Skip to main content

Advertisement

SpringerLink
Log in

Abnormal prefrontal cortex resting state functional connectivity and severity of internet gaming disorder

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

Abstract

Internet Gaming Disorder (IGD) among adolescents has become an important public concern and gained more and more attention internationally. Recent studies focused on IGD and revealed brain abnormalities in the IGD group, especially the prefrontal cortex (PFC). However, the role of PFC-striatal circuits in pathology of IGD remains unknown. Twenty-five adolescents with IGD and 21 age- and gender-matched healthy controls were recruited in our study. Voxel-based morphometric (VBM) and functional connectivity analysis were employed to investigate the abnormal structural and resting-state properties of several frontal regions in individuals with online gaming addiction. Relative to healthy comparison subjects, IGD subjects showed significant decreased gray matter volume in PFC regions including the bilateral dorsolateral prefrontal cortex (DLPFC), orbitofrontal cortex (OFC), anterior cingulate cortex (ACC) and the right supplementary motor area (SMA) after controlling for age and gender effects. We chose these regions as the seeding areas for the resting-state analysis and found that IGD subjects showed decreased functional connectivity between several cortical regions and our seeds, including the insula, and temporal and occipital cortices. Moreover, significant decreased functional connectivity between some important subcortical regions, i.e., dorsal striatum, pallidum, and thalamus, and our seeds were found in the IGD group and some of those changes were associated with the severity of IGD. Our results revealed the involvement of several PFC regions and related PFC-striatal circuits in the process of IGD and suggested IGD may share similar neural mechanisms with substance dependence at the circuit level.

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.

Institutional subscriptions

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

Similar content being viewed by others

References

  • Barke, A., Nyenhuis, N., & Kröner-Herwig, B. (2012). The German version of the internet addiction test: a validation study. Cyberpsychology, Behavior and Social Networking, 15(10), 534–542.

    Article  PubMed  Google Scholar 

  • Blasi, G., Goldberg, T. E., Weickert, T., Das, S., Kohn, P., Zoltick, B., et al. (2006). Brain regions underlying response inhibition and interference monitoring and suppression. European Journal of Neuroscience, 23(6), 1658–1664.

    Article  PubMed  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 

  • Bremer, J. (2005). The internet and children: advantages and disadvantages. Child and Adolescent Psychiatric Clinics of North America, 14(3), 405.

    Article  PubMed  Google Scholar 

  • Brier, M. R., Thomas, J. B., Snyder, A. Z., Benzinger, T. L., Zhang, D., Raichle, M. E., et al. (2012). Loss of intranetwork and internetwork resting state functional connections with Alzheimer’s disease progression. The Journal of Neuroscience, 32(26), 8890–8899.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bunge, S. A., Ochsner, K. N., Desmond, J. E., Glover, G. H., & Gabrieli, J. D. (2001). Prefrontal regions involved in keeping information in and out of mind. Brain, 124(10), 2074–2086.

    Article  CAS  PubMed  Google Scholar 

  • Cao, H., Sun, Y., Wan, Y., Hao, J., & Tao, F. (2011). Problematic internet use in Chinese adolescents and its relation to psychosomatic symptoms and life satisfaction. BMC Public Health, 11(1), 802.

    Article  PubMed  PubMed Central  Google Scholar 

  • Crockford, D. N., Goodyear, B., Edwards, J., Quickfall, J., & El-Guebaly, N. (2005). Cue-induced brain activity in pathological gamblers. Biological Psychiatry, 58(10), 787–795.

    Article  PubMed  Google Scholar 

  • Dimitri, C., Megan, M., Lauren, J., Mon, M., & Chuan, Z. (2011) Problematic internet usage in US college students: a pilot study. BMC Medicine, 9.

  • Dong, G., Lu, Q., Zhou, H., & Zhao, X. (2010). Impulse inhibition in people with Internet addiction disorder: electrophysiological evidence from a Go/NoGo study. Neuroscience Letters, 485(2), 138–142.

    Article  CAS  PubMed  Google Scholar 

  • Durkee, T., Kaess, M., Carli, V., Parzer, P., Wasserman, C., Floderus, B., et al. (2012). Prevalence of pathological internet use among adolescents in Europe: demographic and social factors. Addiction, 107(12), 2210–2222.

    Article  PubMed  Google Scholar 

  • Everitt, B. J., & Robbins, T. W. (2005). Neural systems of reinforcement for drug addiction: from actions to habits to compulsion. Nature Neuroscience, 8(11), 1481–1489.

    Article  CAS  PubMed  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 

  • Forman, S. D., Dougherty, G. G., Casey, B., Siegle, G. J., Braver, T. S., Barch, D. M., et al. (2004). Opiate addicts lack error-dependent activation of rostral anterior cingulate. Biological Psychiatry, 55(5), 531–537.

    Article  CAS  PubMed  Google Scholar 

  • Fox, M. D., & Raichle, M. E. (2007). Spontaneous fluctuations in brain activity observed with functional magnetic resonance imaging. Nature Reviews Neuroscience, 8(9), 700–711.

    Article  CAS  PubMed  Google Scholar 

  • Goldstein, R. Z., & Volkow, N. D. (2002). Drug addiction and its underlying neurobiological basis: neuroimaging evidence for the involvement of the frontal cortex. American Journal of Psychiatry, 159(10), 1642–1652.

    Article  PubMed  PubMed Central  Google Scholar 

  • Goldstein, R. Z., & Volkow, N. D. (2011). Dysfunction of the prefrontal cortex in addiction: neuroimaging findings and clinical implications. Nature Reviews Neuroscience, 12(11), 652–669.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Grant, J. E., Potenza, M. N., Weinstein, A., & Gorelick, D. A. (2010). Introduction to behavioral addictions. The American Journal of Drug and Alcohol Abuse, 36(5), 233–241.

    Article  PubMed  PubMed Central  Google Scholar 

  • Hanlon, C. A., Wesley, M. J., Stapleton, J. R., Laurienti, P. J., & Porrino, L. J. (2011). The association between frontal–striatal connectivity and sensorimotor control in cocaine users. Drug and Alcohol Dependence, 115(3), 240–243.

    Article  PubMed  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 

  • Hong, S.-B., Zalesky, A., Cocchi, L., Fornito, A., Choi, E.-J., Kim, H.-H., et al. (2013). Decreased functional brain connectivity in adolescents with internet addiction. PLoS ONE, 8(2), e57831.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Horn, N., Dolan, M., Elliott, R., Deakin, J., & Woodruff, P. (2003). Response inhibition and impulsivity: an fMRI study. Neuropsychologia, 41(14), 1959–1966.

    Article  CAS  PubMed  Google Scholar 

  • Jelenchick, L. A., Becker, T., & Moreno, M. A. (2012). Assessing the psychometric properties of the Internet Addiction Test (IAT) in US college students. Psychiatry Research, 196(2–3), 296–301.

    Article  PubMed  PubMed Central  Google Scholar 

  • Jin, C., Yuan, K., Zhao, L., Zhao, L., Yu, D., Deneen, K. M., et al. (2013). Structural and functional abnormalities in migraine patients without aura. NMR in Biomedicine, 26(1), 58–64.

    Article  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(8), 1403–1413.

    Article  PubMed  Google Scholar 

  • Kim, S. H., Baik, S.-H., Park, C. S., Kim, S. J., Choi, S. W., & Kim, S. E. (2011). Reduced striatal dopamine D2 receptors in people with Internet addiction. NeuroReport, 22(8), 407.

    Article  CAS  PubMed  Google Scholar 

  • Ko, C. H., Liu, G. C., Yen, J. Y., Chen, C. Y., Yen, C. F., & Chen, C. S. (2011). Brain correlates of craving for online gaming under cue exposure in subjects with Internet gaming addiction and in remitted subjects. Addiction Biology, 18(3), 559–569.

  • Ko, C.-H., Liu, G.-C., Yen, J.-Y., Yen, C.-F., Chen, C.-S., & Lin, W.-C. (2012). The brain activations for both cue-induced gaming urge and smoking craving among subjects comorbid with Internet gaming addiction and nicotine dependence. Journal of Psychiatric Research, 47(4), 486–493.

  • Kober, H., Mende-Siedlecki, P., Kross, E. F., Weber, J., Mischel, W., Hart, C. L., et al. (2010). Prefrontal–striatal pathway underlies cognitive regulation of craving. Proceedings of the National Academy of Sciences, 107(33), 14811–14816.

    Article  CAS  Google Scholar 

  • Lin, F., Zhou, Y., Du, Y., Qin, L., Zhao, Z., Xu, J., et al. (2012). Abnormal white matter integrity in adolescents with Internet Addiction Disorder: a tract-based spatial statistics study. PLoS ONE, 7(1), e30253.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Liston, C., Watts, R., Tottenham, N., Davidson, M. C., Niogi, S., Ulug, A. M., et al. (2006). Frontostriatal microstructure modulates efficient recruitment of cognitive control. Cerebral Cortex, 16(4), 553–560.

    Article  PubMed  Google Scholar 

  • Meda, S. A., Gill, A., Stevens, M. C., Lorenzoni, R. P., Glahn, D. C., Calhoun, V. D., et al. (2012). Differences in resting-state functional magnetic resonance imaging functional network connectivity between schizophrenia and psychotic bipolar probands and their unaffected first-degree relatives. Biological Psychiatry, 71(10), 881–889.

    Article  PubMed  PubMed Central  Google Scholar 

  • Pine, D., Cohen, P., & Brook, J. (2001). Emotional reactivity and risk for psychopathology among adolescents. CNS Spectrums, 6(1), 27.

    Article  CAS  PubMed  Google Scholar 

  • Romano, M., Osborne, L. A., Truzoli, R., & Reed, P. (2013). Differential psychological impact of internet exposure on internet addicts. PLoS ONE, 8(2), e55162.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Schoenbaum, G., Roesch, M. R., & Stalnaker, T. A. (2006). Orbitofrontal cortex, decision-making and drug addiction. Trends in Neurosciences, 29(2), 116–124.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Seeley, W. W., Crawford, R. K., Zhou, J., Miller, B. L., & Greicius, M. D. (2009). Neurodegenerative diseases target large-scale human brain networks. Neuron, 62(1), 42.

    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 

  • Smith, S. M., Jenkinson, M., Woolrich, M. W., Beckmann, C. F., Behrens, T., Johansen-Berg, H., et al. (2004). Advances in functional and structural MR image analysis and implementation as FSL. NeuroImage, 23, S208.

    Article  PubMed  Google Scholar 

  • Steinberg, L. (2005). Cognitive and affective development in adolescence. Trends in Cognitive Sciences, 9(2), 69–74.

    Article  PubMed  Google Scholar 

  • Tanabe, J., Tregellas, J. R., Dalwani, M., Thompson, L., Owens, E., Crowley, T., et al. (2009). Medial orbitofrontal cortex gray matter is reduced in abstinent substance-dependent individuals. Biological Psychiatry, 65(2), 160–164.

    Article  PubMed  Google Scholar 

  • Volkow, N. D., Fowler, J. S., Wang, G. J., Hitzemann, R., Logan, J., Schlyer, D. J., et al. (1993). Decreased dopamine D2 receptor availability is associated with reduced frontal metabolism in cocaine abusers. Synapse, 14(2), 169–177.

    Article  CAS  PubMed  Google Scholar 

  • Volkow, N. D., Wang, G.-J., Begleiter, H., Porjesz, B., Fowler, J. S., Telang, F., et al. (2006). High levels of dopamine D2 receptors in unaffected members of alcoholic families: possible protective factors. Archives of General Psychiatry, 63(9), 999.

    Article  CAS  PubMed  Google Scholar 

  • Volkow, N. D., Wang, G.-J., Telang, F., Fowler, J. S., Thanos, P. K., Logan, J., et al. (2008). Low dopamine striatal D2 receptors are associated with prefrontal metabolism in obese subjects: possible contributing factors. NeuroImage, 42(4), 1537–1543.

    Article  PubMed  PubMed Central  Google Scholar 

  • Volkow, N., Fowler, J., Wang, G., Baler, R., & Telang, F. (2009). Imaging dopamine’s role in drug abuse and addiction. Neuropharmacology, 56, 3–8.

    Article  CAS  PubMed  Google Scholar 

  • Volkow, N. D., Wang, G.-J., Tomasi, D., & Baler, R. D. (2013). Unbalanced neuronal circuits in addiction. Current Opinion in Neurobiology, 23(4), 639–648.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Winkler, A., Dörsing, B., Rief, W., Shen, Y., & Glombiewski, J. A. (2013). Treatment of internet addiction: a meta-analysis. Clinical Psychology Review, 33(2), 317–329.

    Article  PubMed  Google Scholar 

  • 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 

  • 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 

  • Young, K. S. (1998a). Caught in the net: How to recognize the signs of internet addiction--and a winning strategy for recovery. New York: Wiley.

    Google Scholar 

  • Young, K. S. (1998b). Internet addiction: the emergence of a new clinical disorder. CyberPsychology & Behavior, 1(3), 237–244.

    Article  Google Scholar 

  • Yu, D., Yuan, K., Zhao, L., Zhao, L., Dong, M., Liu, P., et al. (2012). Regional homogeneity abnormalities in patients with interictal migraine without aura: a resting‐state study. NMR in Biomedicine, 25(5), 806–812.

    Article  PubMed  Google Scholar 

  • Yuan, K., Qin, W., Dong, M., Liu, J., Sun, J., Liu, P., et al. (2010a). Gray matter deficits and resting-state abnormalities in abstinent heroin-dependent individuals. Neuroscience Letters, 482(2), 101–105.

    Article  CAS  PubMed  Google Scholar 

  • Yuan, K., Qin, W., Liu, J., Guo, Q., Dong, M., Sun, J., et al. (2010b). Altered small-world brain functional networks and duration of heroin use in male abstinent heroin-dependent individuals. Neuroscience Letters, 477(1), 37–42.

    Article  CAS  PubMed  Google Scholar 

  • Yuan, K., Qin, W., Wang, G., Zeng, F., Zhao, L., Yang, X., et al. (2011). Microstructure abnormalities in adolescents with internet addiction disorder. PLoS ONE, 6(6), e20708.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yuan, K., Cheng, P., Dong, T., Bi, Y., Xing, L., Yu, D., et al. (2013a). Cortical thickness abnormalities in late adolescence with online gaming addiction. PLoS ONE, 8(1), e53055.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yuan, K., Jin, C., Cheng, P., Yang, X., Dong, T., Bi, Y., et al. (2013b). Amplitude of low frequency fluctuation abnormalities in adolescents with online gaming addiction. PLoS ONE, 8(11), e78708.

    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. doi:10.1007/s00429-014-0982-7.

  • Zhang, X., Salmeron, B. J., Ross, T. J., Gu, H., Geng, X., Yang, Y., et al. (2011). Anatomical differences and network characteristics underlying smoking cue reactivity. NeuroImage, 54(1), 131–141.

    Article  PubMed  Google Scholar 

  • Zhou, Z., Yuan, G., & Yao, J. (2012). Cognitive biases toward internet game-related pictures and executive deficits in individuals with an internet game addiction. PLoS ONE, 7(11), e48961.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgments

This paper is supported by the Project for the National Key Basic Research and Development Program (973) under Grant nos. 2014CB543203, 2011CB707700, 2012CB518501, the National Natural Science Foundation of China under Grant nos. 81401478, 81401488, 81227901, 81271644, 81271546, 81101036, 81101108, 31200837, 81301281, 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. 8002-72125760, 8002-72135767, 8002-72145760, the Natural Science Foundation of Inner Mongolia under Grant no. 2012MS0908. General Financial Grant the China Post- doctoral Science Foundation under Grant no. 2014 M552416. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.

Author information

Author notes

    Authors and Affiliations

    1. Department of Medical Imaging, the First Affiliated Hospital of Medical College, Xi’an Jiaotong University, Xi’an, China

      Chenwang Jin & Ming Zhang

    2. College of Tourism, Guilin Technology of University, Guilin, Guangxi, China

      Ting Zhang

    3. School of Humanities and Social Sciences, Xi’an Jiaotong University, Xi’an, China

      Ting Zhang

    4. Life Sciences Research Center, School of Life Sciences and Technology, Xidian University, Xi’an, Shaanxi, China

      Chenxi Cai, Yanzhi Bi, Yangding Li & Kai Yuan

    5. Information Processing Laboratory, School of Information Engineering, Inner Mongolia University of Science and Technology, Baotou, Inner Mongolia, China

      Dahua Yu

    Authors
    1. Chenwang Jin
      View author publications

      You can also search for this author in PubMed Google Scholar

    2. Ting Zhang
      View author publications

      You can also search for this author in PubMed Google Scholar

    3. Chenxi Cai
      View author publications

      You can also search for this author in PubMed Google Scholar

    4. Yanzhi Bi
      View author publications

      You can also search for this author in PubMed Google Scholar

    5. Yangding Li
      View author publications

      You can also search for this author in PubMed Google Scholar

    6. Dahua Yu
      View author publications

      You can also search for this author in PubMed Google Scholar

    7. Ming Zhang
      View author publications

      You can also search for this author in PubMed Google Scholar

    8. Kai Yuan
      View author publications

      You can also search for this author in PubMed Google Scholar

    Corresponding authors

    Correspondence to Chenwang Jin or Kai Yuan.

    Additional information

    Chenwang Jin and Ting Zhang contributed equally to this work.

    Rights and permissions

    Reprints and permissions

    About this article

    Check for updates. Verify currency and authenticity via CrossMark

    Cite this article

    Jin, C., Zhang, T., Cai, C. et al. Abnormal prefrontal cortex resting state functional connectivity and severity of internet gaming disorder. Brain Imaging and Behavior 10, 719–729 (2016). https://doi.org/10.1007/s11682-015-9439-8

    Download citation

    • Published:

    • Issue Date:

    • DOI: https://doi.org/10.1007/s11682-015-9439-8

    Keywords

    Search

    Navigation