Smoking-related cue-induced brain activation in adolescent light smokers
Open accessAbstract
Purpose To examine using functional magnetic resonance imaging whether adolescents with low levels of nicotine exposure (light smokers) display neural activation in areas shown to be involved with addiction in response to smoking-related stimuli.Design/setting/participants A total of 12 adolescent light smokers (aged 13-17, who smoked 1-5 cigarettes per day) and 12 nonsmokers (ages 13-17, never smoked a cigarette) from the San Francisco Bay Area underwent functional magnetic resonance imaging scanning. During scanning, the adolescents were shown photographic blocks of smoking and control cues. Smoking cues comprised pictures of individuals smoking cigarettes and smoking-related objects such as lighters and ashtrays. Neutral cues comprised images of everyday objects and individuals engaged in daily activities.Findings For smokers, smoking cues elicited greater activation than neutral cues in the mesolimbic reward circuit (left anterior cingulate: t = 7.04, p < .001; right hippocampus: t = 6.37, p < .001). We found activation from smoking cues versus neutral cues within both the left and right frontal medial orbital regions (t = 5.09, p < .001 and t = 3.94, p = .001, respectively). Nonsmokers showed no significant difference in activation between smoking-related cues and neutral cues.Conclusion Our finding that smoking cues produced activation in adolescent light smokers in brain regions, similar to that seen in adult and teenage heavy smokers, suggests that adolescents exhibit heightened reactivity to smoking cues even at low levels of smoking. This article adds to the existing published data by suggesting that nicotine dependence may begin with exposure to low levels of nicotine, thus underscoring the need for early intervention among adolescent smokers.
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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
Goldstein, R. Z., & Volkow, N. D. (2002) · American Journal of Psychiatry · doi:10.1176/appi.ajp.159.10.1642 · Cited by 2,667 · see citing works
Cellular and molecular mechanisms of drug dependence
Koob, G. F., & Bloom, F. E. (1988) · Science · doi:10.1126/science.2903550 · Cited by 2,070 · see citing works
Limbic Activation During Cue-Induced Cocaine Craving
Childress, A. R., Mozley, P. D., McElgin, W., Fitzgerald, J., Reivich, M., & O’Brien, C. P. (1999) · American Journal of Psychiatry · doi:10.1176/ajp.156.1.11 · Cited by 1,513 · see citing works
Is there a common molecular pathway for addiction?
Nestler, E. J. (2005) · Nature Neuroscience · doi:10.1038/nn1578 · Cited by 1,388 · see citing works
Addiction, a disease of compulsion and drive: involvement of the orbitofrontal cortex
Volkow, N. D. (2000) · Cerebral Cortex · doi:10.1093/cercor/10.3.318 · Cited by 1,240 · see citing works
The addicted human brain: insights from imaging studies
Volkow, N. D., Fowler, J. S., & Wang, G.-J. (2003) · Journal of Clinical Investigation · doi:10.1172/jci18533 · Cited by 916 · see citing works
Dramatic decreases in brain reward function during nicotine withdrawal
Epping-Jordan, M. P., Watkins, S. S., Koob, G. F., & Markou, A. (1998) · Nature · doi:10.1038/30001 · Cited by 674 · 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
Volkow, N. D., Fowler, J. S., & Wang, G.-J. (2004) · Neuropharmacology · doi:10.1016/j.neuropharm.2004.07.019 · Cited by 616 · see citing works
Initial symptoms of nicotine dependence in adolescents
DiFranza, J. R. (2000) · Tobacco Control · doi:10.1136/tc.9.3.313 · Cited by 574 · see citing works
Nicotine-Induced Limbic Cortical Activation in the Human Brain: A Functional MRI Study
Stein, E. A., Pankiewicz, J., Harsch, H. H., Cho, J.-K., Fuller, S. A., Hoffmann, R. G., Hawkins, M., Rao, S. M., Bandettini, P. A., & Bloom, A. S. (1998) · American Journal of Psychiatry · doi:10.1176/ajp.155.8.1009 · Cited by 483 · see citing works
Due, D. L., Huettel, S. A., HALL, W. G., & Rubin, D. C. (2002) · American Journal of Psychiatry · doi:10.1176/appi.ajp.159.6.954 · Cited by 429 · see citing works
(2006) · Neuroscience · doi:10.1016/s0306-4522(05)01473-9 · Cited by 427 · 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
Franklin, T. R., wang, Z., Wang, J., Sciortino, N., Harper, D., Li, Y., Ehrman, R., Kampman, K. M., O’Brien, C. P., Detre, J. A., et al. (2007) · Neuropsychopharmacology · doi:10.1038/sj.npp.1301371 · Cited by 359 · see citing works
Regional brain metabolic activation during craving elicited by recall of previous drug experiences
Wang, G.-J., Volkow, N. D., Fowler, J. S., Cervany, P., Hitzemann, R. J., Pappas, N. R., Wong, C. T., & Felder, C. (1999) · Life Sciences · doi:10.1016/s0024-3205(98)00619-5 · Cited by 336 · see citing works
McBride, D., Barrett, S. P., Kelly, J. T., Aw, A., & Dagher, A. (2006) · Neuropsychopharmacology · doi:10.1038/sj.npp.1301075 · Cited by 323 · see citing works
Neurobiology of Addiction: Toward the Development of New Therapies
Koob, G. F. (2000) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.2000.tb06682.x · Cited by 314 · see citing works
Volkow, N. D., Wang, G.-J., Ma, Y., Fowler, J. S., Wong, C., Ding, Y.-S., Hitzemann, R., Swanson, J. M., & Kalivas, P. (2005) · The Journal of Neuroscience · doi:10.1523/jneurosci.0433-05.2005 · Cited by 304 · see citing works
Effect of the Age at Which Smoking Begins on Frequency of Smoking in Adulthood
Taioli, E., & Wynder, E. L. (1991) · New England Journal of Medicine · doi:10.1056/nejm199109263251318 · Cited by 301 · see citing works
Extent of smoking and nicotine dependence in the United States: 19911993
Chen, D. B. K. (2000) · Nicotine & Tobacco Research · doi:10.1080/14622200050147538 · Cited by 261 · see citing works
Nicotine-dependence symptoms are associated with smoking frequency in adolescents
O'Loughlin, J., DiFranza, J., Tyndale, R. F., Meshefedjian, G., McMillan-Davey, E., Clarke, P. B. S., Hanley, J., & Paradis, G. (2003) · American Journal of Preventive Medicine · doi:10.1016/s0749-3797(03)00198-3 · Cited by 248 · see citing works
McClernon, F. J., Kozink, R. V., Lutz, A. M., & Rose, J. E. (2009) · Psychopharmacology · doi:10.1007/s00213-008-1436-9 · Cited by 244 · 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
McClernon, F. J., Hiott, F. B., Huettel, S. A., & Rose, J. E. (2005) · Neuropsychopharmacology · doi:10.1038/sj.npp.1300780 · Cited by 216 · see citing works
Functional brain imaging of tobacco use and dependence
BRODY, A. (2006) · Journal of Psychiatric Research · doi:10.1016/j.jpsychires.2005.04.012 · Cited by 207 · see citing works
May, J. C., Delgado, M. R., Dahl, R. E., Stenger, V. A., Ryan, N. D., Fiez, J. A., & Carter, C. S. (2004) · Biological Psychiatry · doi:10.1016/j.biopsych.2003.11.008 · Cited by 193 · see citing works
Prokhorov, A. V., de Moor, C., Pallonen, U. E., Hudmon, K. S., Koehly, L. M., & Hu, S. (2000) · Addictive Behaviors · doi:10.1016/s0306-4603(98)00132-4 · Cited by 172 · see citing works
Lee, J.-H., Lim, Y., Wiederhold, B. K., & Graham, S. J. (2005) · Applied Psychophysiology and Biofeedback · doi:10.1007/s10484-005-6377-z · Cited by 153 · see citing works
Jacobsen, L. K., Picciotto, M. R., Heath, C. J., Frost, S. J., Tsou, K. A., Dwan, R. A., Jackowski, M. P., Constable, R. T., & Mencl, W. E. (2007) · The Journal of Neuroscience · doi:10.1523/jneurosci.2402-07.2007 · Cited by 147 · see citing works
Jacobsen, L. K., Slotkin, T. A., Mencl, W. E., Frost, S. J., & Pugh, K. R. (2007) · Neuropsychopharmacology · doi:10.1038/sj.npp.1301398 · Cited by 144 · see citing works
Instructed smoking expectancy modulates cue‐elicited neural activity: A preliminary study
Wilson, S. J., Sayette, M. A., Delgado, M. R., & Fiez, J. A. (2005) · Nicotine & Tobacco Research · doi:10.1080/14622200500185520 · Cited by 143 · see citing works
In vivo Brain Imaging of Human Exposure to Nicotine and Tobacco
Sharma, A., & Brody, A. L. (2009) · Handbook of experimental pharmacology · doi:10.1007/978-3-540-69248-5_6 · Cited by 88 · see citing works
An acute psychosocial stress enhances the neural response to smoking cues
Dagher, A., Tannenbaum, B., Hayashi, T., Pruessner, J. C., & McBride, D. (2009) · Brain Research · doi:10.1016/j.brainres.2009.07.048 · Cited by 80 · see citing works
Cotinine levels in relation to smoking behavior and addiction in young adolescent smokers
Rubinstein, M. L., Thompson, P., Benowitz, N. L., et al. (2007) · Nicotine & Tobacco Research · doi:10.1080/14622200601078517 · Cited by 45 · see citing works
Self-citationReactivity to smoking cues in adolescent cigarette smokers
Upadhyaya, H. P., Drobes, D. J., & Thomas, S. E. (2004) · Addictive Behaviors · doi:10.1016/j.addbeh.2004.02.040 · Cited by 38 · see citing works
Nicotine Replacement Therapy for Teenagers
Adelman, W. P. (2004) · Archives of Pediatrics and Adolescent Medicine · doi:10.1001/archpedi.158.3.205 · Cited by 17 · see citing works
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Neural substrates of smoking cue reactivity: A meta-analysis of fMRI studies
Engelmann, J. M., Versace, F., Robinson, J. D., Minnix, J. A., Lam, C. Y., Cui, Y., Brown, V. L., & Cinciripini, P. M. (2012) · NeuroImage · doi:10.1016/j.neuroimage.2011.12.024 · Cited by 394 · see citing works
England, L. J., Aagaard, K., Bloch, M., Conway, K., Cosgrove, K., Grana, R., Gould, T. J., Hatsukami, D., Jensen, F., Kandel, D., et al. (2017) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2016.11.013 · Cited by 181 · see citing works
Self-citationCounotte, D. S., Smit, A. B., Pattij, T., & Spijker, S. (2011) · Developmental Cognitive Neuroscience · doi:10.1016/j.dcn.2011.05.010 · Cited by 77 · see citing works
Stanger, C., Elton, A., Ryan, S. R., James, G. A., Budney, A. J., & Kilts, C. D. (2013) · Journal of the American Academy of Child & Adolescent Psychiatry · doi:10.1016/j.jaac.2013.04.013 · Cited by 75 · see citing works
Garrison, 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
Cue-elicited craving in heroin addicts at different abstinent time: An fMRI pilot study
Lou, M., Wang, E., Shen, Y., & Wang, J. (2012) · Substance Use & Misuse · doi:10.3109/10826084.2011.646381 · Cited by 61 · see citing works
Laviolette, S. R. (2021) · Neuropharmacology · doi:10.1016/j.neuropharm.2020.108411 · Cited by 57 · see citing works
A developmental perspective on neuroeconomic mechanisms of contingency management.
Stanger, C., Budney, A. J., & Bickel, W. K. (2013) · Psychology of Addictive Behaviors · doi:10.1037/a0028748 · Cited by 50 · see citing works
Rubinstein, M. L., Luks, T. L., Dryden, W. Y., Rait, M. A., & Simpson, G. V. (2011) · Nicotine & Tobacco Research · doi:10.1093/ntr/ntr046 · Cited by 43 · see citing works
Self-citationNeural sensitivity to smoking stimuli is associated with cigarette craving in adolescent smokers
Do, K. T., & Galván, A. (2016) · Journal of Adolescent Health · doi:10.1016/j.jadohealth.2015.10.004 · Cited by 13 · see citing works
- Authors
- Rubinstein, M. L., Luks, T. L., Moscicki, A.-B., Dryden, W., Rait, M. A., & Simpson, G. V.
- Affiliations
- University of California, San Francisco (US)
- Corresponding author
- Rubinstein, Mark L.
- Venue
- Journal of Adolescent Health
- Publisher
- Elsevier BV
- Published
- 2011-01
- Volume
- 48
- Issue
- 1
- Pages
- 7-12
- ISSN
- 1054-139X (ISSN-L)
- PMC
- PMC3058837
- OpenAlex
- W2040833852
- Cited by
- 62
- References
- 38
- Citations by year
- 2026: 1 · 2025: 1 · 2024: 2 · 2023: 1 · 2022: 3 · 2021: 2 · 2020: 3 · 2019: 1 · 2018: 3 · 2017: 4 · 2016: 8 · 2015: 6 · 2014: 5 · 2013: 8 · 2012: 6
- FWCI
- 4.77
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Journal of Adolescent Health (publishedVersion)
- PubMed (publishedVersion)
- Europe PMC (PubMed Central) (acceptedVersion)
- PubMed Central (acceptedVersion)
- Funders
- NIH/NCRR UCSF-CTSI (UL1 RR024131)
- NIH/NCI (R01 CA140216)
- Topics
- Health Sciences › Medicine › Physiology › Smoking Behavior and Cessation
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Nicotinic Acetylcholine Receptors Study
- Health Sciences › Medicine › Epidemiology › Substance Abuse Treatment and Outcomes
- Keywords
- adolescent smoking, light smokers, smoking cues, nicotine dependence, anterior cingulate cortex, hippocampus, nicotine exposure, early intervention
- MeSH terms
- Adolescent, Arousal, Brain Mapping, Cues, Dominance, Cerebral, Female, Frontal Lobe, Hippocampus, Humans, Magnetic Resonance Imaging, Male, Photic Stimulation, Smoking, Substance Withdrawal Syndrome
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