Decreased functional connectivity in an executive control network is related to impaired executive function in Internet gaming disorder

https://doi.org/10.1016/j.pnpbp.2014.10.012Get rights and content

Highlights

  • Lower FC in ECNs in IGD than in HC

  • Positive trends between FC in ECNs and brain activations in Stroop task

  • The FC in ECNs may represent an important feature in IGD.

Abstract

Background

Resting brain spontaneous neural activities across cortical regions have been correlated with specific functional properties in psychiatric groups. Individuals with Internet gaming disorder (IGD) demonstrate impaired executive control. Thus, it is important to examine executive control networks (ECNs) during resting states and their relationships to executive control during task performance.

Methods

Thirty-five IGD and 36 healthy control participants underwent a resting-state fMRI scan and performed a Stroop task inside and outside of the MRI scanner. Correlations between Stroop effect and functional connectivity among ECN regions of interest (ROIs) were calculated within and between groups.

Results

IGD subjects show lower functional connectivity in ECNs than do HC participants during resting state; functional-connectivity measures in ECNs were negatively correlated with Stroop effect and positively correlated with brain activations in executive-control regions across groups. Within groups, negative trends were found between Stroop effect and functional connectivity in ECNs in IGD and HC groups, separately; positive trends were found between functional connectivity in ECNs and brain activations in Stroop task in IGD and HC groups, separately.

Conclusions

Higher functional connectivity in ECNs may underlie better executive control and may provide resilience with respect to IGD. Lower functional connectivity in ECNs may represent an important feature in understanding and treating IGD.

Introduction

Internet addiction disorder (IAD) or problematic Internet use is defined as the excessive or uncontrolled use of the Internet with negative consequences to psychological, social, and/or work functioning aspects (Dong and Potenza, 2014, Young, 1998). It has been proposed as a diagnostic entity and studied for more than a decade; however, a standardized definition is only recently emerging, and this disorder was not included in the fourth edition of the Diagnostic and Statistical Manual (DSM) (Block, 2008, Liu et al., 2011, Shaw and Black, 2008). The DSM-5 committee considering substance-use disorders and addictions generated criteria for Internet gaming disorder (IGD, a subtype of IAD, refers to those who addicted to Internet online games), and this condition is included in the DSM's section 3, for disorders warranting additional study (American Psychiatric Association, 2013, Petry and O'Brien, 2013). People's online experience may change their cognitive function in a manner that may perpetuate Internet use, which may occur in the absence of drug-taking (Dong et al., 2011b, Holden, 2001, Weinstein and Lejoyeux, 2010), and individuals with certain brain and behavioral characteristics may have increased dispositions for developing IAD. However, the precise mechanisms underlying IAD are not well understood (Yau et al., 2012).

Internet addiction may consist of multiple subtypes; for example, subtypes relating to gaming, sexual preoccupations, and email/text messaging have been proposed (Block, 2008). In China, arguably the most important subtype of IAD may be IGD (Dong et al., 2011a, Dong et al., 2012, Dong et al., 2013c). One key feature of IGD is lost or diminished self-control over participation in Internet game-playing. Executive function enables individuals to inhibit their desires and limit engagement in hedonic behaviors under unfavorable circumstances (Dong et al., 2013a, Everitt et al., 2007, Goldstein and Volkow, 2011, Lin et al., 2014, Sofuoglu et al., 2013). Behavioral and/or brain differences between IGD and healthy controls have been observed during task performance on go/no-go (Dong et al., 2010), attention bias (Ko et al., 2013), set-shifting (Dong et al., 2014, Zhou et al., 2012), Stroop (Dong et al., 2011c), and error-processing (Dong et al., 2013c) tasks. Together, these data provide a neurobiological explanation for behavioral control difficulties that individuals with IGD often exhibit.

Although executive control tasks performed during imaging are important for observing effects of IGD within circumscribed brain areas (Dong et al., 2010, Dong et al., 2011c, Dong et al., 2014, Lin et al., 2015, Zhou et al., 2012), additional insight may be obtained by measuring alterations in interactions among brain regions (Chambers et al., 2003, Koob and Volkow, 2010, Soderpalm and Ericson, 2013). Neural activities in the human brain during rest, termed resting-state functional magnetic resonance imaging, have found that spontaneous neural activities are correlated across cortical regions in a non-random fashion (Fox and Raichle, 2007, Greicius et al., 2009, Zhu et al., 2011). These correlations may reflect functional connectivity (FC) among specific brain regions (Honey et al., 2009, Vincent et al., 2007). Studies on the functional connectivity in IAD subjects have already revealed some abnormal features. Hong et al., found a widespread and decrease of functional connectivity in the cortico-subcortical circuit (~ 24% with prefrontal and ~ 27% with parietal cortex) in 12 adolescents who were diagnosed with IAD (Hong et al., 2013); Li et al., found ineffective connectivity in the frontal–basal ganglia pathway in IAD adolescents, which was thought engaged in response inhibition (Li et al., 2014); Wee et al., found significant disruption in the functional connectome between regions located in the frontal, occipital, and parietal lobes in IAD subjects (Wee et al., 2014). Despite findings indicating FC across cortical regions, little is known about the psychological significance of these relationships, especially in clinical diagnoses like IGD.

In this study, we examine FC relationships in executive control networks (ECNs) during resting state and behavioral and neural measures of executive control (during Stroop performance) in 35 subjects with IGD and 36 healthy control (HC) subjects. The temporal binding model suggests that the synchronization of brain signals between neural systems is facilitates neural communications (Engel et al., 2001). Consistent with this model, resting brain activity can relate importantly to behavioral performance. For example, resting-state activity across face-selective cortical regions has been correlated with behavioral performance in a face performance task (Zhu et al., 2011). Individual differences in attitudes toward risk-taking have been related to the brain FC and may have implications for engaging in real-world risky behaviors (Cox et al., 2010). Thus, we hypothesized that executive control function might be indexed by resting-state brain activities in ECNs. To test this hypothesis, we examined correlations in spontaneous blood oxygen level dependence (BOLD) fluctuations among ECN brain regions during resting state and Stroop-related behavioral performance and brain activities.

Resting-state FC has been shown to differ between groups or as a function of clinically relevant measures. Performance deficits in cognitive control in drug-addicted individuals have been associated with reduced FC (Franken et al., 2010, Honey et al., 2009). Amygdala/medial–prefrontal–cortical connectivity at rest has been related to individual differences in anxiety (Kim et al., 2011). The aftermath of acute stress has been related to prolonged activation in an amygdala-related connectivity network (van Marle et al., 2010). Trauma victims (individuals exposed to earthquakes) show reduced temporal synchronization within the ‘default mode’ of resting-state brain function (Lui et al., 2009). Reduced FC between seeds within ECNs is consistent with behavioral and task-based imaging findings and self-reported cognitive deficits in drug-addicted populations (Ersche et al., 2006, Kelly et al., 2011). IGD subjects show impaired executive control ability relative to HC subjects (Dong et al., 2010, Dong et al., 2011c, Dong et al., 2013b, Ko et al., 2013, Zhou et al., 2012). Thus, we hypothesized that the impaired executive control in IGD would relate to decreased resting-state FC. To test this hypothesis, we examined between-group differences in FC in ECNs and examined whether FC related to brain activations and behavioral performance on the Stroop task.

Section snippets

Participant selection

The experiment conforms to The Code of Ethics of the World Medical Association (Declaration of Helsinki). The Human Investigations Committee of Zhejiang Normal University approved this research. Participants were university students and were recruited through advertisements. Participants were right-handed males (35 IGD and 36 HC subjects). IGD and HC groups did not significantly differ in age (IGD mean (SD) = 22.21 (3.08) years; HC mean (SD) = 22.81 (2.36) years; t = 0.69, p = 0.49). All subjects

FC differences in ECNs in IGD and HC subjects

FC was calculated among ECN ROIs in different networks (Fig. 1a). A two-way ANOVA of FC (Hemisphere, ECN ROIs) shows significant hemisphere effect (F(1,71) = 11.32, p < 0.01). This finding is consistent with previous data indicating that the ECN has separable right and left hemisphere components (Damoiseaux et al., 2006, Habas et al., 2009, Shirer et al., 2012). Thus, we separated the whole ECN into left (LECN) and right ECN (RECN). Additionally, we calculated the FC between left and right

Discussion

This study investigated whether synchronized spontaneous neural activity across ECNs is related to the cognitive control executive functioning and may relate to poor executive control in IGD. The results showed that the FC in different ECN ROIs are correlated with individuals' performance in a variety of ways, suggesting that synchronized spontaneous neural activities in ECN is behaviorally relevant.

Conclusions

In summary, the current study found that IGD subjects show lower functional connectivity in ECNs than do HC participants during resting state. In addition, positive trends were found between functional connectivity in ECNs and brain activations in Stroop task in IGD and HC groups, separately. All these may represent important features in understanding and treating IGD.

Role of the funding source

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

Contributors

Guangheng Dong designed the experiment and wrote the first draft of the manuscript. Xiao Lin collected and analyzed the data, prepared the figures. Marc Potenza discussed the results, advised on interpretation and contributed to the final draft of the manuscript. All authors contributed to and have approved the final manuscript.

Competing interests

The authors declared that no competing interests exist.

Acknowledgments

This research was supported by the National Science Foundation of China (31371023), National Institute of Health (R01 DA035058, P50 DA09241, P20 DA027844), the Connecticut Department of Mental Health and Addictive Services, and the National Center for Responsible Gaming.

Dr. Potenza has received financial support or compensation for the following: Dr. Potenza has consulted for and advised Lundbeck, Ironwood and Shire; has received research support from the National Institutes of Health, Mohegan

References (76)

  • I.H. Franken et al.

    Evidence for a deficit in the salience attribution to errors in smokers

    Drug Alcohol Depend

    (2010)
  • K.J. Friston et al.

    Characterizing dynamic brain responses with fMRI: a multivariate approach

    Neuroimage

    (1995)
  • I.I. Goldberg et al.

    When the brain loses its self: prefrontal inactivation during sensorimotor processing

    Neuron

    (2006)
  • C. Kelly et al.

    Reduced interhemispheric resting state functional connectivity in cocaine addiction

    Biol Psychiatry

    (2011)
  • D.L. King et al.

    The cognitive psychology of Internet gaming disorder

    Clin Psychol Rev

    (2014)
  • C.H. Ko et al.

    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

    (2013)
  • T.D. Krmpotich et al.

    Resting-state activity in the left executive control network is associated with behavioral approach and is increased in substance dependence

    Drug Alcohol Depend

    (2013)
  • Y. Lecrubier et al.

    The Mini International Neuropsychiatric Interview (MINI). A short diagnostic structured interview: reliability and validity according to the CIDI

    Eur Psychiatry

    (1997)
  • C.S. Li et al.

    Inhibitory control and emotional stress regulation: neuroimaging evidence for frontal-limbic dysfunction in psycho-stimulant addiction

    Neurosci Biobehav Rev

    (2008)
  • X. Lin et al.

    Impaired risk evaluation in people with Internet gaming disorder: fMRI evidence from a probability discounting task

    Prog Neuro-Psychopharmacol Biol Psychiatry

    (2015)
  • N. Ma et al.

    Addiction related alteration in resting-state brain connectivity

    Neuroimage

    (2010)
  • M. Sofuoglu et al.

    Cognitive enhancement as a treatment for drug addictions

    Neuropharmacology

    (2013)
  • R.N. Spreng et al.

    Default network activity, coupled with the frontoparietal control network, supports goal-directed cognition

    Neuroimage

    (2010)
  • M.T. Sutherland et al.

    Resting state functional connectivity in addiction: lessons learned and a road ahead

    Neuroimage

    (2012)
  • H.J. van Marle et al.

    Enhanced resting-state connectivity of amygdala in the immediate aftermath of acute psychological stress

    Neuroimage

    (2010)
  • H. You et al.

    Altered regional homogeneity in motor cortices in patients with multiple system atrophy

    Neurosci Lett

    (2011)
  • K. Yuan et al.

    Gray matter deficits and resting-state abnormalities in abstinent heroin-dependent individuals

    Neurosci Lett

    (2010)
  • Y. Zang et al.

    Regional homogeneity approach to fMRI data analysis

    Neuroimage

    (2004)
  • American Psychiatric Association

    Diagnostic and statistical manual of mental disorders

    (2013)
  • A.T. Beck et al.

    An inventory for measuring depression

    Arch Gen Psychiatry

    (1961)
  • J.J. Block

    Issues for DSM-V: internet addiction

    Am J Psychiatry

    (2008)
  • M. Brand et al.

    Prefrontal control and internet addiction: a theoretical model and review of neuropsychological and neuroimaging findings

    Front Hum Neurosci

    (2014)
  • R.A. Chambers et al.

    Developmental neurocircuitry of motivation in adolescence: a critical period of addiction vulnerability

    Am J Psychiatry

    (2003)
  • C.L. Cox et al.

    Your resting brain CAREs about your risky behavior

    PLoS ONE

    (2010)
  • J.S. Damoiseaux et al.

    Consistent resting-state networks across healthy subjects

    Proc Natl Acad Sci U S A

    (2006)
  • G. Dong et al.

    Precursor or sequelae: pathological disorders in people with Internet addiction disorder

    PLoS ONE

    (2011)
  • G. Dong et al.

    Alterations in regional homogeneity of resting-state brain activity in internet gaming addicts

    Behav Brain Funct

    (2012)
  • G. Dong et al.

    Impaired error-monitoring function in people with internet addiction disorder: an event-related FMRI study

    Eur Addict Res

    (2013)
  • Cited by (106)

    View all citing articles on Scopus
    View full text