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Altered dynamic interactions within frontostriatal circuits reflect disturbed craving processing in internet gaming disorder

Published online by Cambridge University Press:  21 September 2020

Ningning Zeng
Affiliation:
Center for Cognition and Brain Disorders, The Affiliated Hospital of Hangzhou Normal University, Hangzhou, People’s Republic of China Shenzhen key laboratory of Affective and Social Neuroscience, Center for Brain Disorders and Cognitive Science, Shenzhen University, Shenzhen, People’s Republic of China
Min Wang
Affiliation:
Center for Cognition and Brain Disorders, The Affiliated Hospital of Hangzhou Normal University, Hangzhou, People’s Republic of China
Haohao Dong
Affiliation:
Department of Psychology, Zhejiang Normal University, Jinhua, People’s Republic of China
Xiaoxia Du
Affiliation:
Department of Physics, Shanghai Key Laboratory of Magnetic Resonance, East China Normal University, Shanghai, People’s Republic of China
Guang-Heng Dong*
Affiliation:
Center for Cognition and Brain Disorders, The Affiliated Hospital of Hangzhou Normal University, Hangzhou, People’s Republic of China Zhejiang Key Laboratory for Research in Assessment of Cognitive Impairments, Hangzhou, People’s Republic of China
*
*Author for correspondence: Guang-Heng Dong, PhD, Email: dongguangheng@hznu.edu.cn

Abstract

Background

Individuals with internet gaming disorder (IGD) are generally characterized by impaired executive control, persistent game-craving, and excessive reward-seeking behaviors. However, the causal interactions within the frontostriatal circuits underlying these problematic behaviors remain unclear. Here, spectral dynamic causal modeling (spDCM) was implemented to explore this issue.

Methods

Resting-state functional magnetic resonance imaging data from 317 online game players (148 IGD subjects and 169 recreational game users (RGUs)) were collected. Using independent component analysis, we determined six region of interests within frontostriatal circuits for further spDCM analysis, and further statistical analyses based on the parametric empirical Bayes framework were performed.

Results

Compared with RGUs, IGD subjects showed inhibitory effective connectivity from the right orbitofrontal cortex (OFC) to the right caudate and from the right dorsolateral prefrontal cortex to the left OFC; at the same time, excitatory effective connectivity was observed from the thalamus to the left OFC. Correlation analyses results showed that the directional connection from the right OFC to the right caudate was negatively associated with addiction severity.

Conclusions

These results suggest that the disrupted causal interactions between specific regions might contribute to dysfunctions within frontostriatal circuits in IGD, and the pathway from the right OFC to the right caudate could serve as a target for brain modulation in future IGD interventions.

Type
Original Research
Copyright
© The Author(s), 2020. Published by Cambridge University Press

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References

Starcevic, V, Aboujaoude, E. Internet addiction: reappraisal of an increasingly inadequate concept. CNS Spectr. 2017;22(1):713. doi:10.1017/s1092852915000863 CrossRefGoogle ScholarPubMed
Zheng, H, Hu, Y, Wang, Z, Wang, M, Du, X, Dong, G. Meta-analyses of the functional neural alterations in subjects with internet gaming disorder: similarities and differences across different paradigms. Prog Neuropsychopharmacol Biol Psychiatry. 2019;94:109656109656. doi:10.1016/j.pnpbp.2019.109656 CrossRefGoogle ScholarPubMed
Kuss, DJ, Pontes, HM, Griffiths, MD. Neurobiological correlates in internet gaming disorder: a systematic literature review. Front Psychiatry. 2018;9166. doi:10.3389/fpsyt.2018.00166 Google Scholar
Kuss, DJ, Griffiths, MD, Pontes, HM. DSM-5 diagnosis of internet gaming disorder: some ways forward in overcoming issues and concerns in the gaming studies field. J Behav Addict. 2017;6(2):133141. doi:10.1556/2006.6.2017.032 CrossRefGoogle ScholarPubMed
Aarseth, E, Bean, AM, Boonen, H, et al. Scholars’ open debate paper on the World Health Organization ICD-11 gaming disorder proposal. J Behav Addict. 2017;6(3):267270. doi:10.1556/2006.5.2016.088 CrossRefGoogle ScholarPubMed
Dong, G, Potenza, MN. A cognitive-behavioral model of internet gaming disorder: theoretical underpinnings and clinical implications. J Psychiatr Res. 2014;58:711. doi:10.1016/j.jpsychires.2014.07.005 CrossRefGoogle ScholarPubMed
Bechara, A. Decision making, impulse control and loss of willpower to resist drugs: a neurocognitive perspective. Nat Neurosci. 2005;8(11):14581463. doi:10.1038/nn1584 CrossRefGoogle ScholarPubMed
Petry, NM, Rehbein, F, Gentile, DA, et al. An international consensus for assessing internet gaming disorder using the new DSM-5 approach. Addiction. 2014;109(9):13991406. doi:10.1111/add.12457 CrossRefGoogle ScholarPubMed
Petry, NM, Zajac, K, Ginley, MK. Behavioral addictions as mental disorders: to be or not to be? Ann Rev Clin Psychol. 2018;14:399423.CrossRefGoogle ScholarPubMed
Dong, G, Wang, L, Du, X, Potenza, MN. Gaming increases craving to gaming-related stimuli in individuals with internet gaming disorder. Biol Psychiatry Cogn Neurosci Neuroimaging. 2017;2(5):404412. doi:10.1016/j.bpsc.2017.01.002 Google ScholarPubMed
Dong, G, Wang, L, Du, X, Potenza, MN. Gender-related differences in neural responses to gaming cues before and after gaming: implications for gender-specific vulnerabilities to internet gaming disorder. Soc Cogn Affect Neurosci. 2018;13(11):12031214. doi:10.1093/scan/nsy084 CrossRefGoogle ScholarPubMed
Liu, L, Yip, SW, Zhang, JT, et al. Activation of the ventral and dorsal striatum during cue reactivity in internet gaming disorder. Addict Biol. 2017;22(3):791801. doi:10.1111/adb.12338 CrossRefGoogle ScholarPubMed
Jasinska, AJ, Stein, EA, Kaiser, J, Naumer, MJ, Yalachkov, Y. Factors modulating neural reactivity to drug cues in addiction: a survey of human neuroimaging studies. Neurosci Biobehav Rev. 2014;38:116. doi:10.1016/j.neubiorev.2013.10.013 CrossRefGoogle ScholarPubMed
Courtney, KE, Schacht, JP, Hutchison, K, Roche, DJO, Ray, LA. Neural substrates of cue reactivity: association with treatment outcomes and relapse. Rev Addict Biol. 2016;21(1):322. doi:10.1111/adb.12314 CrossRefGoogle ScholarPubMed
Broadwater, MA, Lee, S-H, Yu, Y, et al. Adolescent alcohol exposure decreases frontostriatal resting-state functional connectivity in adulthood. Addict Biol. 2018;23(2):810823. doi:10.1111/adb.12530 CrossRefGoogle ScholarPubMed
Park, SQ, Kahnt, T, Beck, A, et al. Prefrontal cortex fails to learn from reward prediction errors in alcohol dependence. J Neurosci. 2010;30(22):77497753. doi:10.1523/jneurosci.5587-09.2010 CrossRefGoogle ScholarPubMed
Yuan, K, Yu, D, Bi, Y, et al. The left dorsolateral prefrontal cortex and caudate pathway: new evidence for cue-induced craving of smokers. Hum Brain Mapp. 2017;38(9):46444656. doi:10.1002/hbm.23690 CrossRefGoogle ScholarPubMed
Becker, A, Kirsch, M, Gerchen, MF, Kiefer, F, Kirsch, P. Striatal activation and frontostriatal connectivity during non-drug reward anticipation in alcohol dependence. Addict Biol. 2017;22(3):833843. doi:10.1111/adb.12352 CrossRefGoogle ScholarPubMed
Faulkner, P, Ghahremani, DG, Tyndale, RF, et al. Neural basis of smoking-induced relief of craving and negative affect: contribution of nicotine. Addict Biol. 2019;24(5):10871095. doi:10.1111/adb.12679 CrossRefGoogle ScholarPubMed
Moningka, H, Lichenstein, S, Worhunsky, PD, DeVito, EE, Scheinost, D, Yip, SW. Can neuroimaging help combat the opioid epidemic? A systematic review of clinical and pharmacological challenge fMRI studies with recommendations for future research. Rev Neuropsychopharmacol. 2019;44(2):259273. doi:10.1038/s41386-018-0232-4 CrossRefGoogle ScholarPubMed
Volkow, ND, Wang, G-J, Tomasi, D, Baler, RD. Unbalanced neuronal circuits in addiction. Curr Opin Neurobiol. 2013;23(4):639648. doi:10.1016/j.conb.2013.01.002 CrossRefGoogle ScholarPubMed
Kober, H, Mende-Siedlecki, P, Kross, EF, et al. Prefrontal-striatal pathway underlies cognitive regulation of craving. Proc Natl Acad Sci USA. 2010;107(33):1481114816. doi:10.1073/pnas.1007779107 CrossRefGoogle ScholarPubMed
Jin, C, Zhang, T, Cai, C, et al. Abnormal prefrontal cortex resting state functional connectivity and severity of internet gaming disorder. Brain Imaging Behav. 2016;10(3):719729. doi:10.1007/s11682-015-9439-8 CrossRefGoogle ScholarPubMed
Yuan, K, Yu, D, Cai, C, et al. Frontostriatal circuits, resting state functional connectivity and cognitive control in internet gaming disorder. Addict Biol. 2017;22(3):813822. doi:10.1111/adb.12348 CrossRefGoogle ScholarPubMed
Friston, KJ, Kahan, J, Biswal, B, Razi, A. A DCM for resting state fMRI. Neuroimage. 2014;94:396407. doi:10.1016/j.neuroimage.2013.12.009 CrossRefGoogle ScholarPubMed
Noel, X, Brevers, D, Bechara, A. A neurocognitive approach to understanding the neurobiology of addiction. Curr Opin Neurobiol. 2013;23(4):632638. doi:10.1016/j.conb.2013.01.018 CrossRefGoogle ScholarPubMed
Vink, M, Zandbelt, BB, Gladwin, T, et al. Frontostriatal activity and connectivity increase during proactive inhibition across adolescence and early adulthood. Hum Brain Mapp. 2014;35(9):44154427. doi:10.1002/hbm.22483 CrossRefGoogle ScholarPubMed
Chang, MK, Law, SPM. Factor structure for Young’s internet addiction test: a confirmatory study. Comput Human Behav. 2008;24(6):25972619. doi:10.1016/j.chb.2008.03.001 CrossRefGoogle Scholar
Dong, G, Liu, X, Zheng, H, Du, X, Potenza, MN. Brain response features during forced break could predict subsequent recovery in internet gaming disorder: a longitudinal study. J Psychiatr Res. 2019;113:1726. doi:10.1016/j.jpsychires.2019.03.003 CrossRefGoogle ScholarPubMed
Dong, G, Wang, M, Liu, X, Liang, Q, Du, X, Potenza, MN. Cue-elicited craving-related lentiform activation during gaming deprivation is associated with the emergence of internet gaming disorder. Addict Biol. 2019;25(1):19. doi:10.1111/adb.12713 Google ScholarPubMed
Albrithen, AA, Singleton, EG. Brief Arabic Tobacco Craving Questionnaire: an investigation into craving and heavy smoking in Saudi Arabian males. J Family Community Med. 2015;22(1):812. doi:10.4103/2230-8229.149573 CrossRefGoogle ScholarPubMed
Sheehan, DV, Lecrubier, Y, Sheehan, KH, et al. The Mini-International Neuropsychiatric Interview (M.I.N.I.): the development and validation of a structured diagnostic psychiatric interview for DSM-IV and ICD-10. J Clin Psychiatry. 1998;59(Suppl 20):2233; quiz 34–57. doi:10.4088/JCP.09m05305whi Google ScholarPubMed
Li, Y-O, Adali, T, Calhoun, VD. Estimating the number of independent components for functional magnetic resonance Imaging data. Hum Brain Mapp. 2007;28(11):12511266. doi:10.1002/hbm.20359 CrossRefGoogle ScholarPubMed
Shirer, WR, Ryali, S, Rykhlevskaia, E, Menon, V, Greicius, MD. Decoding subject-driven cognitive states with whole-brain connectivity patterns. Cereb Cortex. 2012;22(1):158165. doi:10.1093/cercor/bhr099 CrossRefGoogle ScholarPubMed
Friston, KJ, Harrison, L, Penny, W. Dynamic causal modelling. NeuroImage. 2003;19(4):12731302. doi:10.1016/s1053-8119(03)00202-7 CrossRefGoogle ScholarPubMed
Friston, KJ, Litvak, V, Oswal, A, et al. Bayesian model reduction and empirical Bayes for group (DCM) studies. Neuroimage. 2016;128:413431. doi:10.1016/j.neuroimage.2015.11.015 CrossRefGoogle Scholar
Tremblay, L, Schultz, W. Relative reward preference in primate orbitofrontal cortex. Nature. 1999;398(6729):704708.CrossRefGoogle ScholarPubMed
Wallis, JD, Miller, EK. Neuronal activity in primate dorsolateral and orbital prefrontal cortex during performance of a reward preference task. Eur J Neurosci. 2003;18(7):20692081. doi:10.1046/j.1460-9568.2003.02922.x CrossRefGoogle ScholarPubMed
Schultz, W, Tremblay, L, Hollerman, JR. Reward processing in primate orbitofrontal cortex and basal ganglia. Cereb Cortex. 2000;10(3):272284. doi:10.1093/cercor/10.3.272 CrossRefGoogle ScholarPubMed
Greicius, MD, Flores, BH, Menon, V, et al. Resting-state functional connectivity in major depression: abnormally increased contributions from subgenual cingulate cortex and thalamus. Biol Psychiatry. 2007;62(5):429437. doi:10.1016/j.biopsych.2006.09.020 CrossRefGoogle ScholarPubMed
Sanchez-Gonzalez, MA, Garcia-Cabezas, MA, Rico, B, Cavada, C. The primate thalamus is a key target for brain dopamine. J Neurosci. 2005;25(26):60766083. doi:10.1523/jneurosci.0968-05.2005 CrossRefGoogle ScholarPubMed
Zhao, Q, Xu, T, Wang, Y, et al. Limbic cortico-striato-thalamo-cortical functional connectivity in drug-naive patients of obsessive-compulsive disorder. Psychol Med. 2019;50:113. doi:10.1017/s0033291719002988 Google Scholar
Dong, G, DeVito, E, Huang, J, Du, X. Diffusion tensor imaging reveals thalamus and posterior cingulate cortex abnormalities in internet gaming addicts. J Psychiatr Res. 2012;46(9):12121216. doi:10.1016/j.jpsychires.2012.05.015 CrossRefGoogle ScholarPubMed
Dong, G, Wu, L, Wang, Z, Wang, Y, Du, X, Potenza, MN. Diffusion-weighted MRI measures suggest increased white-matter integrity in internet gaming disorder: evidence from the comparison with recreational internet game users. Addict Behav. 2018;81:3238. doi:10.1016/j.addbeh.2018.01.030 CrossRefGoogle ScholarPubMed
Kerns, JG, Cohen, JD, MacDonald, AW 3rd, Cho, RY, Stenger, VA, Carter, CS. Anterior cingulate conflict monitoring and adjustments in control. Science. 2004;303(5660):10231026. doi:10.1126/science.1089910 CrossRefGoogle ScholarPubMed
Cieslik, EC, Zilles, K, Caspers, S, et al. Is there one DLPFC in cognitive action control? Evidence for heterogeneity from co-activation-based parcellation. Cereb Cortex. 2013;23(11):26772689. doi:10.1093/cercor/bhs256 CrossRefGoogle ScholarPubMed
Choi, J, Cho, H, Kim, JY, et al. Structural alterations in the prefrontal cortex mediate the relationship between internet gaming disorder and depressed mood. Sci Rep. 2017;7 (10):1245. doi:10.1038/s41598-017-01275-5 CrossRefGoogle ScholarPubMed
Fettes, P, Schulze, L, Downar, J. Cortico-striatal-thalamic loop circuits of the orbitofrontal cortex: promising therapeutic targets in psychiatric illness. Front Syst Neurosci. 2017;1125:123. doi:10.3389/fnsys.2017.00025 Google Scholar
Noonan, MP, Chau, BKH, Rushworth, MFS, Fellows, LK. Contrasting effects of medial and lateral orbitofrontal cortex lesions on credit assignment and decision-making in humans. J Neurosci. 2017;37(29):70237035. doi:10.1523/jneurosci.0692-17.2017 CrossRefGoogle ScholarPubMed
Dong, G, Lin, X, Hu, Y, Xie, C, Du, X. Imbalanced functional link between executive control network and reward network explain the online-game seeking behaviors in internet gaming disorder. Sci Rep. 2015;5:59197. doi:10.1038/srep09197 Google ScholarPubMed
Henssen, A, Zilles, K, Palomero-Gallagher, N, et al. Cytoarchitecture and probability maps of the human medial orbitofrontal cortex. Cortex. 2016;75:87112. doi:10.1016/j.cortex.2015.11.006 CrossRefGoogle ScholarPubMed
Kringelbach, ML. The human orbitofrontal cortex: linking reward to hedonic experience. Nat Rev Neurosci. 2005;6(9):691702. doi:10.1038/nrn1747 CrossRefGoogle ScholarPubMed
Moorman, DE. The role of the orbitofrontal cortex in alcohol use, abuse, and dependence. Prog Neuropsychopharmacol Biol Psychiatry. 2018;87:85107. doi:10.1016/j.pnpbp.2018.01.010 CrossRefGoogle ScholarPubMed
Rudebeck, PH, Ripple, JA, Mitz, AR, Averbeck, BB, Murray, EA. Amygdala contributions to stimulus-reward encoding in the Macaque medial and orbital frontal cortex during learning. J Neurosci. 2017;37(8):21862202. doi:10.1523/jneurosci.0933-16.2017 CrossRefGoogle ScholarPubMed
Zhang, J-T, Ma, S-S, Li, C-SR, et al. Craving behavioral intervention for internet gaming disorder: remediation of functional connectivity of the ventral striatum. Addict Biol. 2018;23(1):337346. doi:10.1111/adb.12474 CrossRefGoogle ScholarPubMed