Neural correlates of craving and resisting craving for tobacco in nicotine dependent smokers

Karen J Hartwell, Kevin A Johnson, Xingbao Li, Hugh Myrick, Todd LeMatty, Mark S George, Kathleen T Brady, Karen J Hartwell, Kevin A Johnson, Xingbao Li, Hugh Myrick, Todd LeMatty, Mark S George, Kathleen T Brady

Abstract

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.

© 2011 The Authors, Addiction Biology © 2011 Society for the Study of Addiction.

Figures

Figure 1
Figure 1
Strategies Employed to Resist Craving
Figure 2
Figure 2
Functional MRI results when cigarette smokers were exposed to smoking-related cues compared to neutral cues during Crave Condition (red) and Resist Condition (blue).
Figure 3
Figure 3
Regional Areas of Activation where Crave Condition is greater than Resist Condition (red) and Resist Condition is greater than Crave Condition (blue) analyzed with FSL’s fixed effects with cluster thresholding at p=.05
Figure 4
Figure 4
Regional Areas of Activation when smokers are using distraction (yellow) and contemplation of adverse effects of smoking (green) while resisting the urge to smoke. The bottom panel (blue) reflects areas of increased activation in distraction compared to thinking about negative effects.

References

    1. Allman JM, Hakeem A, Erwin JM, Nimchinsky E, Hof P. The Anterior Cingulate Cortex. Annals of the New York Academy of Sciences. 2001;935:107–117.
    1. Andreasen NC, O’Leary DS, Cizadlo T, Arndt S, Rezai K, Watkins GL, Ponto LL, Hichwa RD. Remembering the past: two facets of episodic memory explored with positron emission tomography. American Journal of Psychiatry. 1995;152:1576–1585.
    1. Beckmann CF, Jenkinson M, Smith SM. General multilevel linear modeling for group analysis in FMRI. NeuroImage. 2003;20:1052–1063.
    1. Brody AL. Functional brain imaging of tobacco use and dependence. Journal of Psychiatric Research. 2006;40:404–418.
    1. Brody AL, Mandelkern MA, London ED, Childress AR, Lee GS, Bota RG, Ho ML, Saxena S, Baxter LR, Jr, Madsen D, Jarvik ME. Brain Metabolic Changes During Cigarette Craving. Archives of General Psychiatry. 2002;59:1162–1172.
    1. Brody AL, Mandelkern MA, Olmstead RE, Jou J, Tiongson E, Allen V, Scheibal D, London ED, Monterosso JR, Tiffany ST, Korb A, Gan JJ, Cohen MS. Neural Substrates of Resisting Craving During Cigarette Cue Exposure. Biological Psychiatry. 2007;62:642–651.
    1. Burgess PW, Gilbert SJ, Dumontheil I. Function and localization within rostral prefrontal cortex (area 10) Philosophical Transactions of the Royal Society of London - Series B: Biological Sciences. 2007;362:887–899.
    1. Carter BL, Tiffany ST. Meta-analysis of cue-reactivity in addiction research. Addiction. 1999;94:327–340.
    1. Cavanna AE, Trimble MR. The precuneus: a review of its functional anatomy and behavioural correlates. Brain. 2006;129:564–583.
    1. CDC. Cigarettes smoking among adults and trends in smoking cessation--- United States, 2008. MMWR Weekly. 2009;58:1227–1232.
    1. Cox LS, Tiffany ST, Christen AG. Evaluation of the brief questionnaire of smoking urges (QSU-brief) in laboratory and clinical settings. Nicotine & Tobacco Research. 2001;3:7–16.
    1. Crone EA, Wendelken C, Donohue SE, Bunge SA. Neural Evidence for Dissociable Components of Task-switching. Cerebral Cortex. 2006;16:475–486.
    1. Cutini S, Scatturin P, Menon E, Bisiacchi PS, Gamberini L, Zorzi M, Dell’Acqua R. Selective activation of the superior frontal gyrus in task-switching: an event-related fNIRS study. NeuroImage. 2008;42:945–955.
    1. D’Argembeau A, Ruby P, Collette F, Degueldre C, Balteau E, Luxen A, Maquet P, Salmon E. Distinct regions of the medial prefrontal cortex are associated with self-referential processing and perspective taking. Journal of Cognitive Neuroscience. 2007;19:935–944.
    1. du Boisgueheneuc F, Levy R, Volle E, Seassau M, Duffau H, Kinkingnehun S, Samson Y, Zhang S, Dubois B. Functions of the left superior frontal gyrus in humans: a lesion study. Brain. 2006;129:3315–3328.
    1. David SP, Munafo MR, Johansen-Berg H, Smith SM, Rogers RD, Matthews PM, Walton RT. Ventral striatum/nucleus accumbens activation to smoking-related pictorial cues in smokers and nonsmokers: a functional magnetic resonance imaging study. Biological Psychiatry. 2005;58:488–494.
    1. Due DL, Huettel SA, Hall WG, Rubin DC. Activation in Mesolimbic and Visuospatial Neural Circuits Elicited by Smoking Cues: Evidence From Functional Magnetic Resonance Imaging. American Journal of Psychiatry. 2002;159:954–960.
    1. Fagerstrom KO. Measuring degree of physical dependence to tobacco smoking with reference to individualization of treatment. Addictive Behaviors. 1978;3:235–241.
    1. Ferguson SG, Shiffman S. The relevance and treatment of cue-induced cravings in tobacco dependence. Journal of Substance Abuse Treatment. 2009;36:235–243.
    1. Geier A, Mucha R, Pauli P. Appetitive nature of drug cues confirmed with physiological measures in a model using pictures of smoking. Psychopharmacology. 2000;150:283–291.
    1. Gillbert DRN. International Smoking Image Series with Neutral Counterparts. 1998.
    1. Heatherton TF, Kozlowski LT, Frecker RC, Fagerstrom K-O. The Fagerstrom Test for Nicotine Dependence: a revision of the Fagerstrom Tolerance Questionnaire. British Journal of Addiction. 1991;86:1119–1127.
    1. Hughes JR. Measurement of the effects of abstinence from tobacco: a qualitative review. Psychol Addict Behav. 2007;21:127–137.
    1. Hughes JR, Keely J, Naud S. Shape of the relapse curve and long-term abstinence among untreated smokers. Addiction. 2004;99:29–38.
    1. Jenkinson M, Bannister P, Brady M, Smith S. Improved optimization for the robust and accurate linear registration and motion correction of brain images. NeuroImage. 2002;17:825–841.
    1. Johnson-Frey SH, Newman-Norlund R, Grafton ST. A Distributed Left Hemisphere Network Active During Planning of Everyday Tool Use Skills. Cereb Cortex. 2005;15:681–695.
    1. Kennerley SW, Wallis JD. Evaluating choices by single neurons in the frontal lobe: outcome value encoded across multiple decision variables. Eur J Neurosci. 2009;29:2061–2073.
    1. Killen JD, Fortmann SP. Craving is associated with smoking relapse: findings from three prospective studies. Experimental & Clinical Psychopharmacology. 1997;5:137–142.
    1. Lee JH, Lim Y, Wiederhold BK, Graham SJ. A functional magnetic resonance imaging (FMRI) study of cue-induced smoking craving in virtual environments. Applied Psychophysiology & Biofeedback. 2005;30:195–204.
    1. McBride D, Barrett SP, Kelly JT, Aw A, Dagher A. Effects of Expectancy and Abstinence on the Neural Response to Smoking Cues in Cigarette Smokers: an fMRI Study. Neuropsychopharmacology. 2006;31:2728–2738.
    1. McClernon FJ, Hiott FB, Huettel SA, Rose JE, McClernon FJ, Hiott FB, Huettel SA, Rose JE. Abstinence-induced changes in self-report craving correlate with event-related FMRI responses to smoking cues. Neuropsychopharmacology. 2005;30:1940–1947.
    1. McClernon FJ, Hutchinson KE, Rose JE, Kozink RV. DRD4 VNTR polymorphism is associated with transient fMRI-BOLD responses to smoking cues. Psychopharmacology. 2007;194:433–441.
    1. Myrick H, Anton RF, Li X, Henderson S, Drobes D, Voronin K, George MS. Differential Brain Activity in Alcoholics and Social Drinkers to Alcohol Cues: Relationship to Craving. Neuropsychopharmacology. 2004;29:393–402.
    1. Piasecki TM. Relapse to smoking. Clinical Psychology Review. 2006;26:196–215.
    1. Rolls ET, Grabenhorst F. The orbitofrontal cortex and beyond: From affect to decision-making. Progress in Neurobiology. 2008;86:216–244.
    1. Schuh KJ, Stitzer ML. Desire to smoke during spaced smoking intervals. Psychopharmacology. 1995;120:289–295.
    1. Sharma A, Brody AL. In vivo Imaging of Human Exposure to Nicotine and Tobacco. In: Henningfield JE, London ED, Pogun S, editors. Nicotine Psychopharmacology. Berlin, Heidelberg: Springer; 2009. pp. 145–171.
    1. Sheehan DV, Lecrubier Y, Sheehan K, Amorim P, Janavs J, Weiller E, Hergueta T, Baker R, Dunbar GC. The Mini-International Neuropsychiatric Interview (M.I.N.I): The development and validation of a structured diagnostic psychiatric interview for DSM-IV and ICD-10. Journal of Clinical Psychiatry. 1998;59:22–33.
    1. Shiffman S, Engberg JB, Paty JA, Perz WG, Gnys M, Kassel JD, Hickcox M. A day at a time: predicting smoking lapse from daily urge. J Abnorm Psychol. 1997;106:104–116.
    1. Shiffman S, Gnys M, Richards TJ, Paty JA, Hickcox M, Kassel JD. Temptations to smoke after quitting: a comparison of lapsers and maintainers. Health Psychol. 1996;15:455–461.
    1. Smith SM. Fast robust automated brain extraction. Human Brain Mapping. 2002;17:143–155.
    1. Smith SM, Jenkinson M, Woolrich MW, Beckmann CF, Behrens TE, Johansen-Berg H, Bannister PR, De Luca M, Drobnjak I, Flitney DE, Niazy RK, Saunders J, Vickers J, Zhang Y, De Stefano N, Brady JM, Matthews PM. Advances in functional and structural MR image analysis and implementation as FSL. NeuroImage. 2004;23(Suppl1):S208–219.
    1. Smolka MN, Buhler M, Klein S, Zimmermann U, Mann K, Heinz A, Braus DF. Severity of nicotine dependence modulates cue-induced brain activity in regions involved in motor preparation and imagery. Psychopharmacology. 2006;184:577–588.
    1. Talati A, Hirsch J. Functional specialization within the medial frontal gyrus for perceptual go/no-go decisions based on “what,” “when,” and “where” related information: an fMRI study. Journal of Cognitive Neuroscience. 2005;17:981–993.
    1. Tiffany ST, Cox LS, Elash CA. Effects of transdermal nicotine patches on abstinence-induced and cue-elicited craving in cigarette smokers. Journal of Consulting & Clinical Psychology. 2000;68:233–240.
    1. Tiffany ST, Drobes DJ. The development and initial validation of a questionnaire on smoking urges. British Journal of Addiction. 1991;86:1467–1476.
    1. Tulving E. Episodic memory: from mind to brain. Annual Review of Psychology. 2002;53:1–25.
    1. Tunik E, Lo O-Y, Adamovich SV. Transcranial Magnetic Stimulation to the Frontal Operculum and Supramarginal Gyrus Disrupts Planning of Outcome-Based Hand-Object Interactions. J Neurosci. 2008;28:14422–14427.
    1. USDHHS. The health consequences of smoking: a report of the surgeon general. Atlanta, GA: United States Department of Health and Human Services, Centers for Disease Control and Prevention, Office on Smoking and Health; 2004.
    1. Warthen MW, Tiffany ST. Evaluation of cue reactivity in the natural environment of smokers using ecological momentary assessment. Experimental & Clinical Psychopharmacology. 2009;17:70–77.
    1. Wilson SJ, Sayette MA, Delgado MR, Fiez JA. Instructed smoking expectancy modulates cue-elicited neural activity: a preliminary study. Nicotine & Tobacco Research. 2005;7:637–645.
    1. Woolrich MW. Robust group analysis using outlier inference. NeuroImage. 2008;41:286–301.
    1. Woolrich MW, Behrens TE, Beckmann CF, Jenkinson M, Smith SM. Multi-level linear modelling for FMRI group analysis using Bayesian inference. NeuroImage. 2004;21:1732–1747.
    1. Woolrich MW, Jbabdi S, Patenaude B, Chappell M, Makni S, Behrens T, Beckmann C, Jenkinson M, Smith SM. Bayesian analysis of neuroimaging data in FSL. NeuroImage. 2009;45:S173–186.
    1. Woolrich MW, Ripley BD, Brady M, Smith SM. Temporal autocorrelation in univariate linear modeling of FMRI data. NeuroImage. 2001;14:1370–1386.

Source: PubMed

赞助者和合作者

医疗条件

药物干预

3
订阅