Acute nicotine differentially impacts anticipatory valence- and magnitude-related striatal activity

Biological Psychiatry

Volumn 73, Issue 3, 2013, Pages 280-288

  Rose, Emma Jane ^a   Ross, Thomas J ^a   Salmeron, Betty Jo ^a   Lee, Mary ^a   Shakleya, Diaa M ^a   Huestis, Marilyn A ^a   Stein, Elliot A ^a  

^a NATIONAL INSTITUTE ON DRUG ABUSE   (United States)

Author keywords

Functional MRI; incentive salience; nicotine; reward; smoking; striatum

Indexed keywords

NICOTINE; NICOTINE PATCH;

ADULT; ANTICIPATION; ARTICLE; CLINICAL ARTICLE; CONTROLLED STUDY; CORPUS STRIATUM; DOPAMINERGIC SYSTEM; EVENT RELATED POTENTIAL; EXPOSURE; FEMALE; FUNCTIONAL MAGNETIC RESONANCE IMAGING; HUMAN; MALE; MONEY; NEUROIMAGING; OUTCOME ASSESSMENT; PRIORITY JOURNAL; RANDOMIZED CONTROLLED TRIAL; REINFORCEMENT; REWARD; SMOKING; TOBACCO DEPENDENCE;

ADMINISTRATION, CUTANEOUS; ADULT; BRAIN MAPPING; CORPUS STRIATUM; FEMALE; HUMANS; IMAGE PROCESSING, COMPUTER-ASSISTED; MAGNETIC RESONANCE IMAGING; MALE; MIDDLE AGED; MOTIVATION; NICOTINE; SMOKING; TOBACCO USE DISORDER;

EID: 84872679092     PISSN: 00063223     EISSN: 18732402     Source Type: Journal    
DOI: 10.1016/j.biopsych.2012.06.034     Document Type: Article

References (83)

1. S. Ikemoto Dopamine reward circuitry: Two projection systems from the ventral midbrain to the nucleus accumbens-olfactory tubercle complex Brain Res Rev 56 2007 27 78
2. S. Ikemoto, and J. Panksepp Dissociations between appetitive and consummatory responses by pharmacological manipulations of reward-relevant brain regions Behav Neurosci 110 1996 331 345
3. S. Ikemoto, and J. Panksepp The role of nucleus accumbens dopamine in motivated behavior: A unifying interpretation with special reference to reward-seeking Brain Res Rev 31 1999 6 41
4. W.J. McBride, J.M. Murphy, and S. Ikemoto Localization of brain reinforcement mechanisms: intracranial self-administration and intracranial place-conditioning studies Behav Brain Res 101 1999 129 152
5. E.K. Diekhof, P. Falkai, and O. Gruber Functional neuroimaging of reward processing and decision-making: A review of aberrant motivational and affective processing in addiction and mood disorders Brain Res Rev 59 2008 164 184
6. J.P. O'Doherty Reward representations and reward-related learning in the human brain: Insights from neuroimaging Curr Opin Neurobiol 14 2004 769 776
7. S.M. McClure, M.K. York, and P.R. Montague The neural substrates of reward processing in humans: The modern role of fMRI Neuroscientist 10 2004 260 268
8. R.A. Wise Roles for nigrostriatal - not just mesocorticolimbic - dopamine in reward and addiction Trends Neurosci 32 2009 517 524
9. G.F. Koob, and E.J. Nestler The neurobiology of drug addiction J Neuropsychiatry Clin Neurosci 9 1997 482 497
10. K.C. Berridge The debate over dopamine's role in reward: The case for incentive salience Psychopharmacology 191 2007 391 431
11. K.C. Berridge, and T.E. Robinson What is the role of dopamine in reward: hedonic impact, reward learning, or incentive salience? Brain Res Rev 28 1998 309 369
12. K.C. Berridge, and T.E. Robinson Parsing reward Trends Neurosci 26 2003 507 513
13. B. Knutson, C.M. Adams, G.W. Fong, and D. Hommer Anticipation of increasing monetary reward selectively recruits nucleus accumbens J Neurosci 21 2001 RC159
14. B. Knutson, G.W. Fong, C.M. Adams, J.L. Varner, and D. Hommer Dissociation of reward anticipation and outcome with event-related fMRI Neuroreport 12 2001 3683 3687
15. B. Knutson, G.W. Fong, S.M. Bennett, C.M. Adams, and D. Homme A region of mesial prefrontal cortex tracks monetarily rewarding outcomes: Characterization with rapid event-related fMRI NeuroImage 18 2003 263 272
16. B. Knutson, A. Westdorp, E. Kaiser, and D. Hommer FMRI visualization of brain activity during a monetary incentive delay task Neuroimage 12 2000 20 27
17. J.P. O'Doherty, R. Deichmann, H.D. Critchley, and R.J. Dolan Neural responses during anticipation of a primary taste reward Neuron 33 2002 815 826
18. G.S. Berns, S.M. McClure, G. Pagnoni, and P.R. Montague Predictability modulates human brain response to reward J Neurosci 21 2001 2793 2798
19. S.M. McClure, G.S. Berns, and P.R. Montague Temporal prediction errors in a passive learning task activate human striatum Neuron 38 2003 339 346
20. J. O'Doherty, P. Dayan, J. Schultz, R. Deichmann, K. Friston, and R.J. Dolan Dissociable roles of ventral and dorsal striatum in instrumental conditioning Science 304 2004 452 454
21. J. O'Doherty, M.L. Kringelbach, E.T. Rolls, J. Hornak, and C. Andrews Abstract reward and punishment representations in the human orbitofrontal cortex Nat Neurosci 4 2001 95 102
22. H.C. Breiter, I. Aharon, D. Kahneman, A. Dale, and P. Shizgal Functional imaging of neural responses to expectancy and experience of monetary gains and losses Neuron 30 2001 619 639
23. B. Knutson, J.M. Bjork, G.W. Fong, D. Hommer, V.S. Mattay, and D.R. Weinberger Amphetamine modulates human incentive processing Neuron 43 2004 261 269
24. J.A. Dani, and S. Heinemann Molecular and cellular aspects of nicotine abuse Neuron 16 1996 905 908
25. F. Clementi, D. Fornasari, and C. Gotti Neuronal nicotinic acetylcholine receptors: From structure to therapeutics Trends Pharmacol Sci 21 2000 35 37
26. C. Gotti, S. Guiducci, V. Tedesco, S. Corbioli, L. Zanetti, and M. Moretti Nicotinic acetylcholine receptors in the mesolimbic pathway: Primary role of ventral tegmental area alpha6beta2* receptors in mediating systemic nicotine effects on dopamine release, locomotion, and reinforcement J Neurosci 30 2010 5311 5325
27. M. Zoli, M. Moretti, A. Zanardi, J.M. McIntosh, F. Clementi, and C. Gotti Identification of the nicotinic receptor subtypes expressed on dopaminergic terminals in the rat striatum J Neurosci 22 2002 8785 8789
28. A. Azizian, J. Monterosso, J. O'Neill, and E.D. London Magnetic resonance imaging studies of cigarette smoking J.E. Henningfield, E.D. London, S. Pogun, Nicotine Psychopharmacology 2009 Spinger-Verlag Berlin 113 143
29. A.L. Brody, M.A. Mandelkern, R.E. Olmstead, J. Jou, E. Tiongson, and V. Allen Neural substrates of resisting craving during cigarette cue exposure Biol Psychiatry 62 2007 642 651
30. S.P. David, M.R. Munafo, H. Johansen-Berg, J. MacKillop, L.H. Sweet, and R.A. Cohen Effects of acute nicotine abstinence on cue-elicited ventral striatum/nucleus accumbens activation in female cigarette smokers: A functional magnetic resonance imaging study Brain Imaging Behav 1 2007 43 57
31. S.P. David, M.R. Munafo, H. Johansen-Berg, S.M. Smith, R.D. Rogers, and P.M. Matthews Ventral striatum/nucleus accumbens activation to smoking-related pictorial cues in smokers and nonsmokers: A functional magnetic resonance imaging study Biol Psychiatry 58 2005 488 494
32. D.L. Due, S.A. Huettel, W.G. Hall, and D.C. Rubin Activation in mesolimbic and visuospatial neural circuits elicited by smoking cues: Evidence from functional magnetic resonance imaging Am J Psychiatry 159 2002 954 960
33. 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
34. M.N. Smolka, M. Buhler, S. Klein, U. Zimmermann, K. Mann, and A. Heinz Severity of nicotine dependence modulates cue-induced brain activity in regions involved in motor preparation and imagery Psychopharmacology 184 2006 577 588
35. X. Zhang, B.J. Salmeron, T.J. Ross, H. Gu, X. Geng, and Y. Yang Anatomical differences and network characteristics underlying smoking cue reactivity Neuroimage 54 2011 131 141
36. J. Peters, U. Bromberg, S. Schneider, S. Brassen, M. Menz, and T. Banaschewski Lower ventral striatal activation during reward anticipation in adolescent smokers Am J Psychiatry 168 2011 540 549
37. M. Buhler, S. Vollstadt-Klein, A. Kobiella, H. Budde, L.J. Reed, and D.F. Braus Nicotine dependence is characterized by disordered reward processing in a network driving motivation Biol Psychiatry 67 2010 745 752
38. E.J. Rose, T.J. Ross, B.J. Salmeron, M. Lee, D.M. Shakleya, and M. Huestis Chronic exposure to nicotine is associated with reduced reward-related activity in the striatum but not the midbrain Biol Psychiatry 71 2012 206 213
39. E.C. Donny, A.R. Caggiula, M.T. Weaver, M.E. Levin, and A.F. Sved The reinforcement-enhancing effects of nicotine: Implications for the relationship between smoking, eating and weight Physiol Behav 104 2011 143 148
40. E.C. Donny, N. Chaudhri, A.R. Caggiula, F.F. Evans-Martin, S. Booth, and M.A. Gharib Operant responding for a visual reinforcer in rats is enhanced by noncontingent nicotine: Implications for nicotine self-administration and reinforcement Psychopharmacology (Berl) 169 2003 68 76
41. M.I. Palmatier, F.F. Evans-Martin, A. Hoffman, A.R. Caggiula, N. Chaudhri, and E.C. Donny Dissociating the primary reinforcing and reinforcement-enhancing effects of nicotine using a rat self-administration paradigm with concurrently available drug and environmental reinforcers Psychopharmacology (Berl) 184 2006 391 400
42. M.I. Palmatier, X. Liu, A.R. Caggiula, E.C. Donny, and A.F. Sved The role of nicotinic acetylcholine receptors in the primary reinforcing and reinforcement-enhancing effects of nicotine Neuropsychopharmacology 32 2007 1098 1108
43. T.F. Heatherton, L.T. Kozlowski, R.C. Frecker, and K.O. Fagerstrom The Fagerstrom Test for Nicotine Dependence - A revision of the Fagerstrom Tolerance Questionnaire Br J Addict 86 1991 1119 1127
44. J. Gorsline, S.K. Gupta, D. Dye, and C.N. Rolf Steady-state pharmacokinetics and dose relationship of nicotine delivered from Nicoderm (Nicotine Transdermal System) J Clin Pharmacol 33 1993 161 168
45. P.S. Hendricks, J.W. Ditre, D.J. Drobes, and T.J. Brandon The early time course of smoking withdrawal effects Psychopharmacology 187 2006 385 396
46. A.C. Parrott, N.J. Garnham, K. Wesnes, and C. Pincock Cigarette smoking and abstinence: Comparative effects upon cognitive task performance and mood state over 24 hours Hum Psychopharmacol Clin Exp 11 1996 391 400
47. S.J. Heishman, E.G. Singleton, and E.T. Moolchan Tobacco Craving Questionnaire: Reliability and validity of a new multifactorial instrument Nicotine Tob Res 5 2003 645 654
48. S.J. Heishman, E.G. Singleton, and W.B. Pickworth Reliability and validity of a short form of the tobacco craving questionnaire Nicotine Tob Res 10 2007 643 651
49. D. Kahneman, and A. Tversky Prospect theory - Analysis of decision under risk Econometrica 47 1979 263 291
50. D.M. Shakleya, and M.A. Huestis Simultaneous and sensitive measurement of nicotine, cotinine, trans-3'-hydroxycotinine and norcotinine in human plasma by liquid chromatography-tandem mass spectrometry J Chromatogr B Analyt Technol Biomed Life Sci 877 2009 3537 3542
51. R.M. Reitan, and D. Wolfson The Halstead-Reitan Neuropsychological Test Battery 1993 Neuropsychology Press Tuscan, AZ
52. D. Wechsler Wecshler Memory Scale - Revised Manual 1987 The Psychological Corporation San Antonio, TX
53. C.R. Cloninger, T.R. Przybeck, D.M. Svrakic, and R.D. Wetzel The Temperament and Character Inventory (TCI): A Guide to Its Development and Use 1994 Washington University, Center for Psychobiology of Personality St. Louis, MO
54. D.P. Bernstein, L. Fink, L. Handelsman, J. Foote, M. Lovejoy, and K. Wenzel Initial reliability and validity of a new retrospective measure of child abuse and neglect Am J Psychiatry 151 1994 1132 1136
55. T.S. Brugha, P.E. Bebbington, D.D. Stretch, B. MacCarthy, and T. Wykes Predicting the short-term outcome of first episodes and recurrences of clinical depression: A prospective study of life events, difficulties, and social support networks J Clin Psychiatry 58 1997 298 306
56. A.T. Beck The Beck Anxiety Inventory 1993 The Psychological Corporation London
57. A.T. Beck The Beck Depression Inventory - II 1996 The Psychological Corporation London
58. D. Watson, L.A. Clark, and A. Tellegen Development and validation of brief measures of positive and negative affect: The PANAS scales J Pers Soc Psychol 54 1988 1063 1070
59. R.C. Kessler, G. Andrews, L.J. Colpe, E. Hiripi, D.K. Mroczek, and S.L. Normand Short screening scales to monitor population prevalences and trends in non-specific psychological distress Psychol Med 32 2002 959 976
60. R.W. Cox AFNI software for analysis and visualization of functional magnetic resonance neuroimages Comput Biomed Res 29 1996 162 173
61. J. Talairach, and P. Tournoux Co-Planar Stereotaxic Atlas of the Human Brain 1988 Thieme New York
62. A. Sharma, and A.L. Brody In vivo brain imaging of human exposure to nicotine and tobacco Handb Exp Pharmacol 192 2009 145 171
63. S.N. Haber, and B. Knutson The reward circuit: Linking primate anatomy and human imaging Neuropsychopharmacology 35 2010 4 26
64. R.E. Penton, and R.A. Lester Cellular events in nicotine addiction Semin Cell Dev Biol 20 2009 418 431
65. C. Xiao, R. Nashmi, S. McKinney, H. Cai, J.M. McIntosh, and H.A. Lester Chronic nicotine selectively enhances alpha4beta2* nicotinic acetylcholine receptors in the nigrostriatal dopamine pathway J Neurosci 29 2009 12428 12439
66. R. Nashmi, C. Xiao, P. Deshpande, S. McKinney, S.R. Grady, and P. Whiteaker 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 2007 8202 8218
67. S.E. McCallum, N. Parameswaran, T. Bordia, H. Fan, R.F. Tyndale, and J.W. Langston Increases in alpha4* but not alpha3*/alpha6* nicotinic receptor sites and function in the primate striatum following chronic oral nicotine treatment J Neurochem 96 2006 1028 1041
68. N. Champtiaux, C. Gotti, M. Cordero-Erausquin, D.J. David, C. Przybylski, and C. Lena Subunit composition of functional nicotinic receptors in dopaminergic neurons investigated with knock-out mice J Neurosci 23 2003 7820 7829
69. S. Glautier, K. Clements, J.A. White, C. Taylor, and I.P. Stolerman Alcohol and the reward value of cigarette smoking Behav Pharmacol 7 1996 144 154
70. M.R. Delgado, H.M. Locke, V.A. Stenger, and J.A. Fiez Dorsal striatum responds to reward and punishment: Effects of valence and magnitude manipulations Cogn Affect Behav Neurosci 3 2003 27 38
71. B.J. Everitt, D. Belin, D. Economidou, Y. Pelloux, J.W. Dalley, and T.W. Robbins Review Neural mechanisms underlying the vulnerability to develop compulsive drug-seeking habits and addiction Phil Trans R Soc B Biol Sci 363 2008 3125 3135
72. B.J. Everitt, A. Dickinson, and T.W. Robbins The neuropsychological basis of addictive behaviour Brain Res Brain Res Rev 36 2001 129 138
73. T.W. Robbins, and B.J. Everitt Drug addiction: Bad habits add up Nature 398 1999 567 570
74. L.J. Vanderschuren, P. Di Ciano, and B.J. Everitt Involvement of the dorsal striatum in cue-controlled cocaine seeking J Neurosci 25 2005 8665 8670
75. B.W. Balleine, and J.P. O'Doherty Human and rodent homologies in action control: corticostriatal determinants of goal-directed and habitual control Neuropsychopharmacology 35 2010 48 69
76. R.Z. Goldstein, D. Tomasi, N. Alia-Klein, L.A. Cottone, L. Zhang, and F. Telang Subjective sensitivity to monetary gradients is associated with frontolimbic activation to reward in cocaine abusers Drug Alcohol Depend 87 2007 233 240
77. R.Z. Goldstein, N. Alia-Klein, D. Tomasi, L. Zhang, L.A. Cottone, and T. Maloney Is decreased prefrontal cortical sensitivity to monetary reward associated with impaired motivation and self-control in cocaine addiction? Am J Psychiatry 164 2007 43 51
78. T.E. Robinson, and K.C. Berridge The incentive sensitization theory of addiction: Some current issues Phil Trans R Soc B Biol Sci 363 2008 3137 3146
79. C.F. Zink, G. Pagnoni, J. Chappelow, M. Martin-Skurski, and G.S. Berns Human striatal activation reflects degree of stimulus saliency NeuroImage 29 2006 977 983
80. C.F. Zink, G. Pagnoni, M.E. Martin, M. Dhamala, and G.S. Berns Human striatal response to salient nonrewarding stimuli J Neurosci 23 2003 8092 8097
81. C.F. Zink, G. Pagnoni, M.E. Martin-Skurski, J.C. Chappelow, and G.S. Berns Human striatal responses to monetary reward depend on saliency Neuron 42 2004 509 517
82. J.R. Hughes, S.T. Higgins, and W.K. Bickel Nicotine withdrawal versus other drug withdrawal syndromes: Similarities and dissimilarities Addiction 89 1994 1461 1470
83. C. Lerman, C. Jepson, E.P. Wileyto, F. Patterson, R. Schnoll, and M. Mroziewicz Genetic variation in nicotine metabolism predicts the efficacy of extended-duration transdermal nicotine therapy Clin Pharmacol Ther 87 2010 553 557