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Impaired executive control and reward circuit in Internet gaming addicts under a delay discounting task: independent component analysis

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Abstract

This study utilized independent component analysis to explore the abnormal functional connectivity (FC) in male participants with Internet gaming disorder (IGD). Functional magnetic resonance imaging and behavioral data were collected from 21 healthy controls (HC) and 18 IGD patients when they were performing a delay discounting task. Behavioral results revealed that the IGD patients showed higher delay discounting rates than HC. Two networks were found to be associated with IGD: (1) the executive control network containing the anterior cingulate cortex and the medial and superior frontal gyrus, and (2) the basal ganglia network containing the lentiform nucleus. Comparing to HC, IGD exhibited stronger FC when selecting small and now options. In addition, the delay discounting rates were positively correlated with the modulation of the two networks and the reaction time. The results suggested that the IGD patients have enhanced sensitivity to reward and decreased ability to control their impulsivity effectively, which leads to myopic decision making.

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References

  1. Ainslie G (1975) Specious reward: a behavioral theory of impulsiveness and impulse control. Psychol Bull 82(4):463

    Article  CAS  PubMed  Google Scholar 

  2. AmericanPsychiatricAssociation (2013) Diagnostic and statistical manual of mental disorders (DSM-5®). American Psychiatric Pub, Washington DC

  3. Ayas T, Horzum M (2013) Relation between depression, loneliness, self-esteem and internet addiction. Education 133(3):283–290

    Google Scholar 

  4. Beckmann CF, DeLuca M, Devlin JT, Smith SM (2005) Investigations into resting-state connectivity using independent component analysis. Philos Trans R Soc Lond B Biol Sci 360(1457):1001–1013

    Article  PubMed  PubMed Central  Google Scholar 

  5. Belin D, Jonkman S, Dickinson A, Robbins TW, Everitt BJ (2009) Parallel and interactive learning processes within the basal ganglia: relevance for the understanding of addiction. Behav Brain Res 199(1):89–102

    Article  PubMed  Google Scholar 

  6. Bernardi S, Pallanti S (2009) Internet addiction: a descriptive clinical study focusing on comorbidities and dissociative symptoms. Compr Psychiatry 50(6):510–516. doi:10.1016/j.comppsych.2008.11.011

    Article  PubMed  Google Scholar 

  7. Bickel WK, Marsch LA (2001) Toward a behavioral economic understanding of drug dependence: delay discounting processes. Addiction 96(1):73–86

    Article  CAS  PubMed  Google Scholar 

  8. Brand M, Fujiwara E, Borsutzky S, Kalbe E, Kessler J, Markowitsch HJ (2005) Decision-making deficits of korsakoff patients in a new gambling task with explicit rules: associations with executive functions. Neuropsychology 19(3):267–277

    Article  PubMed  Google Scholar 

  9. Calhoun V, Adali T, Hansen LK, Larsen J, Pekar JJ (2003) ICA of functional MRI data: an overview. In: Fourth international symposium on independent component analysis and blind source separation, Nara, Japan

  10. Calhoun V, Adali T, Pearlson G, Pekar J (2001) A method for making group inferences from functional MRI data using independent component analysis. Hum Brain Mapp 14(3):140–151

    Article  CAS  PubMed  Google Scholar 

  11. Calhoun V, Adali T, Pearlson G, Pekar J (2001) Spatial and temporal independent component analysis of functional MRI data containing a pair of task-related waveforms. Hum Brain Mapp 13(1):43–53

    Article  CAS  PubMed  Google Scholar 

  12. Calhoun V, Pekar JJ, McGinty VB, Adali T, Watson TD, Pearlson GD (2002) Different activation dynamics in multiple neural systems during simulated driving. Hum Brain Mapp 16(3):158–167

    Article  PubMed  Google Scholar 

  13. Charlton JP, Danforth ID (2007) Distinguishing addiction and high engagement in the context of online game playing. Comput Hum Behav 23(3):1531–1548

    Article  Google Scholar 

  14. Desmurget M, Grafton S, Vindras P, Grea H, Turner RS (2004) The basal ganglia network mediates the planning of movement amplitude. Eur J Neurosci 19(10):2871–2880

    Article  CAS  PubMed  Google Scholar 

  15. Ding W, Sun J, Sun Y, Chen X, Zhou Y, Zhuang Z, Du Y-S (2014) Trait impulsivity and impaired prefrontal impulse inhibition function in adolescents with internet gaming addiction revealed by a Go/No-Go fMRI study. Behav Brain Funct 10(1):1–9

    Article  CAS  Google Scholar 

  16. Dixon MR, Marley J, Jacobs EA (2003) Delay discounting by pathological gamblers. J Appl Behav Anal 36(4):449–458

    Article  PubMed  PubMed Central  Google Scholar 

  17. Dong G, DeVito EE, Du X, Cui Z (2012) Impaired inhibitory control in ‘internet addiction disorder’: a functional magnetic resonance imaging study. Psychiatry Res Neuroimaging 203(2):153–158

    Article  PubMed  Google Scholar 

  18. Dong G, Huang J, Du X (2011) Enhanced reward sensitivity and decreased loss sensitivity in Internet addicts: an fMRI study during a guessing task. J Psychiatr Res 45(11):1525–1529

    Article  PubMed  Google Scholar 

  19. Dong G, Lin X, Hu Y, Xie C, Du X (2015) Imbalanced functional link between executive control network and reward network explain the online-game seeking behaviors in Internet gaming disorder. Sci Rep 5(5 Suppl 2):1238–1242

    Google Scholar 

  20. Dong G, Lin X, Potenza MN (2015) Decreased functional connectivity in an executive control network is related to impaired executive function in Internet gaming disorder. Prog Neuropsychopharmacol Biol Psychiatry 57:76–85

    Article  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  22. Dong G, Zhou H, Zhao X (2011) Male Internet addicts show impaired executive control ability: evidence from a color-word Stroop task. Neurosci Lett 499(2):114–118

    Article  CAS  PubMed  Google Scholar 

  23. Duncan J (2010) The multiple-demand (MD) system of the primate brain: mental programs for intelligent behaviour. Trends Cogn Sci 14(4):172–179

    Article  PubMed  Google Scholar 

  24. Duncan J (2013) The structure of cognition: attentional episodes in mind and brain. Neuron 80(1):35–50

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  PubMed  Google Scholar 

  26. Everitt BJ, Dickinson A, Robbins TW (2001) The neuropsychological basis of addictive behaviour. Brain Res Rev 36(2):129–138

    Article  CAS  PubMed  Google Scholar 

  27. Field M, Santarcangelo M, Sumnall H, Goudie A, Cole J (2006) Delay discounting and the behavioural economics of cigarette purchases in smokers: the effects of nicotine deprivation. Psychopharmacology 186(2):255–263

    Article  CAS  PubMed  Google Scholar 

  28. Frangos CC, Frangos CC, Sotiropoulos I (2012) A meta-analysis of the reliability of Young’s Internet addiction test. In: Paper presented at the World Congress on Engineering

  29. Fu K-W, Chan WS, Wong PW, Yip PS (2010) Internet addiction: prevalence, discriminant validity and correlates among adolescents in Hong Kong. Br J Psychiatry 196(6):486–492

    Article  PubMed  Google Scholar 

  30. Goudriaan AE, Oosterlaan J, De Beurs E, Van Den Brink W (2006) Neurocognitive functions in pathological gambling: a comparison with alcohol dependence. Tourette syndrome and normal controls. Addiction 101(4):534–547

    PubMed  Google Scholar 

  31. Greicius MD, Flores BH, Menon V, Glover GH, Solvason HB, Kenna H, Schatzberg AF (2007) Resting-state functional connectivity in major depression: abnormally increased contributions from subgenual cingulate cortex and thalamus. Biol Psychiatry 62(5):429–437

    Article  PubMed  PubMed Central  Google Scholar 

  32. Greicius MD, Supekar K, Menon V, Dougherty RF (2009) Resting-state functional connectivity reflects structural connectivity in the default mode network. Cereb Cortex 19(1):72–78

    Article  PubMed  Google Scholar 

  33. Heil SH, Johnson MW, Higgins ST, Bickel WK (2006) Delay discounting in currently using and currently abstinent cocaine-dependent outpatients and non-drug-using matched controls. Addict Behav 31(7):1290–1294

    Article  PubMed  Google Scholar 

  34. Hester R, Lubman DI, Yücel M (2010) The role of executive control in human drug addiction. Behav Neurosci Drug Addict 3:301–318

    Article  Google Scholar 

  35. Hoffman WF, Moore M, Templin R, McFarland B, Hitzemann RJ, Mitchell SH (2006) Neuropsychological function and delay discounting in methamphetamine-dependent individuals. Psychopharmacology 188(2):162–170

    Article  CAS  PubMed  Google Scholar 

  36. Jafri MJ, Pearlson GD, Stevens M, Calhoun VD (2008) A method for functional network connectivity among spatially independent resting-state components in schizophrenia. Neuroimage 39(4):1666–1681

    Article  PubMed  Google Scholar 

  37. Kim DI, Manoach DS, Mathalon DH, Turner JA, Mannell M, Brown GG, Wible C (2009) Dysregulation of working memory and default-mode networks in schizophrenia using independent component analysis, an fBIRN and MCIC study. Hum Brain Mapp 30(11):3795–3811

    Article  PubMed  PubMed Central  Google Scholar 

  38. Király O, Nagygyörgy K, Griffiths M, Demetrovics Z (2014) Problematic online gaming. Behav Addict 61–97

  39. Kirby KN, Petry NM, Bickel WK (1999) Heroin addicts have higher discount rates for delayed rewards than non-drug-using controls. J Exp Psychol Gen 128(1):78–87

    Article  CAS  PubMed  Google Scholar 

  40. Ko CH, Liu G-C, Yen J-Y, Yen C-F, Chen C-S, Lin W-C (2013) The brain activations for both cue-induced gaming urge and smoking craving among subjects comorbid with Internet gaming addiction and nicotine dependence. J Psychiatr Res 47(4):486–493

    Article  PubMed  Google Scholar 

  41. Ko C-H, Yen J-Y, Chen C-C, Chen S-H, Yen C-F (2005) Gender differences and related factors affecting online gaming addiction among Taiwanese adolescents. J Nerv Ment Dis 193(4):273–277

    Article  PubMed  Google Scholar 

  42. Koldovsky Z, Tichavsky P, Oja E (2006) Efficient Variant of Algorithm FastICA for Independent Component Analysis Attaining the CramÉ r-Rao Lower Bound. IEEE Trans Neural Netw 17(5):1265–1277

    Article  PubMed  Google Scholar 

  43. Krmpotich TD, Tregellas JR, Thompson LL, Banich MT, Klenk AM, Tanabe JL (2013) Resting-state activity in the left executive control network is associated with behavioral approach and is increased in substance dependence. Drug Alcohol Depend 129(1):1–7

    Article  PubMed  PubMed Central  Google Scholar 

  44. Ledgerwood DM, Orr ES, Kaploun KA, Milosevic A, Frisch GR, Rupcich N, Lundahl LH (2012) Executive function in pathological gamblers and healthy controls. J Gambl Stud 28(1):89–103

    Article  PubMed  Google Scholar 

  45. Leibovici D, Beckmann C (2001) An introduction to multiway methods for multi-subject fMRI. FMRIB Technical Report

  46. Lemmens JS, Valkenburg PM, Peter J (2009) Development and validation of a game addiction scale for adolescents. Media Psychol 12(1):77–95

    Article  Google Scholar 

  47. Lin X, Dong G, Wang Q, Du X (2014) Abnormal gray matter and white matter volume in ‘Internet gaming addicts’. Addict Behav 40:137–143. doi:10.1016/j.addbeh.2014.09.010

    Article  PubMed  Google Scholar 

  48. Liu J, Gao X, Osunde I, Li X, Zhou S, Zheng H, Li L (2010) Increased regional homogeneity in internet addiction disorder a resting state functional magnetic resonance imaging study (2009). Chin Med J (Engl) 123(14):1904–1908

    Google Scholar 

  49. Madden GJ, Petry NM, Badger GJ, Bickel WK (1997) Impulsive and self-control choices in opioid-dependent patients and non-drug-using control patients: drug and monetary rewards. Exp Clin Psychopharmacol 5(3):256–262

    Article  CAS  PubMed  Google Scholar 

  50. Mazur JE (1987) An adjusting procedure for studying delayed reinforcement. In: Commons ML, Mazur JE, Nevin JA, Rachlin H (eds) Quantitative analyses of behavior: the effect of delay and of intervening events on reinforcement value, vol 5. Psychology Press, New York, London, pp 55–73

  51. McKeown MJ, Hansen LK, Sejnowsk TJ (2003) Independent component analysis of functional MRI: what is signal and what is noise? Curr Opin Neurobiol 13(5):620–629

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  52. McKeown MJ, Makeig S, Brown GG, Jung T-P, Kindermann SS, Bell AJ, Sejnowski TJ (1998) Analysis of fMRI data by blind separation into independent spatial components. Hum Brain Mapp 6(3):160–188

    Article  CAS  PubMed  Google Scholar 

  53. Meade CS, Lowen SB, MacLean RR, Key MD, Lukas SE (2011) fMRI brain activation during a delay discounting task in HIV-positive adults with and without cocaine dependence. Psychiatry Res Neuroimaging 192(3):167–175

    Article  PubMed  Google Scholar 

  54. Meng Y-J, Deng W, Wang H-Y, Guo W-J, Li T, Lam C, Lin X (2014) Reward pathway dysfunction in gambling disorder: a meta-analysis of functional magnetic resonance imaging studies. Behav Brain Res 275:243–251

    Article  PubMed  Google Scholar 

  55. Miedl SF, Peters J, Büchel C (2012) Altered neural reward representations in pathological gamblers revealed by delay and probability discounting. Arch Gen Psychiatry 69(2):177–186

    Article  PubMed  Google Scholar 

  56. Mitchell JM, Fields HL, D’Esposito M, Boettiger CA (2005) Impulsive responding in alcoholics. Alcohol Clin Exp Res 29(12):2158–2169

    Article  PubMed  Google Scholar 

  57. Miyake A, Friedman NP, Emerson MJ, Witzki AH, Howerter A, Wager TD (2000) The unity and diversity of executive functions and their contributions to complex “frontal lobe” tasks: a latent variable analysis. Cogn Psychol 41(1):49–100

    Article  CAS  PubMed  Google Scholar 

  58. Moussa MN, Steen MR, Laurienti PJ, Hayasaka S (2012) Consistency of network modules in resting-state FMRI connectome data. PLoS One 7(8):e44428

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  59. Nestler EJ (2005) Is there a common molecular pathway for addiction? Nat Neurosci 8(11):1445–1449

    Article  CAS  PubMed  Google Scholar 

  60. Petry NM, O’Brien CP (2013) Internet gaming disorder and the DSM-5. Addiction 108(7):1186–1187

    Article  PubMed  Google Scholar 

  61. Potenza MN, Leung H-C, Blumberg HP, Peterson BS, Fulbright RK, Lacadie CM, Gore JC (2014) An FMRI Stroop task study of ventromedial prefrontal cortical function in pathological gamblers. Am J Psychiatry 160(11):1990–1994

    Article  Google Scholar 

  62. Power Y, Goodyear B, Crockford D (2012) Neural correlates of pathological gamblers preference for immediate rewards during the Iowa Gambling Task: an fMRI study. J Gambl Stud 28(4):623–636

    Article  PubMed  Google Scholar 

  63. Rachlin H, Raineri A, Cross D (1991) Subjective probability and delay. J Exp Anal Behav 55(2):233–244

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  64. Reynolds B, Richards JB, Horn K, Karraker K (2004) Delay discounting and probability discounting as related to cigarette smoking status in adults. Behav Process 65(1):35–42

    Article  Google Scholar 

  65. Rui N, Yasuyuki T, Hikaru T, Hiroshi H, Takayuki N, Toshimune K, Haruka N (2013) Brain training game boosts executive functions, working memory and processing speed in the young adults: a randomized controlled trial. PLoS One 8(2):e55518

    Article  Google Scholar 

  66. Rui N, Yasuyuki T, Hikaru T, Hiroshi H, Yuko A, Yayoi S, Yukihito Y (2012) Brain training game improves executive functions and processing speed in the elderly: a randomized controlled trial. PLoS One 7(1):e29676

    Article  Google Scholar 

  67. Saville BK, Gisbert A, Kopp J, Telesco C (2011) Internet addiction and delay discounting in college students. Psychol Rec 60(2):273–286

    Google Scholar 

  68. Schmidt A, Denier N, Magon S, Radue E, Huber C, Riecher-Rossler A, Walter M (2015) Increased functional connectivity in the resting-state basal ganglia network after acute heroin substitution. Transl Psychiatry 5(3):e533

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  69. Schultz W, Tremblay L, Hollerman JR (2000) Reward processing in primate orbitofrontal cortex and basal ganglia. Cereb Cortex 10(3):272–283

    Article  CAS  PubMed  Google Scholar 

  70. Seeley WW, Menon V, Schatzberg AF, Keller J, Glover GH, Kenna H, Greicius MD (2007) Dissociable intrinsic connectivity networks for salience processing and executive control. J Neurosci 27(9):2349–2356

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  71. Sesack SR, Grace AA (2010) Cortico-basal ganglia reward network: microcircuitry. Neuropsychopharmacology 35(1):27–47

    Article  PubMed  Google Scholar 

  72. Shaw M, Black DW (2008) Internet addiction. CNS Drugs 22(5):353–365

    Article  PubMed  Google Scholar 

  73. Shirer W, Ryali S, Rykhlevskaia E, Menon V, Greicius M (2012) Decoding subject-driven cognitive states with whole-brain connectivity patterns. Cereb Cortex 22(1):158–165

    Article  CAS  PubMed  Google Scholar 

  74. Smith EE, Jonides J (1999) Storage and executive processes in the frontal lobes. Science 283(5408):1657–1661

    Article  CAS  PubMed  Google Scholar 

  75. Sutherland MT, McHugh MJ, Pariyadath V, Stein EA (2012) Resting state functional connectivity in addiction: lessons learned and a road ahead. Neuroimage 62(4):2281–2295

    Article  PubMed  PubMed Central  Google Scholar 

  76. Widyanto L, Griffiths MD, Brunsden V (2011) A psychometric comparison of the Internet Addiction Test, the Internet-Related Problem Scale, and self-diagnosis. Cyberpsychol Behav Soc Netw 14(3):141–149

    Article  PubMed  Google Scholar 

  77. Wise RA (1998) Drug-activation of brain reward pathways. Drug Alcohol Depend 51(1):13–22

    Article  CAS  PubMed  Google Scholar 

  78. Wittmann M, Leland DS, Paulus MP (2007) Time and decision making: differential contribution of the posterior insular cortex and the striatum during a delay discounting task. Exp Brain Res 179(4):643–653

    Article  PubMed  Google Scholar 

  79. Yen J-Y, Ko C-H, Yen C-F, Wu H-Y, Yang M-J (2007) The comorbid psychiatric symptoms of Internet addiction: attention deficit and hyperactivity disorder (ADHD), depression, social phobia, and hostility. J Adolesc Health 41(1):93–98

    Article  PubMed  Google Scholar 

  80. Yin HH, Knowlton BJ (2006) The role of the basal ganglia in habit formation. Nat Rev Neurosci 7(6):464–476

    Article  CAS  PubMed  Google Scholar 

  81. Young KS (1998) Internet addiction: the emergence of a new clinical disorder. CyberPsychol Behav 1(3):237–244

    Article  Google Scholar 

  82. Young KS (2009) Internet Addiction Test (IAT). Center for Internet Addiction

  83. Young KS, Rogers RC (1998) The relationship between depression and internet addiction. CyberPsychol Behav 1(1):25–28

    Article  Google Scholar 

  84. Zhang J-T, Yao Y-W, Potenza MN, Xia C-C, Lan J, Liu L, Fang X-Y (2016) Altered resting-state neural activity and changes following a craving behavioral intervention for Internet gaming disorder. Sci Rep 6:28109

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  85. 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 

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Acknowledgments

This research was supported by National Science Foundation of China (31371023).

Funding

The funders had no further role in study design; in the data collection, analyses, and interpretation; the decision to publish, or preparation of the manuscript.

Author contribution

Yifan Wang analyzed the data and wrote the first draft of the manuscript. Hongli Zhou, Xiao Lin, and Yifen Zhang contributed to experimental programming and data preprocessing. Guangheng Dong designed the research. Guangheng Dong and Lingdan Wu revised and improved the manuscript. Xiaoxia Du contributed to fMRI data collection. All authors contributed to and have approved the final manuscript.

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Authors and Affiliations

  1. Department of Psychology, Zhejiang Normal University, 688 Yingbin Road, Jinhua, 321004, Zhejiang Province, People’s Republic of China

    Yifan Wang, Hongli Zhou, Yifen Zhang & Guangheng Dong

  2. Department of Psychology, University of Konstanz, Constance, Germany

    Lingdan Wu

  3. Peking-Tsinghua Center for Life Science, Peking University, Beijing, People’s Republic of China

    Xiao Lin

  4. Department of Physics, Shanghai Key Laboratory of Magnetic Resonance, East China Normal University, Shanghai, People’s Republic of China

    Xiaoxia Du

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  1. Yifan Wang
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  2. Lingdan Wu
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Correspondence to Guangheng Dong.

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Wang, Y., Wu, L., Zhou, H. et al. Impaired executive control and reward circuit in Internet gaming addicts under a delay discounting task: independent component analysis. Eur Arch Psychiatry Clin Neurosci 267, 245–255 (2017). https://doi.org/10.1007/s00406-016-0721-6

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  • DOI: https://doi.org/10.1007/s00406-016-0721-6

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