Skip to main content

Advertisement

Log in

Neurobiological Considerations for Tobacco Use Disorder

  • Addictions (M Potenza and M Brand, Section Editors)
  • Published:
Current Behavioral Neuroscience Reports Aims and scope Submit manuscript

Abstract

Purpose of Review

Neurobiological studies of tobacco/nicotine use examining genetic, molecular, functional, and behavioral correlates have improved our understanding of tobacco/nicotine dependence and have informed treatment. Recent work extending previously established findings and reporting novel methodologies and discoveries in preclinical and human studies are reviewed.

Recent Findings

Recent work in preclinical models has focused on the differential roles of nicotinic receptor subtypes and nicotine’s effects on neural systems beyond cortico-striatal dopaminergic pathways, and utilizing advanced methodologies such as pharmacogenetics, optogenetics, and rodent fMRI to identify targets for treatment. Likewise, human neuroimaging studies have identified molecular and functional dynamic shifts associated with tobacco/nicotine use that further inform treatment.

Summary

Tobacco/nicotine use is associated with widespread neural adaptations that are persistent and function to maintain addiction. The continued identification of genetic, molecular, neural, and behavioral endophenotypes related to tobacco/nicotine use, dependence, and addiction will facilitate the development and delivery of personalized treatment.

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

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References

Papers of particular interest, published recently, have been highlighted as: • Of importance •• Of major importance

  1. World Health Organization. WHO report on the global tobacco epidemic, 2017: Monitoring tobacco use and prevention policies. Geneva, Switzerland: 2017.

  2. National Center for Chronic Disease Prevention and Health Promotion (US) Office on Smoking and Health. The Health Consequences of Smoking—50 Years of Progress: A Report of the Surgeon General. Atlanta (GA): Centers for Disease Control and Prevention (US); 2014. http://www.ncbi.nlm.nih.gov/books/NBK179276/

    Google Scholar 

  3. Schauer GL, Malarcher AM, Asman KJ. Trends in the average age of quitting among U.S. adult cigarette smokers. Am J Prev Med. 2015;49(6):939–44. https://doi.org/10.1016/j.amepre.2015.06.028.

    Article  PubMed  Google Scholar 

  4. Dani JA. Neuronal nicotinic acetylcholine receptor structure and function and response to nicotine. Int Rev Neurobiol. 2015;(124):3–19. https://doi.org/10.1016/bs.irn.2015.07.001.

    Google Scholar 

  5. Picciotto MR, Kenny PJ. Molecular mechanisms underlying behaviors related to nicotine addiction. CSH Perspect Med. 2013;3(1):a012112. https://doi.org/10.1101/cshperspect.a012112.

    Article  CAS  Google Scholar 

  6. • Le Foll B, Guranda M, Wilson AA, Houle S, Rusjan PM, Wing VC, et al. Elevation of dopamine induced by cigarette smoking: novel insights from a [(11)C]-(+)-PHNO PET study in humans. Neuropsychopharmacology. 2014;39(2):415–24. https://doi.org/10.1038/npp.2013.209 This PET study demonstrates nicotine's effects on the dopaminergic pathway in smokers.

    Article  Google Scholar 

  7. Pistillo F, Clementi F, Zoli M, Gatti C. Nicotinic, glutamatergic and dopaminergic synaptic transmission and plasticity in the mesocorticolimbic system: focus on nicotine effects. Prog Neurobiol. 2015;124:1–27. https://doi.org/10.1016/j.pneurobio.2014.10.002.

    Article  CAS  PubMed  Google Scholar 

  8. Drever BD, Riedel G, Platt B. The cholinergic system and hippocampal plasticity. Behav Brain Res. 2011;221(2):505–14. https://doi.org/10.1016/j.bbr.2010.11.037.

    Article  CAS  PubMed  Google Scholar 

  9. Everitt BJ, Robbins TW. From the ventral to the dorsal striatum: devolving views of their roles in drug addiction. Neurosci Biobehav Rev. 2013;37(9, Part A):1946–54. https://doi.org/10.1016/j.neubiorev.2013.02.010.

    Article  PubMed  Google Scholar 

  10. •• Bruijnzeel AW, Alexander JC, Perez PD, Bauzo-Rodriguez R, Hall G, Klausner R et al. Acute nicotine administration increases BOLD fMRI signal in brain regions involved in reward signaling and compulsive drug intake in rats. Int J Neuropsychoph. 2015;18(2). https://doi.org/10.1093/ijnp/pyu011. This BOLD fMRI study in rats shows dose-dependent effects of nicotine in brain regions typically implicated in nicotine use and addiction.

    Article  Google Scholar 

  11. D'Souza MS, Markou A. The “stop” and “go” of nicotine dependence: role of GABA and glutamate. CSH Perspect Med. 2013;3(6):a012146. https://doi.org/10.1101/cshperspect.a012146.

    Article  CAS  Google Scholar 

  12. Lenoir M, Kiyatkin EA. Intravenous nicotine injection induces rapid, experience-dependent sensitization of glutamate release in the ventral tegmental area and nucleus accumbens. J Neurochem. 2013;127(4):541–51. https://doi.org/10.1111/jnc.12450.

    Article  CAS  Google Scholar 

  13. •• Ryu IS, Kim J, Seo SY, Yang JH, Oh JH, Lee DK et al. Repeated administration of cigarette smoke condensate increases glutamate levels and behavioral sensitization. Front Behav Neurosci. 2018;12. https://doi.org/10.3389/fnbeh.2018.00047. This study uses real-time in vivo biosensing of glutamatergic neurotransmission in the rat dorsal striatum.

  14. De Biasi M, Dani JA. Reward, addiction, withdrawal to nicotine. Annu Rev Neurosci. 2011;34:105–30. https://doi.org/10.1146/annurev-neuro-061010-113734.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  15. • Gozen O, Balkan B, Yildirim E, Koylu EO, Pogun S. The epigenetic effect of nicotine on dopamine D1 receptor expression in rat prefrontal cortex. Synapse. 2013;67(9):545–52. https://doi.org/10.1002/syn.21659 This study demonstrates that nicotine induces epigenetic changes in dopamine receptor genes.

    Article  CAS  PubMed  Google Scholar 

  16. Changeux JP. Nicotine addiction and nicotinic receptors: lessons from genetically modified mice. Nat Rev Neurosci. 2010;11(6):389–401. https://doi.org/10.1038/nrn2849.

    Article  CAS  PubMed  Google Scholar 

  17. Cohen A, George O. Animal models of nicotine exposure: relevance to second-hand smoking, electronic cigarette use, and compulsive smoking. Front Psychiatry. 2013;4:41. https://doi.org/10.3389/fpsyt.2013.00041.

    Article  PubMed  PubMed Central  Google Scholar 

  18. Salloum NC, Buchalter ELF, Chanani S, Espejo G, Ismail MS, Laine RO, et al. From genes to treatments: a systematic review of the pharmacogenetics in smoking cessation. Pharmacogenomics. 2018;19(10):861–71. https://doi.org/10.2217/pgs-2018-0023.

    Article  CAS  PubMed  Google Scholar 

  19. Fowler CD, Lu Q, Johnson PM, Marks MJ, Kenny PJ. Habenular α5 nicotinic receptor subunit signalling controls nicotine intake. Nature. 2011;471:597–601. https://doi.org/10.1038/nature09797 https://www.nature.com/articles/nature09797.

    Article  CAS  Google Scholar 

  20. Jensen KP, DeVito EE, Herman AI, Valentine GW, Gelernter J, Sofuoglu M. A CHRNA5 smoking risk variant decreases the aversive effects of nicotine in humans. Neuropsychopharmacology. 2015;40:2813–21. https://doi.org/10.1038/npp.2015.131 https://www.nature.com/articles/npp2015131.

    Article  CAS  Google Scholar 

  21. •• Chen L-S, Baker TB, Jorenby D, Piper M, Saccone N, Johnson E, et al. Genetic variation (CHRNA5), medication (combination nicotine replacement therapy vs. varenicline), and smoking cessation. Drug Alcohol Depend. 2015;154:278–82. https://doi.org/10.1016/j.drugalcdep.2015.06.022 This study uses pharmacogenetic methods to study smoking cessation in two randomized trials.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  22. MacQueen DA, Heckman BW, Blank MD, Janse Van Rensburg K, Park JY, Drobes DJ, et al. Variation in the α 5 nicotinic acetylcholine receptor subunit gene predicts cigarette smoking intensity as a function of nicotine content. Pharmacogenomics J. 2013;14:70–6. https://doi.org/10.1038/tpj.2012.50.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  23. Jackson KJ, Muldoon PP, De Biasi M, Damaj MI. New mechanisms and perspectives in nicotine withdrawal. Neuropharmacology. 2015;96(0 0):223–34. https://doi.org/10.1016/j.neuropharm.2014.11.009.

    Article  CAS  PubMed  Google Scholar 

  24. Nuechterlein EB, Ni L, Domino EF, Zubieta J-K. Nicotine-specific and non-specific effects of cigarette smoking on endogenous opioid mechanisms. Prog Neuropsychopharmacol Biol Psych. 2016;69:69–77. https://doi.org/10.1016/j.pnpbp.2016.04.006.

    Article  CAS  Google Scholar 

  25. Zilverstand A, Huang AS, Alia-Klein N, Goldstein RZ. Neuroimaging impaired response inhibition and salience attribution in human drug addiction: a systematic review. Neuron. 2018;98(5):886–903. https://doi.org/10.1016/j.neuron.2018.03.048.

    Article  CAS  PubMed  Google Scholar 

  26. Volkow ND, Morales M. The brain on drugs: from reward to addiction. Cell. 2015;162(4):712–25. https://doi.org/10.1016/j.cell.2015.07.046.

    Article  CAS  PubMed  Google Scholar 

  27. Clemens KJ, Castino MR, Cornish JL, Goodchild AK, Holmes NM. Behavioral and neural substrates of habit formation in rats intravenously self-administering nicotine. Neuropsychopharmacology. 2014;39(11):2584–93. https://doi.org/10.1038/npp.2014.111.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  28. Hogarth L, Balleine BW, Corbit LH, Killcross S. Associative learning mechanisms underpinning the transition from recreational drug use to addiction. Ann N Y Acad Sci. 2013;1282:12–24. https://doi.org/10.1111/j.1749-6632.2012.06768.x.

    Article  CAS  PubMed  Google Scholar 

  29. Hogarth L, Chase HW. Parallel goal-directed and habitual control of human drug-seeking: implications for dependence vulnerability. J Exp Psychol Anim Behav Process. 2011;37(3):261–76. https://doi.org/10.1037/a0022913.

    Article  PubMed  Google Scholar 

  30. Hogarth L. Goal-directed and transfer-cue-elicited drug-seeking are dissociated by pharmacotherapy: evidence for independent additive controllers. J Exp Psychol Anim Behav Process. 2012;38(3):266–78. https://doi.org/10.1037/a0028914.

    Article  PubMed  Google Scholar 

  31. Belin D, Belin-Rauscent A, Murray JE, Everitt BJ. Addiction: failure of control over maladaptive incentive habits. Curr Opin Neurobiol. 2013;23(4):564–72. https://doi.org/10.1016/j.conb.2013.01.025.

    Article  CAS  PubMed  Google Scholar 

  32. Kedikian X, Faillace MP, Bernabeu R. Behavioral and molecular analysis of nicotine-conditioned place preference in zebrafish. PLoS One. 2013;8(7):e69453. https://doi.org/10.1371/journal.pone.0069453.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  33. Ignatowska-Jankowska BM, Muldoon PP, Lichtman AH, Damaj MI. The cannabinoid CB2 receptor is necessary for nicotine-conditioned place preference, but not other behavioral effects of nicotine in mice. Psychopharmacology. 2013;229(4):591–601. https://doi.org/10.1007/s00213-013-3117-6.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  34. Parsons LH, Hurd YL. Endocannabinoid signalling in reward and addiction. Nat Rev Neurosci. 2015;16:579–94. https://doi.org/10.1038/nrn4004.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  35. Menon V. Salience network. In: Toga AW, editor. Brain mapping: an encyclopedic reference. Academic Press: Elsevier; 2015. p. 597–611.

    Chapter  Google Scholar 

  36. Janes AC, Farmer S, Peechatka AL, Frederick BD, Lukas SE. Insula-dorsal anterior cingulate cortex coupling is associated with enhanced brain reactivity to smoking cues. Neuropsychopharmacology. 2015;40(7):1561–8. https://doi.org/10.1038/npp.2015.9.

    Article  PubMed  PubMed Central  Google Scholar 

  37. Hall FS, Der-Avakian A, Gould TJ, Markou A, Shoaib M, Young JW. Negative affective states and cognitive impairments in nicotine dependence. Neurosci Biobehav Rev. 2015;58:168–85. https://doi.org/10.1016/j.neubiorev.2015.06.004.

    Article  PubMed  PubMed Central  Google Scholar 

  38. Shiyko M, Naab P, Shiffman S, Li R. Modeling complexity of EMA data: time-varying lagged effects of negative affect on smoking urges for subgroups of nicotine addiction. Nicotine Tob Res. 2014;16(Suppl 2):S144–50. https://doi.org/10.1093/ntr/ntt109.

    Article  CAS  PubMed  Google Scholar 

  39. •• Lesage E, Aronson SE, Sutherland MT, Ross TJ, Salmeron BJ, Stein EA. Neural signatures of cognitive flexibility and reward sensitivity following nicotinic receptor stimulation in dependent smokers: A randomized trial. JAMA Psychiatry. 2017;74(6):632–40. https://doi.org/10.1001/jamapsychiatry.2017.0400 This report is of two-drug randomized controlled trial examining the effects of nicotine and nicotine replacement therapy on cognition and reward in smokers and non-smokers.

    Article  Google Scholar 

  40. Jastreboff AM, Sinha R, Lacadie CM, Balodis IM, Sherwin R, Potenza MN. Blunted striatal responses to favorite-food cues in smokers. Drug Alcohol Depend. 2015;146:103–6. https://doi.org/10.1016/j.drugalcdep.2014.09.006.

    Article  PubMed  Google Scholar 

  41. Garrison KA, Sinha R, Lacadie CM, Scheinost D, Jastreboff AM, Constable RT, et al. Functional connectivity during exposure to favorite-food, stress, and neutral-relaxing imagery differs between smokers and nonsmokers. Nicotine Tob Res. 2016;18(9):1820–9. https://doi.org/10.1093/ntr/ntw088.

    Article  PubMed  PubMed Central  Google Scholar 

  42. Versace F, Lam CY, Engelmann JM, Robinson JD, Minnix JA, Brown VL, et al. Beyond cue reactivity: blunted brain responses to pleasant stimuli predict long-term smoking abstinence. Addict Biol. 2012;17(6):991–1000. https://doi.org/10.1111/j.1369-1600.2011.00372.x.

    Article  PubMed  Google Scholar 

  43. Wilcox CE, Claus ED, Calhoun VD, Rachakonda S, Littlewood RA, Mickey J, et al. Default mode network deactivation to smoking cue relative to food cue predicts treatment outcome in nicotine use disorder. Addict Biol. 2018;23(1):412–24. https://doi.org/10.1111/adb.12498.

    Article  CAS  PubMed  Google Scholar 

  44. Peechatka AL, Whitton AE, Farmer SL, Pizzagalli DA, Janes AC. Cigarette craving is associated with blunted reward processing in nicotine-dependent smokers. Drug Alcohol Depend. 2015;155:202–7. https://doi.org/10.1016/j.drugalcdep.2015.07.015.

    Article  PubMed  PubMed Central  Google Scholar 

  45. Goldstein RZ, Volkow ND. Dysfunction of the prefrontal cortex in addiction: neuroimaging findings and clinical implications. Nat Rev Neurosci. 2011;12(11):652–69 https://www.nature.com/articles/nrn3119.

    Article  CAS  Google Scholar 

  46. Bi Y, Yuan K, Guan Y, Cheng J, Zhang Y, Li Y, et al. Altered resting state functional connectivity of anterior insula in young smokers. Brain Imaging Behav. 2017;11(1):155–65. https://doi.org/10.1007/s11682-016-9511-z.

    Article  PubMed  Google Scholar 

  47. Sutherland MT, Carroll AJ, Salmeron BJ, Ross TJ, Stein EA. Insula’s functional connectivity with ventromedial prefrontal cortex mediates the impact of trait alexithymia on state tobacco craving. Psychopharmacology. 2013;228(1):143–55. https://doi.org/10.1007/s00213-013-3018-8.

    Article  CAS  PubMed  Google Scholar 

  48. •• Sutherland MT, Riedel MC, Flannery JS, Yanes JA, Fox PT, Stein EA, et al. Chronic cigarette smoking is linked with structural alterations in brain regions showing acute nicotinic drug-induced functional modulations. Behav Brain Funct. 2016;12(1):16. https://doi.org/10.1186/s12993-016-0100-5 A multi-modal meta-analysis using data-driven methods is used to demonstrate overlap between regions implicated in structural and functional studies of nicotine effects.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  49. Jasinska AJ, Zorick T, Brody AL, Stein EA. Dual role of nicotine in addiction and cognition: a review of neuroimaging studies in humans. Neuropharmacology. 2014;84:111–22. https://doi.org/10.1016/j.neuropharm.2013.02.015.

    Article  CAS  PubMed  Google Scholar 

  50. Sutherland MT, Ray KL, Riedel MC, Yanes JA, Stein EA, Laird AR. Neurobiological impact of nicotinic acetylcholine receptor agonists: an activation likelihood estimation meta-analysis of pharmacologic neuroimaging studies. Biol Psychiatry. 2015;78(10):711–20. https://doi.org/10.1016/j.biopsych.2014.12.021.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  51. Anstey KJ, von Sanden C, Salim A, O'Kearney R. Smoking as a risk factor for dementia and cognitive decline: a meta-analysis of prospective studies. Am J Epidemiol. 2007;166(4):367–78. https://doi.org/10.1093/aje/kwm116.

    Article  PubMed  Google Scholar 

  52. Insel T, Cuthbert B, Garvey M, Heinssen R, Pine DS, Quinn K, et al. Research domain criteria (RDoC): toward a new classification framework for research on mental disorders. Am J Psychiatry. 2010;167(7):748–51. https://doi.org/10.1176/appi.ajp.2010.09091379.

    Article  PubMed  Google Scholar 

  53. Belin D, Belin-Rauscent A, Everitt BJ, Dalley JW. In search of predictive endophenotypes in addiction: insights from preclinical research. Genes. Brain Behav. 2016;15(1):74–88. https://doi.org/10.1111/gbb.12265.

    Article  CAS  Google Scholar 

  54. McLaughlin I, Dani JA, De Biasi M. Nicotine withdrawal. Curr Top Behav Neurosci. 2015;24:99–123. https://doi.org/10.1007/978-3-319-13482-6_4.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  55. Franklin TR, Jagannathan K, Hager N, Fang Z, Xu S, Wong J, et al. Brain substrates of early (4h) cigarette abstinence: identification of treatment targets. Drug Alcohol Depend. 2018;182:78–85. https://doi.org/10.1016/j.drugalcdep.2017.10.010.

    Article  PubMed  Google Scholar 

  56. Cahill K, Stevens S, Perera R, Lancaster T. Pharmacological interventions for smoking cessation: an overview and network meta-analysis. Cochrane Database Syst Rev. 2013;5:CD009329. https://doi.org/10.1002/14651858.CD009329.pub2.

    Article  Google Scholar 

  57. Pistillo F, Fasoli F, Moretti M, McClure-Begley T, Zoli M, Marks MJ, et al. Chronic nicotine and withdrawal affect glutamatergic but not nicotinic receptor expression in the mesocorticolimbic pathway in a region-specific manner. Pharmacol Res. 2016;103:167–76. https://doi.org/10.1016/j.phrs.2015.11.016.

    Article  CAS  PubMed  Google Scholar 

  58. Antolin-Fontes B, Ables JL, Görlich A, Ibañez-Tallon I. The habenulo-interpeduncular pathway in nicotine aversion and withdrawal. Neuropharmacology. 2015;96:213–22. https://doi.org/10.1016/j.neuropharm.2014.11.019.

    Article  CAS  PubMed  Google Scholar 

  59. Zhao-Shea R, Liu L, Pang X, Gardner Paul D, Tapper AR. Activation of GABAergic neurons in the interpeduncular nucleus triggers physical nicotine withdrawal symptoms. Curr Biol. 2013;23(23):2327–35. https://doi.org/10.1016/j.cub.2013.09.041.

    Article  CAS  PubMed  Google Scholar 

  60. Abdolahi A, Williams GC, Benesch CG, Wang HZ, Spitzer EM, Scott BE, et al. Damage to the insula leads to decreased nicotine withdrawal during abstinence. Addiction. 2015;110(12):1994–2003. https://doi.org/10.1111/add.13061.

    Article  PubMed  PubMed Central  Google Scholar 

  61. Sutherland MT, Stein EA. Functional neurocircuits and neuroimaging biomarkers of tobacco use disorder. Trends Mol Med. 2018;24(2):129–43. https://doi.org/10.1016/j.molmed.2017.12.002.

    Article  CAS  PubMed  Google Scholar 

  62. Sutherland MT, McHugh MJ, Pariyadath V, Stein EA. Resting state functional connectivity in addiction: lessons learned and a road ahead. NeuroImage. 2012;62(4):2281–95. https://doi.org/10.1016/j.neuroimage.2012.01.117.

    Article  PubMed  PubMed Central  Google Scholar 

  63. Lerman C, Gu H, Loughead J, Ruparel K, Yang YH, Stein EA. Large-scale brain network coupling predicts acute nicotine abstinence effects on craving and cognitive function. JAMA Psychiatry. 2014;71(5):523–30. https://doi.org/10.1001/jamapsychiatry.2013.4091.

    Article  PubMed  PubMed Central  Google Scholar 

  64. Loughead J, Wileyto EP, Ruparel K, Falcone M, Hopson R, Gur R, et al. Working memory-related neural activity predicts future smoking relapse. Neuropsychopharmacology. 2014;40:1311–20. https://doi.org/10.1038/npp.2014.318.

    Article  PubMed  Google Scholar 

  65. •• Rademacher L, Prinz S, Winz O, Henkel K, Dietrich CA, Schmaljohann J, et al. Effects of smoking cessation on presynaptic dopamine function of addicted male smokers. Biol Psychiat. 2016;80(3):198–206. https://doi.org/10.1016/j.biopsych.2015.11.009 Steady-state modeling of PET data in smokers is used to demonstrate nicotine effects on dopamine synthesis capacity.

    Article  CAS  PubMed  Google Scholar 

  66. Nestor LJ, McCabe E, Jones J, Clancy L, Garavan H. Smokers and ex-smokers have shared differences in the neural substrates for potential monetary gains and losses. Addict Biol. 2018;23(1):369–78. https://doi.org/10.1111/adb.12484.

    Article  CAS  PubMed  Google Scholar 

  67. Nestor LJ, McCabe E, Jones J, Clancy L, Garavan H. Shared and divergent neural reactivity to non-drug operant response outcomes in current smokers and ex-smokers. Brain Res. 1680;2018:54–61. https://doi.org/10.1016/j.brainres.2017.12.003.

    Article  CAS  Google Scholar 

  68. Nestor L, McCabe E, Jones J, Clancy L, Garavan H. Differences in “bottom-up” and “top-down” neural activity in current and former cigarette smokers: evidence for neural substrates which may promote nicotine abstinence through increased cognitive control. NeuroImage. 2011;56(4):2258–75. https://doi.org/10.1016/j.neuroimage.2011.03.054.

    Article  PubMed  Google Scholar 

  69. Krönke K-M, Wolff M, Benz A, Goschke T. Successful smoking cessation is associated with prefrontal cortical function during a Stroop task: a preliminary study. Psychiatry Res Neuroimaging. 2015;234(1):52–6. https://doi.org/10.1016/j.pscychresns.2015.08.005.

    Article  Google Scholar 

  70. Amlung M, MacKillop J. Clarifying the relationship between impulsive delay discounting and nicotine dependence. Psychol Addict Behav. 2014;28(3):761–8. https://doi.org/10.1037/a0036726.

    Article  PubMed  PubMed Central  Google Scholar 

  71. Clewett D, Luo S, Hsu E, Ainslie G, Mather M, Monterosso J. Increased functional coupling between the left fronto-parietal network and anterior insula predicts steeper delay discounting in smokers. Hum Brain Mapp. 2014;35(8):3774–87. https://doi.org/10.1002/hbm.22436.

    Article  PubMed  Google Scholar 

  72. Barlow P, McKee M, Reeves A, Galea G, Stuckler D. Time-discounting and tobacco smoking: a systematic review and network analysis. Int J Epidemiol. 2017;46(3):860–9. https://doi.org/10.1093/ije/dyw233.

    Article  PubMed  Google Scholar 

  73. Secades-Villa R, Weidberg S, García-Rodríguez O, Fernández-Hermida JR, Yoon JH. Decreased delay discounting in former cigarette smokers at one year after treatment. Addict Behav. 2014;39(6):1087–93. https://doi.org/10.1016/j.addbeh.2014.03.015.

    Article  PubMed  Google Scholar 

  74. Stein JS, Heckman BW, Pope DA, Perry ES, Fong GT, Cummings KM, et al. Delay discounting and e-cigarette use: an investigation in current, former, and never cigarette smokers. Drug Alcohol Depend. 2018;191:165–73. https://doi.org/10.1016/j.drugalcdep.2018.06.034.

    Article  PubMed  Google Scholar 

  75. Weinberger AH, Sofuoglu M. The impact of cigarette smoking on stimulant addiction. Am J Drug Alcohol Abuse. 2009;35(1):12–7. https://doi.org/10.1080/00952990802326280.

    Article  PubMed  PubMed Central  Google Scholar 

  76. Falk D, Yi HY, Hiller-Sturmhofel S. An epidemiologic analysis of co-occurring alcohol and drug use and disorders: findings from the National Epidemiologic Survey of Alcohol and Related Conditions (NESARC). Alcohol Res Health. 2008;31(2):100–10.

    PubMed  PubMed Central  Google Scholar 

  77. Cross SJ, Lotfipour S, Leslie FM. Mechanisms and genetic factors underlying co-use of nicotine and alcohol or other drugs of abuse. Am J Drug Alcohol Abuse. 2017;43(2):171–85. https://doi.org/10.1080/00952990.2016.1209512.

    Article  PubMed  Google Scholar 

  78. Powers MS, Broderick HJ, Drenan RM, Chester JA. Nicotinic acetylcholine receptors containing alpha6 subunits contribute to alcohol reward-related behaviours. Genes Brain Behav. 2013;12(5):543–53. https://doi.org/10.1111/gbb.12042.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  79. Kandel ER, Kandel DB. A molecular basis for nicotine as a gateway drug. New Engl J Med. 2014;371(10):932–43. https://doi.org/10.1056/NEJMsa1405092.

    Article  CAS  PubMed  Google Scholar 

  80. Palmer RHC, Brick L, Nugent NR, Bidwell LC, McGeary JE, Knopik VS, et al. Examining the role of common genetic variants on alcohol, tobacco, cannabis and illicit drug dependence: genetics of vulnerability to drug dependence. Addiction. 2015;110(3):530–7. https://doi.org/10.1111/add.12815.

    Article  PubMed  PubMed Central  Google Scholar 

  81. Rosen LJ, Galili T, Kott J, Goodman M, Freedman LS. Diminishing benefit of smoking cessation medications during the first year: a meta-analysis of randomized controlled trials. Addiction. 2018;113(5):805–16.

    Article  Google Scholar 

  82. Stead LF, Koilpillai P, Lancaster T. Additional behavioural support as an adjunct to pharmacotherapy for smoking cessation. Cochrane Database Syst Rev. 2015;10:CD009670. https://doi.org/10.1002/14651858.CD009670.pub3.

    Article  Google Scholar 

  83. •• Schuit E, Panagiotou OA, Munafo MR, Bennett DA, Bergen AW, David SP. Pharmacotherapy for smoking cessation: effects by subgroup defined by genetically informed biomarkers. Biol Psychiat. 2016;80(3):198–206. https://doi.org/10.1016/j.biopsych.2015.11.009 A large-scale meta-analysis of randomized control trials examined the interaction of smoking cessation pharmacotherapy with genotypes.

    Article  CAS  Google Scholar 

  84. Lynch WJ, Sofuoglu M. Role of progesterone in nicotine addiction: evidence from initiation to relapse. Exp Clin Psychopharmacol. 2010;18(6):451–61. https://doi.org/10.1037/a0021265.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  85. DeVito EE, Herman AI, Waters AJ, Valentine GW, Sofuoglu M. Subjective, physiological, and cognitive responses to intravenous nicotine: effects of sex and menstrual cycle phase. Neuropsychopharmacology. 2014;39(6):1431–40. https://doi.org/10.1038/npp.2013.339.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  86. Piazza PV, Cota D, Marsicano G. The CB1 receptor as the cornerstone of exostasis. Neuron. 2017;93(6):1252–74. https://doi.org/10.1016/j.neuron.2017.02.002.

    Article  CAS  PubMed  Google Scholar 

  87. Cahill K, Ussher MH. Cannabinoid type 1 receptor antagonists for smoking cessation. Cochrane Database Syst Rev. 2011;3:CD005353. https://doi.org/10.1002/14651858.CD005353.pub4.

    Article  Google Scholar 

  88. •• Johnson MW, Garcia-Romeu A, Cosimano MP, Griffiths RR. Pilot study of the 5-HT2AR agonist psilocybin in the treatment of tobacco addiction. J Psychopharmacol. 2014;28(11):983–92. https://doi.org/10.1177/0269881114548296 This interesting pilot study tests the potential efficacy of psilocybin for smoking cessation.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  89. Johnson MW, Garcia-Romeu A, Griffiths RR. Long-term follow-up of psilocybin-facilitated smoking cessation. Am J Drug Alcohol Abuse. 2017;43(1):55–60. https://doi.org/10.3109/00952990.2016.1170135.

    Article  PubMed  Google Scholar 

  90. Carhart-Harris RL, Erritzoe D, Williams T, Stone JM, Reed LJ, Colasanti A, et al. Neural correlates of the psychedelic state as determined by fMRI studies with psilocybin. Proc Natl Acad Sci U S A. 2012;109(6):2138–43. https://doi.org/10.1073/pnas.1119598109.

    Article  PubMed  PubMed Central  Google Scholar 

  91. Hartwell KJ, Hanlon CA, Li X, Borckardt JJ, Canterberry M, Prisciandaro JJ, et al. Individualized real-time fMRI neurofeedback to attenuate craving in nicotine-dependent smokers. J Psychiatry Neurosci. 2016;41(1):48–55.

    Article  Google Scholar 

  92. Stoeckel LE, Garrison KA, Ghosh S, Wighton P, Hanlon CA, Gilman JM, et al. Optimizing real time fMRI neurofeedback for therapeutic discovery and development. Neuroimage Clin. 2014;5:245–55. https://doi.org/10.1016/j.nicl.2014.07.002.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  93. Sulzer J, Haller S, Scharnowski F, Weiskopf N, Birbaumer N, Blefari ML, et al. Real-time fMRI neurofeedback: progress and challenges. NeuroImage. 2013;76:386–99. https://doi.org/10.1016/j.neuroimage.2013.03.033.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  94. Diana M, Raij T, Melis M, Nummenmaa A, Leggio L, Bonci A. Rehabilitating the addicted brain with transcranial magnetic stimulation. Nat Rev Neurosci. 2017;18:685–93. https://doi.org/10.1038/nrn.2017.113.

    Article  CAS  PubMed  Google Scholar 

  95. •• Dinur-Klein L, Dannon P, Hadar A, Rosenberg O, Roth Y, Kotler M, et al. Smoking cessation induced by deep repetitive transcranial magnetic stimulation of the prefrontal and insular cortices: a prospective, randomized controlled trial. Biol Psychiat. 2014;76(9):742–9. https://doi.org/10.1016/j.biopsych.2014.05.020 This randomized control trial demonstrates potential efficacy of rTMS for smoking cessation.

    Article  PubMed  Google Scholar 

  96. Sheffer CE, Bickel WK, Brandon TH, Franck CT, Deen D, Panissidi L, et al. Preventing relapse to smoking with transcranial magnetic stimulation: feasibility and potential efficacy. Drug Alcohol Depend. 2018;182:8–18. https://doi.org/10.1016/j.drugalcdep.2017.09.037.

    Article  PubMed  Google Scholar 

  97. Tang YY, Holzel BK, Posner MI. The neuroscience of mindfulness meditation. Nat Rev Neurosci. 2015;16(4):213–25. https://doi.org/10.1038/nrn3916.

    Article  CAS  PubMed  Google Scholar 

  98. Vidrine JI, Spears CA, Heppner WL, Reitzel LR, Marcus MT, Cinciripini PM, et al. Efficacy of mindfulness-based addiction treatment (MBAT) for smoking cessation and lapse recovery: a randomized clinical trial. J Consult Clin Psychol. 2016;84(9):824–38. https://doi.org/10.1037/ccp0000117.

    Article  PubMed  PubMed Central  Google Scholar 

  99. Levy DT, Borland R, Lindblom EN, Goniewicz ML, Meza R, Holford TR, et al. Potential deaths averted in USA by replacing cigarettes with e-cigarettes. Tob Control. 2018;27(1):18–25. https://doi.org/10.1136/tobaccocontrol-2017-053759.

    Article  PubMed  Google Scholar 

  100. Baldassarri SR, Hillmer AT, Anderson JM, Jatlow P, Nabulsi N, Labaree D, et al. Use of electronic cigarettes leads to significant beta2-nicotinic acetylcholine receptor occupancy: evidence from a PET imaging study. Nicotine Tob Res. 2018;20(4):425–33. https://doi.org/10.1093/ntr/ntx091.

    Article  PubMed  Google Scholar 

  101. Yuan M, Cross SJ, Loughlin SE, Leslie FM. Nicotine and the adolescent brain. J Physiol. 2015;593(16):3397–412. https://doi.org/10.1113/JP270492.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  102. Thomas AM, Ostroumov A, Kimmey BA, Taormina MB, Holden WM, Kim K, et al. Adolescent nicotine exposure alters GABAA receptor signaling in the ventral tegmental area and increases adult ethanol self-administration. Cell Rep. 2018;23(1):68–77. https://doi.org/10.1016/j.celrep.2018.03.030.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  103. Beard E, West R, Michie S, Brown J. Association between electronic cigarette use and changes in quit attempts, success of quit attempts, use of smoking cessation pharmacotherapy, and use of stop smoking services in England: time series analysis of population trends. BMJ. 2016;354:i4645. https://doi.org/10.1136/bmj.i4645.

    Article  PubMed  Google Scholar 

  104. Kalkhoran S, Glantz SA. E-cigarettes and smoking cessation in real-world and clinical settings: a systematic review and meta-analysis. Lancet Respir Med. 2016;4(2):116–28. https://doi.org/10.1016/S2213-2600(15)00521-4.

    Article  PubMed  PubMed Central  Google Scholar 

  105. Belin-Rauscent A, Fouyssac M, Bonci A, Belin D. How preclinical models evolved to resemble the diagnostic criteria of drug addiction. Biol Psychiatry. 2016;79(1):39–46. https://doi.org/10.1016/j.biopsych.2015.01.004.

    Article  PubMed  Google Scholar 

  106. Munafò MR, Nosek BA, Bishop DVM, Button KS, Chambers CD, Sert NPD et al. A manifesto for reproducible science. Nat Human Behav. 2017;1(0021). https://doi.org/10.1038/s41562-016-0021.

    Article  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Kathleen A. Garrison.

Ethics declarations

Conflict of Interest

The authors declare that they have no conflict of interest.

Human and Animal Rights and Informed Consent

This article does not contain any studies with human or animal subjects performed by any of the authors.

Additional information

This article is part of the Topical Collection on Addictions

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Chawla, M., Garrison, K.A. Neurobiological Considerations for Tobacco Use Disorder. Curr Behav Neurosci Rep 5, 238–248 (2018). https://doi.org/10.1007/s40473-018-0168-3

Download citation

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s40473-018-0168-3

Keywords

Navigation