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Altered spontaneous activity of posterior cingulate cortex and superior temporal gyrus are associated with a smoking cessation treatment outcome using varenicline revealed by regional homogeneity

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Abstract

Compared to nonsmokers, smokers exhibit a number of potentially important differences in regional brain function. However, little is known about the associations between the local spontaneous brain activity and smoking cessation treatment outcomes. In the present analysis, we aimed to evaluate whether the local features of spontaneous brain activity prior to the target quit date was associated with the smoking cessation outcomes. All the participants underwent magnetic resonance imaging scans and smoking-related behavioral assessments. After a 12-week treatment with varenicline, 23 smokers succeeded in quitting smoking and 32 failed. Smokers underwent functional magnetic resonance imaging (fMRI) scanning prior to an open label smoking cessation treatment trial. Regional homogeneity (ReHo) was used to measure spontaneous brain activity, and whole-brain voxel-wise comparisons of ReHo were performed to detect brain regions with altered spontaneous brain activity between relapser and quitter groups. After controlling for potentially confounding factors including years of education, years smoked, cigarettes smoked per day and FTND score as covariates, compared to quitters, relapsers displayed significantly decreased ReHo in bilateral posterior cingulate cortex (PCC), as well as increased ReHo in left superior temporal gyrus (STG). These preliminary results suggest that regional brain function variables may be promising predictors of smoking relapse. This study provided novel insights into the neurobiological mechanisms underlying smoking relapse. A deeper understanding of the neurobiological mechanisms associated with relapse may result in novel pharmacological and behavioral interventions.

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References

  • Bentley, P., Husain, M., & Dolan, R. J. (2004). Effects of cholinergic enhancement on visual stimulation, spatial attention, and spatial working memory. Neuron, 41, 969–982.

    Article  CAS  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 

  • Buckner, R. L., Andrews-Hanna, J. R., & Schacter, D. L. (2008). The brain’s default network: anatomy, function, and relevance to disease. Annals of the New York Academy of Sciences, 1124, 1–38.

    Article  PubMed  Google Scholar 

  • Coe, J. W., Brooks, P. R., Vetelino, M. G., Wirtz, M. C., Arnold, E. P., Huang, J., et al. (2005). Varenicline: an alpha4beta2 nicotinic receptor partial agonist for smoking cessation. Journal of Medicinal Chemistry, 48, 3474–3477.

    Article  CAS  PubMed  Google Scholar 

  • Costello, M. R., Mandelkern, M. A., Shoptaw, S., Shulenberger, S., Baker, S. K., Abrams, A. L., et al. (2010). Effects of treatment for tobacco dependence on resting cerebral glucose metabolism. Neuropsychopharmacology: official publication of the American College of Neuropsychopharmacology, 35, 605–612.

    Article  CAS  Google Scholar 

  • David, S. P., Munafo, M. R., Johansen-Berg, H., Smith, S. M., Rogers, R. D., Matthews, P. M., & Walton, R. T. (2005). Ventral striatum/nucleus accumbens activation to smoking-related pictorial cues in smokers and nonsmokers: a functional magnetic resonance imaging study. Biological Psychiatry, 58, 488–494.

    Article  PubMed  PubMed Central  Google Scholar 

  • Dome, P., Lazary, J., Kalapos, M. P., & Rihmer, Z. (2010). Smoking, nicotine and neuropsychiatric disorders. Neuroscience and Biobehavioral Reviews, 34, 295–342.

    Article  CAS  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. The American Journal of Psychiatry, 159, 954–960.

    Article  PubMed  Google Scholar 

  • Engelmann, J. M., Versace, F., Robinson, J. D., Minnix, J. A., Lam, C. Y., Cui, Y., et al. (2012). Neural substrates of smoking cue reactivity: a meta-analysis of fMRI studies. NeuroImage, 60, 252–262.

    Article  PubMed  Google Scholar 

  • Fiore, M.C., Jaén, C. R., Baker, T. B., Bailey, W. C., Benowitz, N. L., Curry, S. J., et al. (2008) Treating Tobacco Use and Dependence: 2008 Update. Clinical Practice Guideline PhD thesis, US Department of Health and Human Services Public Health Service, Rockville, MD.

  • Franklin, T.R., Wang, Z., Wang, J., Sciortino, N., Harper, D., Li, Y., et al. (2007). Limbic activation to cigarette smoking cues independent of nicotine withdrawal: a perfusion fMRI study. Neuropsychopharmacology: official publication of the American College of Neuropsychopharmacology, 32, 2301–2309.

  • Franklin, T., Wang, Z., Suh, J. J., Hazan, R., Cruz, J., Li, Y., et al. (2011). Effects of varenicline on smoking cue-triggered neural and craving responses. Archives of General Psychiatry, 68, 516–526.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Froeliger, B., Kozink, R. V., Rose, J. E., Behm, F. M., Salley, A. N., & McClernon, F. J. (2010). Hippocampal and striatal gray matter volume are associated with a smoking cessation treatment outcome: results of an exploratory voxel-based morphometric analysis. Psychopharmacology, 210, 577–583.

    Article  CAS  PubMed  Google Scholar 

  • Froeliger, B., Modlin, L. A., Kozink, R. V., Wang, L., Garland, E. L., Addicott, M. A., & McClernon, F. J. (2013). Frontoparietal attentional network activation differs between smokers and nonsmokers during affective cognition. Psychiatry Research, 211, 57–63.

    Article  PubMed  Google Scholar 

  • Gallinat, J., Meisenzahl, E., Jacobsen, L. K., Kalus, P., Bierbrauer, J., Kienast, T., et al. (2006). Smoking and structural brain deficits: a volumetric MR investigation. The European Journal of Neuroscience, 24, 1744–1750.

    Article  PubMed  Google Scholar 

  • Giessing, C., Thiel, C. M., Rosler, F., & Fink, G. R. (2006). The modulatory effects of nicotine on parietal cortex activity in a cued target detection task depend on cue reliability. Neuroscience, 137, 853–864.

    Article  CAS  PubMed  Google Scholar 

  • Greicius, M. D., Krasnow, B., Reiss, A. L., & Menon, V. (2003). Functional connectivity in the resting brain: a network analysis of the default mode hypothesis. Proceedings of the National Academy of Sciences of the United States of America, 100, 253–258.

    Article  CAS  PubMed  Google Scholar 

  • Hahn, B., Ross, T. J., Yang, Y., Kim, I., Huestis, M. A., & Stein, E. A. (2007). Nicotine enhances visuospatial attention by deactivating areas of the resting brain default network. The Journal of Neuroscience, 27, 3477–3489.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hartwell, K. J., Johnson, K. A., Li, X., Myrick, H., LeMatty, T., George, M. S., & Brady, K. T. (2011). Neural correlates of craving and resisting craving for tobacco in nicotine dependent smokers. Addiction Biology, 16, 654–666.

    Article  PubMed  PubMed Central  Google Scholar 

  • Heatherton, T. F., Kozlowski, L. T., Frecker, R. C., & Fagerstrom, K. O. (1991). The fagerstrom test for nicotine dependence: a revision of the fagerstrom tolerance questionnaire. British Journal of Addiction, 86, 1119–1127.

    Article  CAS  PubMed  Google Scholar 

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

    Google Scholar 

  • Hong, L. E., Gu, H., Yang, Y., Ross, T. J., Salmeron, B. J., Buchholz, B., et al. (2009). Association of nicotine addiction and nicotine’s actions with separate cingulate cortex functional circuits. Archives of General Psychiatry, 66(4), 431–441.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Janse Van Rensburg, K., Taylor, A., Hodgson, T., & Benattayallah, A. (2009). Acute exercise modulates cigarette cravings and brain activation in response to smoking-related images: an fMRI study. Psychopharmacology, 203, 589–598.

    Article  CAS  PubMed  Google Scholar 

  • Jiang, L., Xu, T., He, Y., Hou, X. H., Wang, J., Cao, X. Y., et al. (2015a). Toward neurobiological characterization of functional homogeneity in the human cortex: regional variation, morphological association and functional covariance network organization. Brain Structure & Function, 220, 2485–2507.

  • Jiang, L., & Zuo, X.N., (2015b). Regional homogeneity: a multimodal, multiscale neuroimaging marker of the human connectome. Neuroscientist, 7,1–20.

  • Jorenby, D. E., Hays, J. T., Rigotti, N. A., Azoulay, S., Watsky, E. J., Williams, K. E., et al. (2006). Efficacy of varenicline, an α4β2 nicotinic acetylcholine receptor partial agonist, vs placebo or sustained-release bupropion for smoking cessation: a randomized controlled trial. JAMA, 296, 56–63.

    Article  CAS  PubMed  Google Scholar 

  • Karnath, H. O. (2001). New insights into the functions of the superior temporal cortex. Nature Reviews Neuroscience, 2, 568–576.

    Article  CAS  PubMed  Google Scholar 

  • Lee, J. H., Lim, Y., Wiederhold, B. K., & Graham, S. J. (2005). A functional magnetic resonance imaging (FMRI) study of cue-induced smoking craving in virtual environments. Applied Psychophysiology and Biofeedback, 30, 195–204.

    Article  PubMed  Google Scholar 

  • Liao, Y., Tang, J., Liu, T., Chen, X., & Hao, W. (2012). Differences between smokers and non-smokers in regional gray matter volumes: a voxel-based morphometry study. Addiction Biology, 17, 977–980.

    Article  PubMed  Google Scholar 

  • Lin, F., Wu, G., Zhu, L., & Lei, H. (2015). Altered brain functional networks in heavy smokers. Addiction Biology, 20(4), 809–819.

    Article  PubMed  Google Scholar 

  • Liu, D., Yan, C., Ren, J., Yao, L., Kiviniemi, V. J., & Zang, Y. (2010). Using coherence to measure regional homogeneity of resting-state FMRI signal. Frontiers in Systems Neuroscience, 4, 24.

    PubMed  PubMed Central  Google Scholar 

  • Luijten, M., Veltman, D. J., van den Brink, W., Hester, R., Field, M., Smits, M., & Franken, I. H. (2011). Neurobiological substrate of smoking-related attentional bias. NeuroImage, 54, 2374–2381.

    Article  PubMed  Google Scholar 

  • Mathers, C. D., & Loncar, D. (2006). Projections of global mortality and burden of disease from 2002 to 2030. PLoS Medicine, 3, e442.

    Article  PubMed  PubMed Central  Google Scholar 

  • May, J. C., Delgado, M. R., Dahl, R. E., Stenger, V. A., Ryan, N. D., Fiez, J. A., & Carter, C. S. (2004). Event-related functional magnetic resonance imaging of reward-related brain circuitry in children and adolescents. Biological Psychiatry, 55(4), 359–366.

    Article  PubMed  Google Scholar 

  • Mesulam, M. M. (1998). From sensation to cognition. Brain, 121, 1013–1052.

    Article  PubMed  Google Scholar 

  • Nides, M., Oncken, C., Gonzales, D., Rennard, S., Watsky, E. J., Anziano, R., & Reeves, K. R. (2006). Smoking cessation with varenicline, a selective α4β2 nicotinic receptor partial agonist: results from a 7-week, randomized, placebo-and bupropion-controlled trial with 1-year follow-up. Archives of Internal Medicine, 166, 1561–1568.

    Article  PubMed  Google Scholar 

  • Picciotto, M. R., & Zoli, M. (2008). Neuroprotection via nAChRs: the role of nAChRs in neurodegenerative disorders such as Alzheimer’s and Parkinson’s disease. Frontiers In Bioscience, 13, 492–504.

    Article  CAS  PubMed  Google Scholar 

  • Rose, J.E., Behm, F.M., Salley, A.N., Bates, J.E., Coleman, R.E., Hawk, T.C., & Turkington, T.G., (2007). Regional brain activity correlates of nicotine dependence. Neuropsychopharmacology: official publication of the American College of Neuropsychopharmacology, 32, 2441–2452.

  • Song, X. W., Dong, Z. Y., Long, X. Y., Li, S. F., Zuo, X. N., Zhu, C. Z., et al. (2011). REST: a toolkit for resting-state functional magnetic resonance imaging data processing. PloS One, 6, e25031.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sutherland, M. T., Carroll, A. J., Salmeron, B. J., Ross, T. J., Hong, L. E., & Stein, E. A. (2013a). Down-regulation of amygdala and insula functional circuits in abstinent cigarette smokers by varenicline and nicotine. Biological Psychiatry, 74, 538–546.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sutherland, M. T., Carroll, A. J., Salmeron, B. J., Ross, T. J., Hong, L. E., & Stein, E. A. (2013b). Individual differences in amygdala reactivity following nicotinic receptor engagement in abstinent smokers. NeuroImage, 66, 585–593.

    Article  CAS  PubMed  Google Scholar 

  • Sutherland, M. T., Carroll, A. J., Salmeron, B. J., Ross, T. J., & Stein, E. A. (2013c). Insula’s functional connectivity with ventromedial prefrontal cortex mediates the impact of trait alexithymia on state tobacco craving. Psychopharmacology, 228, 143–155.

    Article  CAS  PubMed  Google Scholar 

  • Tanabe, J., Nyberg, E., Martin, L. F., Martin, J., Cordes, D., Kronberg, E., & Tregellas, J. R. (2011). Nicotine effects on default mode network during resting state. Psychopharmacology, 216, 287–295.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tang, J., Liao, Y., Deng, Q., Liu, T., Chen, X., Wang, X., et al. (2012). Altered spontaneous activity in young chronic cigarette smokers revealed by regional homogeneity. Behavioral and Brain Functions, 8, 44.

    Article  PubMed  PubMed Central  Google Scholar 

  • Thiel, C. M., & Fink, G. R. (2008). Effects of the cholinergic agonist nicotine on reorienting of visual spatial attention and top-down attentional control. Neuroscience, 152, 381–390.

    Article  CAS  PubMed  Google Scholar 

  • Thiel, C. M., Zilles, K., & Fink, G. R. (2005). Nicotine modulates reorienting of visuospatial attention and neural activity in human parietal cortex. Neuropsychopharmacology, 30, 810–820.

    CAS  PubMed  Google Scholar 

  • Tregellas, J. R., Shatti, S., Tanabe, J. L., Martin, L. F., Gibson, L., Wylie, K., & Rojas, D. C. (2007). Gray matter volume differences and the effects of smoking on gray matter in schizophrenia. Schizophrenia Research, 97, 242–249.

    Article  PubMed  Google Scholar 

  • Wu, G., Yang, S., Zhu, L., & Lin, F. (2015). Altered spontaneous brain activity in heavy smokers revealed by regional homogeneity. Psychopharmacology, 232(14), 2481–2489.

    Article  CAS  PubMed  Google Scholar 

  • Yu, R., Zhao, L., & Lu, L. (2011). Regional grey and white matter changes in heavy male smokers. PloS one, 6, e27440.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yu, R., Zhao, L., Tian, J., Qin, W., Wang, W., Yuan, K., Li, Q., & Lu, L. (2013). Regional homogeneity changes in heavy male smokers: a resting-state functional magnetic resonance imaging study. Addiction Biology, 18, 729–731.

    Article  PubMed  Google Scholar 

  • Zang, Y., Jiang, T., Lu, Y., He, Y., & Tian, L. (2004). Regional homogeneity approach to fMRI data analysis. NeuroImage, 22, 394–400.

    Article  PubMed  Google Scholar 

  • Zhang, D., & Raichle, M. E. (2010). Disease and the brain's dark energy. Nature Reviews Neurology, 6, 15–28.

  • Zhang, X., Salmeron, B. J., Ross, T. J., Geng, X., Yang, Y., & Stein, E. A. (2011). Factors underlying prefrontal and insula structural alterations in smokers. NeuroImage, 54, 42–48.

    Article  PubMed  Google Scholar 

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Correspondence to Minming Zhang.

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This work was supported by the Natural Science Foundation of China surface project (grant nos. 81171310) and science and technology planning project of Zhejiang Province (grant 2011C23094).

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The authors declare that they have no conflict of interest.

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All procedures performed in studies involving human participants were in accordance with the ethical standards of the institutional and/or national research committee and with the 1964 Helsinki declaration and its later amendments or comparable ethical standards.

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Wang, C., Shen, Z., Huang, P. et al. Altered spontaneous activity of posterior cingulate cortex and superior temporal gyrus are associated with a smoking cessation treatment outcome using varenicline revealed by regional homogeneity. Brain Imaging and Behavior 11, 611–618 (2017). https://doi.org/10.1007/s11682-016-9538-1

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