Abstract
Studying the neural correlates of smoking behaviors in young adulthood is of great importance to improve treatment outcomes. In previous addiction studies, the important roles of the salience network (SN) in drug cue processing and cognitive control have been revealed. Unfortunately, few studies focused on the resting-state functional connectivity and structural integrity abnormalities of SN in young adult smokers, and less is known about its association with smoking behaviors and cognitive control deficits. Thirty-one young male adult smokers and 30 age-, education- and gender-matched nonsmokers participated in this study. The structural and functional connectivity differences of SN were investigated between young adult smokers and nonsmokers by using diffusion tensor imaging (DTI) and resting-state functional connectivity (RSFC), which were then correlated with the smoking behavioral assessments (pack-years and Fagerström Test for Nicotine Dependence (FTND)) as well as impaired cognitive control measured by the Stroop task. Within SN, reduced RSFC and increased fractional anisotropy (FA) were found between the anterior cingulate cortex (ACC) and the right insula in young adult smokers relative to nonsmokers. The RSFC between the ACC and right insula was negatively correlated with the number of errors during the incongruent condition of the Stroop task in young adult smokers. Additionally, the right insula-ACC RSFC was negatively correlated with pack-years in young adult smokers. Our results revealed abnormal RSFC and structural integrity within the SN in young adult smokers, which shed new insights into the neural mechanism of nicotine dependence.
Similar content being viewed by others
References
Addicott, M. A., Sweitzer, M. M., Froeliger, B., Rose, J. E., & McClernon, F. J. (2015). Increased functional connectivity in an insula-based network is associated with improved smoking cessation outcomes. Neuropsychopharmacology, 40(11), 2648–2656.
Azizian, A., Nestor, L. J., Payer, D., Monterosso, J. R., Brody, A. L., & London, E. D. (2010). Smoking reduces conflict-related anterior cingulate activity in abstinent cigarette smokers performing a Stroop task. Neuropsychopharmacology, 35(3), 775–782.
Beckmann, C. F., & Smith, S. M. (2004). Probabilistic independent component analysis for functional magnetic resonance imaging. IEEE Transactions on Medical Imaging, 23(2), 137–152.
Benowitz, N. (2008). Clinical pharmacology of nicotine: implications for understanding, preventing, and treating tobacco addiction. Clinical Pharmacology & Therapeutics, 83(4), 531–541.
Bi, Y., Yuan, K., Guan, Y., Cheng, J., Zhang, Y., Li, Y., et al. (2016). Altered resting state functional connectivity of anterior insula in young smokers. Brain Imaging and Behavior. doi:10.1007/s11682-016-9511-z [Epub ahead of print].
Bonnelle, V., Ham, T. E., Leech, R., Kinnunen, K. M., Mehta, M. A., Greenwood, R. J., et al. (2012). Salience network integrity predicts default mode network function after traumatic brain injury. Proceedings of the National Academy of Sciences, 109(12), 4690–4695.
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(1), 77–84.
Cai, C., Yuan, K., Yin, J., Feng, D., Bi, Y., Li, Y., Yu, D., Jin, C., Qin, W., & Tian, J. (2015). Striatum morphometry is associated with cognitive control deficits and symptom severity in internet gaming disorder. Brain Imaging and Behavior, 10(1), 12–20.
Carroll, A. J., Sutherland, M. T., Salmeron, B. J., Ross, T. J., & Stein, E. A. (2014). Greater externalizing personality traits predict less error-related insula and anterior cingulate cortex activity in acutely abstinent cigarette smokers. Addiction Biology, 20(2), 377–389.
Casey, B., Galvan, A., & Hare, T. A. (2005a). Changes in cerebral functional organization during cognitive development. Current Opinion in Neurobiology, 15(2), 239–244.
Casey, B., Tottenham, N., Liston, C., & Durston, S. (2005b). Imaging the developing brain: what have we learned about cognitive development? Trends in Cognitive Sciences, 9(3), 104–110.
Cox, L. S., Tiffany, S. T., & Christen, A. G. (2001). Evaluation of the brief questionnaire of smoking urges (QSU-brief) in laboratory and clinical settings. Nicotine & Tobacco Research, 3(1), 7–16.
Ding, J.-R., An, D., Liao, W., Li, J., Wu, G.-R., Xu, Q., et al. (2013). Altered functional and structural connectivity networks in psychogenic non-epileptic seizures. PloS One, 8(5), e63850.
Domier, C. P., Monterosso, J. R., Brody, A. L., Simon, S. L., Mendrek, A., Olmstead, R., et al. (2007). Effects of cigarette smoking and abstinence on Stroop task performance. Psychopharmacology, 195(1), 1–9.
Fedota, J. R., & Stein, E. A. (2015). Resting-state functional connectivity and nicotine addiction: prospects for biomarker development. Annals of the New York Academy of Sciences, 1349(1), 64–82.
Feil, J., Sheppard, D., Fitzgerald, P. B., Yücel, M., Lubman, D. I., & Bradshaw, J. L. (2010). Addiction, compulsive drug seeking, and the role of frontostriatal mechanisms in regulating inhibitory control. Neuroscience & Biobehavioral Reviews, 35(2), 248–275.
Filippini, N., MacIntosh, B. J., Hough, M. G., Goodwin, G. M., Frisoni, G. B., Smith, S. M., et al. (2009). Distinct patterns of brain activity in young carriers of the APOE-ε4 allele. Proceedings of the National Academy of Sciences, 106(17), 7209–7214.
Forget, B., Pushparaj, A., & Le Foll, B. (2010). Granular insular cortex inactivation as a novel therapeutic strategy for nicotine addiction. Biological Psychiatry, 68(3), 265–271.
Fritz, H.-C., Wittfeld, K., Schmidt, C. O., Domin, M., Grabe, H. J., Hegenscheid, K., et al. (2014). Current smoking and reduced gray matter volume—a voxel-based morphometry study. Neuropsychopharmacology, 39(11), 2594–2600.
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. European Journal of Neuroscience, 24(6), 1744–1750.
Hanlon, C. A., Owens, M. M., Joseph, J. E., Zhu, X., George, M. S., Brady, K. T., et al. (2014). Lower subcortical gray matter volume in both younger smokers and established smokers relative to non-smokers. Addiction Biology, 21(1), 185–195.
Hu, Y., Salmeron, B. J., Gu, H., Stein, E. A., & Yang, Y. (2015). Impaired functional connectivity within and between frontostriatal circuits and its association with compulsive drug use and trait impulsivity in cocaine addiction. JAMA Psychiatry, 72(6), 584–592.
Hudkins, M., O’Neill, J., Tobias, M. C., Bartzokis, G., & London, E. D. (2012). Cigarette smoking and white matter microstructure. Psychopharmacology, 221(2), 285–295.
Ilan, A. B., & Polich, J. (2001). Tobacco smoking and event-related brain potentials in a Stroop task. International Journal of Psychophysiology, 40(2), 109–118.
Janes, A. C., Pizzagalli, D. A., Richardt, S., Chuzi, S., Pachas, G., Culhane, M. A., et al. (2010). Brain reactivity to smoking cues prior to smoking cessation predicts ability to maintain tobacco abstinence. Biological Psychiatry, 67(8), 722–729.
Janes, A., Farmer, S., Peechatka, A., Frederick, B., & Lukas, S. (2015). Insula-dorsal anterior cingulate cortex coupling is associated with enhanced brain reactivity to smoking cues. Neuropsychopharmacology, 40(7), 1561–1568.
Jasinska, A. J., Zorick, T., Brody, A. L., & Stein, E. A. (2014). Dual role of nicotine in addiction and cognition: a review of neuroimaging studies in humans. Neuropharmacology, 84, 111–122.
Kochunov, P., Du, X., Moran, L. V., Sampath, H., Wijtenburg, S. A., Yang, Y., et al. (2013). Acute nicotine administration effects on fractional anisotropy of cerebral white matter and associated attention performance. Frontiers in Pharmacology, 4, 117.
Lerman, C., Gu, H., Loughead, J., Ruparel, K., Yang, Y., & Stein, E. A. (2014). Large-scale brain network coupling predicts acute nicotine abstinence effects on craving and cognitive function. JAMA Psychiatry, 71(5), 523–530.
Li, X., Hartwell, K. J., Borckardt, J., Prisciandaro, J. J., Saladin, M. E., Morgan, P. S., et al. (2013). Volitional reduction of anterior cingulate cortex activity produces decreased cue craving in smoking cessation: a preliminary real-time fMRI study. Addiction Biology, 18(4), 739–748.
Li, Y., Yuan, K., Cai, C., Feng, D., Yin, J., Bi, Y., et al. (2015). Reduced frontal cortical thickness and increased caudate volume within fronto-striatal circuits in young adult smokers. Drug and Alcohol Dependence, 151, 211–219.
Li, Y., Yuan, K., Bi, Y., Guan, Y., Cheng, J., Zhang, Y., et al. (2016). Neural correlates of 12-h abstinence-induced craving in young adult smokers: a resting-state study. Brain Imaging and Behavior. doi:10.1007/s11682-016-9544-3.
Lin, F., Wu, G., Zhu, L., & Lei, H. (2013). Heavy smokers show abnormal microstructural integrity in the anterior corpus callosum: a diffusion tensor imaging study with tract-based spatial statistics. Drug and Alcohol Dependence, 129(1), 82–87.
Liu, J. J., Mohila, C. A., Gong, Y., Govindarajan, N., & Onn, S. P. (2005). Chronic nicotine exposure during adolescence differentially influences calcium-binding proteins in rat anterior cingulate cortex. European Journal of Neuroscience, 22(10), 2462–2474.
Lydon, D. M., Wilson, S. J., Child, A., & Geier, C. F. (2014). Adolescent brain maturation and smoking: what we know and where we’re headed. Neuroscience & Biobehavioral Reviews, 45, 323–342.
Maria, M. S., Megan, M., Hartwell, K. J., Hanlon, C. A., Canterberry, M., Lematty, T., et al. (2015). Right anterior insula connectivity is important for cue-induced craving in nicotine-dependent smokers. Addiction Biology, 20(2), 407–414.
Menon, V. (2011). Large-scale brain networks and psychopathology: a unifying triple network model. Trends in Cognitive Sciences, 15(10), 483–506.
Menon, V., & Uddin, L. Q. (2010). Saliency, switching, attention and control: a network model of insula function. Brain Structure and Function, 214(5–6), 655–667.
Morales, A. M., Ghahremani, D., Kohno, M., Hellemann, G. S., & London, E. D. (2014). Cigarette exposure, dependence, and craving are related to insula thickness in young adult smokers. Neuropsychopharmacology, 39(8), 1816–1822.
Moran, L. V., Sampath, H., Stein, E. A., & Hong, L. E. (2012). Insular and anterior cingulate circuits in smokers with schizophrenia. Schizophrenia Research, 142(1), 223–229.
Naqvi, N. H., Rudrauf, D., Damasio, H., & Bechara, A. (2007). Damage to the insula disrupts addiction to cigarette smoking. Science, 315(5811), 531–534.
Opanashuk, L. A., Pauly, J. R., & Hauser, K. F. (2001). Effect of nicotine on cerebellar granule neuron development. European Journal of Neuroscience, 13(1), 48–56.
Padula, M. C., Schaer, M., Scariati, E., Schneider, M., Van De Ville, D., Debbané, M., et al. (2015). Structural and functional connectivity in the default mode network in 22q11.2 deletion syndrome. Journal of Neurodevelopmental Disorders, 7(1), 23.
Seeley, W. W., Menon, V., Schatzberg, A. F., Keller, J., Glover, G. H., Kenna, H., et al. (2007). Dissociable intrinsic connectivity networks for salience processing and executive control. The Journal of Neuroscience, 27(9), 2349–2356.
Silveri, M. M., Tzilos, G. K., Pimentel, P. J., & Yurgelun-Todd, D. A. (2004). Trajectories of adolescent emotional and cognitive development: effects of sex and risk for drug use. Annals of the New York Academy of Sciences, 1021(1), 363–370.
Sridharan, D., Levitin, D. J., & Menon, V. (2008). A critical role for the right fronto-insular cortex in switching between central-executive and default-mode networks. Proceedings of the National Academy of Sciences, 105(34), 12569–12574.
Stoeckel, L. E., Chai, X. J., Zhang, J., Whitfield-Gabrieli, S., & Evins, A. E. (2015). Lower gray matter density and functional connectivity in the anterior insula in smokers compared with never smokers. Addiction Biology. doi:10.1111/adb.12262.
Sutherland, M. T., McHugh, M. J., Pariyadath, V., & Stein, E. A. (2012). Resting state functional connectivity in addiction: lessons learned and a road ahead. NeuroImage, 62(4), 2281–2295.
Sutherland, M. T., Carroll, A. J., Salmeron, B. J., Ross, T. J., & Stein, E. A. (2013). Insula’s functional connectivity with ventromedial prefrontal cortex mediates the impact of trait alexithymia on state tobacco craving. Psychopharmacology, 228(1), 143–155.
Swan, G. E., & Lessov-Schlaggar, C. N. (2007). The effects of tobacco smoke and nicotine on cognition and the brain. Neuropsychology Review, 17(3), 259–273.
Uddin, L. Q., Supekar, K. S., Ryali, S., & Menon, V. (2011). Dynamic reconfiguration of structural and functional connectivity across core neurocognitive brain networks with development. The Journal of Neuroscience, 31(50), 18578–18589.
Wagner, M., Schulze-Rauschenbach, S., Petrovsky, N., Brinkmeyer, J., von der Goltz, C., Gründer, G., et al. (2013). Neurocognitive impairments in non-deprived smokers—results from a population-based multi-center study on smoking-related behavior. Addiction Biology, 18(4), 752–761.
Wang, Z., Faith, M., Patterson, F., Tang, K., Kerrin, K., Wileyto, E. P., et al. (2007). Neural substrates of abstinence-induced cigarette cravings in chronic smokers. The Journal of Neuroscience, 27(51), 14035–14040.
Wang, K., Yang, J., Zhang, S., Wei, D., Hao, X., Tu, S., et al. (2014). The neural mechanisms underlying the acute effect of cigarette smoking on chronic smokers. PloS One, 9(7), e102828.
World Health Organization (2013). WHO report on the global tobacco epidemic, 2013: enforcing bans on tobacco advertising, promotion and sponsorship. World Health Organization. Available: http://apps.who.int/iris/bitstream/10665/85380/1/9789241505871_eng.pdf?ua=1.
Xing, L., Yuan, K., Bi, Y., Yin, J., Cai, C., Feng, D., et al. (2014). Reduced fiber integrity and cognitive control in adolescents with internet gaming disorder. Brain Research, 1586, 109–117.
Xu, J., Mendrek, A., Cohen, M. S., Monterosso, J., Simon, S., Jarvik, M., et al. (2007). Effect of cigarette smoking on prefrontal cortical function in nondeprived smokers performing the Stroop task. Neuropsychopharmacology, 32(6), 1421–1428.
Xue, T., Yuan, K., Zhao, L., Yu, D., Zhao, L., Dong, T., et al. (2012). Intrinsic brain network abnormalities in migraines without aura revealed in resting-state fMRI. PloS One, 7(12), e52927.
Yu, D., Yuan, K., Zhang, B., Liu, J., Dong, M., Jin, C., et al. (2015). White matter integrity in young smokers: a tract-based spatial statistics study. Addiction Biology, 21(3), 679–687.
Yuan, K., Cheng, P., Dong, T., Bi, Y., Xing, L., Yu, D., et al. (2013). Cortical thickness abnormalities in late adolescence with online gaming addiction. PloS One, 8(1), e53055.
Yuan, K., Qin, W., Yu, D., Bi, Y., Xing, L., Jin, C., et al. (2015). Core brain networks interactions and cognitive control in internet gaming disorder individuals in late adolescence/early adulthood. Brain Structure and Function, 221(3), 1427–1442.
Yuan, K., Yu, D., Bi, Y., Li, Y., Guan, Y., Liu, J., et al. (2016a). The implication of frontostriatal circuits in young smokers: a resting-state study. Human Brain Mapping, 37(6), 2013–2026.
Yuan, K., Yu, D., Cai, C., Feng, D., Li, Y., Bi, Y., et al. (2016b). Frontostriatal circuits, resting state functional connectivity and cognitive control in internet gaming disorder. Addiction Biology. doi:10.1111/adb.12348.
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(1), 42–48.
Acknowledgments
This paper is supported by the National Natural Science Foundation of China under Grant nos. 81571751, 81571753, 61502376, 81401478, 81401488, 81470816, 81471737, 81301281, 81271546, 81271549, the Natural Science Basic Research Plan in Shaanxi Province of China under Grant no. 2014JQ4118, and the Fundamental Research Funds for the Central Universities under the Grant nos. JB151204, JB121405, the Natural Science Foundation of Inner Mongolia under Grant no. 2014BS0610, the Innovation Fund Project of Inner Mongolia University of Science and Technology Nos. 2015QNGG03, 2014QDL002, General Financial Grant the China Post- doctoral Science Foundation under Grant no. 2014 M552416.
Author information
Authors and Affiliations
Corresponding authors
Ethics declarations
Conflict of interest
Yangding Li, Kai Yuan, Yanyan Guan, Jiadong Cheng, Yanzhi Bi, Sha Shi, Ting Xue, Xiaoqi Lu, Wei Qin, Dahua Yu, Jie Tian declare that they have no conflict of interest.
Ethical approval
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.
Ethical statements
Informed consent was obtained from all individual participants included in the study.
Rights and permissions
About this article
Cite this article
Li, Y., Yuan, K., Guan, Y. et al. The implication of salience network abnormalities in young male adult smokers. Brain Imaging and Behavior 11, 943–953 (2017). https://doi.org/10.1007/s11682-016-9568-8
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11682-016-9568-8