Transcranial magnetic stimulation of the left dorsolateral prefrontal cortex decreases cue-induced nicotine craving and EEG delta power

Brain Stimulation

Volumn 7, Issue 2, 2014, Pages 226-233

  Pripfl, Jürgen ^a   Tomova, Livia ^a   Riecansky, Igor ^a,b   Lamm, Claus ^a  

^a UNIVERSITY OF VIENNA   (Austria)

^b INSTITUTE OF CHEMISTRY   (Slovakia)

Author keywords

Dorsolateral prefrontal cortex; Electroencephalography; Nicotine craving; Smoking cessation; Transcranial magnetic stimulation

Indexed keywords

NICOTINE;

ADULT; AMPLIFIER; ARTICLE; CLINICAL ARTICLE; CONTROLLED STUDY; CUE INDUCED NICOTINE CRAVING; DELTA RHYTHM; ELECTROENCEPHALOGRAM; ELECTROENCEPHALOGRAPH; ELECTROENCEPHALOGRAPH ELECTRODE; FEMALE; HUMAN; ICD-10; MALE; NERVE STIMULATOR; NEURONAVIGATION; PREFRONTAL CORTEX; PRIORITY JOURNAL; REPETITIVE TRANSCRANIAL MAGNETIC STIMULATION; REST; REWARD; SMOKING; SMOKING CESSATION; TOBACCO DEPENDENCE; TRANSCRANIAL MAGNETIC STIMULATION; WITHDRAWAL SYNDROME; YOUNG ADULT; ASSOCIATION; ELECTROENCEPHALOGRAPHY; PATHOPHYSIOLOGY; PHYSIOLOGY; PROCEDURES; PSYCHOLOGY; TOBACCO USE DISORDER;

ADULT; CRAVING; CUES; ELECTROENCEPHALOGRAPHY; FEMALE; HUMANS; MALE; NEURONAVIGATION; NICOTINE; PREFRONTAL CORTEX; REWARD; SMOKING CESSATION; TOBACCO USE DISORDER; TRANSCRANIAL MAGNETIC STIMULATION; YOUNG ADULT;

EID: 84896389699     PISSN: 1935861X     EISSN: 18764754     Source Type: Journal    
DOI: 10.1016/j.brs.2013.11.003     Document Type: Article

References (93)

1. M.C. Fiore, C.R. Jaén, T.B. Baker, W.C. Bailey, N.L. Benowitz, and S.J. Curry et al. Treating tobacco use and dependence: 2008 update. Clinical practice guideline 2008 U.S. Department of Health and Human Services. Public Health Service Rockville, MD.
2. B.L. Carter, and S.T. Tiffany Meta-analysis of cue-reactivity in addiction research Addiction 94 3 1999 327 340.
3. S. Shiffman, J.B. Engberg, J.A. Paty, W.G. Perz, M. Gnys, and J.D. Kassel et al. A day at a time: predicting smoking lapse from daily urge J Abnorm Psychol 106 1 1997 104 116.
4. M. Johann, R. Wiegand, A. Kharraz, G. Bobbe, G. Sommer, and G. Hajak et al. Transkranielle Magnetstimulation bei Nikotinabhängigkeit Psychiatr Prax Suppl. 2003 129 131.
5. R. Amiaz, D. Levy, D. Vainiger, L. Grunhaus, and A. Zangen Repeated high-frequency transcranial magnetic stimulation over the dorsolateral prefrontal cortex reduces cigarette craving and consumption Addiction 104 2009 653 660.
6. X. Li, K.J. Hartwell, M. Owens, T. Lematty, J.J. Borckardt, and C.A. Hanlon et al. Repetitive transcranial magnetic stimulation of the dorsolateral prefrontal cortex reduces nicotine cue craving Biol Psychiatry 73 8 2013 Apr 15 714 720.
7. T. Hayashi, J.H. Ko, A.P. Strafella, and A. Dagher Dorsolateral prefrontal and orbitofrontal cortex interactions during self-control of cigarette craving Proc Natl Acad Sci U S A 110 11 2013 4422 4427.
8. V.C. Wing, M.S. Barr, C.E. Wass, N. Lipsman, A.M. Lozano, and Z.J. Daskalakis et al. Brain stimulation methods to treat tobacco addiction Brain Stimul 6 3 2013 221 230.
9. P. Eichhammer, M. Johann, A. Kharraz, H. Binder, D. Pittrow, and N. Wodarz et al. High-frequency repetitive transcranial magnetic stimulation decreases cigarette smoking J Clin Psychiatry 64 2003 951 953.
10. M.E. Keck, T. Welt, M.B. Müller, A. Erhardt, F. Ohl, and N. Toschi et al. Repetitive transcranial magnetic stimulation increases the release of dopamine in the mesolimbic and mesostriatal system Neuropharmacology 43 2002 101 109.
11. A. Zangen, and K. Hyodo Transcranial magnetic stimulation induces increases in extracellular levels of dopamine and glutamate in the nucleus accumbens NeuroReport 13 18 2002 2401 2405.
12. A.P. Strafella, T. Paus, J. Barrett, and A. Dagher Repetitive transcranial magnetic stimulation of the human prefrontal cortex induces dopamine release in the caudate nucleus J Neurosci 21 2001 RC157.
13. T. Graf, J. Engeler, P. Achermann, U.P. Mosimann, R. Noss, and H.U. Fisch et al. High frequency repetitive transcranial magnetic stimulation (rTMS) of the left dorsolateral cortex: EEG topography during waking and subsequent sleep Psychiatry Res 107 1 2001 1 9.
14. I. Griskova, O. Ruksenas, K. Dapsys, S. Herpertz, and J. Hoppner The effects of 10 Hz repetitive transcranial magnetic stimulation on resting EEG power spectrum in healthy subjects Neurosci Lett 419 2 2007 May 29 162 167.
15. H. Okamura, H. Jing, and M. Takigawa EEG modification induced by repetitive transcranial magnetic stimulation J Clin Neurophysiol 18 4 2001 318 325.
16. V.J. Knott Dynamic EEG changes during cigarette smoking Neuropsychobiology 19 1 1988 54 60.
17. E.F. Domino, M. Riskalla, Y. Zhang, and E. Kim Effects of tobacco smoking on the topographic EEG II Prog Neuropsychopharmacol Biol Psychiatry 16 4 1992 463 482.
18. E.F. Domino, and S. Matsuoka Effects of tobacco smoking on the topographic EEG I Prog Neuropsychopharmacol Biol Psychiatry 18 5 1994 879 889.
19. V.J. Knott, A. Harr, V. Ilivitsky, and C. Mahoney The cholinergic basis of the smoking-induced EEG activation profile Neuropsychobiology 38 2 1998 97 107.
20. V. Knott, M. Bosman, C. Mahoney, V. Ilivitsky, and K. Quirt Transdermal nicotine: single dose effects on mood, EEG, performance, and event-related potentials Pharmacol Biochem Behav 63 2 1999 253 261.
21. M. Lindgren, L. Molander, C. Verbaan, E. Lunell, and I. Rosén Electroencephalographic effects of intravenous nicotine - a dose-response study Psychopharmacology 145 3 1999 342 350.
22. X. Xiaojuan, and E.F. Domino Effects of tobacco smoking on topographic EEG and Stroop test in smoking deprived smokers Prog Neuropsychopharmacol Biol Psychiatry 24 4 2000 535 546.
23. V.J. Knott Electroencephalographic characterization of cigarette smoking behavior Alcohol 24 2 2001 95 97.
24. V.J. Knott, M. Raegele, D. Fisher, N. Robertson, A. Millar, and J. McIntosh et al. Clonidine pre-treatment fails to block acute smoking-induced EEG arousal/mood in cigarette smokers Pharmacol Biochem Behav 80 1 2005 161 171.
25. V.J. Knott, and D.J. Fisher Naltrexone alteration of the nicotine-induced EEG and mood activation response in tobacco-deprived cigarette smokers Exp Clin Psychopharmacol 15 4 2007 368 381.
26. D.J. Fisher, R. Daniels, A. Knobelsdorf, N. Jaworska, and V.J. Knott Effects of acute nicotine administration on resting EEG in nonsmokers Exp Clin Psychopharmacol 20 1 2012 71 75.
27. G.G. Knyazev Motivation, emotion, and their inhibitory control mirrored in brain oscillations Neurosci Biobehav Rev 31 3 2007 377 395.
28. G.G. Knyazev EEG delta oscillations as a correlate of basic homeostatic and motivational processes Neurosci Biobehav Rev 36 1 2012 677 695.
29. U. Krugel, H. Kittner, H. Franke, and P. Illes Purinergic modulation of neuronal activity in the mesolimbic dopaminergic system in vivo Synapse 47 2 2003 134 142.
30. J. Wacker, D.G. Dillon, and D.A. Pizzagalli The role of the nucleus accumbens and rostral anterior cingulate cortex in anhedonia: integration of resting EEG, fMRI, and volumetric techniques NeuroImage 46 1 2009 327 337.
31. T.F. Heatherton, L.T. Kozlowski, R.C. Frecker, and K.O. Fagerstrom The Fagerström test for nicotine dependence: a revision of the Fagerstrom Tolerance Questionnaire Br J Addict 86 9 1991 1119 1127.
32. R.C. Oldfield The assessment and analysis of handedness: the Edinburgh inventory Neuropsychologia 9 1971 97 113.
33. M.E. Jarvik, D.C. Madsen, R.E. Olmstead, P.N. Iwamoto-Schaap, J.L. Elins, and N.L. Benowitz Nicotine blood levels and subjective craving for cigarettes Pharmacol Biochem Behav 66 2000 553 558.
34. D. McBride, S.P. Barrett, J.T. Kelly, A. Aw, and A. Dagher Effects of expectancy and abstinence on the neural response to smoking cues in cigarette smokers: an fMRI study Neuropsychopharmacology 31 2006 2728 2738.
35. R. Gloria, L. Angelos, H.S. Schaefer, J.M. Davis, M. Majeskie, and B.S. Richmond et al. An fMRI investigation of the impact of withdrawal on regional brain activity during nicotine anticipation Psychophysiology 46 2009 681 693.
36. S.J. Wilson, M.A. Sayette, M.R. Delgado, and J.A. Fiez Instructed smoking expectancy modulates cue-elicited neural activity: a preliminary study Nicotine Tob Res 7 4 2005 Aug 637 645.
37. A. Droungas, R.N. Ehrman, A.R. Childress, and C.P. O'Brien Effect of smoking cues and cigarette availability on craving and smoking behavior Addict Behav 20 5 1995 657 673.
38. L.M. Juliano, and T.H. Brandon Reactivity to instructed smoking availability and environmental cues: evidence with urge and reaction time Exp Clin Psychopharmacol 6 1 1998 45 53.
39. B.L. Carter, and S.T. Tiffany The cue-availability paradigm: the effects of cigarette availability on cue reactivity in smokers Exp Clin Psychopharmacol 9 2 2001 183 190.
40. M.A. Sayette, J.M. Wertz, C.S. Martin, J.F. Cohn, M.A. Perrott, and J. Hobel Effects of smoking opportunity on cue-elicited urge: a facial coding analysis Exp Clin Psychopharmacol 11 3 2003 218 227.
41. P.J. Lang, M.M. Bradley, and B.N. Cuthbert International affective picture system (lAPS): affective ratings of pictures and instruction manual 2008 Technical Report A-8 Gainesville, FL.
42. D.J.L.G. Schutter, and J. van Honk A standardized motor threshold estimation procedure for transcranial magnetic stimulation research J ECT 22 3 2006 176 178.
43. J. Loughead, E.P. Wileyto, J.N. Valdez, P. Sanborn, K. Tang, and A.A. Strasser et al. Effect of abstinence challenge on brain function and cognition in smokers differs by COMT genotype Mol Psychiatry 14 8 2009 Aug 820 826.
44. F. Duecker, T.A. de Graaf, C. Jacobs, and A.T. Sack Time- and task-dependent non-neural effects of real and sham TMS PLoS One 9 2013 8.
45. P. Arias, J. Vivas, K.L. Grieve, and J. Cudeiro Controlled trial on the effect of 10 days low-frequency repetitive transcranial magnetic stimulation (rTMS) on motor signs in Parkinson's disease Mov Disord 25 12 2010 1830 1838.
46. P.L. Lockwood, G.D. Iannetti, and P. Haggard Transcranial magnetic stimulation over human secondary somatosensory cortex disrupts perception of pain intensity Cortex 49 8 2013 2201 2209.
47. I. Obeso, N. Robles, E. Muñoz-Marrón, and D. Redolar-Ripoll Dissociating the role of the pre-SMA in response inhibition and switching: a combined online and offline TMS approach Front Hum Neurosci 7 Apr 2013 150.
48. J.H. Ko, O. Monchi, A. Ptito, P. Bloomfield, S. Houle, and A.P. Strafella Theta burst stimulation-induced inhibition of dorsolateral prefrontal cortex reveals hemispheric asymmetry in striatal dopamine release during a set-shifting task - a TMS-[11C]raclopride PET study Eur J Neurosci 28 10 2008 2147 2155.
49. E. Kalbe, M. Schlegel, A.T. Sack, D.A. Nowak, M. Dafotakis, and C. Bangard et al. Dissociating cognitive from affective theory of mind: a TMS study Cortex 46 6 2010 769 780.
50. V. Dormal, M. Andres, and M. Pesenti Dissociation of numerosity and duration processing in the left intraparietal sulcus: a transcranial magnetic stimulation study Cortex 44 4 2008 462 469.
51. A. Knops, H.C. Nuerk, R. Sparing, H. Foltys, and K. Willmes On the functional role of human parietal cortex in number processing: how gender mediates the impact of a 'virtual lesion' induced by rTMS Neuropsychologia 44 12 2006 2270 2283.
52. C.C. Ruff, F. Blankenburg, O. Bjoertomt, S. Bestmann, E. Freeman, and J.D. Haynes et al. Concurrent TMS-fMRI and psychophysics reveal frontal influences on human retinotopic visual cortex Curr Biol 16 15 2006 1479 1488.
53. H. Bauer, C. Korunka, and M. Leodolter Technical requirements for high-quality scalp DC recordings Electroencephalogr Clin Neurophysiol 72 6 1989 545 547.
54. A. Delorme, T. Sejnowski, and S. Makeig Enhanced detection of artifacts in EEG data using higher-order statistics and independent component analysis NeuroImage 34 4 2007 1443 1449.
55. A.J. Bell, and T.J. Sejnowski An information-maximization approach to blind separation and blind deconvolution Neural Comput 7 6 1995 1129 1159.
56. T.W. Lee, M. Girolami, and T.J. Sejnowski Independent component analysis using an extended infomax algorithm for mixed subgaussian and supergaussian sources Neural Comput 11 2 1999 417 441.
57. G. Thut, and A. Pascual-Leone A review of combined TMS-EEG studies to characterize lasting effects of repetitive TMS and assess their usefulness in cognitive and clinical neuroscience Brain Topogr 22 4 2010 219 232.
58. A. Delorme, and S. Makeig EEGLAB: an open source toolbox for analysis of single-trial EEG dynamics including independent component analysis J Neurosci Methods 134 2004 9 21.
59. R. Gueorguieva, and J.H. Krystal Move over ANOVA: progress in analyzing repeated-measures data and its reflection in papers published in the Archives of General Psychiatry Arch Gen Psychiatry 61 3 2004 Mar 310 317.
60. C.E. McCulloch, and S.R. Searle Linear mixed models (LMMs). Generalized, linear, and mixed models 2005 John Wiley & Sons, Inc. Hoboken, NJ, USA 156 186.
61. R.H. Heck, S.L. Thomas, and L.N. Tabata Multilevel and longitudinal modeling with IBM SPSS 2011 Taylor & Francis Group New York: Routledge.
62. C. Metcalfe The analysis of cross-over trials with baseline measurements Stat Med 29 30 2010 3211 3218.
63. S. Senn Change from baseline and analysis of covariance revisited Stat Med 25 24 2006 4334 4344.
64. G. Schwarz Estimating the dimension of a model Ann Stat 6 1978 461 464.
65. R.C. Littell, J. Pendergast, and R. Natarajan Modelling covariance structure in the analysis of repeated measures data Stat Med 19 2000 1793 1819.
66. J.E. Rose, F.J. McClernon, B. Froeliger, F.M. Behm, X. Preud'Homme, and A.D. Krystal Repetitive transcranial magnetic stimulation of the superior frontal gyrus modulates craving for cigarettes Biol Psychiatry 70 8 2011 794 799.
67. V.C. Wing, I. Bacher, B.S. Wu, Z.J. Daskalakis, and T.P. George High frequency repetitive transcranial magnetic stimulation reduces tobacco craving in schizophrenia Schizophr Res 139 1-3 2012 264 266.
68. P.D. Livingstone, and S. Wonnacott Nicotinic acetylcholine receptors and the ascending dopamine pathways Biochem Pharmacol 78 7 2009 744 755.
69. S.P. Barrett, I. Boileau, J. Okker, R.O. Pihl, and A. Dagher The hedonic response to cigarette smoking is proportional to dopamine release in the human striatum as measured by positron emission tomography and [11C]raclopride Synapse 54 2 2004 65 71.
70. A.J. Montgomery, A.R. Lingford-Hughes, A. Egerton, D.J. Nutt, and P.M. Grasby The effect of nicotine on striatal dopamine release in man: a [11C]raclopride PET study Synapse 61 8 2007 637 645.
71. A.J. Jasinska, T. Zorick, A.L. Brody, and E.A. Stein Dual role of nicotine in addiction and cognition: a review of neuroimaging studies in humans Neuropharmacology 2013 http://dx.doi.org/10.1016/j.neuropharm.2013.02.015.
72. J. Roeper Dissecting the diversity of midbrain dopamine neurons Trends Neurosci 36 6 2013 336 342.
73. A.L. Krain, A.M. Wilson, R. Arbuckle, F.X. Castellanos, and M.P. Milham Distinct neural mechanisms of risk and ambiguity: a meta-analysis of decision-making NeuroImage 32 1 2006 477 484.
74. H.A. Diggs, B. Froeliger, J. Michael Carlson, and D. George Gilbert Smoker-nonsmoker differences in neural response to smoking-related and affective cues: an fMRI investigation Psychiatry Res 211 1 2013 85 87.
75. J. Pripfl, R. Neumann, U. Köhler, and C. Lamm Effects of transcranial direct current stimulation on risky decision making are mediated by 'hot' and 'cold' decisions, personality, and hemisphere Eur J Neurosci 2013 10.1111/ejn.12375.
76. A. Bechara Decision making, impulse control and loss of willpower to resist drugs: a neurocognitive perspective Nat Neurosci 8 11 2005 Nov 1458 1463 [Research Support, N.I.H., Extramural Review].
77. H. Garavan, K.L. Brennan, R. Hester, and R. Whelan The neurobiology of successful abstinence Curr Opin Neurobiol 23 4 2013 668 674.
78. M. Field, M.R. Munafò, and I.H.A. Franken A meta-analytic investigation of the relationship between attentional bias and subjective craving in substance abuse Psychol Bull 135 4 2009 589 607.
79. S. Fecteau, F. Fregni, P.S. Boggio, J.A. Camprodon, and A. Pascual-Leone Neuromodulation of decision-making in the addictive brain Subst Use Misuse 45 11 2010 1766 1786.
80. A. Hasenstaub, Y. Shu, B. Haider, U. Kraushaar, A. Duque, and D.A. McCormick Inhibitory postsynaptic potentials carry synchronized frequency information in active cortical networks Neuron 47 3 2005 423 435.
81. M.S. Barr, F. Farzan, K.D. Davis, P.B. Fitzgerald, and Z.J. Daskalakis Measuring GABAergic inhibitory activity with TMS-EEG and its potential clinical application for chronic pain J Neuroimmune Pharmacol 8 3 2013 535 546.
82. B. Takano, A. Drzezga, M. Peller, I. Sax, M. Schwaiger, and L. Lee et al. Short-term modulation of regional excitability and blood flow in human motor cortex following rapid-rate transcranial magnetic stimulation NeuroImage 23 3 2004 849 859.
83. F. Boy, C.J. Evans, R.A.E. Edden, A.D. Lawrence, K.D. Singh, and M. Husain et al. Dorsolateral prefrontal γ-aminobutyric acid in men predicts individual differences in rash impulsivity Biol Psychiatry 70 9 2011 866 872.
84. M.M. Silveri, J.T. Sneider, D.J. Crowley, M.J. Covell, D. Acharya, and I.M. Rosso et al. Frontal lobe γ-aminobutyric acid levels during adolescence: associations with impulsivity and response inhibition Biol Psychiatry 74 4 2013 296 304.
85. M.S. Barr, F. Farzan, P.M. Rusjan, R. Chen, P.B. Fitzgerald, and Z.J. Daskalakis Potentiation of gamma oscillatory activity through repetitive transcranial magnetic stimulation of the dorsolateral prefrontal cortex Neuropsychopharmacology 34 11 2009 Oct 2359 2367.
86. S. Sadaghiani, R. Scheeringa, K. Lehongre, B. Morillon, A.L. Giraud, and M. D'Esposito et al. Alpha-band phase synchrony is related to activity in the fronto-parietal adaptive control network J Neurosci 32 41 2012 14305 14310.
87. E. Azañón, M.R. Longo, S. Soto-Faraco, and P. Haggard The posterior parietal cortex remaps touch into external space Curr Biol 20 14 2010 1304 1309.
88. F. Versace, J.A. Minnix, J.D. Robinson, C.Y. Lam, V.L. Brown, and P.M. Cinciripini Brain reactivity to emotional, neutral and cigarette-related stimuli in smokers Addict Biol 16 2 2011 296 307.
89. M. Littel, I.H.A. Franken, and J.W. Van Strien Changes in the electroencephalographic spectrum in response to smoking cues in smokers and ex-smokers Neuropsychobiology 59 2009 43 50.
90. F.J. McClernon, R.V. Kozink, A.M. Lutz, and J.E. Rose 24-h smoking abstinence potentiates fMRI-BOLD activation to smoking cues in cerebral cortex and dorsal striatum Psychopharmacology 204 1 2009 May 25 35.
91. N.L. Watson, M.J. Carpenter, M.E. Saladin, K.M. Gray, and H.P. Upadhyaya Evidence for greater cue reactivity among low-dependent vs. high-dependent smokers Addict Behav 35 7 2010 673 677.
92. M.N. Smolka, M. Bühler, S. Klein, U. Zimmermann, K. Mann, and A. Heinz et al. Severity of nicotine dependence modulates cue-induced brain activity in regions involved in motor preparation and imagery Psychopharmacology 184 3-4 2006 577 588.
93. F.J. McClernon, R.V. Kozink, and J.E. Rose Individual differences in nicotine dependence, withdrawal symptoms, and sex predict transient fMRI-BOLD responses to smoking cues Neuropsychopharmacology 33 9 2008 2148 2157