Skip to main content
SpringerLink
Log in
Book cover

The Neuropharmacology of Alcohol pp 187–212Cite as

Molecular, Neuronal, and Behavioral Effects of Ethanol and Nicotine Interactions

  • Chapter
  • First Online:

Part of the book series: Handbook of Experimental Pharmacology ((HEP,volume 248))

Abstract

Ethanol and nicotine can modulate the activity of several neurotransmitter systems and signalling pathways. Interactions between ethanol and nicotine can also occur via common molecular targets including nicotinic acetylcholine receptors (nAChRs). These effects can induce molecular and synaptic adaptations that over time, are consolidated in brain circuits that reinforce drug-seeking behavior, contribute to the development of withdrawal symptoms during abstinence and increase the susceptibility to relapse. This chapter will discuss the acute and chronic effects of ethanol and nicotine within the mesolimbic reward pathway and brain circuits involved in learning, memory, and withdrawal. Individual and common molecular targets of ethanol and nicotine within these circuits are also discussed. Finally, we review studies that have identified potential molecular and neuronal processes underlying the high incidence of ethanol and nicotine co-use that may contribute to the development of ethanol and nicotine co-addiction.

This is a preview of subscription content, log in via an institution.

Chapter
USD   29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD   189.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Hardcover Book
USD   249.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Learn about institutional subscriptions

References

  • Aistrup GL, Marszalec W, Narahashi T (1999) Ethanol modulation of nicotinic acetylcholine receptor currents in cultured cortical neurons. Mol Pharmacol 55:39–49

    CAS  PubMed  Google Scholar 

  • Balfour DJ (2009) The neuronal pathways mediating the behavioral and addictive properties of nicotine. Handb Exp Pharmacol 209–233

    Google Scholar 

  • Bechtholt AJ, Cunningham CL (2005) Ethanol-induced conditioned place preference is expressed through a ventral tegmental area dependent mechanism. Behav Neurosci 119:213–223

    CAS  PubMed  Google Scholar 

  • Benowitz NL (2003) Basic cardiovascular research and its implications for the medicinal use of nicotine. J Am Coll Cardiol 41:497–498

    PubMed  Google Scholar 

  • Benowitz NL (2008) Neurobiology of nicotine addiction: implications for smoking cessation treatment. Am J Med 121:S3–S10

    CAS  PubMed  Google Scholar 

  • Bernier BE, Whitaker LR, Morikawa H (2011) Previous ethanol experience enhances synaptic plasticity of NMDA receptors in the ventral tegmental area. J Neurosci 31:5205–5212

    CAS  PubMed  PubMed Central  Google Scholar 

  • Bhandage AK, Jin Z, Bazov I, Kononenko O, Bakalkin G, Korpi ER, Birnir B (2014) GABA-A and NMDA receptor subunit mRNA expression is altered in the caudate but not the putamen of the postmortem brains of alcoholics. Front Cell Neurosci 8(415)

    Google Scholar 

  • Bierut LJ, Stitzel JA, Wang JC, Hinrichs AL, Grucza RA, Xuei X, Saccone NL, Saccone SF, Bertelsen S, Fox L, Horton WJ, Breslau N, Budde J, Cloninger CR, Dick DM, Foroud T, Hatsukami D, Hesselbrock V, Johnson EO, Kramer J, Kuperman S, Madden PA, Mayo K, Nurnberger J Jr, Pomerleau O, Porjesz B, Reyes O, Schuckit M, Swan G, Tischfield JA, Edenberg HJ, Rice JP, Goate AM (2008) Variants in nicotinic receptors and risk for nicotine dependence. Am J Psychiatry 165:1163–1171

    PubMed  PubMed Central  Google Scholar 

  • Blomqvist O, Soderpalm B, Engel JA (1992) Ethanol-induced locomotor activity: involvement of central nicotinic acetylcholine receptors? Brain Res Bull 29:173–178

    CAS  PubMed  Google Scholar 

  • Bobo JK (1992) Nicotine dependence and alcoholism epidemiology and treatment. J Psychoactive Drugs 24:123–129

    CAS  PubMed  Google Scholar 

  • Bobo JK, Husten C (2000) Sociocultural influences on smoking and drinking. Alcohol Res Health 24:225–232

    CAS  PubMed  Google Scholar 

  • Carboni E, Bortone L, Giua C, Di Chiara G (2000) Dissociation of physical abstinence signs from changes in extracellular dopamine in the nucleus accumbens and in the prefrontal cortex of nicotine dependent rats. Drug Alcohol Depend 58:93–102

    CAS  PubMed  Google Scholar 

  • Champtiaux N, Gotti C, Cordero-Erausquin M, David DJ, Przybylski C, Lena C, Clementi F, Moretti M, Rossi FM, Le Novere N, Mcintosh JM, Gardier AM, Changeux JP (2003) Subunit composition of functional nicotinic receptors in dopaminergic neurons investigated with knock-out mice. J Neurosci 23:7820–7829

    CAS  PubMed  Google Scholar 

  • Changeux JP, Bertrand D, Corringer PJ, Dehaene S, Edelstein S, Lena C, Le Novere N, Marubio L, Picciotto M, Zoli M (1998) Brain nicotinic receptors: structure and regulation, role in learning and reinforcement. Brain Res Brain Res Rev 26:198–216

    CAS  PubMed  Google Scholar 

  • Chatterjee S, Bartlett SE (2010) Neuronal nicotinic acetylcholine receptors as pharmacotherapeutic targets for the treatment of alcohol use disorders. CNS Neurol Disord Drug Targets 9:60–76

    CAS  PubMed  PubMed Central  Google Scholar 

  • Clark A, Lindgren S, Brooks SP, Watson WP, Little HJ (2001) Chronic infusion of nicotine can increase operant self-administration of alcohol. Neuropharmacology 41:108–117

    CAS  PubMed  Google Scholar 

  • Clarke RB, Adermark L (2010) Acute ethanol treatment prevents endocannabinoid-mediated long-lasting disinhibition of striatal output. Neuropharmacology 58:799–805

    CAS  PubMed  Google Scholar 

  • 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 30:145–155

    CAS  PubMed  Google Scholar 

  • Cohen A, Treweek J, Edwards S, Leao RM, Schulteis G, Koob GF, George O (2015) Extended access to nicotine leads to a CRF1 receptor dependent increase in anxiety-like behavior and hyperalgesia in rats. Addict Biol 20:56–68

    CAS  PubMed  Google Scholar 

  • Collins AC, Wilkins LH, Slobe BS, Cao JZ, Bullock AE (1996) Long-term ethanol and nicotine treatment elicit tolerance to ethanol. Alcohol Clin Exp Res 20:990–999

    CAS  PubMed  Google Scholar 

  • Couey JJ, Meredith RM, Spijker S, Poorthuis RB, Smit AB, Brussaard AB, Mansvelder HD (2007) Distributed network actions by nicotine increase the threshold for spike-timing-dependent plasticity in prefrontal cortex. Neuron 54:73–87

    CAS  PubMed  Google Scholar 

  • Crombag HS, Bossert JM, Koya E, Shaham Y (2008) Review. Context-induced relapse to drug seeking: a review. Philos Trans R Soc Lond Ser B Biol Sci 363:3233–3243

    Google Scholar 

  • Dajas-Bailador F, Wonnacott S (2004) Nicotinic acetylcholine receptors and the regulation of neuronal signalling. Trends Pharmacol Sci 25:317–324

    CAS  PubMed  Google Scholar 

  • Dar MS, Li C, Bowman ER (1993) Central behavioral interactions between ethanol, (−)-nicotine, and (−)-cotinine in mice. Brain Res Bull 32:23–28

    CAS  PubMed  Google Scholar 

  • Dar MS, Bowman ER, Li C (1994) Intracerebellar nicotinic-cholinergic participation in the cerebellar adenosinergic modulation of ethanol-induced motor incoordination in mice. Brain Res 644:117–127

    CAS  PubMed  Google Scholar 

  • De Biasi M, Dani JA (2011) Reward, addiction, withdrawal to nicotine. Annu Rev Neurosci 34:105–130

    PubMed  PubMed Central  Google Scholar 

  • De Fiebre CM, Collins AC (1993) A comparison of the development of tolerance to ethanol and cross-tolerance to nicotine after chronic ethanol treatment in long- and short-sleep mice. J Pharmacol Exp Ther 266:1398–1406

    PubMed  Google Scholar 

  • Difranza JR, Guerrera MP (1990) Alcoholism and smoking. J Stud Alcohol 51:130–135

    CAS  PubMed  Google Scholar 

  • Dopico AM, Lovinger DM (2009) Acute alcohol action and desensitization of ligand-gated ion channels. Pharmacol Rev 61:98–114

    CAS  PubMed  PubMed Central  Google Scholar 

  • 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 52:263–269

    CAS  PubMed  Google Scholar 

  • Ericson M, Molander A, Lof E, Engel JA, Soderpalm B (2003) Ethanol elevates accumbal dopamine levels via indirect activation of ventral tegmental nicotinic acetylcholine receptors. Eur J Pharmacol 467:85–93

    CAS  PubMed  Google Scholar 

  • Feduccia AA, Chatterjee S, Bartlett SE (2012) Neuronal nicotinic acetylcholine receptors: neuroplastic changes underlying alcohol and nicotine addictions. Front Mol Neurosci 5(83)

    Google Scholar 

  • Feduccia AA, Simms JA, Mill D, Yi HY, Bartlett SE (2014) Varenicline decreases ethanol intake and increases dopamine release via neuronal nicotinic acetylcholine receptors in the nucleus accumbens. Br J Pharmacol 171:3420–3431

    CAS  PubMed  PubMed Central  Google Scholar 

  • Flatscher-Bader T, Zuvela N, Landis N, Wilce PA (2008) Smoking and alcoholism target genes associated with plasticity and glutamate transmission in the human ventral tegmental area. Hum Mol Genet 17:38–51

    CAS  PubMed  Google Scholar 

  • Flores CM, Rogers SW, Pabreza LA, Wolfe BB, Kellar KJ (1992) A subtype of nicotinic cholinergic receptor in rat brain is composed of alpha 4 and beta 2 subunits and is up-regulated by chronic nicotine treatment. Mol Pharmacol 41:31–37

    CAS  PubMed  Google Scholar 

  • Floyd DW, Jung KY, Mccool BA (2003) Chronic ethanol ingestion facilitates N-methyl-D-aspartate receptor function and expression in rat lateral/basolateral amygdala neurons. J Pharmacol Exp Ther 307:1020–1029

    CAS  PubMed  Google Scholar 

  • Ford MM, Mccracken AD, Davis NL, Ryabinin AE, Grant KA (2012) Discrimination of ethanol-nicotine drug mixtures in mice: dual interactive mechanisms of overshadowing and potentiation. Psychopharmacology 224:537–548

    CAS  PubMed  PubMed Central  Google Scholar 

  • Ford MM, Davis NL, Mccracken AD, Grant KA (2013) Contribution of NMDA glutamate and nicotinic acetylcholine receptor mechanisms in the discrimination of ethanol-nicotine mixtures. Behav Pharmacol 24:617–622

    CAS  PubMed  PubMed Central  Google Scholar 

  • Forget B, Hamon M, Thiebot MH (2009) Involvement of alpha1-adrenoceptors in conditioned place preference supported by nicotine in rats. Psychopharmacology 205:503–515

    CAS  PubMed  Google Scholar 

  • Forman SA, Zhou Q (1999) Novel modulation of a nicotinic receptor channel mutant reveals that the open state is stabilized by ethanol. Mol Pharmacol 55:102–108

    CAS  PubMed  Google Scholar 

  • Fowler CD, Kenny PJ (2014) Nicotine aversion: neurobiological mechanisms and relevance to tobacco dependence vulnerability. Neuropharmacology 76(Pt B):533–544

    CAS  PubMed  Google Scholar 

  • Fu Y, Matta SG, Gao W, Sharp BM (2000) Local alpha-bungarotoxin-sensitive nicotinic receptors in the nucleus accumbens modulate nicotine-stimulated dopamine secretion in vivo. Neuroscience 101:369–375

    CAS  PubMed  Google Scholar 

  • Fujii S, Jia Y, Yang A, Sumikawa K (2000) Nicotine reverses GABAergic inhibition of long-term potentiation induction in the hippocampal CA1 region. Brain Res 863:259–265

    CAS  PubMed  Google Scholar 

  • Funk CK, Zorrilla EP, Lee MJ, Rice KC, Koob GF (2007) Corticotropin-releasing factor 1 antagonists selectively reduce ethanol self-administration in ethanol-dependent rats. Biol Psychiatry 61:78–86

    CAS  PubMed  Google Scholar 

  • George O, Ghozland S, Azar MR, Cottone P, Zorrilla EP, Parsons LH, O’dell LE, Richardson HN, Koob GF (2007) CRF-CRF1 system activation mediates withdrawal-induced increases in nicotine self-administration in nicotine-dependent rats. Proc Natl Acad Sci U S A 104:17198–17203

    CAS  PubMed  PubMed Central  Google Scholar 

  • 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 U S A 110:9124–9129

    CAS  PubMed  PubMed Central  Google Scholar 

  • Glover EJ, Mcdougle MJ, Siegel GS, Jhou TC, Chandler LJ (2016) Role for the rostromedial tegmental nucleus in signaling the aversive properties of alcohol. Alcohol Clin Exp Res 40:1651–1661

    CAS  PubMed  PubMed Central  Google Scholar 

  • Gotti C, Moretti M, Gaimarri A, Zanardi A, Clementi F, Zoli M (2007) Heterogeneity and complexity of native brain nicotinic receptors. Biochem Pharmacol 74:1102–1111

    CAS  PubMed  Google Scholar 

  • Gould TJ, Lommock JA (2003) Nicotine enhances contextual fear conditioning and ameliorates ethanol-induced deficits in contextual fear conditioning. Behav Neurosci 117:1276–1282

    CAS  PubMed  Google Scholar 

  • Gould TJ, Collins AC, Wehner JM (2001) Nicotine enhances latent inhibition and ameliorates ethanol-induced deficits in latent inhibition. Nicotine Tob Res 3:17–24

    CAS  PubMed  Google Scholar 

  • Grady SR, Moretti M, Zoli M, Marks MJ, Zanardi A, Pucci L, Clementi F, Gotti C (2009) Rodent habenulo-interpeduncular pathway expresses a large variety of uncommon nAChR subtypes, but only the alpha3beta4* and alpha3beta3beta4* subtypes mediate acetylcholine release. J Neurosci 29:2272–2282

    CAS  PubMed  PubMed Central  Google Scholar 

  • Grant BF, Hasin DS, Chou SP, Stinson FS, Dawson DA (2004) Nicotine dependence and psychiatric disorders in the United States: results from the national epidemiologic survey on alcohol and related conditions. Arch Gen Psychiatry 61:1107–1115

    PubMed  Google Scholar 

  • Gray R, Rajan AS, Radcliffe KA, Yakehiro M, Dani JA (1996) Hippocampal synaptic transmission enhanced by low concentrations of nicotine. Nature 383:713–716

    CAS  PubMed  Google Scholar 

  • Gremel CM, Cunningham CL (2008) Roles of the nucleus accumbens and amygdala in the acquisition and expression of ethanol-conditioned behavior in mice. J Neurosci 28:1076–1084

    CAS  PubMed  Google Scholar 

  • Gremel CM, Cunningham CL (2009) Involvement of amygdala dopamine and nucleus accumbens NMDA receptors in ethanol-seeking behavior in mice. Neuropsychopharmacology 34:1443–1453

    CAS  PubMed  Google Scholar 

  • Gremel CM, Cunningham CL (2010) Effects of disconnection of amygdala dopamine and nucleus accumbens N-methyl-d-aspartate receptors on ethanol-seeking behavior in mice. Eur J Neurosci 31:148–155

    PubMed  Google Scholar 

  • Grieder TE, George O, Tan H, George SR, Le Foll B, Laviolette SR, van der Kooy D (2012) Phasic D1 and tonic D2 dopamine receptor signaling double dissociate the motivational effects of acute nicotine and chronic nicotine withdrawal. Proc Natl Acad Sci U S A 109:3101–3106

    CAS  PubMed  PubMed Central  Google Scholar 

  • Grieder TE, Herman MA, Contet C, Tan LA, Vargas-Perez H, Cohen A, Chwalek M, Maal-Bared G, Freiling J, Schlosburg JE, Clarke L, Crawford E, Koebel P, Repunte-Canonigo V, Sanna PP, Tapper AR, Roberto M, Kieffer BL, Sawchenko PE, Koob GF, van der Kooy D, George O (2014) VTA CRF neurons mediate the aversive effects of nicotine withdrawal and promote intake escalation. Nat Neurosci 17:1751–1758

    CAS  PubMed  PubMed Central  Google Scholar 

  • Guildford MJ, Sacino AV, Tapper AR (2016) Modulation of ethanol reward sensitivity by nicotinic acetylcholine receptors containing the α6 subunit. Alcohol 57:65–70

    CAS  PubMed  PubMed Central  Google Scholar 

  • Haller G, Kapoor M, Budde J, Xuei X, Edenberg H, Nurnberger J, Kramer J, Brooks A, Tischfield J, Almasy L, Agrawal A, Bucholz K, Rice J, Saccone N, Bierut L, Goate A (2014) Rare missense variants in CHRNB3 and CHRNA3 are associated with risk of alcohol and cocaine dependence. Hum Mol Genet 23:810–819

    CAS  PubMed  Google Scholar 

  • Hashemizadeh S, Sardari M, Rezayof A (2014) Basolateral amygdala CB1 cannabinoid receptors mediate nicotine-induced place preference. Prog Neuro-Psychopharmacol Biol Psychiatry 51:65–71

    CAS  Google Scholar 

  • Hauser SR, Getachew B, Oster SM, Dhaher R, Ding ZM, Bell RL, Mcbride WJ, Rodd ZA (2012) Nicotine modulates alcohol-seeking and relapse by alcohol-preferring (P) rats in a time-dependent manner. Alcohol Clin Exp Res 36:43–54

    CAS  PubMed  Google Scholar 

  • Henderson BJ, Srinivasan R, Nichols WA, Dilworth CN, Gutierrez DF, Mackey ED, Mckinney S, Drenan RM, Richards CI, Lester HA (2014) Nicotine exploits a COPI-mediated process for chaperone-mediated up-regulation of its receptors. J Gen Physiol 143:51–66

    CAS  PubMed  PubMed Central  Google Scholar 

  • Hendrickson LM, Zhao-Shea R, Pang X, Gardner PD, Tapper AR (2010) Activation of alpha4* nAChRs is necessary and sufficient for varenicline-induced reduction of alcohol consumption. J Neurosci 30:10169–10176

    CAS  PubMed  PubMed Central  Google Scholar 

  • Hendrickson LM, Guildford MJ, Tapper AR (2013) Neuronal nicotinic acetylcholine receptors: common molecular substrates of nicotine and alcohol dependence. Front Psych 4(29)

    Google Scholar 

  • Herman MA, Contet C, Justice NJ, Vale W, Roberto M (2013) Novel subunit-specific tonic GABA currents and differential effects of ethanol in the central amygdala of CRF receptor-1 reporter mice. J Neurosci 33:3284–3298

    CAS  PubMed  PubMed Central  Google Scholar 

  • Hernandez CM, Terry AV Jr (2005) Repeated nicotine exposure in rats: effects on memory function, cholinergic markers and nerve growth factor. Neuroscience 130:997–1012

    CAS  PubMed  Google Scholar 

  • Hildebrand BE, Nomikos GG, Hertel P, Schilstrom B, Svensson TH (1998) Reduced dopamine output in the nucleus accumbens but not in the medial prefrontal cortex in rats displaying a mecamylamine-precipitated nicotine withdrawal syndrome. Brain Res 779:214–225

    CAS  PubMed  Google Scholar 

  • Howard EC, Schier CJ, Wetzel JS, Gonzales RA (2009) The dopamine response in the nucleus accumbens core-shell border differs from that in the core and shell during operant ethanol self-administration. Alcohol Clin Exp Res 33:1355–1365

    CAS  PubMed  PubMed Central  Google Scholar 

  • Huang YY, Kandel ER, Levine A (2008) Chronic nicotine exposure induces a long-lasting and pathway-specific facilitation of LTP in the amygdala. Learn Mem 15:603–610

    PubMed  PubMed Central  Google Scholar 

  • Hwang BH, Suzuki R, Lumeng L, Li TK, Mcbride WJ (2004) Innate differences in neuropeptide Y (NPY) mRNA expression in discrete brain regions between alcohol-preferring (P) and -nonpreferring (NP) rats: a significantly low level of NPY mRNA in dentate gyrus of the hippocampus and absence of NPY mRNA in the medial habenular nucleus of P rats. Neuropeptides 38:359–368

    CAS  PubMed  Google Scholar 

  • 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 325:302–312

    CAS  PubMed  Google Scholar 

  • Jackson KJ, Mcintosh JM, Brunzell DH, Sanjakdar SS, Damaj MI (2009) The role of alpha6-containing nicotinic acetylcholine receptors in nicotine reward and withdrawal. J Pharmacol Exp Ther 331:547–554

    CAS  PubMed  PubMed Central  Google Scholar 

  • Jackson KJ, Sanjakdar SS, Muldoon PP, Mcintosh JM, Damaj MI (2013) The alpha3beta4* nicotinic acetylcholine receptor subtype mediates nicotine reward and physical nicotine withdrawal signs independently of the alpha5 subunit in the mouse. Neuropharmacology 70:228–235

    CAS  PubMed  PubMed Central  Google Scholar 

  • Jamal M, Ameno K, Miki T, Wang W, Kumihashi M, Isse T, Kawamoto T, Kitagawa K, Nakayama K, Ijiri I, Kinoshita H (2009) Cholinergic alterations following alcohol exposure in the frontal cortex of Aldh2-deficient mice models. Brain Res 1295:37–43

    CAS  PubMed  Google Scholar 

  • Jerlhag E, Grotli M, Luthman K, Svensson L, Engel JA (2006) Role of the subunit composition of central nicotinic acetylcholine receptors for the stimulatory and dopamine-enhancing effects of ethanol. Alcohol Alcohol 41:486–493

    CAS  PubMed  Google Scholar 

  • Ji D, Dani JA (2000) Inhibition and disinhibition of pyramidal neurons by activation of nicotinic receptors on hippocampal interneurons. J Neurophysiol 83:2682–2690

    CAS  PubMed  Google Scholar 

  • Jiang L, Role LW (2008) Facilitation of cortico-amygdala synapses by nicotine: activity-dependent modulation of glutamatergic transmission. J Neurophysiol 99:1988–1999

    CAS  PubMed  PubMed Central  Google Scholar 

  • Jin Z, Bazov I, Kononenko O, Korpi ER, Bakalkin G, Birnir B (2011) Selective changes of GABA(A) channel subunit mRNAs in the hippocampus and orbitofrontal cortex but not in prefrontal cortex of human alcoholics. Front Cell Neurosci 5:30

    CAS  PubMed  Google Scholar 

  • Jin Z, Bhandage AK, Bazov I, Kononenko O, Bakalkin G, Korpi ER, Birnir B (2014a) Expression of specific ionotropic glutamate and GABA-A receptor subunits is decreased in central amygdala of alcoholics. Front Cell Neurosci 8(288)

    Google Scholar 

  • Jin Z, Bhandage AK, Bazov I, Kononenko O, Bakalkin G, Korpi ER, Birnir B (2014b) Selective increases of AMPA, NMDA, and kainate receptor subunit mRNAs in the hippocampus and orbitofrontal cortex but not in prefrontal cortex of human alcoholics. Front Cell Neurosci 8(11)

    Google Scholar 

  • Kash TL, Baucum AJ 2nd, Conrad KL, Colbran RJ, Winder DG (2009) Alcohol exposure alters NMDAR function in the bed nucleus of the stria terminalis. Neuropsychopharmacology 34:2420–2429

    CAS  PubMed  PubMed Central  Google Scholar 

  • 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 13:181–190

    CAS  PubMed  Google Scholar 

  • Kleijn J, Folgering JH, van der Hart MC, Rollema H, Cremers TI, Westerink BH (2011) Direct effect of nicotine on mesolimbic dopamine release in rat nucleus accumbens shell. Neurosci Lett 493:55–58

    CAS  PubMed  Google Scholar 

  • Klink R, de Kerchove D’exaerde A, Zoli M, Changeux JP (2001) Molecular and physiological diversity of nicotinic acetylcholine receptors in the midbrain dopaminergic nuclei. J Neurosci 21:1452–1463

    CAS  PubMed  Google Scholar 

  • Koob GF (2014) Neurocircuitry of alcohol addiction: synthesis from animal models. Handb Clin Neurol 125:33–54

    PubMed  Google Scholar 

  • Koob GF, Le Moal M (1997) Drug abuse: hedonic homeostatic dysregulation. Science 278:52–58

    CAS  PubMed  Google Scholar 

  • Koob GF, Volkow ND (2010) Neurocircuitry of addiction. Neuropsychopharmacology 35:217–238

    PubMed  Google Scholar 

  • Kouri EM, Mccarthy EM, Faust AH, Lukas SE (2004) Pretreatment with transdermal nicotine enhances some of ethanol’s acute effects in men. Drug Alcohol Depend 75:55–65

    CAS  PubMed  Google Scholar 

  • Kuner T, Schoepfer R, Korpi ER (1993) Ethanol inhibits glutamate-induced currents in heteromeric NMDA receptor subtypes. Neuroreport 5:297–300

    CAS  PubMed  Google Scholar 

  • Kuryatov A, Luo J, Cooper J, Lindstrom J (2005) Nicotine acts as a pharmacological chaperone to up-regulate human alpha4beta2 acetylcholine receptors. Mol Pharmacol 68:1839–1851

    CAS  PubMed  Google Scholar 

  • Kuzmin A, Jerlhag E, Liljequist S, Engel J (2009) Effects of subunit selective nACh receptors on operant ethanol self-administration and relapse-like ethanol-drinking behavior. Psychopharmacology 203:99–108

    CAS  PubMed  Google Scholar 

  • Läck AK, Diaz MR, Chappell A, DuBois DW, McCool BA (2007) Chronic ethanol and withdrawal differentially modulate pre- and postsynaptic function at glutamatergic synapses in rat basolateral amygdala. J Neurophysiol 98(6):3185–3196. Epub 2007 Sep 26

    PubMed  PubMed Central  Google Scholar 

  • Larsson A, Svensson L, Soderpalm B, Engel JA (2002) Role of different nicotinic acetylcholine receptors in mediating behavioral and neurochemical effects of ethanol in mice. Alcohol 28:157–167

    CAS  PubMed  Google Scholar 

  • Larsson A, Jerlhag E, Svensson L, Soderpalm B, Engel JA (2004) Is an alpha-conotoxin MII-sensitive mechanism involved in the neurochemical, stimulatory, and rewarding effects of ethanol? Alcohol 34:239–250

    CAS  PubMed  Google Scholar 

  • Laviolette SR, Alexson TO, van der Kooy D (2002) Lesions of the tegmental pedunculopontine nucleus block the rewarding effects and reveal the aversive effects of nicotine in the ventral tegmental area. J Neurosci 22:8653–8660

    CAS  PubMed  Google Scholar 

  • Law-Tho D, Desce JM, Crepel F (1995) Dopamine favours the emergence of long-term depression versus long-term potentiation in slices of rat prefrontal cortex. Neurosci Lett 188:125–128

    CAS  PubMed  Google Scholar 

  • Le AD, Corrigall WA, Harding JW, Juzytsch W, Li TK (2000) Involvement of nicotinic receptors in alcohol self-administration. Alcohol Clin Exp Res 24:155–163

    CAS  PubMed  Google Scholar 

  • Le AD, Wang A, Harding S, Juzytsch W, Shaham Y (2003) Nicotine increases alcohol self-administration and reinstates alcohol seeking in rats. Psychopharmacology 168:216–221

    CAS  PubMed  Google Scholar 

  • Leao RM, Cruz FC, Vendruscolo LF, De Guglielmo G, Logrip ML, Planeta CS, Hope BT, Koob GF, George O (2015) Chronic nicotine activates stress/reward-related brain regions and facilitates the transition to compulsive alcohol drinking. J Neurosci 35:6241–6253

    CAS  PubMed  PubMed Central  Google Scholar 

  • Lecca S, Melis M, Luchicchi A, Ennas MG, Castelli MP, Muntoni AL, Pistis M (2011) Effects of drugs of abuse on putative rostromedial tegmental neurons, inhibitory afferents to midbrain dopamine cells. Neuropsychopharmacology 36:589–602

    CAS  PubMed  Google Scholar 

  • 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 27:9077–9085

    CAS  PubMed  Google Scholar 

  • Lind PA, Macgregor S, Vink JM, Pergadia ML, Hansell NK, De Moor MH, Smit AB, Hottenga JJ, Richter MM, Heath AC, Martin NG, Willemsen G, De Geus EJ, Vogelzangs N, Penninx BW, Whitfield JB, Montgomery GW, Boomsma DI, Madden PA (2010) A genomewide association study of nicotine and alcohol dependence in Australian and Dutch populations. Twin Res Hum Genet 13:10–29

    PubMed  PubMed Central  Google Scholar 

  • 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 17:105–116

    CAS  PubMed  Google Scholar 

  • 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 21:153–160

    CAS  PubMed  PubMed Central  Google Scholar 

  • Liu L, Hendrickson LM, Guildford MJ, Zhao-Shea R, Gardner PD, Tapper AR (2013a) Nicotinic acetylcholine receptors containing the alpha4 subunit modulate alcohol reward. Biol Psychiatry 73:738–746

    CAS  PubMed  Google Scholar 

  • Liu L, Zhao-Shea R, Mcintosh JM, Tapper AR (2013b) Nicotinic acetylcholine receptors containing the alpha6 subunit contribute to ethanol activation of ventral tegmental area dopaminergic neurons. Biochem Pharmacol 86:1194–1200

    CAS  PubMed  Google Scholar 

  • Livingstone PD, Srinivasan J, Kew JN, Dawson LA, Gotti C, Moretti M, Shoaib M, Wonnacott S (2009) alpha7 and non-alpha7 nicotinic acetylcholine receptors modulate dopamine release in vitro and in vivo in the rat prefrontal cortex. Eur J Neurosci 29:539–550

    PubMed  Google Scholar 

  • Lobo IA, Harris RA (2008) GABA(A) receptors and alcohol. Pharmacol Biochem Behav 90:90–94

    CAS  PubMed  PubMed Central  Google Scholar 

  • Lof E, Olausson P, Debejczy A, Stomberg R, Mcintosh JM, Taylor JR, Soderpalm B (2007) Nicotinic acetylcholine receptors in the ventral tegmental area mediate the dopamine activating and reinforcing properties of ethanol cues. Psychopharmacology 195:333–343

    PubMed  Google Scholar 

  • Lotfipour S, Byun JS, Leach P, Fowler CD, Murphy NP, Kenny PJ, Gould TJ, Boulter J (2013) Targeted deletion of the mouse alpha2 nicotinic acetylcholine receptor subunit gene (Chrna2) potentiates nicotine-modulated behaviors. J Neurosci 33:7728–7741

    CAS  PubMed  Google Scholar 

  • Lovinger DM (1993) High ethanol sensitivity of recombinant AMPA-type glutamate receptors expressed in mammalian cells. Neurosci Lett 159:83–87

    CAS  PubMed  Google Scholar 

  • Lovinger DM, White G (1991) Ethanol potentiation of 5-hydroxytryptamine3 receptor-mediated ion current in neuroblastoma cells and isolated adult mammalian neurons. Mol Pharmacol 40:263–270

    CAS  PubMed  Google Scholar 

  • Lovinger DM, White G, Weight FF (1989) Ethanol inhibits NMDA-activated ion current in hippocampal neurons. Science 243:1721–1724

    CAS  PubMed  Google Scholar 

  • 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 50:911–921

    CAS  PubMed  Google Scholar 

  • Mansvelder HD, Mcgehee DS (2000) Long-term potentiation of excitatory inputs to brain reward areas by nicotine. Neuron 27:349–357

    CAS  PubMed  Google Scholar 

  • Mansvelder HD, De Rover M, Mcgehee DS, Brussaard AB (2003) Cholinergic modulation of dopaminergic reward areas: upstream and downstream targets of nicotine addiction. Eur J Pharmacol 480:117–123

    CAS  PubMed  Google Scholar 

  • Marshall DL, Redfern PH, Wonnacott S (1997) Presynaptic nicotinic modulation of dopamine release in the three ascending pathways studied by in vivo microdialysis: comparison of naive and chronic nicotine-treated rats. J Neurochem 68:1511–1519

    CAS  PubMed  Google Scholar 

  • Marubio LM, Gardier AM, Durier S, David D, Klink R, Arroyo-Jimenez MM, Mcintosh JM, Rossi F, Champtiaux N, Zoli M, Changeux JP (2003) Effects of nicotine in the dopaminergic system of mice lacking the alpha4 subunit of neuronal nicotinic acetylcholine receptors. Eur J Neurosci 17:1329–1337

    CAS  PubMed  Google Scholar 

  • Masood K, Wu C, Brauneis U, Weight FF (1994) Differential ethanol sensitivity of recombinant N-methyl-D-aspartate receptor subunits. Mol Pharmacol 45:324–329

    CAS  PubMed  Google Scholar 

  • Matsuyama S, Matsumoto A (2003) Epibatidine induces long-term potentiation (LTP) via activation of alpha4beta2 nicotinic acetylcholine receptors (nAChRs) in vivo in the intact mouse dentate gyrus: both alpha7 and alpha4beta2 nAChRs essential to nicotinic LTP. J Pharmacol Sci 93:180–187

    CAS  PubMed  Google Scholar 

  • Mccool BA, Frye GD, Pulido MD, Botting SK (2003) Effects of chronic ethanol consumption on rat GABA(A) and strychnine-sensitive glycine receptors expressed by lateral/basolateral amygdala neurons. Brain Res 963:165–177

    CAS  PubMed  PubMed Central  Google Scholar 

  • Mcdaid J, Abburi C, Wolfman SL, Gallagher K, Mcgehee DS (2016) Ethanol-induced motor impairment mediated by inhibition of alpha7 nicotinic receptors. J Neurosci 36:7768–7778

    CAS  PubMed  PubMed Central  Google Scholar 

  • Meredith GE, Blank B, Groenewegen HJ (1989) The distribution and compartmental organization of the cholinergic neurons in nucleus accumbens of the rat. Neuroscience 31:327–345

    CAS  PubMed  Google Scholar 

  • Merlo Pich E, Lorang M, Yeganeh M, Rodriguez De Fonseca F, Raber J, Koob GF, Weiss F (1995) Increase of extracellular corticotropin-releasing factor-like immunoreactivity levels in the amygdala of awake rats during restraint stress and ethanol withdrawal as measured by microdialysis. J Neurosci 15:5439–5447

    CAS  PubMed  Google Scholar 

  • Miller NS, Gold MS (1998) Comorbid cigarette and alcohol addiction: epidemiology and treatment. J Addict Dis 17:55–66

    CAS  PubMed  Google Scholar 

  • Morel C, Fattore L, Pons S, Hay YA, Marti F, Lambolez B, De Biasi M, Lathrop M, Fratta W, Maskos U, Faure P (2014) Nicotine consumption is regulated by a human polymorphism in dopamine neurons. Mol Psychiatry 19:930–936

    CAS  PubMed  Google Scholar 

  • Moykkynen T, Korpi ER, Lovinger DM (2003) Ethanol inhibits alpha-amino-3-hydyroxy-5-methyl-4-isoxazolepropionic acid (AMPA) receptor function in central nervous system neurons by stabilizing desensitization. J Pharmacol Exp Ther 306:546–555

    PubMed  Google Scholar 

  • Nashmi R, Xiao C, Deshpande P, Mckinney S, Grady SR, Whiteaker P, Huang Q, Mcclure-Begley T, Lindstrom JM, Labarca C, Collins AC, Marks MJ, Lester HA (2007) Chronic nicotine cell specifically upregulates functional alpha 4* nicotinic receptors: basis for both tolerance in midbrain and enhanced long-term potentiation in perforant path. J Neurosci 27:8202–8218

    CAS  PubMed  Google Scholar 

  • Navarrete F, Rodriguez-Arias M, Martin-Garcia E, Navarro D, Garcia-Gutierrez MS, Aguilar MA, Aracil-Fernandez A, Berbel P, Minarro J, Maldonado R, Manzanares J (2013) Role of CB2 cannabinoid receptors in the rewarding, reinforcing, and physical effects of nicotine. Neuropsychopharmacology 38:2515–2524

    CAS  PubMed  PubMed Central  Google Scholar 

  • Ngolab J, Liu L, Zhao-Shea R, Gao G, Gardner PD, Tapper AR (2015) Functional Upregulation of alpha4* nicotinic acetylcholine receptors in VTA GABAergic neurons increases sensitivity to nicotine reward. J Neurosci 35:8570–8578

    CAS  PubMed  PubMed Central  Google Scholar 

  • Nie Z, Schweitzer P, Roberts AJ, Madamba SG, Moore SD, Siggins GR (2004) Ethanol augments GABAergic transmission in the central amygdala via CRF1 receptors. Science 303:1512–1514

    CAS  PubMed  Google Scholar 

  • Nisell M, Nomikos GG, Svensson TH (1994) Systemic nicotine-induced dopamine release in the rat nucleus accumbens is regulated by nicotinic receptors in the ventral tegmental area. Synapse 16:36–44

    CAS  PubMed  Google Scholar 

  • Office of the Surgeon General (2016) Facing addiction in America: the surgeon General’s report on alcohol, drugs, and health. Washington, DC

    Google Scholar 

  • Olive MF, Koenig HN, Nannini MA, Hodge CW (2002) Elevated extracellular CRF levels in the bed nucleus of the stria terminalis during ethanol withdrawal and reduction by subsequent ethanol intake. Pharmacol Biochem Behav 72:213–220

    CAS  PubMed  Google Scholar 

  • Otani S, Blond O, Desce JM, Crepel F (1998) Dopamine facilitates long-term depression of glutamatergic transmission in rat prefrontal cortex. Neuroscience 85:669–676

    CAS  PubMed  Google Scholar 

  • Pang X, Liu L, Ngolab J, Zhao-Shea R, Mcintosh JM, Gardner PD, Tapper AR (2016) Habenula cholinergic neurons regulate anxiety during nicotine withdrawal via nicotinic acetylcholine receptors. Neuropharmacology 107:294–304

    CAS  PubMed  PubMed Central  Google Scholar 

  • Paolini M, De Biasi M (2011) Mechanistic insights into nicotine withdrawal. Biochem Pharmacol 82:996–1007

    CAS  PubMed  PubMed Central  Google Scholar 

  • Perez E, Quijano-Carde N, De Biasi M (2015) Nicotinic mechanisms modulate ethanol withdrawal and modify time course and symptoms severity of simultaneous withdrawal from alcohol and nicotine. Neuropsychopharmacology 40:2327–2336

    CAS  PubMed  PubMed Central  Google Scholar 

  • Perkins KA (1997) Combined effects of nicotine and alcohol on subjective, behavioral and physiological responses in humans. Addict Biol 2:255–268

    CAS  PubMed  Google Scholar 

  • Phelps PE, Houser CR, Vaughn JE (1985) Immunocytochemical localization of choline acetyltransferase within the rat neostriatum: a correlated light and electron microscopic study of cholinergic neurons and synapses. J Comp Neurol 238:286–307

    CAS  PubMed  Google Scholar 

  • Picciotto MR, Zoli M, Rimondini R, Lena C, Marubio LM, Pich EM, Fuxe K, Changeux JP (1998) Acetylcholine receptors containing the beta2 subunit are involved in the reinforcing properties of nicotine. Nature 391:173–177

    CAS  PubMed  Google Scholar 

  • Pina MM, Young EA, Ryabinin AE, Cunningham CL (2015) The bed nucleus of the stria terminalis regulates ethanol-seeking behavior in mice. Neuropharmacology 99:627–638

    CAS  PubMed  PubMed Central  Google Scholar 

  • Pons S, Fattore L, Cossu G, Tolu S, Porcu E, Mcintosh JM, Changeux JP, Maskos U, Fratta W (2008) Crucial role of alpha4 and alpha6 nicotinic acetylcholine receptor subunits from ventral tegmental area in systemic nicotine self-administration. J Neurosci 28:12318–12327

    CAS  PubMed  PubMed Central  Google Scholar 

  • Potthoff AD, Ellison G, Nelson L (1983) Ethanol intake increases during continuous administration of amphetamine and nicotine, but not several other drugs. Pharmacol Biochem Behav 18:489–493

    CAS  PubMed  Google Scholar 

  • Powers MS, Broderick HJ, Drenan RM, Chester JA (2013) Nicotinic acetylcholine receptors containing alpha6 subunits contribute to alcohol reward-related behaviours. Genes Brain Behav 12:543–553

    CAS  PubMed  PubMed Central  Google Scholar 

  • Rada P, Jensen K, Hoebel BG (2001) Effects of nicotine and mecamylamine-induced withdrawal on extracellular dopamine and acetylcholine in the rat nucleus accumbens. Psychopharmacology 157:105–110

    CAS  PubMed  Google Scholar 

  • Radcliffe KA, Dani JA (1998) Nicotinic stimulation produces multiple forms of increased glutamatergic synaptic transmission. J Neurosci 18:7075–7083

    CAS  PubMed  Google Scholar 

  • Rassnick S, Heinrichs SC, Britton KT, Koob GF (1993) Microinjection of a corticotropin-releasing factor antagonist into the central nucleus of the amygdala reverses anxiogenic-like effects of ethanol withdrawal. Brain Res 605(1):25–32

    CAS  PubMed  Google Scholar 

  • Roberto M, Madamba SG, Stouffer DG, Parsons LH, Siggins GR (2004a) Increased GABA release in the central amygdala of ethanol-dependent rats. J Neurosci 24:10159–10166

    CAS  PubMed  Google Scholar 

  • Roberto M, Schweitzer P, Madamba SG, Stouffer DG, Parsons LH, Siggins GR (2004b) Acute and chronic ethanol alter glutamatergic transmission in rat central amygdala: an in vitro and in vivo analysis. J Neurosci 24:1594–1603

    CAS  PubMed  Google Scholar 

  • Roberto M, Cruz MT, Gilpin NW, Sabino V, Schweitzer P, Bajo M, Cottone P, Madamba SG, Stouffer DG, Zorrilla EP, Koob GF, Siggins GR, Parsons LH (2010) Corticotropin releasing factor-induced amygdala gamma-aminobutyric acid release plays a key role in alcohol dependence. Biol Psychiatry 67:831–839

    CAS  PubMed  PubMed Central  Google Scholar 

  • Roberts AJ, Cole M, Koob GF (1996) Intra-amygdala muscimol decreases operant ethanol self-administration in dependent rats. Alcohol Clin Exp Res 20:1289–1298

    CAS  PubMed  Google Scholar 

  • Room R (2004) Smoking and drinking as complementary behaviours. Biomed Pharmacother 58:111–115

    PubMed  Google Scholar 

  • Salas R, Orr-Urtreger A, Broide RS, Beaudet A, Paylor R, De Biasi M (2003a) The nicotinic acetylcholine receptor subunit alpha 5 mediates short-term effects of nicotine in vivo. Mol Pharmacol 63:1059–1066

    CAS  PubMed  Google Scholar 

  • Salas R, Pieri F, Fung B, Dani JA, De Biasi M (2003b) Altered anxiety-related responses in mutant mice lacking the beta4 subunit of the nicotinic receptor. J Neurosci 23:6255–6263

    CAS  PubMed  Google Scholar 

  • Salas R, Pieri F, De Biasi M (2004) Decreased signs of nicotine withdrawal in mice null for the beta4 nicotinic acetylcholine receptor subunit. J Neurosci 24:10035–10039

    CAS  PubMed  Google Scholar 

  • Salas R, Sturm R, Boulter J, De Biasi M (2009) Nicotinic receptors in the habenulo-interpeduncular system are necessary for nicotine withdrawal in mice. J Neurosci 29:3014–3018

    CAS  PubMed  PubMed Central  Google Scholar 

  • Sallette J, Bohler S, Benoit P, Soudant M, Pons S, Le Novere N, Changeux JP, Corringer PJ (2004) An extracellular protein microdomain controls up-regulation of neuronal nicotinic acetylcholine receptors by nicotine. J Biol Chem 279:18767–18775

    CAS  PubMed  Google Scholar 

  • Sanjakdar SS, Maldoon PP, Marks MJ, Brunzell DH, Maskos U, Mcintosh JM, Bowers MS, Damaj MI (2015) Differential roles of alpha6beta2* and alpha4beta2* neuronal nicotinic receptors in nicotine- and cocaine-conditioned reward in mice. Neuropsychopharmacology 40:350–360

    CAS  PubMed  Google Scholar 

  • Sasco AJ, Secretan MB, Straif K (2004) Tobacco smoking and cancer: a brief review of recent epidemiological evidence. Lung Cancer 45(Suppl 2):S3–S9

    PubMed  Google Scholar 

  • Schilstrom B, Rawal N, Mameli-Engvall M, Nomikos GG, Svensson TH (2003) Dual effects of nicotine on dopamine neurons mediated by different nicotinic receptor subtypes. Int J Neuropsychopharmacol 6:1–11

    PubMed  Google Scholar 

  • Schlaepfer IR, Hoft NR, Collins AC, Corley RP, Hewitt JK, Hopfer CJ, Lessem JM, Mcqueen MB, Rhee SH, Ehringer MA (2008) The CHRNA5/A3/B4 gene cluster variability as an important determinant of early alcohol and tobacco initiation in young adults. Biol Psychiatry 63:1039–1046

    CAS  PubMed  Google Scholar 

  • Schoedel KA, Tyndale RF (2003) Induction of nicotine-metabolizing CYP2B1 by ethanol and ethanol-metabolizing CYP2E1 by nicotine: summary and implications. Biochim Biophys Acta 1619:283–290

    CAS  PubMed  Google Scholar 

  • Sharpe AL, Samson HH (2002) Repeated nicotine injections decrease operant ethanol self-administration. Alcohol 28:1–7

    CAS  PubMed  Google Scholar 

  • Shih PY, Engle SE, Oh G, Deshpande P, Puskar NL, Lester HA, Drenan RM (2014) Differential expression and function of nicotinic acetylcholine receptors in subdivisions of medial habenula. J Neurosci 34(29):9789–9802

    PubMed  PubMed Central  Google Scholar 

  • Smith BR, Horan JT, Gaskin S, Amit Z (1999) Exposure to nicotine enhances acquisition of ethanol drinking by laboratory rats in a limited access paradigm. Psychopharmacology 142:408–412

    CAS  PubMed  Google Scholar 

  • Srinivasan R, Pantoja R, Moss FJ, Mackey ED, Son CD, Miwa J, Lester HA (2011) Nicotine up-regulates alpha4beta2 nicotinic receptors and ER exit sites via stoichiometry-dependent chaperoning. J Gen Physiol 137:59–79

    CAS  PubMed  PubMed Central  Google Scholar 

  • Stuber GD, Hopf FW, Hahn J, Cho SL, Guillory A, Bonci A (2008) Voluntary ethanol intake enhances excitatory synaptic strength in the ventral tegmental area. Alcohol Clin Exp Res 32:1714–1720

    CAS  PubMed  PubMed Central  Google Scholar 

  • Tandon S, Keefe KA, Taha SA (2017) Excitation of lateral habenula neurons as a neural mechanism underlying ethanol-induced conditioned taste aversion. J Physiol 595:1393–1412

    CAS  PubMed  Google Scholar 

  • Tang J, Dani JA (2009) Dopamine enables in vivo synaptic plasticity associated with the addictive drug nicotine. Neuron 63:673–682

    CAS  PubMed  PubMed Central  Google Scholar 

  • Tapper AR, Mckinney SL, Nashmi R, Schwarz J, Deshpande P, Labarca C, Whiteaker P, Marks MJ, Collins AC, Lester HA (2004) Nicotine activation of alpha4* receptors: sufficient for reward, tolerance, and sensitization. Science 306:1029–1032

    CAS  PubMed  Google Scholar 

  • Tawa EA, Hall SD, Lohoff FW (2016) Overview of the genetics of alcohol use disorder. Alcohol Alcohol 51:507–514

    CAS  PubMed  PubMed Central  Google Scholar 

  • Theberge FR, Milton AL, Belin D, Lee JL, Everitt BJ (2010) The basolateral amygdala and nucleus accumbens core mediate dissociable aspects of drug memory reconsolidation. Learn Mem 17:444–453

    CAS  PubMed  PubMed Central  Google Scholar 

  • Thorgeirsson TE, Geller F, Sulem P, Rafnar T, Wiste A, Magnusson KP, Manolescu A, Thorleifsson G, Stefansson H, Ingason A, Stacey SN, Bergthorsson JT, Thorlacius S, Gudmundsson J, Jonsson T, Jakobsdottir M, Saemundsdottir J, Olafsdottir O, Gudmundsson LJ, Bjornsdottir G, Kristjansson K, Skuladottir H, Isaksson HJ, Gudbjartsson T, Jones GT, Mueller T, Gottsater A, Flex A, Aben KKH, De Vegt F, Mulders PFA, Isla D, Vidal MJ, Asin L, Saez B, Murillo L, Blondal T, Kolbeinsson H, Stefansson JG, Hansdottir I, Runarsdottir V, Pola R, Lindblad B, Van Rij AM, Dieplinger B, Haltmayer M, Mayordomo JI, Kiemeney LA, Matthiasson SE, Oskarsson H, Tyrfingsson T, Gudbjartsson DF, Gulcher JR, Jonsson S, Thorsteinsdottir U, Kong A, Stefansson K (2008) A variant associated with nicotine dependence, lung cancer and peripheral arterial disease. Nature 452:638–642

    CAS  PubMed  PubMed Central  Google Scholar 

  • Thorgeirsson TE, Gudbjartsson DF, Surakka I, Vink JM, Amin N, Geller F, Sulem P, Rafnar T, Esko T, Walter S, Gieger C, Rawal R, Mangino M, Prokopenko I, Magi R, Keskitalo K, Gudjonsdottir IH, Gretarsdottir S, Stefansson H, Thompson JR, Aulchenko YS, Nelis M, Aben KK, Den Heijer M, Dirksen A, Ashraf H, Soranzo N, Valdes AM, Steves C, Uitterlinden AG, Hofman A, Tonjes A, Kovacs P, Hottenga JJ, Willemsen G, Vogelzangs N, Doring A, Dahmen N, Nitz B, Pergadia ML, Saez B, De Diego V, Lezcano V, Garcia-Prats MD, Ripatti S, Perola M, Kettunen J, Hartikainen AL, Pouta A, Laitinen J, Isohanni M, Huei-Yi S, Allen M, Krestyaninova M, Hall AS, Jones GT, Van Rij AM, Mueller T, Dieplinger B, Haltmayer M, Jonsson S, Matthiasson SE, Oskarsson H, Tyrfingsson T, Kiemeney LA, Mayordomo JI, Lindholt JS, Pedersen JH, Franklin WA, Wolf H, Montgomery GW, Heath AC, Martin NG, Madden PA, Giegling I, Rujescu D, Jarvelin MR, Salomaa V, Stumvoll M, Spector TD, Wichmann HE, Metspalu A, Samani NJ, Penninx BW, Oostra BA, Boomsma DI, Tiemeier H, Van Duijn CM, Kaprio J, Gulcher JR, Consortium E, Mccarthy MI, Peltonen L, Thorsteinsdottir U, Stefansson K (2010) Sequence variants at CHRNB3-CHRNA6 and CYP2A6 affect smoking behavior. Nat Genet 42:448–453

    CAS  PubMed  PubMed Central  Google Scholar 

  • Tizabi Y, Copeland RL Jr, Louis VA, Taylor RE (2002) Effects of combined systemic alcohol and central nicotine administration into ventral tegmental area on dopamine release in the nucleus accumbens. Alcohol Clin Exp Res 26:394–399

    CAS  PubMed  Google Scholar 

  • Tizabi Y, Bai L, Copeland RL Jr, Taylor RE (2007) Combined effects of systemic alcohol and nicotine on dopamine release in the nucleus accumbens shell. Alcohol Alcohol 42:413–416

    CAS  PubMed  Google Scholar 

  • Tolu S, Eddine R, Marti F, David V, Graupner M, Pons S, Baudonnat M, Husson M, Besson M, Reperant C, Zemdegs J, Pages C, Hay YA, Lambolez B, Caboche J, Gutkin B, Gardier AM, Changeux JP, Faure P, Maskos U (2013) Co-activation of VTA DA and GABA neurons mediates nicotine reinforcement. Mol Psychiatry 18:382–393

    CAS  PubMed  Google Scholar 

  • Tolu S, Marti F, Morel C, Perrier C, Torquet N, Pons S, De Beaurepaire R, Faure P (2017) Nicotine enhances alcohol intake and dopaminergic responses through beta2* and beta4* nicotinic acetylcholine receptors. Sci Rep 7:45116

    CAS  PubMed  PubMed Central  Google Scholar 

  • Tritto T, Marley RJ, Bastidas D, Stitzel JA, Collins AC (2001) Potential regulation of nicotine and ethanol actions by alpha4-containing nicotinic receptors. Alcohol 24:69–78

    CAS  PubMed  Google Scholar 

  • Tumkosit P, Kuryatov A, Luo J, Lindstrom J (2006) Beta3 subunits promote expression and nicotine-induced up-regulation of human nicotinic alpha6* nicotinic acetylcholine receptors expressed in transfected cell lines. Mol Pharmacol 70:1358–1368

    CAS  PubMed  Google Scholar 

  • Turner JR, Castellano LM, Blendy JA (2011) Parallel anxiolytic-like effects and upregulation of neuronal nicotinic acetylcholine receptors following chronic nicotine and varenicline. Nicotine Tob Res 13:41–46

    CAS  PubMed  Google Scholar 

  • Unwin N (2003) Structure and action of the nicotinic acetylcholine receptor explored by electron microscopy. FEBS Lett 555:91–95

    CAS  PubMed  Google Scholar 

  • Valenzuela CF, Cardoso RA, Lickteig R, Browning MD, Nixon KM (1998) Acute effects of ethanol on recombinant kainate receptors: lack of role of protein phosphorylation. Alcohol Clin Exp Res 22:1292–1299

    CAS  PubMed  Google Scholar 

  • Walker BM, Ettenberg A (2007) Intracerebroventricular ethanol-induced conditioned place preferences are prevented by fluphenazine infusions into the nucleus accumbens of rats. Behav Neurosci 121:401–410

    CAS  PubMed  Google Scholar 

  • Walters CL, Brown S, Changeux JP, Martin B, Damaj MI (2006) The beta2 but not alpha7 subunit of the nicotinic acetylcholine receptor is required for nicotine-conditioned place preference in mice. Psychopharmacology 184:339–344

    CAS  PubMed  Google Scholar 

  • Wang F, Nelson ME, Kuryatov A, Olale F, Cooper J, Keyser K, Lindstrom J (1998) Chronic nicotine treatment up-regulates human alpha3 beta2 but not alpha3 beta4 acetylcholine receptors stably transfected in human embryonic kidney cells. J Biol Chem 273:28721–28732

    CAS  PubMed  Google Scholar 

  • Wang JC, Grucza R, Cruchaga C, Hinrichs AL, Bertelsen S, Budde JP, Fox L, Goldstein E, Reyes O, Saccone N, Saccone S, Xuei X, Bucholz K, Kuperman S, Nurnberger J Jr, Rice JP, Schuckit M, Tischfield J, Hesselbrock V, Porjesz B, Edenberg HJ, Bierut LJ, Goate AM (2009) Genetic variation in the CHRNA5 gene affects mRNA levels and is associated with risk for alcohol dependence. Mol Psychiatry 14:501–510

    CAS  PubMed  Google Scholar 

  • Warnock G, Prickaerts J, Thomas S (2006) Interactions between CRF and acetylcholine in the modulation of cognitive behaviour. In: Levin ED (ed) Neurotransmitter interactions and cognitive function. Birkhauser Verlag, Basel, Switzerland

    Google Scholar 

  • Welsby P, Rowan M, Anwyl R (2006) Nicotinic receptor-mediated enhancement of long-term potentiation involves activation of metabotropic glutamate receptors and ryanodine-sensitive calcium stores in the dentate gyrus. Eur J Neurosci 24:3109–3118

    PubMed  Google Scholar 

  • World Health Organization (2014) Global status report on alcohol and health, Geneva

    Google Scholar 

  • World Health Organization (2015) WHO global report on trends in prevalence of tobacco smoking, Geneva

    Google Scholar 

  • Xu H, Wang F, Kranzler HR, Gelernter J, Zhang H (2017) Alcohol and nicotine codependence-associated DNA methylation changes in promoter regions of addiction-related genes. Sci Rep 7:41816

    CAS  PubMed  PubMed Central  Google Scholar 

  • Yamazaki Y, Jia Y, Hamaue N, Sumikawa K (2005) Nicotine-induced switch in the nicotinic cholinergic mechanisms of facilitation of long-term potentiation induction. Eur J Neurosci 22:845–860

    PubMed  Google Scholar 

  • Yang J, Li MD (2016) Converging findings from linkage and association analyses on susceptibility genes for smoking and other addictions. Mol Psychiatry 21:992–1008

    CAS  PubMed  Google Scholar 

  • Yin HH, Park BS, Adermark L, Lovinger DM (2007) Ethanol reverses the direction of long-term synaptic plasticity in the dorsomedial striatum. Eur J Neurosci 25:3226–3232

    PubMed  Google Scholar 

  • Young EA, Dreumont SE, Cunningham CL (2014) Role of nucleus accumbens dopamine receptor subtypes in the learning and expression of alcohol-seeking behavior. Neurobiol Learn Mem 108:28–37

    CAS  PubMed  Google Scholar 

  • Zacny JP (1990) Behavioral aspects of alcohol-tobacco interactions. Recent Dev Alcohol 8:205–219

    CAS  PubMed  Google Scholar 

  • Zhang L, Dong Y, Doyon WM, Dani JA (2012) Withdrawal from chronic nicotine exposure alters dopamine signaling dynamics in the nucleus accumbens. Biol Psychiatry 71:184–191

    CAS  PubMed  Google Scholar 

  • Zhao-Shea R, Liu L, Soll LG, Improgo MR, Meyers EE, Mcintosh JM, Grady SR, Marks MJ, Gardner PD, Tapper AR (2011) Nicotine-mediated activation of dopaminergic neurons in distinct regions of the ventral tegmental area. Neuropsychopharmacology 36:1021–1032

    CAS  PubMed  PubMed Central  Google Scholar 

  • Zhao-Shea R, Liu L, Pang X, Gardner PD, Tapper AR (2013) Activation of GABAergic neurons in the interpeduncular nucleus triggers physical nicotine withdrawal symptoms. Curr Biol 23:2327–2335

    CAS  PubMed  Google Scholar 

  • Zhao-Shea R, Degroot SR, Liu L, Vallaster M, Pang X, Su Q, Gao G, Rando OJ, Martin GE, George O, Gardner PD, Tapper AR (2015) Increased CRF signalling in a ventral tegmental area-interpeduncular nucleus-medial habenula circuit induces anxiety during nicotine withdrawal. Nat Commun 6:6770

    CAS  PubMed  PubMed Central  Google Scholar 

  • Zhou FM, Wilson CJ, Dani JA (2002) Cholinergic interneuron characteristics and nicotinic properties in the striatum. J Neurobiol 53:590–605

    CAS  PubMed  Google Scholar 

  • Zorrilla EP, Logrip ML, Koob GF (2014) Corticotropin releasing factor: a key role in the neurobiology of addiction. Front Neuroendocrinol 35:234–244

    CAS  PubMed  PubMed Central  Google Scholar 

  • Zorumski CF, Mennerick S, Izumi Y (2014) Acute and chronic effects of ethanol on learning-related synaptic plasticity. Alcohol 48:1–17

    CAS  PubMed  Google Scholar 

  • Zuo Y, Yeh JZ, Narahashi T (2004) Octanol modulation of neuronal nicotinic acetylcholine receptor single channels. Alcohol Clin Exp Res 28:1648–1656

    CAS  PubMed  Google Scholar 

  • Zuo L, Zhang XY, Wang F, Li CS, Lu L, Ye L, Zhang H, Krystal JH, Deng HW, Luo X (2013) Genome-wide significant association signals in IPO11-HTR1A region specific for alcohol and nicotine codependence. Alcohol Clin Exp Res 37:730–739

    CAS  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Neurobiology, Brudnick Neuropsychiatric Research Institute, University of Massachusetts Medical School, Worcester, MA, USA

    Paul M. Klenowski & Andrew R. Tapper

Authors
  1. Paul M. Klenowski
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Andrew R. Tapper
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Andrew R. Tapper .

Editor information

Editors and Affiliations

  1. Department of Behavioral Neuroscience, Oregon Health & Science University, Portland, OR, USA

    Kathleen A. Grant

  2. Laboratory for Integrative Neuroscience, National Institutes of Health, Bethesda, MD, USA

    David M. Lovinger

Rights and permissions

Reprints and permissions

Copyright information

© 2018 Springer International Publishing AG

About this chapter

Check for updates. Verify currency and authenticity via CrossMark

Cite this chapter

Klenowski, P.M., Tapper, A.R. (2018). Molecular, Neuronal, and Behavioral Effects of Ethanol and Nicotine Interactions. In: Grant, K., Lovinger, D. (eds) The Neuropharmacology of Alcohol . Handbook of Experimental Pharmacology, vol 248. Springer, Cham. https://doi.org/10.1007/164_2017_89

Download citation

Publish with us

Policies and ethics

Search

Navigation