Neural correlates of craving and resisting craving for tobacco in nicotine dependent smokers
Open accessAbstract
Craving is a significant factor which can lead to relapse during smoking quit attempts. Attempts to resist urges to smoke during cue‐elicited craving have been shown to activate regions in the brain associated with decision‐making, anxiety regulation and visual processing. In this study, 32 treatment‐seeking, nicotine‐dependent smokers viewed blocks of smoking and neutral cues alternating with rest periods during magnetic resonance imaging scanning in a 3T Siemens scanner (Siemens AG, Erlangen, Bavaria, Germany). While viewing cues or control images, participants were instructed either to ‘allow yourself to crave’ or ‘resist craving.’ Data were analyzed with FSL 4.1.5, focused on the smoking cues versus neutral cues contrast, using cluster thresholding (Z > 2.3 and corrected cluster threshold of P = 0.05) at the individual and group levels. During the Crave condition, activation was seen on the left anterior cingulated cortex (LACC), medial prefrontal cortex, left middle cingulate gyrus, bilateral posterior cingulated gyrus and bilateral precuneus, areas associated with attention, decision‐making and episodic memory. The LACC and areas of the prefrontal cortex associated with higher executive functioning were activated during the Resist condition. No clear distinctions between group crave and resist analyses as a whole were seen without taking into account specific strategies used to resist the urge to smoke, supporting the idea that craving is associated with some degree of resisting the urge to smoke, and trying to resist is almost always accompanied by some degree of craving. Different strategies for resisting, such as distraction, activated different regions. Understanding the underlying neurobiology of resisting craving to smoke may identify new foci for treatments.
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
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?
Complementary strategies to promote acceptance of emotional states could be useful to overcome automatic reactions.
“Complementary strategies to promote acceptance of emotional states could be useful to overcome such automatic reactions.7–9”
From Feasibility, acceptability and preliminary outcomes of a mindfulness-based relapse prevention program in a naturalistic setting among treatment-seeking patients with alcohol use disorder: A prospective observational study (2019) · cites this paper as [9]
The Discussion (page unavailable) suggests that resisting cue-elicited tobacco craving may require overriding learned associations and identifies cognitive therapies as a possible way to enhance resistance. It does not discuss promoting acceptance of emotional states, so it supports the idea of overcoming learned reactions but not the proposed acceptance strategy. (LLM, conf=0.79)
Experimental — accuracy not yet measured
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Cites
(1998) · The Journal of Clinical Psychiatry · Cited by 19,139 · see citing works
Advances in functional and structural MR image analysis and implementation as FSL
Smith, S. M., Jenkinson, M., Woolrich, M. W., Beckmann, C. F., Behrens, T. E. J., Johansen-Berg, H., Bannister, P. R., De Luca, M., Drobnjak, I., Flitney, D. E., et al. (2004) · NeuroImage · doi:10.1016/j.neuroimage.2004.07.051 · Cited by 13,630 · see citing works
Jenkinson, M., Bannister, P., Brady, M., & Smith, S. (2002) · NeuroImage · doi:10.1006/nimg.2002.1132 · Cited by 11,888 · 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
Fast robust automated brain extraction
Smith, S. M. (2002) · Human Brain Mapping · doi:10.1002/hbm.10062 · Cited by 10,496 · see citing works
(1998) · PubMed · Cited by 10,216 · see citing works
The precuneus: a review of its functional anatomy and behavioural correlates
Cavanna, A. E., & Trimble, M. R. (2006) · Brain · doi:10.1093/brain/awl004 · Cited by 5,128 · see citing works
Episodic memory: from mind to brain
Tulving, E. (2002) · Annual Review of Psychology · doi:10.1146/annurev.psych.53.100901.135114 · Cited by 4,950 · see citing works
The basis of anisotropic water diffusion in the nervous system—A technical review.
Beaulieu, C. (2002) · NMR in Biomedicine · doi:10.1002/nbm.782 · Cited by 4,653 · see citing works
Temporal Autocorrelation in Univariate Linear Modeling of FMRI Data
Woolrich, M. W., Ripley, B. D., Brady, M., & Smith, S. M. (2001) · NeuroImage · doi:10.1006/nimg.2001.0931 · Cited by 2,859 · see citing works
Bayesian analysis of neuroimaging data in FSL
Woolrich, M., Jbabdi, S., Patenaude, B., Chappell, M., Makni, S., Behrens, T. E. J., Beckmann, C., Jenkinson, M., & Smith, S. M. (2009) · NeuroImage · doi:10.1016/j.neuroimage.2008.10.055 · Cited by 2,774 · see citing works
The Health Consequences of Smoking: A Report of the Surgeon General
Office on Smoking (2004) · Cited by 2,414 · see citing works
Fagerström, K.-O. (1978) · Addictive Behaviors · doi:10.1016/0306-4603(78)90024-2 · Cited by 2,221 · see citing works
Multilevel linear modelling for FMRI group analysis using Bayesian inference
Woolrich, M. W., Behrens, T. E. J., Beckmann, C. F., Jenkinson, M., & Smith, S. M. (2004) · NeuroImage · doi:10.1016/j.neuroimage.2003.12.023 · Cited by 1,719 · see citing works
Meta‐analysis of cue‐reactivity in addiction research
Carter, B. L., & Tiffany, S. T. (1999) · Addiction · doi:10.1046/j.1360-0443.1999.9433273.x · Cited by 1,638 · cited 1× · see citing works
“These smoking-related cues readily elicit craving in both laboratory and naturalistic studies (Carter & Tiffany 1999; Warthen & Tiffany 2009).”
BackgroundGeneral multilevel linear modeling for group analysis in FMRI
Beckmann, C. F., Jenkinson, M., & Smith, S. M. (2003) · NeuroImage · doi:10.1016/s1053-8119(03)00435-x · Cited by 1,464 · see citing works
Shape of the relapse curve and long-term abstinence among untreated smokers
Hughes, J. R., Keely, J., & Naud, S. (2004) · Addiction · doi:10.1111/j.1360-0443.2004.00540.x · Cited by 1,414 · see citing works
Cox, L. S., Tiffany, S. T., & Christen, A. G. (2001) · Nicotine & Tobacco Research · doi:10.1080/14622200020032051 · Cited by 1,188 · see citing works
The development and initial validation of a questionnaire on smoking urges
TIFFANY, S. T., & DROBES, D. J. (1991) · British Journal of Addiction · doi:10.1111/j.1360-0443.1991.tb01732.x · Cited by 974 · see citing works
Allman, J. M., Hakeem, A. Y., Erwin, J. M., Nimchinsky, E. A., & Hof, P. R. (2001) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.2001.tb03476.x · Cited by 903 · see citing works
Functions of the left superior frontal gyrus in humans: a lesion study
Boisguéheneuc, F. D., Lévy, R., Emmanuelle Volle, C., Seassau, M., Duffau, H., Kinkingnéhun, S., Samson, Y., Zhang, S., & Dubois, B. (2006) · Brain · doi:10.1093/brain/awl244 · Cited by 856 · see citing works
The orbitofrontal cortex and beyond: From affect to decision-making
Rolls, E. T., & Fabian Grabenhorst, B. (2008) · Progress in Neurobiology · doi:10.1016/j.pneurobio.2008.09.001 · Cited by 808 · see citing works
Remembering the past: two facets of episodic memory explored with positron emission tomography
(1995) · American Journal of Psychiatry · doi:10.1176/ajp.152.11.1576 · Cited by 593 · see citing works
A distributed left hemisphere network active during planning of everyday tool use skills
Johnson-Frey, S. H., Newman-Norlund, R., & Grafton, S. T. (2005) · Cerebral Cortex · doi:10.1093/cercor/bhh169 · Cited by 558 · see citing works
Myrick, H., Anton, R. F., Li, X., Henderson, S., Drobes, D., Voronin, K., & George, M. S. (2004) · Neuropsychopharmacology · doi:10.1038/sj.npp.1300295 · Cited by 521 · see citing works
Self-citationRobust group analysis using outlier inference
Woolrich, M. (2008) · NeuroImage · doi:10.1016/j.neuroimage.2008.02.042 · Cited by 504 · see citing works
D'Argembeau, A., Ruby, P., Collette, F., Degueldre, C., Balteau, E., Luxen, A., Maquet, P., & Salmon, E. (2007) · Journal of Cognitive Neuroscience · doi:10.1162/jocn.2007.19.6.935 · Cited by 495 · cited 3× · see citing works
“Contemplation of the adverse effects is restricted cognitive strategy and higher MR signal was found in the areas associated with decision-making (left ACC) (Allman et al. 2001) and self-referential processing (right MPFC) (D’Argembeau et al. 2007).”
BackgroundDue, 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
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
Craving is associated with smoking relapse: Findings from three prospective studies.
Killen, J. D., & Fortmann, S. P. (1997) · Experimental and Clinical Psychopharmacology · doi:10.1037//1064-1297.5.2.137 · Cited by 413 · see citing works
A day at a time: Predicting smoking lapse from daily urge.
Shiffman, S. M., Engberg, J., Paty, J. A., Perz, W. G., Gnys, M., Kassel, J. D., & Hickcox, M. (1997) · Journal of Abnormal Psychology · doi:10.1037//0021-843x.106.1.104 · Cited by 370 · see citing works
Piasecki, T. M. (2006) · Clinical Psychology Review · doi:10.1016/j.cpr.2005.11.007 · Cited by 370 · see citing works
Neural Evidence for Dissociable Components of Task-switching
Crone, E. A., Wendelken, C., Donohue, S. E., & Bunge, S. A. (2005) · Cerebral Cortex · doi:10.1093/cercor/bhi127 · Cited by 359 · see citing works
The relevance and treatment of cue-induced cravings in tobacco dependence
Ferguson, S. G., & Shiffman, S. S. (2008) · Journal of Substance Abuse Treatment · doi:10.1016/j.jsat.2008.06.005 · Cited by 357 · see citing works
Craving is associated with smoking relapse: Findings from three prospective studies.
Killen, J. D., & Fortmann, S. P. (1997) · Experimental and Clinical Psychopharmacology · doi:10.1037/1064-1297.5.2.137 · Cited by 342 · 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
Neural Substrates of Resisting Craving During Cigarette Cue Exposure
Brody, A. L., Mandelkern, M. A., Olmstead, R. E., Jou, J., Tiongson, E., Allen, V., Scheibal, D., London, E. D., Monterosso, J. R., Tiffany, S. T., et al. (2007) · Biological Psychiatry · doi:10.1016/j.biopsych.2006.10.026 · Cited by 312 · 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
A day at a time: Predicting smoking lapse from daily urge.
Shiffman, S. M., Engberg, J., Paty, J. A., et al. (1997) · Journal of Abnormal Psychology · doi:10.1037/0021-843x.106.1.104 · Cited by 273 · see citing works
Function and localization within rostral prefrontal cortex (area 10)
Burgess, P. W., Gilbert, S. J., & Dumontheil, I. (2007) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2007.2095 · Cited by 263 · see citing works
Myrick, H., Anton, R. F., Li, X., Henderson, S., Randall, P. K., & Voronin, K. (2008) · Archives of General Psychiatry · doi:10.1001/archpsyc.65.4.466 · Cited by 258 · see citing works
Self-citationSmolka, 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
Talati, A., & Hirsch, J. (2005) · Journal of Cognitive Neuroscience · doi:10.1162/0898929054475226 · Cited by 223 · 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
Kennerley, S. W., & Wallis, J. D. (2009) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2009.06743.x · Cited by 204 · see citing works
Tiffany, S. T., Cox, L. S., & Elash, C. A. (2000) · Journal of Consulting and Clinical Psychology · doi:10.1037//0022-006x.68.2.233 · Cited by 196 · see citing works
Color of Scents: Chromatic Stimuli Modulate Odor Responses in the Human Brain
Österbauer, R. A., Matthews, P. M., Jenkinson, M., Beckmann, C. F., Hansen, P. C., & Calvert, G. A. (2005) · Journal of Neurophysiology · doi:10.1152/jn.00555.2004 · Cited by 193 · see citing works
Parry, A. M. M. (2003) · Brain · doi:10.1093/brain/awg284 · Cited by 171 · 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
Temptations to smoke after quitting: A comparison of lapsers and maintainers
Shiffman, S., Gnys, M., Richards, T. J., Paty, J. A., Hickcox, M., & Kassel, J. D. (1996) · Health Psychology · doi:10.1037/0278-6133.15.6.455 · Cited by 149 · cited 1× · see citing works
“…from the pharmacologically rewarding properties of nicotine, smoking is also maintained by the repeated pairing of the effects of nicotine with non-pharmacological stimuli or cues such as the sight of preferred cigarette pack, lighter, or sight and smell of cigarette smoke (Shiffman et al. 1996).”
BackgroundTemptations to smoke after quitting: A comparison of lapsers and maintainers.
Shiffman, S. S., Gnys, M., Richards, T. J., Paty, J. A., Hickcox, M., & Kassel, J. D. (1996) · Health Psychology · doi:10.1037//0278-6133.15.6.455 · Cited by 149 · see citing works
Geier, A., Pauli, P., & Mucha, R. F. (2000) · Psychopharmacology · doi:10.1007/s002130000404 · Cited by 147 · 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
Tiffany, S. T., Cox, L. S., & Elash, C. A. (2000) · Journal of Consulting and Clinical Psychology · doi:10.1037/0022-006x.68.2.233 · Cited by 141 · see citing works
Desire to smoke during spaced smoking intervals
Schuh, K. J., & Stitzer, M. L. (1995) · Psychopharmacology · doi:10.1007/bf02311176 · Cited by 131 · see citing works
Selective activation of the superior frontal gyrus in task-switching: An event-related fNIRS study
Cutini, S., Scatturin, P., Menon, E., Bisiacchi, P. S., Gamberini, L., Zorzi, M., & Dell’Acqua, R. (2008) · NeuroImage · doi:10.1016/j.neuroimage.2008.05.013 · Cited by 95 · 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
DRD4 VNTR polymorphism is associated with transient fMRI-BOLD responses to smoking cues
McClernon, F. J., Hutchison, K. E., Rose, J. E., & Kozink, R. V. (2007) · Psychopharmacology · doi:10.1007/s00213-007-0860-6 · Cited by 86 · see citing works
Measurement of the effects of abstinence from tobacco: A qualitative review.
Hughes, J. R. (2007) · Psychology of Addictive Behaviors · doi:10.1037/0893-164x.21.2.127 · Cited by 76 · see citing works
Tunik, E., Lo, O., & Adamovich, S. (2008) · Journal of Neuroscience · doi:10.1523/jneurosci.4734-08.2008 · Cited by 73 · see citing works
The Effect of Aripiprazole on Cue-Induced Brain Activation and Drinking Parameters in Alcoholics
Myrick, H., Li, X., Randall, P. K., Henderson, S., Voronin, K. E., & Anton, R. F. (2010) · Journal of Clinical Psychopharmacology · doi:10.1097/jcp.0b013e3181e75cff · Cited by 72 · see citing works
Self-citationWarthen, M. W., & Tiffany, S. T. (2009) · Experimental and Clinical Psychopharmacology · doi:10.1037/a0015617 · Cited by 64 · see citing works
Flagged first, then by citations
Research works printed but not linked: 1
- CDC 2009 Cigarettes smoking among adults and trends in smoking cessation--- United States, 2008 MMWR Weekly 58 1227 1232 19910909
Cited by
Sorted by citations
Jasinska, A. J., Stein, E. A., Kaiser, J., Naumer, M. J., & Yalachkov, Y. (2014) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2013.10.013 · Cited by 513 · see citing works
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
Circuitry of self-control and its role in reducing addiction
Tang, Y.-Y., Posner, M. I., Rothbart, M. K., & Volkow, N. D. (2015) · Trends in Cognitive Sciences · doi:10.1016/j.tics.2015.06.007 · Cited by 236 · see citing works
Li, X., Hartwell, K. J., Owens, M., LeMatty, T., Borckardt, J. J., Hanlon, C. A., Brady, K. T., & George, M. S. (2013) · Biological Psychiatry · doi:10.1016/j.biopsych.2013.01.003 · Cited by 206 · see citing works
Self-citationBrief meditation training induces smoking reduction
Tang, Y.-Y., Tang, R., & Posner, M. I. (2013) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1311887110 · Cited by 202 · see citing works
Addicott, M. A., Sweitzer, M. M., Froeliger, B., Rose, J. E., & McClernon, F. J. (2015) · Neuropsychopharmacology · doi:10.1038/npp.2015.114 · Cited by 85 · see citing works
Oxytocin enhances cognitive control of food craving in women
Striepens, N., Schröter, F., Stoffel‐Wagner, B., Maier, W., Hurlemann, R., & Scheele, D. (2016) · Human Brain Mapping · doi:10.1002/hbm.23308 · Cited by 63 · see citing works
Controlling the self: The role of the dorsal frontomedian cortex in intentional inhibition
Lynn, M. T., Muhle-Karbe, P. S., & Brass, M. (2014) · Neuropsychologia · doi:10.1016/j.neuropsychologia.2014.09.009 · Cited by 27 · see citing works
von Hammerstein, C., Khazaal, Y., Dupuis, M., Aubin, H.-J., Benyamina, A., Luquiens, A., & Romo, L. (2019) · BMJ Open · doi:10.1136/bmjopen-2018-026839 · Cited by 24 · see citing works
“Neuroimaging studies showed that craving and resisting craving often activates the same brain networks.(9) Trying to resist the urge could then lead to an extension of craving intensity.”
Background
- Authors
- Hartwell, K. J., Johnson, K. A., Li, X., Myrick, H., LeMatty, T., George, M. S., & Brady, K. T.
- Affiliations
- Medical University of South Carolina (US)
- Stanford University (US)
- Corresponding author
- Hartwell, Karen J.
- Venue
- Addiction Biology
- Publisher
- Wiley
- Published
- 2011-07-25
- Volume
- 16
- Issue
- 4
- Pages
- 654-666
- ISSN
- 1355-6215 (ISSN-L)
- 1369-1600
- PMC
- PMC3182826
- OpenAlex
- W2150980655
- Cited by
- 129
- References
- 63
- Citations by year
- 2026: 4 · 2025: 6 · 2024: 3 · 2023: 7 · 2022: 6 · 2021: 13 · 2020: 2 · 2019: 7 · 2018: 6 · 2017: 10 · 2016: 9 · 2015: 19 · 2014: 7 · 2013: 16 · 2012: 11
- FWCI
- 8.08
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Addiction Biology (publishedVersion)
- PubMed (publishedVersion)
- Europe PMC (PubMed Central) (acceptedVersion)
- PubMed Central (acceptedVersion)
- Funders
- Medical University of South Carolina (UL1 RR029882, K12HD055885)
- Georgia Clinical and Translational Science Alliance
- National Institutes of Health (RR029882)
- National Institute on Drug Abuse (R21DA026085, R33DA026085)
- National Center for Research Resources (UL1RR029882)
- Eunice Kennedy Shriver National Institute of Child Health and Human Development (K12HD055885)
- 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
- nicotine craving, nicotine dependence, smoking cues, cue reactivity, anterior cingulate cortex, medial prefrontal cortex, decision-making, executive function, smoking cessation, relapse, distraction techniques
- MeSH terms
- Adult, Arousal, Brain, Brain Mapping, Cues, Dominance, Cerebral, Female, Humans, Image Processing, Computer-Assisted, Magnetic Resonance Imaging, Male, Middle Aged, Motivation, Substance Withdrawal Syndrome, Tobacco Use Disorder, Smoking Cessation, Young Adult
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