Nicotine Dependence Is Characterized by Disordered Reward Processing in a Network Driving Motivation
Abstract
Background Drug addiction is characterized by an unhealthy priority for drug consumption with a compulsive, uncontrolled drug-intake pattern due to a disordered motivational system. However, only some individuals become addicted, whereas others maintain regular but controlled drug use. Whether the transition occurs might depend on how individuals process drug relative to nondrug reward.Methods We applied functional magnetic resonance imaging to measure mesocorticolimbic activity to stimuli predicting monetary or cigarette reward, together with behavioral assessment of subsequent motivation to obtain the respective reward on a trial-by-trial basis, in 21 nicotine-dependent and 21 nondependent, occasional smokers.Results Occasional smokers showed increased reactivity of the mesocorticolimbic system to stimuli predicting monetary reward relative to cigarette reward and subsequently spent more effort to obtain money. In the group of dependent smokers, we found equivalent anticipatory activity and subsequent instrumental response rates for both reward types. Additionally, anticipatory mesocorticolimbic activation predicted subsequent motivation to obtain reward.Conclusions This imbalance in the incentive salience of drug relative to nondrug reward-predicting cues, in a network that drives motivation to obtain reward, could represent a central mechanism of drug addiction.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
Nicotine-dependent participants show mesocorticolimbic hypoactivation during monetary-reward motivation, which predicts motivation to obtain rewards.
“Bühler and collegues [154] reported mesocorticolimbic hypoactivation during monetary-reward motivation in nicotine-dependent participants, which predicted motivation to obtain rewards.”
From Reward circuitry dysfunction in psychiatric and neurodevelopmental disorders and genetic syndromes: animal models and clinical findings (2012) · cites this paper as [154]
The few studies that have evaluated potential relations between mesolimbic neural activity and subjectively experienced reward or motivation to work for rewards have yielded promising initial results suggesting the external validity of laboratory-based measures of reward processes.
“The few studies that have evaluated potential relations between mesolimbic neural activity and subjectively experienced reward [220] or motivation to work for rewards [154] have yielded promising initial results suggesting the external validity of laboratory-based measures of reward processes”
From Reward circuitry dysfunction in psychiatric and neurodevelopmental disorders and genetic syndromes: animal models and clinical findings (2012) · cites this paper as [154]
Cites
Tzourio-Mazoyer, N., Landeau, B., Papathanassiou, D., Crivello, F., Etard, O., Delcroix, N., Mazoyer, B., & Joliot, M. (2002) · NeuroImage · doi:10.1006/nimg.2001.0978 · Cited by 16,319 · see citing works
The Fagerstrom Test for Nicotine Dependence: a revision of the Fagerstrom Tolerance Questionnaire
HEATHERTON, T. F., KOZLOWSKI, L. T., FRECKER, R. C., & FAGERSTROM, K. (1991) · British Journal of Addiction · doi:10.1111/j.1360-0443.1991.tb01879.x · Cited by 10,738 · see citing works
Neural systems of reinforcement for drug addiction: from actions to habits to compulsion
Everitt, B. J., & Robbins, T. W. (2005) · Nature Neuroscience · doi:10.1038/nn1579 · Cited by 3,785 · see citing works
The debate over dopamine’s role in reward: the case for incentive salience
Berridge, K. C. (2007) · Psychopharmacology · doi:10.1007/s00213-006-0578-x · Cited by 2,347 · see citing works
Robinson, T. E., & Berridge, K. C. (2003) · Annual Review of Psychology · doi:10.1146/annurev.psych.54.101601.145237 · Cited by 1,509 · see citing works
Relative reward preference in primate orbitofrontal cortex
Tremblay, L., & Schultz, W. (1999) · Nature · doi:10.1038/19525 · Cited by 1,314 · see citing works
Optimal decision making and the anterior cingulate cortex
Kennerley, S. W., Walton, M. E., Behrens, T. E. J., Buckley, M. J., & Rushworth, M. F. S. (2006) · Nature Neuroscience · doi:10.1038/nn1724 · Cited by 948 · see citing works
Cue-induced cocaine craving: neuroanatomical specificity for drug users and drug stimuli
Garavan, H., Pankiewicz, J., Bloom, A., Cho, J.-K., Sperry, L., Ross, T. J., Salmeron, B. J., Risinger, R., Kelley, D., & Stein, E. A. (2000) · American Journal of Psychiatry · doi:10.1176/appi.ajp.157.11.1789 · Cited by 931 · see citing works
Optimized EPI for fMRI studies of the orbitofrontal cortex
Deichmann, R., Gottfried, J. A., Hutton, C., & Turner, R. (2003) · NeuroImage · doi:10.1016/s1053-8119(03)00073-9 · Cited by 821 · see citing works
BOLD responses reflecting dopaminergic signals in the human ventral tegmental area
D'Ardenne, K., McClure, S. M., Nystrom, L. E., & Cohen, J. D. (2008) · Science · doi:10.1126/science.1150605 · Cited by 661 · see citing works
How the Brain Translates Money into Force: A Neuroimaging Study of Subliminal Motivation
Pessiglione, M., Schmidt, L., Draganski, B., Kalisch, R., Lau, H., Dolan, R. J., & Frith, C. D. (2007) · Science · doi:10.1126/science.1140459 · Cited by 634 · see citing works
Gr�sser, S. M., Wrase, J., Klein, S., Hermann, D., Smolka, M. N., Ruf, M., Weber-Fahr, W., Flor, H., Mann, K., Braus, D. F., et al. (2004) · Psychopharmacology · doi:10.1007/s00213-004-1828-4 · Cited by 598 · see citing works
Self-citationDysfunction of reward processing correlates with alcohol craving in detoxified alcoholics
Wrase, J., Schlagenhauf, F., Kienast, T., Wüstenberg, T., Bermpohl, F., Kahnt, T., Beck, A., Ströhle, A., Juckel, G., Knutson, B. D., et al. (2007) · NeuroImage · doi:10.1016/j.neuroimage.2006.11.043 · Cited by 480 · see citing works
The neural substrates of reward processing in humans: the modern role of FMRI
McClure, S. M., York, M. K., & Montague, P. R. (2004) · The Neuroscientist · doi:10.1177/1073858404263526 · Cited by 480 · cited 1× · see citing works
“e focus our report on the mesocorticolimbic system including he anterior cingulate cortex (Brodmann’s area 24, 25, 32, and 3), orbitofrontal and medial prefrontal regions, globus pallidus, audate nucleus, and putamen comprising the ventral striatum nd the ventral tegmental area because this brain network is ritically…”
BackgroundSalamone, J. D., Correa, M., Mingote, S., & Weber, S. M. (2003) · The Journal of Pharmacology and Experimental Therapeutics · doi:10.1124/jpet.102.035063 · Cited by 433 · see citing works
Brain metabolic changes during cigarette craving
Brody, A. L., Mandelkern, M. A., London, E. D., Childress, A. R., Lee, G. S., Bota, R. G., Ho, M. L., Saxena, S., Baxter, L. R., Madsen, D., et al. (2002) · Archives of General Psychiatry · doi:10.1001/archpsyc.59.12.1162 · Cited by 425 · see citing works
Cue Reactivity and Cue Reactivity Interventions in Drug Dependence
Childress, A. R., Hole, A. V., Ehrman, R. N., Robbins, S. J., McLellan, A. T., & O’Brien, C. P. (1993) · PsycEXTRA Dataset · doi:10.1037/e495912006-006 · Cited by 368 · see citing works
David, S. P., Munafo, M. R., Johansen‐Berg, H., Smith, S. M., Rogers, R. D., Matthews, P. M., & Walton, R. T. (2005) · Biological Psychiatry · doi:10.1016/j.biopsych.2005.04.028 · Cited by 275 · see citing works
Goldstein, R. Z., Alia-Klein, N., Tomasi, D., Zhang, L., Cottone, L. A., Maloney, T., Telang, F., Caparelli, E. C., Chang, L., Ernst, T., et al. (2007) · American Journal of Psychiatry · doi:10.1176/ajp.2007.164.1.43 · Cited by 258 · see citing works
Smolka, M. N., Bühler, M., Klein, S., Zimmermann, U., Mann, K., Heinz, A., & Braus, D. F. (2006) · Psychopharmacology · doi:10.1007/s00213-005-0080-x · Cited by 230 · see citing works
Self-citationCue exposure treatment for smoking relapse prevention: a controlled clinical trial
NIAURA, R. S., Abrams, D. B., Shadel, W. G., Rohsenow, D. J., Monti, P. M., & Sirota, A. D. (1999) · Addiction · doi:10.1046/j.1360-0443.1999.9456856.x · Cited by 188 · see citing works
Neural activity related to the processing of increasing monetary reward in smokers and nonsmokers
Martin-Söelch, C., Missimer, J. H., Leenders, K. L., & Schultz, W. (2003) · European Journal of Neuroscience · doi:10.1046/j.1460-9568.2003.02791.x · Cited by 66 · see citing works
Ooteman, W., Koeter, M. W. J., Verheul, R., Schippers, G. M., & van den Brink, W. (2007) · European Neuropsychopharmacology · doi:10.1016/j.euroneuro.2007.02.012 · Cited by 65 · see citing works
Peters, Y. M., O’Donnell, P., & Carelli, R. M. (2005) · Synapse · doi:10.1002/syn.20129 · Cited by 49 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
Dysfunction of the prefrontal cortex in addiction: neuroimaging findings and clinical implications
Goldstein, R. Z., & Volkow, N. D. (2011) · Nature Reviews Neuroscience · doi:10.1038/nrn3119 · Cited by 2,749 · see citing works
The neural mechanisms of inter-temporal decision-making: understanding variability
Peters, J., & Büchel, C. (2011) · Trends in Cognitive Sciences · doi:10.1016/j.tics.2011.03.002 · Cited by 693 · see citing works
Self-citationDysfunctional reward circuitry in obsessive-compulsive disorder
Figee, M., Vink, M., de Geus, F., Vulink, N., Veltman, D. J., Westenberg, H., & Denys, D. (2011) · Biological Psychiatry · doi:10.1016/j.biopsych.2010.12.003 · Cited by 315 · see citing works
Dichter, G. S., Damiano, C. A., & Allen, J. A. (2012) · Journal of Neurodevelopmental Disorders · doi:10.1186/1866-1955-4-19 · Cited by 299 · see citing works
Hogarth, L., & Chase, H. W. (2011) · Journal of Experimental Psychology: Animal Behavior Processes · doi:10.1037/a0022913 · Cited by 225 · see citing works
Lower Ventral Striatal Activation During Reward Anticipation in Adolescent Smokers
Peters, J., Bromberg, U., Schneider, S., Brassen, S., Menz, M., Banaschewski, T., Conrod, P. J., Flor, H., Gallinat, J., Garavan, H., et al. (2011) · American Journal of Psychiatry · doi:10.1176/appi.ajp.2010.10071024 · Cited by 218 · see citing works
Self-citationMeasuring wanting and liking from animals to humans: a systematic review
Pool, E., Sennwald, V., Delplanque, S., Brosch, T., & Sander, D. (2016) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2016.01.006 · Cited by 211 · see citing works
Risk taking and the adolescent reward system: A potential common link to substance abuse
Schneider, S., Peters, J., Bromberg, U., Brassen, S., Miedl, S. F., Banaschewski, T., Barker, G. J., Conrod, P., Flor, H., Garavan, H., et al. (2012) · American Journal of Psychiatry · doi:10.1176/appi.ajp.2011.11030489 · Cited by 186 · see citing works
Self-citationImaging brain response to reward in addictive disorders
Hommer, D. W., Bjork, J. M., & Gilman, J. M. (2011) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.2010.05898.x · Cited by 163 · see citing works
Jia, Z., Worhunsky, P. D., Carroll, K. M., Rounsaville, B. J., Stevens, M. C., Pearlson, G. D., & Potenza, M. N. (2011) · Biological Psychiatry · doi:10.1016/j.biopsych.2011.05.008 · Cited by 147 · see citing works
Efficacy of invasive and non-invasive brain modulation interventions for addiction
Luigjes, J., Segrave, R., de Joode, N., Figee, M., & Denys, D. (2019) · Neuropsychology Review · doi:10.1007/s11065-018-9393-5 · Cited by 125 · see citing works
Pathological choice: the neuroscience of gambling and gambling addiction
Clark, L., Averbeck, B., Payer, D., Sescousse, G., Winstanley, C. A., & Xue, G. (2013) · The Journal of Neuroscience · doi:10.1523/jneurosci.3231-13.2013 · Cited by 116 · see citing works
Klugah‐Brown, B., Di, X., Zweerings, J., Mathiak, K., Becker, B., & Biswal, B. (2020) · Human Brain Mapping · doi:10.1002/hbm.25085 · Cited by 86 · see citing works
Striatal dopamine release codes uncertainty in pathological gambling
Linnet, J., Mouridsen, K., Peterson, E., Møller, A., Doudet, D. J., & Gjedde, A. (2012) · Psychiatry Research: Neuroimaging · doi:10.1016/j.pscychresns.2012.04.012 · Cited by 82 · see citing works
Neural substrates of smoking and reward cue reactivity in smokers: a meta-analysis of fMRI studies
Lin, X., Deng, J., Shi, L., Wang, Q., Li, P., Li, H., Liu, J., Que, J., Chang, S., Bao, Y., et al. (2020) · Translational Psychiatry · doi:10.1038/s41398-020-0775-0 · Cited by 78 · see citing works
Bjork, J. M., Smith, A. R., Chen, G., & Hommer, D. W. (2012) · Human Brain Mapping · doi:10.1002/hbm.21351 · Cited by 70 · see citing works
Kroemer, N. B., Guevara, A., Ciocanea Teodorescu, I., Wuttig, F., Kobiella, A., & Smolka, M. N. (2014) · NeuroImage · doi:10.1016/j.neuroimage.2014.07.060 · Cited by 64 · see citing works
Self-citationGarrison, K. A., Yip, S. W., Balodis, I. M., Carroll, K. M., Potenza, M. N., & Krishnan-Sarin, S. (2017) · Drug and Alcohol Dependence · doi:10.1016/j.drugalcdep.2017.03.035 · Cited by 65 · see citing works
Altered Reward Processing in Adolescents With Prenatal Exposure to Maternal Cigarette Smoking
Müller, K. U. (2013) · JAMA Psychiatry · doi:10.1001/jamapsychiatry.2013.44 · Cited by 64 · see citing works
Jansma, J. M., van Hell, H. H., Vanderschuren, L. J. M. J., Bossong, M. G., Jager, G., Kahn, R. S., & Ramsey, N. F. (2013) · Translational Psychiatry · doi:10.1038/tp.2013.6 · Cited by 58 · see citing works
The developmental psychopathology of motivation in adolescence
Fairchild, G. (2011) · Developmental Cognitive Neuroscience · doi:10.1016/j.dcn.2011.07.009 · Cited by 53 · see citing works
Implicit and explicit reward learning in chronic nicotine use
Paelecke-Habermann, Y., Paelecke, M., Giegerich, K., Reschke, K., & Kübler, A. (2013) · Drug and Alcohol Dependence · doi:10.1016/j.drugalcdep.2012.09.004 · Cited by 13 · see citing works
Isomura, T., Suzuki, J., & Murai, T. (2014) · Addiction Research & Theory · doi:10.3109/16066359.2013.793312 · Cited by 12 · see citing works
Moses-Kolko, E. L., Forbes, E. E., Stepp, S., Fraser, D., Keenan, K. E., Guyer, A. E., Chase, H. W., Phillips, M. L., Zevallos, C. R., Guo, C., et al. (2016) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2016.01.009 · Cited by 6 · see citing works
- Authors
- Bühler, M., Vollstädt-Klein, S., Kobiella, A., Budde, H., Reed, L. J., Braus, D. F., Büchel, C., & Smolka, M. N.
- Affiliations
- Heidelberg University (DE)
- Humboldt-Universität zu Berlin (DE)
- King's College London (GB)
- University Medical Center Hamburg-Eppendorf (DE)
- Neuroimaging Center (DE)
- Corresponding author
- Smolka, Michael N.
- Venue
- Biological Psychiatry
- Publisher
- Elsevier BV
- Published
- 2010-04
- Volume
- 67
- Issue
- 8
- Pages
- 745-752
- ISSN
- 0006-3223 (ISSN-L)
- OpenAlex
- W1988708433
- Cited by
- 185
- References
- 24
- Citations by year
- 2026: 1 · 2025: 2 · 2024: 5 · 2023: 5 · 2022: 5 · 2021: 6 · 2020: 16 · 2019: 10 · 2018: 9 · 2017: 14 · 2016: 22 · 2015: 10 · 2014: 20 · 2013: 25 · 2012: 13
- FWCI
- 7.50
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Biological Psychiatry (publishedVersion)
- PubMed (publishedVersion)
- Research Portal (King's College London) (submittedVersion)
- Funders
- Deutsche Forschungsgemeinschaft (SM 80/1-1, SM 80/1-2, SM 80/5-1)
- Pfizer
- Topics
- Health Sciences › Medicine › Physiology › Smoking Behavior and Cessation
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neurotransmitter Receptor Influence on Behavior
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Nicotinic Acetylcholine Receptors Study
- Keywords
- nicotine dependence, drug addiction, reward processing, incentive salience, mesocorticolimbic system, motivation, monetary rewards, occasional smokers
- MeSH terms
- Algorithms, Cerebral Cortex, Cues, Humans, Functional Laterality, Limbic System, Magnetic Resonance Imaging, Motivation, Nerve Net, Oxygen, Reward, Smoking, Substance Withdrawal Syndrome, Tobacco Use Disorder, Feedback, Psychological
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review