine d4 receptors attenuates reinstatement of extinguished nicotine-seeking behavior in rats. Neuropsychopharmacology 37:685–696Google Scholar

Copyright information

© Springer International Publishing Switzerland 2015

Authors and Affiliations

  1. 1.Department of Psychiatry, School of MedicineUniversity of California San DiegoLa JollaUSA
  2. 2.Department of Pharmacology and Systems TherapeuticsIcahn School of Medicine at Mount SinaiNew YorkUSA
  3. 3.Department of Psychiatry, M/C 0603, School of MedicineUniversity of California San DiegoLa JollaUSA

Personalised recommendations