Skip to main content

Advertisement

SpringerLink
Log in

The implication of salience network abnormalities in young male adult smokers

  • Original Research
  • Published:
Brain Imaging and Behavior Aims and scope Submit manuscript

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.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3

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.

    Article  PubMed  PubMed Central  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • Benowitz, N. (2008). Clinical pharmacology of nicotine: implications for understanding, preventing, and treating tobacco addiction. Clinical Pharmacology & Therapeutics, 83(4), 531–541.

    Article  CAS  Google Scholar 

  • 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].

    Google Scholar 

  • 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.

    Article  CAS  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(1), 77–84.

    Article  PubMed  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • Casey, B., Galvan, A., & Hare, T. A. (2005a). Changes in cerebral functional organization during cognitive development. Current Opinion in Neurobiology, 15(2), 239–244.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  PubMed  PubMed Central  Google Scholar 

  • 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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Article  PubMed  PubMed Central  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. European Journal of Neuroscience, 24(6), 1744–1750.

    Article  PubMed  Google Scholar 

  • 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.

    Article  PubMed  PubMed Central  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • 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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Article  PubMed  PubMed Central  Google Scholar 

  • 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.

    Article  PubMed  PubMed Central  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Article  PubMed  PubMed Central  Google Scholar 

  • 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.

    Article  PubMed  PubMed Central  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • 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.

    Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • Menon, V. (2011). Large-scale brain networks and psychopathology: a unifying triple network model. Trends in Cognitive Sciences, 15(10), 483–506.

    Article  PubMed  Google Scholar 

  • 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.

    Article  PubMed  PubMed Central  Google Scholar 

  • 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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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.

    Article  PubMed  PubMed Central  Google Scholar 

  • Naqvi, N. H., Rudrauf, D., Damasio, H., & Bechara, A. (2007). Damage to the insula disrupts addiction to cigarette smoking. Science, 315(5811), 531–534.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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.

    CAS  PubMed  PubMed Central  Google Scholar 

  • 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.

    Article  PubMed  PubMed Central  Google Scholar 

  • 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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    PubMed  PubMed Central  Google Scholar 

  • 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.

    Article  PubMed  PubMed Central  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • 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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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.

    Article  PubMed  PubMed Central  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • 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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • 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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • 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.

    Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

Download references

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

  1. School of Life Science and Technology, Xidian University, Xi’an, Shaanxi, 710071, People’s Republic of China

    Yangding Li, Kai Yuan, Yanyan Guan, Jiadong Cheng, Yanzhi Bi, Sha Shi, Wei Qin & Jie Tian

  2. Engineering Research Center of Molecular and Neuro Imaging, Ministry of Education, Xi’an, People’s Republic of China

    Yangding Li, Kai Yuan, Yanyan Guan, Jiadong Cheng, Yanzhi Bi, Sha Shi, Wei Qin & Jie Tian

  3. Information Processing Laboratory, School of Information Engineering, Inner Mongolia Key Laboratory of Pattern Recognition and Intelligent Image Processing, Inner Mongolia University of Science and Technology, Baotou, Inner Mongolia, 014010, People’s Republic of China

    Kai Yuan, Xiaoqi Lu & Dahua Yu

  4. School of Mathematics, Physics and Biological Engineering, Inner Mongolia University of Science and Technology, Baotou, Inner Mongolia, 014010, People’s Republic of China

    Ting Xue

  5. Institute of Automation, Chinese Academy of Sciences, Beijing, 100190, People’s Republic of China

    Jie Tian

Authors
  1. Yangding Li
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Kai Yuan
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Yanyan Guan
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Jiadong Cheng
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Yanzhi Bi
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Sha Shi
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Ting Xue
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Xiaoqi Lu
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Wei Qin
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Dahua Yu
    View author publications

    You can also search for this author in PubMed Google Scholar

  11. Jie Tian
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding authors

Correspondence to Kai Yuan or Dahua Yu.

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

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

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

Download citation

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11682-016-9568-8

Keywords

Search

Navigation