Skip to main content

Advertisement

Log in

Abnormal brain white matter network in young smokers: a graph theory analysis study

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

Abstract

Previous diffusion tensor imaging (DTI) studies had investigated the white matter (WM) integrity abnormalities in some specific fiber bundles in smokers. However, little is known about the changes in topological organization of WM structural network in young smokers. In current study, we acquired DTI datasets from 58 male young smokers and 51 matched nonsmokers and constructed the WM networks by the deterministic fiber tracking approach. Graph theoretical analysis was used to compare the topological parameters of WM network (global and nodal) and the inter-regional fractional anisotropy (FA) weighted WM connections between groups. The results demonstrated that both young smokers and nonsmokers had small-world topology in WM network. Further analysis revealed that the young smokers exhibited the abnormal topological organization, i.e., increased network strength, global efficiency, and decreased shortest path length. In addition, the increased nodal efficiency predominately was located in frontal cortex, striatum and anterior cingulate gyrus (ACG) in smokers. Moreover, based on network-based statistic (NBS) approach, the significant increased FA-weighted WM connections were mainly found in the PFC, ACG and supplementary motor area (SMA) regions. Meanwhile, the network parameters were correlated with the nicotine dependence severity (FTND) scores, and the nodal efficiency of orbitofrontal cortex was positive correlation with the cigarette per day (CPD) in young smokers. We revealed the abnormal topological organization of WM network in young smokers, which may improve our understanding of the neural mechanism of young smokers form WM topological organization level.

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

Access this article

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

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Achard, S., & Bullmore, E. (2007). Efficiency and cost of economical brain functional networks. PLoS Computational Biology, 3, e17.

    Article  PubMed  PubMed Central  Google Scholar 

  • Almeida, O. P., Garrido, G. J., Lautenschlager, N. T., Hulse, G. K., Jamrozik, K., & Flicker, L. (2008). Smoking is associated with reduced cortical regional gray matter density in brain regions associated with incipient Alzheimer disease. The American Journal of Geriatric Psychiatry, 16, 92–98.

    Article  PubMed  Google Scholar 

  • Baler, R. D., & Volkow, N. D. (2006). Drug addiction: The neurobiology of disrupted self-control. Trends in Molecular Medicine, 12, 559–566.

    Article  CAS  PubMed  Google Scholar 

  • Boccaletti, S., Latora, V., Moreno, Y., Chavez, M., & Hwang, D.-U. (2006). Complex networks: Structure and dynamics. Physics Reports, 424, 175–308.

    Article  Google Scholar 

  • Brody, A. L., Mandelkern, M. A., Lee, G., Smith, E., Sadeghi, M., Saxena, S., Jarvik, M. E., & London, E. D. (2004). Attenuation of cue-induced cigarette craving and anterior cingulate cortex activation in bupropion-treated smokers: A preliminary study. Psychiatry Research: Neuroimaging, 130, 269–281.

    Article  PubMed  PubMed Central  Google Scholar 

  • Bruni, J. E., & Montemurro, D. G. (2009). Human neuroanatomy: A text, brain atlas, and laboratory dissection guide. USA: Oxford University Press.

    Google Scholar 

  • Bruno, J., Hosseini, S. H., & Kesler, S. (2012). Altered resting state functional brain network topology in chemotherapy-treated breast cancer survivors. Neurobiology of Disease, 48, 329–338.

    Article  PubMed  PubMed Central  Google Scholar 

  • Bullmore, E., & Sporns, O. (2009). Complex brain networks: Graph theoretical analysis of structural and functional systems. Nature Reviews Neuroscience, 10, 186–198.

    Article  CAS  PubMed  Google Scholar 

  • Butts, C. T. (2009). Revisiting the foundations of network analysis. Science, 325, 414–416.

    Article  CAS  PubMed  Google Scholar 

  • Cai, C., Yuan, K., Yin, J., Feng, D., Bi, Y., Li, Y., Yu, D., Jin, C., Wei, Q., & Tian, J. (2016). Striatum morphometry is associated with cognitive control deficits and symptom severity in internet gaming disorder. Brain Imaging and Behavior, 10, 1–9.

    Article  Google Scholar 

  • Cui, Z., Zhong, S., Xu, P., He, Y., Gong, G., 2013. PANDA: A pipeline toolbox for analyzing brain diffusion images.

    Google Scholar 

  • Fagerström, K.-O. (1978). Measuring degree of physical dependence to tobacco smoking with reference to individualization of treatment. Addictive Behaviors, 3, 235–241.

    Article  PubMed  Google Scholar 

  • Feng, D., Yuan, K., Li, Y., Cai, C., Yin, J., Bi, Y., Cheng, J., Guan, Y., Shi, S., & Yu, D. (2015). Intra-regional and inter-regional abnormalities and cognitive control deficits in young adult smokers. Brain Imaging and Behavior, 1–11.

  • Fornito, A., Zalesky, A., Bullmore, E., 2016. Fundamentals of brain network analysis. Academic Press.

  • Gong, G., He, Y., Concha, L., Lebel, C., Gross, D. W., Evans, A. C., & Beaulieu, C. (2009b). Mapping anatomical connectivity patterns of human cerebral cortex using in vivo diffusion tensor imaging tractography. Cerebral Cortex, 19, 524–536.

    Article  PubMed  Google Scholar 

  • Hagmann, P., Cammoun, L., Gigandet, X., Meuli, R., Honey, C. J., Wedeen, V. J., & Sporns, O. (2008). Mapping the structural core of human cerebral cortex. PLoS Biology, 6, e159.

    Article  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Hoeft, F., Barneagoraly, N., Haas, B. W., Golarai, G., Ng, D., Mills, D., Korenberg, J., Bellugi, U., Galaburda, A., & Reiss, A. L. (2007). More is not always better: Increased fractional anisotropy of superior longitudinal fasciculus associated with poor visuospatial abilities in Williams syndrome. The Journal of Neuroscience: the Official Journal of the Society for Neuroscience, 27, 11960–11965.

    Article  CAS  Google Scholar 

  • Hudkins, M., O’Neill, J., Tobias, M. C., Bartzokis, G., & London, E. D. (2012). Cigarette smoking and white matter microstructure. Psychopharmacology, 221, 285–295.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Humphries, M. D., Gurney, K., & Prescott, T. J. (2005). Is there an integrative center in the vertebrate brain-stem? A robotic evaluation of a model of the reticular formation viewed as an action selection device. Adaptive Behavior, 13, 97–113.

    Article  Google Scholar 

  • Jacobsen, L. K., Giedd, J. N., Gottschalk, C., Kosten, T. R., & Krystal, J. H. (2001). Quantitative morphology of the caudate and putamen in patients with cocaine dependence. American Journal of Psychiatry, 158, 486–489.

    Article  CAS  PubMed  Google Scholar 

  • Jacobsen, L. K., Picciotto, M. R., Heath, C. J., Frost, S. J., Tsou, K. A., Dwan, R. A., Jackowski, M. P., Constable, R. T., & Mencl, W. E. (2007). Prenatal and adolescent exposure to tobacco smoke modulates the development of white matter microstructure. The Journal of Neuroscience, 27, 13491–13498.

    Article  CAS  PubMed  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 

  • Kalivas, P. W., & Volkow, N. D. (2005). The neural basis of addiction: A pathology of motivation and choice. American Journal of Psychiatry, 162, 1403–1413.

    Article  PubMed  Google Scholar 

  • Kim, D.-J., Skosnik, P. D., Cheng, H., Pruce, B. J., Brumbaugh, M. S., Vollmer, J. M., Hetrick, W. P., O'Donnell, B. F., Sporns, O., & Puce, A. (2011). Structural network topology revealed by white matter tractography in cannabis users: A graph theoretical analysis. Brain Connectivity, 1, 473–483.

    Article  PubMed  PubMed Central  Google Scholar 

  • Koehler, S., Hasselmann, E., Wüstenberg, T., Heinz, A., & Romanczuk-Seiferth, N. (2015). Higher volume of ventral striatum and right prefrontal cortex in pathological gambling. Brain Structure and Function, 220, 469–477.

    Article  PubMed  Google Scholar 

  • Koob, G. F., & Volkow, N. D. (2010). Neurocircuitry of addiction. Neuropsychopharmacology, 35, 217–238.

    Article  PubMed  Google Scholar 

  • Kringelbach, M. L. (2005). The human orbitofrontal cortex: Linking reward to hedonic experience. Nature Reviews Neuroscience, 6, 691–702.

    Article  CAS  PubMed  Google Scholar 

  • Kühn, S., Schubert, F., & Gallinat, J. (2010). Reduced thickness of medial orbitofrontal cortex in smokers. Biological Psychiatry, 68, 1061–1065.

    Article  PubMed  Google Scholar 

  • Latora, V., & Marchiori, M. (2001). Efficient behavior of small-world networks. Physical Review Letters, 87, 198701.

    Article  CAS  PubMed  Google Scholar 

  • Le Bihan, D. (2003). Looking into the functional architecture of the brain with diffusion MRI. Nature Reviews Neuroscience, 4, 469–480.

    Article  CAS  PubMed  Google Scholar 

  • Li, Y., Yuan, K., Cai, C., Feng, D., Yin, J., Bi, Y., Shi, S., Yu, D., Jin, C., & von Deneen, K. M. (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 

  • Liao, Y., Tang, J., Deng, Q., Deng, Y., Luo, T., Wang, X., Chen, H., Liu, T., Chen, X., & Brody, A. L. (2011). Bilateral fronto-parietal integrity in young chronic cigarette smokers: A diffusion tensor imaging study. PloS One, 6, e26460.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Limbrick-Oldfield, E. H., van Holst, R. J., & Clark, L. (2013). Fronto-striatal dysregulation in drug addiction and pathological gambling: Consistent inconsistencies? Neuro Image: Clinical, 2, 385–393.

    Google Scholar 

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

    Article  PubMed  Google Scholar 

  • Makris, N., Kennedy, D. N., McInerney, S., Sorensen, A. G., Wang, R., Caviness, V. S., & Pandya, D. N. (2005). Segmentation of subcomponents within the superior longitudinal fascicle in humans: A quantitative, in vivo, DT-MRI study. Cerebral Cortex, 15, 854–869.

    Article  PubMed  Google Scholar 

  • Maslov, S., & Sneppen, K. (2002). Specificity and stability in topology of protein networks. Science, 296, 910–913.

    Article  CAS  PubMed  Google Scholar 

  • Mori, S., 2013. MRI atlas of human white matter -, S. Wakana.

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

    Article  CAS  PubMed  Google Scholar 

  • Paul, R. H., Grieve, S. M., Niaura, R., David, S. P., Laidlaw, D. H., Cohen, R., Sweet, L., Taylor, G., Clark, C. R., & Pogun, S. (2008). Chronic cigarette smoking and the microstructural integrity of white matter in healthy adults: A diffusion tensor imaging study. Nicotine & Tobacco Research, 10, 137–147.

    Article  CAS  Google Scholar 

  • Rubinov, M., & Sporns, O. (2010). Complex network measures of brain connectivity: Uses and interpretations. NeuroImage, 52, 1059–1069.

    Article  PubMed  Google Scholar 

  • Shu, N., Liu, Y., Li, J., Li, Y., Yu, C., & Jiang, T. (2009). Altered anatomical network in early blindness revealed by diffusion tensor tractography. PloS One, 4, e7228.

    Article  PubMed  PubMed Central  Google Scholar 

  • Shu, N., Liu, Y., Li, K., Duan, Y., Wang, J., Yu, C., Dong, H., Ye, J., & He, Y. (2011). Diffusion tensor tractography reveals disrupted topological efficiency in white matter structural networks in multiple sclerosis. Cerebral Cortex, 21, 2565–2577.

    Article  PubMed  Google Scholar 

  • Sporns, O. (2011). The human connectome: A complex network. Annals of the New York Academy of Sciences, 1224, 109–125.

    Article  PubMed  Google Scholar 

  • Sun, Y., Wang, G.B., Lin, Q.X., Lu, L., Shu, N., Meng, S.Q., Wang, J., Han, H.B., He, Y., Shi, J., 2015. Disrupted white matter structural connectivity in heroin abusers. Addiction biology.

    Google Scholar 

  • Tuch, D. S., Wedeen, V. J., Dale, A. M., George, J. S., & Belliveau, J. W. (2001). Conductivity tensor mapping of the human brain using diffusion tensor MRI. Proceedings of the National Academy of Sciences, 98, 11697–11701.

    Article  CAS  Google Scholar 

  • Watts, D. J., & Strogatz, S. H. (1998). Collective dynamics of ‘small-world’networks. Nature, 393, 440–442.

    Article  CAS  PubMed  Google Scholar 

  • Wise, R. A. (2009). Roles for nigrostriatal—Not just mesocorticolimbic—Dopamine in reward and addiction. Trends in Neurosciences, 32, 517–524.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wylie, K. P., Rojas, D. C., Tanabe, J., Martin, L. F., & Tregellas, J. R. (2012). Nicotine increases brain functional network efficiency. NeuroImage, 63, 73–80.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yu, D., Yuan, K., Zhang, B., Liu, J., Dong, M., Jin, C., Luo, L., Zhai, J., Zhao, L., Zhao, Y., 2015. White matter integrity in young smokers: A tract-based spatial statistics study. Addiction biology.

  • Yuan, K., Yu, D., Bi, Y., Li, Y., Guan, Y., Liu, J., Zhang, Y., Qin, W., Lu, X., Tian, J., 2016. The implication of frontostriatal circuits in young smokers: A resting-state study. Human brain mapping.

  • Zalesky, A., Fornito, A., Harding, I. H., Cocchi, L., Yücel, M., Pantelis, C., & Bullmore, E. T. (2010). Whole-brain anatomical networks: Does the choice of nodes matter? NeuroImage, 50, 970–983.

    Article  PubMed  Google Scholar 

  • Zhang, J., Wang, J., Wu, Q., Kuang, W., Huang, X., He, Y., & Gong, Q. (2011a). Disrupted brain connectivity networks in drug-naive, first-episode major depressive disorder. Biological Psychiatry, 70, 334–342.

    Article  PubMed  Google Scholar 

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

    Article  PubMed  Google Scholar 

  • Zhang, R., Jiang, G., Tian, J., Qiu, Y., Wen, X., Zalesky, A., Li, M., Ma, X., Wang, J., & Li, S. (2015). Abnormal white matter structural networks characterize heroin-dependent individuals: A network analysis. Addiction Biology. doi:10.1111/adb.12234.

    Google Scholar 

  • Zhang, R., Jiang, G., Tian, J., Qiu, Y., Wen, X., Zalesky, A., Li, M., Ma, X., Wang, J., & Li, S. (2016). Abnormal white matter structural networks characterize heroin-dependent individuals: A network analysis. Addiction Biology, 21, 667.

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

This paper is supported by the Project for the National Natural Science Foundation of China under Grant nos. 81571751, 81571753, 61502376, 81401478, 81401488, 81470816, 61431013, 81471737, 81301281, 81271644, 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. JBG151207, JB161201 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

Authors

Corresponding authors

Correspondence to Dahua Yu or Kai Yuan.

Ethics declarations

Ethical statements

Informed consent was obtained from all individual participants included in the study.

Ethics 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

Conflict of interest

The authors declare that we have no conflict of interest.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Zhang, Y., Li, M., Wang, R. et al. Abnormal brain white matter network in young smokers: a graph theory analysis study. Brain Imaging and Behavior 12, 345–356 (2018). https://doi.org/10.1007/s11682-017-9699-6

Download citation

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11682-017-9699-6

Keywords

Navigation