The two-way relationship between nicotine and cortical activity: a systematic review of neurobiological and treatment aspects

Abstract

Nicotine intake and cortical activity are closely related, as they can influence each other. Nicotine is implicated in the induction and modification of cortical plasticity and excitability, whereas a change on cortical plasticity and excitability can also lead to a modification of the smoking behaviour of an individual. The aim of this systematic review was, on the one hand, to evaluate the effects of nicotinergic modulation on cortical excitability and plasticity, and, on the other hand, to assess if modifying the brain’s excitability and plasticity could influence one’s smoking behaviour. Two systematic literature searches in the PubMed/MEDLINE and PsycINFO databases were conducted. Studies focusing either on the impact of nicotinergic modulation on cortical activity or the treatment effect of non-invasive brain stimulation techniques (NIBS) on smoking behaviour were included. A total of 22 studies for the first systematic search and 35 studies for the second one were included after full-text screening. Nicotine’s effect on cortical activity appeared to depend on smoking status of the individual. While deprived smokers seem to generally profit from nicotine consumption in terms of cortical excitability and plasticity, the contrary was true for non-smokers. Regarding the questions of how changes in cortical excitability can influence smoking behaviour, a trend points towards NIBS being a potential intervention technique for smoking cessation.

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References

  1. 1.

    Heishman SJ, Kleykamp BA, Singleton EG (2010) Meta-analysis of the acute effects of nicotine and smoking on human performance. Psychopharmacology 210(4):453–469. https://doi.org/10.1007/s00213-010-1848-1

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  2. 2.

    Grundey J, Amu R, Batsikadze G, Paulus W, Nitsche MA (2017) Diverging effects of nicotine on motor learning performance: Improvement in deprived smokers and attenuation in non-smokers. Addict Behav 74:90–97. https://doi.org/10.1016/j.addbeh.2017.05.017

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  3. 3.

    Grundey J, Amu R, Ambrus GG, Batsikadze G, Paulus W, Nitsche MA (2015) Double dissociation of working memory and attentional processes in smokers and non-smokers with and without nicotine. Psychopharmacology 232(14):2491–2501. https://doi.org/10.1007/s00213-015-3880-7

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  4. 4.

    Oberman L, Pascual-Leone A (2013) Changes in plasticity across the lifespan: cause of disease and target for intervention. Prog Brain Res 207:91–120. https://doi.org/10.1016/b978-0-444-63327-9.00016-3

    Article  PubMed  PubMed Central  Google Scholar 

  5. 5.

    Mansvelder HD, van Aerde KI, Couey JJ, Brussaard AB (2006) Nicotinic modulation of neuronal networks: from receptors to cognition. Psychopharmacology 184(3):292–305. https://doi.org/10.1007/s00213-005-0070-z

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  6. 6.

    Dajas-Bailador F, Wonnacott S (2004) Nicotinic acetylcholine receptors and the regulation of neuronal signalling. Trends Pharmacol Sci 25(6):317–324. https://doi.org/10.1016/j.tips.2004.04.006

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  7. 7.

    Cooke SF, Bliss TV (2006) Plasticity in the human central nervous system. Brain 129(Pt 7):1659–1673. https://doi.org/10.1093/brain/awl082

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  8. 8.

    Gandelman JA, Kang H, Antal A, Albert K, Boyd BD, Conley AC, Newhouse P, Taylor WD (2018) Transdermal nicotine for the treatment of mood and cognitive symptoms in nonsmokers with late-life depression. J Clin Psychiatry 79(5):1812137. https://doi.org/10.4088/JCP.18m12137

    Article  Google Scholar 

  9. 9.

    Barr RS, Culhane MA, Jubelt LE, Mufti RS, Dyer MA, Weiss AP, Deckersbach T, Kelly JF, Freudenreich O, Goff DC, Evins AE (2008) The effects of transdermal nicotine on cognition in nonsmokers with schizophrenia and nonpsychiatric controls. Neuropsychopharmacology 33(3):480–490. https://doi.org/10.1038/sj.npp.1301423

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  10. 10.

    Holmes AD, Copland DA, Silburn PA, Chenery HJ (2011) Acute nicotine enhances strategy-based semantic processing in Parkinson's disease. Int J Neuropsychopharmacol 14(7):877–885. https://doi.org/10.1017/s1461145710001665

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  11. 11.

    Peacock A, Leung J, Larney S, Colledge S, Hickman M, Rehm J, Giovino GA, West R, Hall W, Griffiths P, Ali R, Gowing L, Marsden J, Ferrari AJ, Grebely J, Farrell M, Degenhardt L (2018) Global statistics on alcohol, tobacco and illicit drug use: 2017 status report. Addiction 113(10):1905–1926. https://doi.org/10.1111/add.14234

    Article  PubMed  PubMed Central  Google Scholar 

  12. 12.

    Reitsma MB, Fullman N, Ng M, Salama JS, Abajobir A, Abate KH, Abbafati C, Abera SF, Abraham B, Abyu GY, Adebiyi AO, Al-Aly Z, Aleman AV, Ali R, Aa AA, Allebeck P, Al-Raddadi RM, Amare AT, Amberbir A, Ammar W, Amrock SM, Antonio CAT, Asayesh H, Atnafu NT, Azzopardi P, Banerjee A, Barac A, Barrientos-Gutierrez T, Basto-Abreu AC, Bazargan-Hejazi S, Bedi N, Bell B, Bello AK, Bensenor IM, Beyene AS, Bhala N, Biryukov S, Bolt K, Brenner H, Butt Z, Cavalleri F, Cercy K, Chen H, Christopher DJ, Ciobanu LG, Colistro V, Colomar M, Cornaby L, Dai X, Damtew SA, Dandona L, Dandona R, Dansereau E, Davletov K, Dayama A, Degfie TT, Deribew A, Dharmaratne SD, Dimtsu BD, Doyle KE, Endries AY, Ermakov SP, Estep K, Faraon EJA, Farzadfar F, Feigin VL, Feigl AB, Fischer F, Friedman J, Ghiwot TT, Gall SL, Gao W, Gillum RF, Gold AL, Gopalani SV, Gotay CC, Gupta R, Gupta R, Gupta V, Hamadeh RR, Hankey G, Harb HL, Hay SI, Horino M, Horita N, Hosgood HD, Husseini A, Ileanu BV, Islami F, Jiang G, Jiang Y, Jonas JB, Kabir Z, Kamal R, Kasaeian A, Kesavachandran CN, Khader YS, Khalil I, Khang Y-H, Khera S, Khubchandani J, Kim D, Kim YJ, Kimokoti RW, Kinfu Y, Knibbs LD, Kokubo Y, Kolte D, Kopec J, Kosen S, Kotsakis GA, Koul PA, Koyanagi A, Krohn KJ, Krueger H, Defo BK, Bicer BK, Kulkarni C, Kumar GA, Leasher JL, Lee A, Leinsalu M, Li T, Linn S, Liu P, Liu S, Lo L-T, Lopez AD, Ma S, El Razek HMA, Majeed A, Malekzadeh R, Malta DC, Manamo WA, Martinez-Raga J, Mekonnen AB, Mendoza W, Miller TR, Mohammad KA, Morawska L, Musa KI, Nagel G, Neupane SP, Nguyen Q, Nguyen G, Oh I-H, Oyekale AS, Pa M, Pana A, Park E-K, Patil ST, Patton GC, Pedro J, Qorbani M, Rafay A, Rahman M, Rai RK, Ram U, Ranabhat CL, Refaat AH, Reinig N, Roba HS, Rodriguez A, Roman Y, Roth G, Roy A, Sagar R, Salomon JA, Sanabria J, de Souza SI, Sartorius B, Satpathy M, Sawhney M, Sawyer S, Saylan M, Schaub MP, Schluger N, Schutte AE, Sepanlou SG, Serdar B, Shaikh MA, She J, Shin M-J, Shiri R, Shishani K, Shiue I, Sigfusdottir ID, Silverberg JI, Singh J, Singh V, Slepak EL, Soneji S, Soriano JB, Soshnikov S, Sreeramareddy CT, Stein DJ, Stranges S, Subart ML, Swaminathan S, Szoeke CEI, Tefera WM, Topor-Madry R, Tran B, Tsilimparis N, Tymeson H, Ukwaja KN, Updike R, Uthman OA, Violante FS, Vladimirov SK, Vlassov V, Vollset SE, Vos T, Weiderpass E, Wen C-P, Werdecker A, Wilson S, Wubshet M, Xiao L, Yakob B, Yano Y, Ye P, Yonemoto N, Yoon S-J, Younis MZ, Yu C, Zaidi Z, El Sayed ZM, Zhang AL, Zipkin B, Murray CJL, Forouzanfar MH, Gakidou E (2017) Smoking prevalence and attributable disease burden in 195 countries and territories, 1990–2015: a systematic analysis from the Global Burden of Disease Study 2015. The Lancet 389(10082):1885–1906. https://doi.org/10.1016/S0140-6736(17)30819-X

    Article  Google Scholar 

  13. 13.

    Taylor G, McNeill A, Girling A, Farley A, Lindson-Hawley N, Aveyard P (2014) Change in mental health after smoking cessation: systematic review and meta-analysis. BMJ 348:g1151. https://doi.org/10.1136/bmj.g1151

    Article  PubMed  PubMed Central  Google Scholar 

  14. 14.

    Kropotov JD (2016) Chapter 4.5 - Transcranial Magnetic Stimulation. In: Kropotov JD (ed) Functional Neuromarkers for Psychiatry. Academic Press, San Diego, pp 281–283. https://doi.org/10.1016/B978-0-12-410513-3.00019-X

  15. 15.

    Nitsche MA, Paulus W (2001) Sustained excitability elevations induced by transcranial DC motor cortex stimulation in humans. Neurology 57(10):1899–1901. https://doi.org/10.1212/wnl.57.10.1899

    CAS  Article  Google Scholar 

  16. 16.

    Nitsche MA, Fricke K, Henschke U, Schlitterlau A, Liebetanz D, Lang N, Henning S, Tergau F, Paulus W (2003) Pharmacological modulation of cortical excitability shifts induced by transcranial direct current stimulation in humans. J Physiol 553(Pt 1):293–301. https://doi.org/10.1113/jphysiol.2003.049916

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  17. 17.

    Brunoni A, Nitsche M, Loo C (2016) Transcranial direct current stimulation in neuropsychiatric disorders: Clinical principles and management. 1 edn. Springer, Amsterdam. doi:10.1007/978-3-319-33967-2

  18. 18.

    Bunge SA, Kahn I (2009) Cognition: an overview of neuroimaging techniques. In: Squire LR (ed) Encyclopedia of Neuroscience. Academic Press, Oxford, pp 1063–1067. https://doi.org/10.1016/B978-008045046-9.00298-9

  19. 19.

    Badawy RA, Loetscher T, Macdonell RA, Brodtmann A (2012) Cortical excitability and neurology: insights into the pathophysiology. Funct Neurol 27(3):131–145

    PubMed  PubMed Central  Google Scholar 

  20. 20.

    Moher D, Liberati A, Tetzlaff J, Altman DG, Group P (2009) Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement. PLoS Med 6(7):e1000097. https://doi.org/10.1371/journal.pmed.1000097

    Article  Google Scholar 

  21. 21.

    Golding JF (1988) Effects of cigarette smoking on resting EEG, visual evoked potentials and photic driving. Pharmacol Biochem Behav 29(1):23–32. https://doi.org/10.1016/0091-3057(88)90268-7

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  22. 22.

    Knott VJ (1988) Dynamic EEG changes during cigarette smoking. Neuropsychobiology 19(1):54–60. https://doi.org/10.1159/000118434

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  23. 23.

    Michel C, Hasenfratz M, Nil R, Battig K (1988) Cardiovascular, electrocortical, and behavioral effects of nicotine chewing gum. Klin Wochenschr 66(Suppl 11):72–79

    CAS  PubMed  PubMed Central  Google Scholar 

  24. 24.

    Knott V, Bosman M, Mahoney C, Ilivitsky V, Quirt K (1999) Transdermal nicotine: single dose effects on mood, EEG, performance, and event-related potentials. Pharmacol Biochem Behav 63(2):253–261. https://doi.org/10.1016/s0091-3057(99)00006-4

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  25. 25.

    Lindgren M, Molander L, Verbaan C, Lunell E, Rosen I (1999) Electroencephalographic effects of intravenous nicotine–a dose-response study. Psychopharmacology 145(3):342–350. https://doi.org/10.1007/s002130051067

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  26. 26.

    Domino EF (2003) Effects of tobacco smoking on electroencephalographic, auditory evoked and event related potentials. Brain Cogn 53(1):66–74. https://doi.org/10.1016/s0278-2626(03)00204-5

    Article  PubMed  PubMed Central  Google Scholar 

  27. 27.

    Teneggi V, Squassante L, Milleri S, Polo A, Lanteri P, Ziviani L, Bye A (2004) EEG power spectra and auditory P300 during free smoking and enforced smoking abstinence. Pharmacol Biochem Behav 77(1):103–109. https://doi.org/10.1016/j.pbb.2003.10.002

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  28. 28.

    Orth M, Amann B, Robertson MM, Rothwell JC (2005) Excitability of motor cortex inhibitory circuits in Tourette syndrome before and after single dose nicotine. Brain 128(Pt 6):1292–1300. https://doi.org/10.1093/brain/awh473

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  29. 29.

    Lang N, Hasan A, Sueske E, Paulus W, Nitsche MA (2008) Cortical hypoexcitability in chronic smokers? A transcranial magnetic stimulation study. Neuropsychopharmacology 33(10):2517–2523. https://doi.org/10.1038/sj.npp.1301645

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  30. 30.

    Swayne OBC, Teo JTH, Greenwood RJ, Rothwell JC (2009) The facilitatory effects of intermittent theta burst stimulation on corticospinal excitability are enhanced by nicotine. Clin Neurophysiol 120(8):1610–1615. https://doi.org/10.1016/j.clinph.2009.06.013

    Article  PubMed  PubMed Central  Google Scholar 

  31. 31.

    Thirugnanasambandam N, Grundey J, Adam K, Drees A, Skwirba AC, Lang N, Paulus W, Nitsche MA (2011) Nicotinergic impact on focal and non-focal neuroplasticity induced by non-invasive brain stimulation in non-smoking humans. Neuropsychopharmacology 36(4):879–886. https://doi.org/10.1038/npp.2010.227

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  32. 32.

    Grundey J, Thirugnanasambandam N, Kaminsky K, Drees A, Skwirba AC, Lang N, Paulus W, Nitsche MA (2012) Rapid effect of nicotine intake on neuroplasticity in non-smoking humans. Front Pharmacol 3:186. https://doi.org/10.3389/fphar.2012.00186

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  33. 33.

    Grundey J, Thirugnanasambandam N, Kaminsky K, Drees A, Skwirba AC, Lang N, Paulus W, Nitsche MA (2012) Neuroplasticity in cigarette smokers is altered under withdrawal and partially restituted by nicotine exposition. J Neurosci 32(12):4156–4162. https://doi.org/10.1523/jneurosci.3660-11.2012

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  34. 34.

    Grundey J, Freznosa S, Klinker F, Lang N, Paulus W, Nitsche MA (2013) Cortical excitability in smoking and not smoking individuals with and without nicotine. Psychopharmacology 229(4):653–664. https://doi.org/10.1007/s00213-013-3125-6

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  35. 35.

    Batsikadze G, Paulus W, Grundey J, Kuo M-F, Nitsche MA (2015) Effect of the nicotinic α4β2-receptor partial agonist varenicline on non-invasive brain stimulation-induced neuroplasticity in the human motor cortex. Cereb Cortex 25(9):3249–3259. https://doi.org/10.1093/cercor/bhu126

    Article  PubMed  PubMed Central  Google Scholar 

  36. 36.

    Strube W, Bunse T, Nitsche MA, Wobrock T, Aborowa R, Misewitsch K, Herrmann M, Falkai P, Hasan A (2015) Smoking restores impaired LTD-like plasticity in schizophrenia: a transcranial direct current stimulation study. Neuropsychopharmacology 40(4):822–830. https://doi.org/10.1038/npp.2014.275

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  37. 37.

    Bridgman AC, Barr MS, Goodman MS, Zomorrodi R, Rajji T, Le Foll B, Chen R, Daskalakis ZJ, George TP (2016) Effects of varenicline on motor cortical plasticity in non-smokers with schizophrenia. Schizophr Res 178(1–3):50–55. https://doi.org/10.1016/j.schres.2016.08.031

    Article  PubMed  PubMed Central  Google Scholar 

  38. 38.

    Batsikadze G, Paulus W, Hasan A, Grundey J, Kuo MF, Nitsche MA (2017) Compromised neuroplasticity in cigarette smokers under nicotine withdrawal is restituted by the nicotinic alpha4beta2-receptor partial agonist varenicline. Sci Rep 7(1):1387. https://doi.org/10.1038/s41598-017-01428-6

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  39. 39.

    Lugon M, Batsikadze G, Fresnoza S, Grundey J, Kuo MF, Paulus W, Nakamura-Palacios EM, Nitsche MA (2017) Mechanisms of nicotinic modulation of glutamatergic neuroplasticity in humans. Cereb Cortex 27(1):544–553. https://doi.org/10.1093/cercor/bhv252

    Article  PubMed  PubMed Central  Google Scholar 

  40. 40.

    Grundey J, Barlay J, Batsikadze G, Kuo MF, Paulus W, Nitsche M (2018) Nicotine modulates human brain plasticity via calcium-dependent mechanisms. J Physiol 596(22):5429–5441. https://doi.org/10.1113/jp276502

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  41. 41.

    Grundey J, Thirugnasambandam N, Amu R, Paulus W, Nitsche MA (2018) Nicotinic restoration of excitatory neuroplasticity is linked to improved implicit motor learning skills in deprived smokers. Front Neurol 9:367. https://doi.org/10.3389/fneur.2018.00367

    Article  PubMed  PubMed Central  Google Scholar 

  42. 42.

    Lavender AP, Obata H, Kawashima N, Nakazawa K (2019) Effect of paired associative stimulation on corticomotor excitability in chronic smokers. Brain Sci. https://doi.org/10.3390/brainsci9030062

    Article  PubMed  PubMed Central  Google Scholar 

  43. 43.

    Eichhammer P, Johann M, Kharraz A, Binder H, Pittrow D, Wodarz N, Hajak G (2003) High-frequency repetitive transcranial magnetic stimulation decreases cigarette smoking. J Clin Psychiatry 64(8):951–953. https://doi.org/10.4088/jcp.v64n0815

    Article  PubMed  PubMed Central  Google Scholar 

  44. 44.

    Johann M, Wiegand R, Kharraz A, Bobbe G, Sommer G, Hajak G, Wodarz N, Eichhammer P (2003) Transcranial magnetic stimulation for nicotine dependence. Psychiatr Prax 30(Suppl 2):S129–131

    PubMed  PubMed Central  Google Scholar 

  45. 45.

    Fregni F, Liguori P, Fecteau S, Nitsche MA, Pascual-Leone A, Boggio PS (2008) Cortical stimulation of the prefrontal cortex with transcranial direct current stimulation reduces cue-provoked smoking craving: a randomized, sham-controlled study. J Clin Psychiatry 69(1):32–40. https://doi.org/10.4088/jcp.v69n0105

    Article  PubMed  PubMed Central  Google Scholar 

  46. 46.

    Amiaz R, Levy D, Vainiger D, Grunhaus L, Zangen A (2009) Repeated high-frequency transcranial magnetic stimulation over the dorsolateral prefrontal cortex reduces cigarette craving and consumption. Addiction 104(4):653–660. https://doi.org/10.1111/j.1360-0443.2008.02448.x

    Article  PubMed  PubMed Central  Google Scholar 

  47. 47.

    Boggio PS, Liguori P, Sultani N, Rezende L, Fecteau S, Fregni F (2009) Cumulative priming effects of cortical stimulation on smoking cue-induced craving. Neurosci Lett 463(1):82–86. https://doi.org/10.1016/j.neulet.2009.07.041

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  48. 48.

    Rose JE, McClernon FJ, Froeliger B, Behm FM, Preud'homme X, Krystal AD (2011) Repetitive transcranial magnetic stimulation of the superior frontal gyrus modulates craving for cigarettes. Biol Psychiatry 70(8):794–799. https://doi.org/10.1016/j.biopsych.2011.05.031

    Article  PubMed  PubMed Central  Google Scholar 

  49. 49.

    Wing VC, Bacher I, Wu BS, Daskalakis ZJ, George TP (2012) High frequency repetitive transcranial magnetic stimulation reduces tobacco craving in schizophrenia. Schizophr Res 139(1–3):264–266. https://doi.org/10.1016/j.schres.2012.03.006

    Article  PubMed  PubMed Central  Google Scholar 

  50. 50.

    Hayashi T, Ko JH, Strafella AP, Dagher A (2013) Dorsolateral prefrontal and orbitofrontal cortex interactions during self-control of cigarette craving. Proc Natl Acad Sci USA 110(11):4422–4427. https://doi.org/10.1073/pnas.1212185110

    Article  PubMed  PubMed Central  Google Scholar 

  51. 51.

    Li X, Hartwell KJ, Owens M, Lematty T, Borckardt JJ, Hanlon CA, Brady KT, George MS (2013) Repetitive transcranial magnetic stimulation of the dorsolateral prefrontal cortex reduces nicotine cue craving. Biol Psychiatry 73(8):714–720. https://doi.org/10.1016/j.biopsych.2013.01.003

    Article  PubMed  PubMed Central  Google Scholar 

  52. 52.

    Sheffer CE, Mennemeier M, Landes RD, Bickel WK, Brackman S, Dornhoffer J, Kimbrell T, Brown G (2013) Neuromodulation of delay discounting, the reflection effect, and cigarette consumption. J Subst Abuse Treat 45(2):206–214. https://doi.org/10.1016/j.jsat.2013.01.012

    Article  PubMed  PubMed Central  Google Scholar 

  53. 53.

    Xu J, Fregni F, Brody AL, Rahman AS (2013) Transcranial direct current stimulation reduces negative affect but not cigarette craving in overnight abstinent smokers. Front Psychiatry 4:112. https://doi.org/10.3389/fpsyt.2013.00112

    Article  PubMed  PubMed Central  Google Scholar 

  54. 54.

    Cailhol L, Roussignol B, Klein R, Bousquet B, Simonetta-Moreau M, Schmitt L, Thalamas C, Tap G, Birmes P (2014) Borderline personality disorder and rTMS: a pilot trial. Psychiatry Res 216(1):155–157. https://doi.org/10.1016/j.psychres.2014.01.030

    Article  PubMed  PubMed Central  Google Scholar 

  55. 55.

    Dieler AC, Dresler T, Joachim K, Deckert J, Herrmann MJ, Fallgatter AJ (2014) Can intermittent theta burst stimulation as add-on to psychotherapy improve nicotine abstinence? Results from a pilot study. Eur Addict Res 20(5):248–253. https://doi.org/10.1159/000357941

    Article  PubMed  PubMed Central  Google Scholar 

  56. 56.

    Dinur-Klein L, Dannon P, Hadar A, Rosenberg O, Roth Y, Kotler M, Zangen A (2014) Smoking cessation induced by deep repetitive transcranial magnetic stimulation of the prefrontal and insular cortices: a prospective, randomized controlled trial. Biol Psychiatry 76(9):742–749. https://doi.org/10.1016/j.biopsych.2014.05.020

    Article  PubMed  PubMed Central  Google Scholar 

  57. 57.

    Fecteau S, Agosta S, Hone-Blanchet A, Fregni F, Boggio P, Ciraulo D, Pascual-Leone A (2014) Modulation of smoking and decision-making behaviors with transcranial direct current stimulation in tobacco smokers: a preliminary study. Drug Alcohol Depend 140:78–84. https://doi.org/10.1016/j.drugalcdep.2014.03.036

    Article  PubMed  PubMed Central  Google Scholar 

  58. 58.

    Meng Z, Liu C, Yu C, Ma Y (2014) Transcranial direct current stimulation of the frontal-parietal-temporal area attenuates smoking behavior. J Psychiatr Res 54:19–25. https://doi.org/10.1016/j.jpsychires.2014.03.007

    Article  PubMed  PubMed Central  Google Scholar 

  59. 59.

    Prikryl R, Ustohal L, Kucerova HP, Kasparek T, Jarkovsky J, Hublova V, Vrzalova M, Ceskova E (2014) Repetitive transcranial magnetic stimulation reduces cigarette consumption in schizophrenia patients. Prog Neuropsychopharmacol Biol Psychiatry 49:30–35. https://doi.org/10.1016/j.pnpbp.2013.10.019

    Article  PubMed  PubMed Central  Google Scholar 

  60. 60.

    Pripfl J, Tomova L, Riecansky I, Lamm C (2014) Transcranial magnetic stimulation of the left dorsolateral prefrontal cortex decreases cue-induced nicotine craving and EEG delta power. Brain Stimul 7(2):226–233. https://doi.org/10.1016/j.brs.2013.11.003

    Article  PubMed  PubMed Central  Google Scholar 

  61. 61.

    Pripfl J, Lamm C (2015) Focused transcranial direct current stimulation (tDCS) over the dorsolateral prefrontal cortex modulates specific domains of self-regulation. Neurosci Res 91:41–47. https://doi.org/10.1016/j.neures.2014.09.007

    Article  PubMed  PubMed Central  Google Scholar 

  62. 62.

    Smith RC, Boules S, Mattiuz S, Youssef M, Tobe RH, Sershen H, Lajtha A, Nolan K, Amiaz R, Davis JM (2015) Effects of transcranial direct current stimulation (tDCS) on cognition, symptoms, and smoking in schizophrenia: a randomized controlled study. Schizophr Res 168(1–2):260–266. https://doi.org/10.1016/j.schres.2015.06.011

    Article  PubMed  PubMed Central  Google Scholar 

  63. 63.

    Trojak B, Meille V, Achab S, Lalanne L, Poquet H, Ponavoy E, Blaise E, Bonin B, Chauvet-Gelinier J-C (2015) Transcranial magnetic stimulation combined with nicotine replacement therapy for smoking cessation: a randomized controlled trial. Brain Stimul 8(6):1168–1174. https://doi.org/10.1016/j.brs.2015.06.004

    Article  PubMed  PubMed Central  Google Scholar 

  64. 64.

    Falcone M, Bernardo L, Ashare RL, Hamilton R, Faseyitan O, McKee SA, Loughead J, Lerman C (2016) Transcranial direct current brain stimulation increases ability to resist smoking. Brain Stimul 9(2):191–196. https://doi.org/10.1016/j.brs.2015.10.004

    Article  PubMed  PubMed Central  Google Scholar 

  65. 65.

    Huang W, Shen F, Zhang J, Xing B (2016) Effect of repetitive transcranial magnetic stimulation on cigarette smoking in patients with schizophrenia. Shanghai Arch Psychiatry 28(6):309–317. https://doi.org/10.11919/j.issn.1002-0829.216044

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  66. 66.

    Kroczek AM, Haussinger FB, Rohe T, Schneider S, Plewnia C, Batra A, Fallgatter AJ, Ehlis AC (2016) Effects of transcranial direct current stimulation on craving, heart-rate variability and prefrontal hemodynamics during smoking cue exposure. Drug Alcohol Depend 168:123–127. https://doi.org/10.1016/j.drugalcdep.2016.09.006

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  67. 67.

    Yang L-Z, Shi B, Li H, Zhang W, Liu Y, Wang H, Zhou Y, Wang Y, Lv W, Ji X, Hudak J, Zhou Y, Fallgatter AJ, Zhang X (2017) Electrical stimulation reduces smokers’ craving by modulating the coupling between dorsal lateral prefrontal cortex and parahippocampal gyrus. Soc Cognit Affect Neurosci 12(8):1296–1302. https://doi.org/10.1093/scan/nsx055

    Article  Google Scholar 

  68. 68.

    Kamp D, Engelke C, Wobrock T, Kunze B, Wölwer W, Winterer G, Schmidt-Kraepelin C, Gaebel W, Langguth B, Landgrebe M, Eichhammer P, Frank E, Hajak G, Ohmann C, Verde PE, Rietschel M, Raees A, Honer WG, Malchow B, Schneider-Axmann T, Falkai P, Hasan A, Cordes J (2018) Influence of rTMS on smoking in patients with schizophrenia. Schizophr Res 192:481–484. https://doi.org/10.1016/j.schres.2017.05.036

    Article  PubMed  PubMed Central  Google Scholar 

  69. 69.

    Kozak K, Sharif-Razi M, Morozova M, Gaudette EV, Barr MS, Daskalakis ZJ, Blumberger DM, George TP (2018) Effects of short-term, high-frequency repetitive transcranial magnetic stimulation to bilateral dorsolateral prefrontal cortex on smoking behavior and cognition in patients with schizophrenia and non-psychiatric controls. Schizophr Res 197:441–443. https://doi.org/10.1016/j.schres.2018.02.015

    Article  PubMed  PubMed Central  Google Scholar 

  70. 70.

    Chang D, Zhang J, Peng W, Shen Z, Gao X, Du Y, Ge Q, Song D, Shang Y, Wang Z (2018) Smoking cessation with 20 Hz repetitive transcranial magnetic stimulation (rTMS) applied to two brain regions: a pilot study. Front Hum Neurosci 12:344. https://doi.org/10.3389/fnhum.2018.00344

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  71. 71.

    Mondino M, Luck D, Grot S, Januel D, Suaud-Chagny MF, Poulet E, Brunelin J (2018) Effects of repeated transcranial direct current stimulation on smoking, craving and brain reactivity to smoking cues. Sci Rep 8(1):8724. https://doi.org/10.1038/s41598-018-27057-1

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  72. 72.

    Sheffer CE, Bickel WK, Brandon TH, Franck CT, Deen D, Panissidi L, Abdali SA, Pittman JC, Lunden SE, Prashad N, Malhotra R, Mantovani A (2018) Preventing relapse to smoking with transcranial magnetic stimulation: feasibility and potential efficacy. Drug Alcohol Depend 182:8–18. https://doi.org/10.1016/j.drugalcdep.2017.09.037

    Article  PubMed  PubMed Central  Google Scholar 

  73. 73.

    de Souza V, Brangioni MC, Pereira DA, Thibaut A, Fregni F, Brasil-Neto JP, Boechat-Barros R (2018) Effects of prefrontal transcranial direct current stimulation and motivation to quit in tobacco smokers: a randomized, sham controlled, double-blind trial. Front Pharmacol 9:14. https://doi.org/10.3389/fphar.2018.00014

    CAS  Article  Google Scholar 

  74. 74.

    Alghamdi F, Alhussien A, Alohali M, Alatawi A, Almusned T, Fecteau S, Habib SS, Bashir S (2019) Effect of transcranial direct current stimulation on the number of smoked cigarettes in tobacco smokers. PLoS ONE 14(2):e0212312. https://doi.org/10.1371/journal.pone.0212312

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  75. 75.

    Falcone M, Bernardo L, Wileyto EP, Allenby C, Burke AM, Hamilton R, Cristancho M, Ashare RL, Loughead J, Lerman C (2019) Lack of effect of transcranial direct current stimulation (tDCS) on short-term smoking cessation: results of a randomized, sham-controlled clinical trial. Drug Alcohol Depend 194:244–251. https://doi.org/10.1016/j.drugalcdep.2018.10.016

    Article  PubMed  PubMed Central  Google Scholar 

  76. 76.

    Friedrich D, Li X, Hartwell KJ, Short EB, Sahlem GL, George MS (2019) Tolerability and feasibility of accelerated repetitive transcranial stimulation for reduction of nicotine craving. Brain Stimul 12(5):1315–1316. https://doi.org/10.1016/j.brs.2019.06.023

    Article  PubMed  PubMed Central  Google Scholar 

  77. 77.

    Ghorbani Behnam S, Mousavi SA, Emamian MH (2019) The effects of transcranial direct current stimulation compared to standard bupropion for the treatment of tobacco dependence: a randomized sham-controlled trial. Eur Psychiatry 60:41–48. https://doi.org/10.1016/j.eurpsy.2019.04.010

    Article  PubMed  PubMed Central  Google Scholar 

  78. 78.

    Conrin J (1980) The EEG effects of tobacco smoking–a review. Clin Electroencephalogr 11(4):180–187. https://doi.org/10.1177/155005948001100407

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  79. 79.

    Hauer L, Scarano GI, Brigo F, Golaszewski S, Lochner P, Trinka E, Sellner J, Nardone R (2019) Effects of repetitive transcranial magnetic stimulation on nicotine consumption and craving: a systematic review. Psychiatry Res 281:112562. https://doi.org/10.1016/j.psychres.2019.112562

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  80. 80.

    Kedzior KK, Gerkensmeier I, Schuchinsky M (2018) Can deep transcranial magnetic stimulation (DTMS) be used to treat substance use disorders (SUD)? A systematic review. BMC Psychiatry 18(1):137. https://doi.org/10.1186/s12888-018-1704-0

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  81. 81.

    Zhang JJQ, Fong KNK, Ouyang RG, Siu AMH, Kranz GS (2019) Effects of repetitive transcranial magnetic stimulation (rTMS) on craving and substance consumption in patients with substance dependence: a systematic review and meta-analysis. Addiction 114(12):2137–2149. https://doi.org/10.1111/add.14753

    Article  PubMed  PubMed Central  Google Scholar 

  82. 82.

    Kang N, Kim RK, Kim HJ (2019) Effects of transcranial direct current stimulation on symptoms of nicotine dependence: a systematic review and meta-analysis. Addict Behav 96:133–139. https://doi.org/10.1016/j.addbeh.2019.05.006

    Article  PubMed  PubMed Central  Google Scholar 

  83. 83.

    Song S, Zilverstand A, Gui W, Li H-j, Zhou X (2019) Effects of single-session versus multi-session non-invasive brain stimulation on craving and consumption in individuals with drug addiction, eating disorders or obesity: a meta-analysis. Brain Stimul 12(3):606–618. https://doi.org/10.1016/j.brs.2018.12.975

    Article  Google Scholar 

  84. 84.

    Hone-Blanchet A, Ciraulo DA, Pascual-Leone A, Fecteau S (2015) Noninvasive brain stimulation to suppress craving in substance use disorders: review of human evidence and methodological considerations for future work. Neurosci Biobehav Rev 59:184–200. https://doi.org/10.1016/j.neubiorev.2015.10.001

    Article  PubMed  PubMed Central  Google Scholar 

  85. 85.

    Coles AS, Kozak K, George TP (2018) A review of brain stimulation methods to treat substance use disorders. Am J Addict 27(2):71–91. https://doi.org/10.1111/ajad.12674

    Article  PubMed  PubMed Central  Google Scholar 

  86. 86.

    Rachid F (2016) Neurostimulation techniques in the treatment of nicotine dependence: a review. Am J Addict 25(6):436–451. https://doi.org/10.1111/ajad.12405

    Article  PubMed  PubMed Central  Google Scholar 

  87. 87.

    Wing VC, Barr MS, Wass CE, Lipsman N, Lozano AM, Daskalakis ZJ, George TP (2013) Brain stimulation methods to treat tobacco addiction. Brain Stimul 6(3):221–230. https://doi.org/10.1016/j.brs.2012.06.008

    Article  PubMed  PubMed Central  Google Scholar 

  88. 88.

    Pomerleau OF, Flessland KA, Pomerleau CS, Hariharan M (1992) Controlled dosing of nicotine via an Intranasal Nicotine Aerosol Delivery Device (INADD). Psychopharmacology 108(4):519–526. https://doi.org/10.1007/bf02247431

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  89. 89.

    Fant RV, Henningfield JE, Shiffman S, Strahs KR, Reitberg DP (2000) A pharmacokinetic crossover study to compare the absorption characteristics of three transdermal nicotine patches. Pharmacol Biochem Behav 67(3):479–482. https://doi.org/10.1016/s0091-3057(00)00399-3

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  90. 90.

    Faessel HM, Obach RS, Rollema H, Ravva P, Williams KE, Burstein AH (2010) A review of the clinical pharmacokinetics and pharmacodynamics of varenicline for smoking cessation. Clin Pharmacokinet 49(12):799–816. https://doi.org/10.2165/11537850-000000000-00000

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  91. 91.

    Guerra A, López-Alonso V, Cheeran B, Suppa A (2020) Solutions for managing variability in non-invasive brain stimulation studies. Neurosci Lett 719:133332. https://doi.org/10.1016/j.neulet.2017.12.060

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  92. 92.

    D'Souza MS (2019) Brain and cognition for addiction medicine: from prevention to recovery neural substrates for treatment of psychostimulant-induced cognitive deficits. Front Psychiatry 10:509. https://doi.org/10.3389/fpsyt.2019.00509

    Article  PubMed  PubMed Central  Google Scholar 

  93. 93.

    Tregellas JR, Wylie KP (2019) Alpha7 nicotinic receptors as therapeutic targets in schizophrenia. Nicotine Tob Res 21(3):349–356. https://doi.org/10.1093/ntr/nty034

    Article  PubMed  PubMed Central  Google Scholar 

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Acknowledgements

This work is supported by the Deutsche Forschungsgemeinschaft via a grant to Alkomiet Hasan (DFG GZ: HA 6091/5–1). Carlota de Miquel received funding by the European Commission via an Erasmus + grant (Erasmus code: NL MAASTRI01).

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Communicated by Sebastian Walther.

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de Miquel, C., Pross, B., Papazova, I. et al. The two-way relationship between nicotine and cortical activity: a systematic review of neurobiological and treatment aspects. Eur Arch Psychiatry Clin Neurosci (2020). https://doi.org/10.1007/s00406-020-01155-6

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Keywords

  • Nicotine
  • Smoking
  • Plasticity
  • Cortical excitability
  • NIBS