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A Functional Magnetic Resonance Imaging (fMRI) Study of Cue-Induced Smoking Craving in Virtual Environments

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Abstract

Smokers who are exposed to smoking-related cues show cardiovascular reactivity and smoking craving compared with their responses to neutral cues, and increased cue reactivity predicts decreased likelihood of successful cessation. Several brain imaging studies suggested four candidate brain regions that might differ in gray matter volumes and densities between smokers and nonsmokers. However, in these studies, smokers were only exposed to smoking-related objects. In our pilot study utilizing a virtual reality (VR) technique, virtual environments (VEs) were more immersive and evoked smoking craving more effectively than traditionally used methods. In this study, we sought to test whether smokers could experience cue-induced smoking craving inside the MRI scanner by using the VR system. The smoking cue reactivity scenario was based in part on our preliminary task and consisted of 2D and 3D (or VE) conditions. The group mean of participants had increased activity in the prefrontal cortex (PFC), left anterior cingulate gyrus (ACC), left supplementary motor area, left uncus, right inferior temporal gyrus, right lingual gyrus, and right precuneus in the 2D condition. Areas of differential activation in the 3D condition were as follows: left superior temporal gyrus, right superior frontal gyrus, and left inferior occipital gyrus in the 3D condition. This finding is consistent with those of previous studies of nicotine craving showing PFC and ACC activation. However, in the 3D condition, the PFC including the superior frontal gyrus as well as the superior temporal gyrus, inferior occipital gyrus, and cerebellum were activated. Therefore, in the 3D condition, participants seemed to have more attention, visual balance, and coordinating movement than in the 2D condition.

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References

  • Baumann, S., Neff, C., Fetzick, S., Stangl, G., Basler, L., Vereneck, R., et al. (2003). A virtual reality system for neurobehavioral and functional MRI studies. CyberPsychology and Behavior, 6, 259–266.

    Article  PubMed  Google Scholar 

  • Brody, A. L., Mandelkern, M. A., Jarvik, M. E., Lee, G. S., Smith, E. C., Huang, J. C., et al. (2004). Differences between smokers and nonsmokers in regional gray matter volumes and densities. Biological Psychiatry, 55, 77–84.

    Article  PubMed  Google Scholar 

  • Brody, A. L., Mandelkern, M. A., London, E. D., Childress, A. R., Bota, R. G., Ho, M. L., et al. (2002). Brain metabolic changes during cigarette craving. Archives of General Psychiatry, 59, 1162–1172.

    Article  PubMed  Google Scholar 

  • Childress, A. R., Mozley, P. D., McElgin, W., Fitzgerald, J., Reivich, M., & O’Brien, C. P. (1999). Limbic activation during cue-induced cocaine craving. American Journal of Psychiatry, 156, 11–18.

    PubMed  Google Scholar 

  • Cox, R. W. (1996). AFNI: Software for analysis and visualization of functional magnetic resonance neuroimages. Computers and Biomedical Research, 29, 162–173.

    Article  PubMed  Google Scholar 

  • Devinsky, O., Morrell, M. J., & Vogt, B. A. (1995). Contributions of anterior cingulate cortex to behavior. Brain, 118, 279–306.

    PubMed  Google Scholar 

  • Dewey, S. L., Brodie, J. D., Gerasimov, M., Horan, B., Gardner, E. L., & Ashby, C. R. J. (1999). A pharmacologic strategy for the treatment of nicotine addiction. Synapse, 31, 76–86.

    Article  PubMed  Google Scholar 

  • Domino, E. F., Minoshima, S., Guthrie, S., Ohl, L., Ni, L., Koeppe, R. A., et al. (2000). Nicotine effects on regional cerebral blood flow in awake, resting tobacco smokers. Synapse, 38, 313–321.

    Article  PubMed  Google Scholar 

  • Due, D. L., Huettel, S. A., Hall, W. G., & Rubin, D. C. (2002). Activation in mesolimbic and visuospatial neural circuits elicited by smoking cues: Evidence from functional magnetic resonance imaging. American Journal of Psychiatry, 159(6), 954–960.

    Article  PubMed  Google Scholar 

  • Garavan, H., Pankiewicz, J., Bloom, A., Cho, J.-K., Sperry, L., Ross, T. J., et al. (2000). Cue-induced cocaine craving: Neuroanatomical specificity for drug users and drug stimuli. American Journal of Psychiatry, 157, 1789–1798.

    Article  PubMed  Google Scholar 

  • Grant, S., London, E. D., Newlin, D. B., Villemagne, V. L., Liu, X., Contoreggi, C., et al. (1996). Activation of memory circuits during cue-elicited cocaine craving. Proceedings of the National Academy of Sciences of the United States of America, 93, 12040–12045.

    Article  PubMed  Google Scholar 

  • Hegemann, S., Fitzek, S., Fitzek, C., & Fetter, M. (2004). Cortical vestibular representation in the superior temporal gyrus. Journal of Vestibular Research, 14(1), 33–35.

    PubMed  Google Scholar 

  • Hoffman, H. G., Richards, T., Coda, B., Richards, A., & Sharar, S. R. (2003). The illusion of presence in immersive virtual reality during an fMRI brain scan. CyberPsychology and Behavior, 6, 127–131.

    Article  PubMed  Google Scholar 

  • Horti, A. G., Scheffel, U., Kimes, A., Musachio, J., Ravert, H., Mathews, W., et al. (1998). Synthesis and evaluation of N-[11C] methylated analogues of epibatidine as tracers for positron emission tomographic studies of nicotinic acetylcholine receptors. Journal of Medicinal Chemistry, 41, 4199–4206.

    Article  PubMed  Google Scholar 

  • Kennedy, R. S., Lane, N. E., Berbaum, K. S., & Lillienthal, M. G. (1993). A simulator sickness questionnaire (SSQ) : A new method for quantifying simulator sickness. International Journal of Aviation Psychology, 3(3), 203–220.

    Google Scholar 

  • Killen, J. D., & Fortmann, S. P. (1997). Craving is associated with smoking relapse: Findings from three prospective studies. Experimental and Clinical Psychopharmacology, 5(2), 137–142.

    Article  Google Scholar 

  • Lee, J. H., Ku, J. H., Kim, K. U., Kim, B. N., Kim, I. Y., Yang, B. H., et al. (2003). Experimental application of virtual reality for nicotine craving through cue exposure. CyberPsychology and Behavior, 6(3), 275–280.

    Article  PubMed  Google Scholar 

  • Longstreth, W. T., Arnold, A. M., Manolio, T. A., Burke, G. L., Bryan, N., Jungreis, C. A., et al. (2000). Clinical correlates of ventricular and sulcal size on cranial magnetic resonance imaging of 3,301 elderly people: The cardiovascular health study. Neuroepidemiology, 19, 30–42.

    Article  PubMed  Google Scholar 

  • Longstreth, W. T., Diehr, P., Manolio, T. A., Beauchamp, N. J., Jungreis, C. A., & Lefkowitz, D. (2001). Cluster analysis and patterns of findings on cranial magnetic resonance imaging of the elderly: The cardiovascular health study. Archives of Neurology, 58, 635–640.

    Article  PubMed  Google Scholar 

  • Maas, L. C., Lukas, S. E., Kaufman, M. J., Weiss, R. D., Daniels, S. L., Rogers, V. W., et al. (1998). Functional magnetic resonance imaging of human brain activation during cue-induced cocaine craving. American Journal of Psychiatry, 155, 124–126.

    PubMed  Google Scholar 

  • Maude-Griffin, P. M., & Tiffany, S. T. (1996). Production of smoking urges through imagery: The impact of affect and smoking abstinence. Experimental and Clinical Psychopharmacology, 4, 198–202.

    Article  Google Scholar 

  • Mraz, R., Hong, J., Quintin, G., Staines, W. R., McIlroy, W. E., Zakzanis, K. K., et al. (2003). A platform for combining virtual reality experiments with functional magnetic resonance imaging. CyberPsychology and Behavior, 6(4), 383–388.

    Article  PubMed  Google Scholar 

  • Musachio, J., Villemagne, V., Scheffel, U., Stathis, M., Finley, P., Horti, A., et al. (1997). [125I/123I] IPH: A radioiodinated analog of epibatidine for in vivo studies of nicotinic acetylcholine receptors. Synapse, 26, 392–399.

    Article  PubMed  Google Scholar 

  • Nakamura, H., Tanaka, A., Nomoto, Y., Ueno, Y., & Nakayama, Y. (2000). Activation of fronto-limbic system in the human brain by cigarette smoking: Evaluated by a CBF measurement. Keio Journal of Medicine, 49, A122–A124.

    PubMed  Google Scholar 

  • Niaura, R., Abrams, D. B., Pedraza, M., Monti, P. M., & Rohsenow, D. J. (1992). Smokers’ reactions to interpersonal interaction cues and presentation of smoking cues. Addictive Behaviors, 17, 557–566.

    Article  PubMed  Google Scholar 

  • Niaura, R., Abrams, D., Demuth, B., Pinto, R., & Monti, P. (1989a). Response to smoking-related stimuli and early relapse to smoking. Addictive Behaviors, 14, 419–428.

    Article  Google Scholar 

  • Niaura, R., Abrams, D., Monti, P., & Pedraza, M. (1989b). Reactivity to high risk situations and smoking outcome. Journal of Substance Abuse, 1, 393–405.

    Google Scholar 

  • Niaura, R., Rohsenow, D. J., Binnkoff, J. A., Monti, P. M., Pedrazza, M., & Abrams, D. B. (1988). Relevance of cue reactivity to understanding alcohol and smoking relapse. Journal of Abnormal Psychology, 97(2), 133–152.

    Article  PubMed  Google Scholar 

  • Oldfield, R. C. (1971). The assessment and analysis of handedness: The Edinburgh inventory. Neuropsychologia, 9, 97–113.

    Article  PubMed  Google Scholar 

  • Payne, T. J., Schare, M. L., Levis, D. J., & Colletti, G. (1991). Exposure to smoking-relevant cues: Effects in desire to smoke and topographical components of smoking behavior. Addictive Behavior, 16, 467–479.

    Article  Google Scholar 

  • Prokhorov, A. V., Koehly, L. M., Pallonen, U. E., & Hudmon, K. S. (1996). Adolescent nicotine dependence measured by the modified Fagerstrom tolerance questionnaire at two time points. Journal of Child and Adolescent substance Abuse, 7(4), 35–47.

    Article  Google Scholar 

  • Reiman, E. M. (1997). The application of positronemission tomography to the study of normal and phathologic emotions. Journal of Clinical Psychiatry, 58, 4–12.

    Google Scholar 

  • Rose, J. E., Behm, F. M., Westman, E. C., Mathew, R. J., London, E. D., Hawk, T. C., et al. (2003). PET studies of the influences of nicotine on neural systems in cigarette smokers. American Journal of Psychiatry, 160, 323–333.

    Article  PubMed  Google Scholar 

  • Schneider, F., Habel, U., Wagner, M., Franke, P., Salloum, J. B., Shah, J., et al. (2001). Subcortical correlates of craving in recently abstinent alcoholic patients. American Journal of Psychiatry, 158, 1075–1083.

    Article  PubMed  Google Scholar 

  • Stein, E., Pankiewicz, J., Harsch, H. H., Cho, J. K., Fuller, S. A., Hoffmann, R. G., et al. (1998). Nicotine-induced limbic cortical activation in the human brain: A functional MRI study. American Journal of Psychiatry, 155, 1009 –1015.

    PubMed  Google Scholar 

  • Vogt, B. A., Finch, D. M., & Olson, C. R. (1992). Functional heterogeneity in cingualte cortex: The anterior executive and posterior evaluative regions. Cerebral Cortex, 2, 435–443.

    PubMed  Google Scholar 

  • Wexler, B. E., Gottschalk, C. H., Fulbright, R. K., Prohovnik, I., Lacadie, C. M., Rounsaville, B. J., et al. (2001). Functional magnetic resonance imaging of cocaine craving. American Journal of Psychiatry, 158, 86–95.

    Article  PubMed  Google Scholar 

  • Witmer, B. G., & Singer, M. J. (1998). Measuring presence in virtual environments: A presence questionnaire. Presence, 7(3), 225–240.

    Article  Google Scholar 

  • Zubieta, J., Lombardi, U., Minoshima, S., Guthrie, S., Ni, L., Ohl, L. E., et al. (2001). Regional cerebral blood flow effects of nicotine in overnight abstinent smokers. Biological Psychiatry, 49, 906–913.

    Article  PubMed  Google Scholar 

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Authors and Affiliations

  1. Department of Psychology, Chung-Ang University, Seoul, Korea

    Jang-Han Lee

  2. Department of Adolescent Science, Chung-Ang University, 221, Heukseok-dong, Dongjak-gu, Seoul, Korea, 156-756

    Youngsik Lim

  3. The Virtual Reality Medical Center, San Diego, USA

    Brenda K. Wiederhold

  4. Imaging Research, Sunnybrook & Women’s College Health Science Centre, Toronto, ON, Canada

    Simon J. Graham

  5. Department of Medical Biophysics, University of Toronto, ON, Canada

    Simon J. Graham

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  1. Jang-Han Lee
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  2. Youngsik Lim
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  3. Brenda K. Wiederhold
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  4. Simon J. Graham
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Correspondence to Youngsik Lim.

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Lee, JH., Lim, Y., Wiederhold, B.K. et al. A Functional Magnetic Resonance Imaging (fMRI) Study of Cue-Induced Smoking Craving in Virtual Environments. Appl Psychophysiol Biofeedback 30, 195–204 (2005). https://doi.org/10.1007/s10484-005-6377-z

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