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<journal-meta>
<journal-id journal-id-type="publisher-id">Front. Psychiatry</journal-id>
<journal-title>Frontiers in Psychiatry</journal-title>
<abbrev-journal-title abbrev-type="pubmed">Front. Psychiatry</abbrev-journal-title>
<issn pub-type="epub">1664-0640</issn>
<publisher>
<publisher-name>Frontiers Media S.A.</publisher-name>
</publisher>
</journal-meta>
<article-meta>
<article-id pub-id-type="doi">10.3389/fpsyt.2017.00285</article-id>
<article-categories>
<subj-group subj-group-type="heading">
<subject>Psychiatry</subject>
<subj-group>
<subject>Review</subject>
</subj-group>
</subj-group>
</article-categories>
<title-group>
<article-title>A Tripartite Neurocognitive Model of Internet Gaming Disorder</article-title>
</title-group>
<contrib-group>
<contrib contrib-type="author">
<name><surname>Wei</surname> <given-names>Lei</given-names></name>
<xref ref-type="aff" rid="aff1"><sup>1</sup></xref>
<uri xlink:href="http://frontiersin.org/people/u/491521"/>
</contrib>
<contrib contrib-type="author">
<name><surname>Zhang</surname> <given-names>Shuyue</given-names></name>
<xref ref-type="aff" rid="aff2"><sup>2</sup></xref>
</contrib>
<contrib contrib-type="author">
<name><surname>Turel</surname> <given-names>Ofir</given-names></name>
<xref ref-type="aff" rid="aff3"><sup>3</sup></xref>
<xref ref-type="aff" rid="aff4"><sup>4</sup></xref>
<uri xlink:href="http://frontiersin.org/people/u/181900"/>
</contrib>
<contrib contrib-type="author">
<name><surname>Bechara</surname> <given-names>Antoine</given-names></name>
<xref ref-type="aff" rid="aff4"><sup>4</sup></xref>
<uri xlink:href="http://frontiersin.org/people/u/8018"/>
</contrib>
<contrib contrib-type="author" corresp="yes">
<name><surname>He</surname> <given-names>Qinghua</given-names></name>
<xref ref-type="aff" rid="aff1"><sup>1</sup></xref>
<xref ref-type="aff" rid="aff4"><sup>4</sup></xref>
<xref ref-type="aff" rid="aff5"><sup>5</sup></xref>
<xref ref-type="aff" rid="aff6"><sup>6</sup></xref>
<xref ref-type="aff" rid="aff7"><sup>7</sup></xref>
<xref ref-type="corresp" rid="cor1">&#x0002A;</xref>
<uri xlink:href="http://frontiersin.org/people/u/184645"/>
</contrib>
</contrib-group>
<aff id="aff1"><sup>1</sup><institution>Faculty of Psychology, Southwest University</institution>, <addr-line>Chongqing</addr-line>, <country>China</country></aff>
<aff id="aff2"><sup>2</sup><institution>Department of Psychology, Guangxi University</institution>, <addr-line>Guangxi</addr-line>, <country>China</country></aff>
<aff id="aff3"><sup>3</sup><institution>College of Business and Economics, California State University, Fullerton</institution>, <addr-line>Fullerton, CA</addr-line>, <country>United States</country></aff>
<aff id="aff4"><sup>4</sup><institution>Department of Psychology, University of Southern California</institution>, <addr-line>Los Angeles, CA</addr-line>, <country>United States</country></aff>
<aff id="aff5"><sup>5</sup><institution>Key Laboratory of Mental Health, Institute of Psychology, Chinese Academy of Sciences</institution>, <addr-line>Beijing</addr-line>, <country>China</country></aff>
<aff id="aff6"><sup>6</sup><institution>Southwest University Branch, Collaborative Innovation Center of Assessment toward Basic Education Quality at Beijing Normal University</institution>, <addr-line>Chongqing</addr-line>, <country>China</country></aff>
<aff id="aff7"><sup>7</sup><institution>Chongqing Collaborative Innovation Center for Brain Science</institution>, <addr-line>Chongqing</addr-line>, <country>China</country></aff>
<author-notes>
<fn fn-type="edited-by"><p>Edited by: Jintao Zhang, Beijing Normal University, China</p></fn>
<fn fn-type="edited-by"><p>Reviewed by: Gilly Koritzky, Argosy University, United States; Valentin Flaudias, Centre hospitalier universitaire de Clermont-Ferrand, France</p></fn>
<corresp content-type="corresp" id="cor1">&#x0002A;Correspondence: Qinghua He, <email>heqinghua&#x00040;gmail.com</email></corresp>
<fn fn-type="other" id="fn001"><p>Specialty section: This article was submitted to Psychopathology, a section of the journal Frontiers in Psychiatry</p></fn>
</author-notes>
<pub-date pub-type="epub">
<day>14</day>
<month>12</month>
<year>2017</year>
</pub-date>
<pub-date pub-type="collection">
<year>2017</year>
</pub-date>
<volume>8</volume>
<elocation-id>285</elocation-id>
<history>
<date date-type="received">
<day>28</day>
<month>08</month>
<year>2017</year>
</date>
<date date-type="accepted">
<day>01</day>
<month>12</month>
<year>2017</year>
</date>
</history>
<permissions>
<copyright-statement>Copyright &#x000A9; 2017 Wei, Zhang, Turel, Bechara and He.</copyright-statement>
<copyright-year>2017</copyright-year>
<copyright-holder>Wei, Zhang, Turel, Bechara and He</copyright-holder>
<license xlink:href="http://creativecommons.org/licenses/by/4.0/"><p>This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) or licensor are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.</p></license>
</permissions>
<abstract>
<p>Playing Internet games has emerged as a growing in prevalence leisure activity. In some cases, excess gaming can lead to addiction-like symptoms and aversive outcomes that may be seen by some as manifestations of a behavioral addiction. Even though agreement regarding the pathologizing of excessive video gaming is not yet achieved and perhaps because the field requires more research, many works have examined the antecedents and outcomes of what is termed internet gaming disorder (IGD). In this article, we aim at summarizing perspectives and findings related to the neurocognitive processes that may underlie IGD and map such findings onto the triadic-system that governs behavior and decision-making, the deficits in which have been shown to be associated with many addictive disorders. This tripartite system model includes the following three brain systems: (1) the impulsive system, which often mediates fast, automatic, unconscious, and habitual behaviors; (2) the reflective system, which mediates deliberating, planning, predicting future outcomes of selected behaviors, and exerting inhibitory control; and (3) the interoceptive awareness system, which generates a state of craving through the translation of somatic signals into a subjective state of drive. We suggest that IGD formation and maintenance can be associated with (1) a hyperactive &#x0201C;impulsive&#x0201D; system; (2) a hypoactive &#x0201C;reflective&#x0201D; system, as exacerbated by (3) an interoceptive awareness system that potentiates the activity of the impulsive system, and/or hijacks the goal-driven cognitive resources needed for the normal operation of the reflective system. Based on this review, we propose ways to improve the therapy and treatment of IGD and reduce the risk of relapse among recovering IGD populations.</p>
</abstract>
<kwd-group>
<kwd>Internet gaming disorder</kwd>
<kwd>insula</kwd>
<kwd>decision-making</kwd>
<kwd>fMRI</kwd>
<kwd>striatum</kwd>
</kwd-group>
<contract-num rid="cn01">31400959</contract-num>
<contract-sponsor id="cn01">National Natural Science Foundation of China<named-content content-type="fundref-id">10.13039/501100001809</named-content></contract-sponsor>
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</front>
<body>
<sec id="S1" sec-type="introduction">
<title>Introduction</title>
<p>The Internet offers a large variety of video games, including First Person or Ego-Shooters (FPS), Massively Multiplayer Online Role Playing Games (MMORPG), Multiplayer Online Battle Arena (MOBA) games, and hybrid forms of online games, such as Overwatch, which include the elements of both MOBA and FPS. MMORPG is the most popular game type among young adults and has been the focus of many IGD studies (<xref ref-type="bibr" rid="B1">1</xref>). Regardless of the nature and type of the game, videogames are possibly addictive since they provide strong rewards that are difficult to resist, and which are largely encouraged by videogame developers in order to ensure that gamers keep on using their games (<xref ref-type="bibr" rid="B2">2</xref>). For example, they serve various functional needs of users, such as need for escapism, socialization achievement, and mastery, and are hence appealing to many young adults (<xref ref-type="bibr" rid="B3">3</xref>).</p>
<p>Research has shown that given such psychological benefits that stem from the needs served by videogames and the inability of some people to regulate their reward seeking behaviors, some players can present addiction-like symptoms in relation to videogames and that these symptoms can produce a range of aversive effects, on children (<xref ref-type="bibr" rid="B2">2</xref>, <xref ref-type="bibr" rid="B4">4</xref>), young-adults (<xref ref-type="bibr" rid="B5">5</xref>, <xref ref-type="bibr" rid="B6">6</xref>), and organizational employees (<xref ref-type="bibr" rid="B7">7</xref>&#x02013;<xref ref-type="bibr" rid="B9">9</xref>). The concept of internet gaming disorder (IGD) has been suggested as a way to encapsulate such phenomenology and symptoms. IGD is a behavioral addiction on the spectrum of Internet addiction. It can be defined as persistent and recurrent use of the Internet to engage in games, often with other players, leading to clinically significant impairment or distress in a 12-month period (<xref ref-type="bibr" rid="B10">10</xref>, <xref ref-type="bibr" rid="B11">11</xref>). Many studies have used adaptations or derivatives of this definition, though there is still a great deal of confusion regarding the boundaries of IGD and its measurement (<xref ref-type="bibr" rid="B12">12</xref>). The multiplicity of conceptualizations and measures may contribute to the different prevalence rates estimated in different studies; ranging from 0.1% to over 50% (<xref ref-type="bibr" rid="B13">13</xref>).</p>
<p>In 2013, the newly updated version of the Diagnosis and Statistical Manual for Mental Disorders (DSM-5) included IGD in its appendix and suggested nine criteria for characterizing this disorder (<xref ref-type="bibr" rid="B10">10</xref>, <xref ref-type="bibr" rid="B11">11</xref>). These criteria are:
<list list-type="bullet">
<list-item><p>preoccupation with Internet games</p></list-item>
<list-item><p>withdrawal symptoms of irritability, anxiety, or sadness</p></list-item>
<list-item><p>development of tolerance</p></list-item>
<list-item><p>unsuccessful attempts to control the behavior</p></list-item>
<list-item><p>loss of interest in other activities</p></list-item>
<list-item><p>continued excessive use despite knowledge of psychosocial problems</p></list-item>
<list-item><p>deceiving others regarding the amount of time spent gaming</p></list-item>
<list-item><p>use of this behavior to escape or relieve a negative mood</p></list-item>
<list-item><p>jeopardizing/losing a significant relationship/job/educational opportunity.</p></list-item>
</list></p>
<p>These criteria have been traditionally associated with substance-related addiction (<xref ref-type="bibr" rid="B14">14</xref>). Subjects should respond with yes/no to questions like &#x0201C;Do you spend a lot of time thinking about games even when you are not playing, or planning when you can play next?&#x0201D;; there is a proposed cut-off point of five criteria in DSM-5 (<xref ref-type="bibr" rid="B15">15</xref>). Nevertheless, proposing such criteria and cutoffs have raised a multitude of concerns regarding their ambiguity, reliance on addiction models from other domains, and reliance on prior research, which in many cases used non-clinical samples (<xref ref-type="bibr" rid="B12">12</xref>). Hence, many conclude that moving forward we need to conduct more research on IGD and/or better synthesize prior studies (<xref ref-type="bibr" rid="B16">16</xref>). Here, we venture to provide a synthesis of prior research on IGD, using a very specific angle, a neuro-cognitive one.</p>
<p>On the basis of recent neuro-cognitive models of addiction (<xref ref-type="bibr" rid="B17">17</xref>&#x02013;<xref ref-type="bibr" rid="B20">20</xref>), and possible similarities between IGD and other addictions (<xref ref-type="bibr" rid="B13">13</xref>, <xref ref-type="bibr" rid="B21">21</xref>&#x02013;<xref ref-type="bibr" rid="B24">24</xref>), we suggest that the neural substrates involved in IGD development and maintenance can include the key brain systems that govern behavior and decision-making. Deficits in such systems have been shown to be associated with a broad range of addictions, including behavioral ones (<xref ref-type="bibr" rid="B17">17</xref>). Adapting this view, we contend that IGD may be associated with an imbalance between several inter-connected neural systems: (1) an hyperactive &#x0201C;impulsive&#x0201D; system, which is fast, automatic, and unconscious; it promotes automatic and habitual actions; (2) a hypoactive &#x0201C;reflective&#x0201D; system, which is slow and deliberative, forecasts the future consequences of a behavior and exerts inhibitory control; and (3) the interoceptive awareness system, which translates bottom-up somatic signals into a subjective state of craving, which in turn potentiates the activity of the impulsive system, and/or hijacks the goal-driven cognitive resources needed for the normal operation of the reflective system (<xref ref-type="bibr" rid="B17">17</xref>). In this article, we describe the connection between these three neural systems and IGD and evidence that supports this tripartite model. We use this description for pointing to potential interventions and directions for future studies.</p>
</sec>
<sec id="S2">
<title>Addictive Properties of Internet Gaming</title>
<p>Addiction forms through a sensitization process (<xref ref-type="bibr" rid="B25">25</xref>) that changes behaviors from impulsive to compulsive. Similar to other addictive disorders that focus on behaviors (e.g., gambling), IGD cases develop an addictive state without substance intake. This can happen given the rewarding and immersive properties of videogames (<xref ref-type="bibr" rid="B26">26</xref>, <xref ref-type="bibr" rid="B27">27</xref>) as well as their ability to address a broad spectrum of human functional needs (<xref ref-type="bibr" rid="B3">3</xref>). These include: relationship building, escapism, need for achievement, and mastering the game mechanics. Such motivations increase playtime and desire to play more (<xref ref-type="bibr" rid="B3">3</xref>), which in turn sensitizes the brain reward system (<xref ref-type="bibr" rid="B28">28</xref>, <xref ref-type="bibr" rid="B29">29</xref>) and can lead to addiction symptoms in vulnerable populations (<xref ref-type="bibr" rid="B30">30</xref>).</p>
<p>Not all gamers will present addiction-like symptoms and meet IGD criteria, even if they play for extended periods of time (<xref ref-type="bibr" rid="B1">1</xref>). Research has indicates that personality traits such as avoidant traits, schizoid personality, diminished self-control, narcissism, and low self-esteem are significantly related to IGD (<xref ref-type="bibr" rid="B31">31</xref>). Hence, people with such traits may be more prone than others to present IGD. In addition, social-environmental factors such as pressure from school (<xref ref-type="bibr" rid="B32">32</xref>), which tends to be high especially in East Asia, may propel a higher prevalence rate of IGD cases in Asian countries (<xref ref-type="bibr" rid="B33">33</xref>, <xref ref-type="bibr" rid="B34">34</xref>). Males seem to present higher IGD rates compared to women (<xref ref-type="bibr" rid="B35">35</xref>); and this changes when the focus is not just on games, but more broadly on Internet use (<xref ref-type="bibr" rid="B36">36</xref>). In the absence of prevention and harm reduction strategies that parents and educators can follow, young adults are more prone than others to lose control over online gaming (<xref ref-type="bibr" rid="B3">3</xref>).</p>
<p>Here, without discounting the importance of the many addictive features of video games, we emphasize two largely overlooked properties that many videogames have and can drive addictive behavior, if a person has deficits in the brain systems that govern decision-making:
<list list-type="simple">
<list-item><label>(1)</label> <p>Providing a freedom space for players</p>
<p>A virtual environment means that gamers can fulfill their desires that could not be met in real life and be, at least temporarily, other people with better qualities [see, for example, the notion of False Online Self in Ref. (<xref ref-type="bibr" rid="B37">37</xref>)]. These attributes can be highly rewarding, and present a possible reason for why game players persist in online gaming despite aversive outcomes (<xref ref-type="bibr" rid="B38">38</xref>). For instance, during such games, the role acted by a player could easily destroy and damage others in the virtual world and have a strong dominant personality, which may differ from the true-self of the gamer. The game space can be appealing also because it allows levels of violence that are often not afforded in real world. Many Internet games contain elements of violence; this feature may enhance interest in games and make them more rewarding, especially for young adults (<xref ref-type="bibr" rid="B39">39</xref>).</p>
<p>In addition to violence features, Internet games also provide an environment to fulfill gamers&#x02019; desire to build an association, challenge one&#x02019;s abilities, and command others (<xref ref-type="bibr" rid="B40">40</xref>, <xref ref-type="bibr" rid="B41">41</xref>). In other words, the virtual world provides a place to escape stress from real life and one&#x02019;s emotional state can be improved by playing online (<xref ref-type="bibr" rid="B3">3</xref>). Moreover, many Internet games allow players to pay in order to enhance the ability of the avatar representing them [in-game purchases, see, for example, Ref. (<xref ref-type="bibr" rid="B42">42</xref>)]. This process allows fast and easy enhancement compared to real-life attempts to enhance one&#x02019;s image and persona (<xref ref-type="bibr" rid="B41">41</xref>). Thus, vulnerable individuals can get sucked into the virtual world and avoid the real world (<xref ref-type="bibr" rid="B43">43</xref>). In sum, the virtual world includes many elements that help game players fulfill voids in their real life and provide enjoyable shortcuts for achieving aspirations in a simulation world. This process brings is psychologically rewarding, sometimes more than real life. It can hence motivate consumptions that over time may translate into compulsion.</p></list-item>
<list-item><label>(2)</label> <p>Anonymity</p>
<p>Anonymity has traditionally been conceived as the inability of others to identify an individual (<xref ref-type="bibr" rid="B44">44</xref>). Anonymity is common in many video games in which users use pseudonyms to describe themselves. This gives Internet game players a sense of security (false or not), which makes the virtual environment very appealing. In such environments, people can present abnormal behaviors and be free of direct judgment; for example, vulnerable individuals can show antisocial behaviors in online games (<xref ref-type="bibr" rid="B45">45</xref>). These antisocial behaviors may be linked to a loss of inhibition control (<xref ref-type="bibr" rid="B46">46</xref>). As such, the perceived-to-be safe environment afforded by anonymity features allows addicted users to engage in antisocial behaviors, which are aligned with their deficits in self-control abilities. When one&#x02019;s true identity is not revealed, anti-social gamers do not need to take responsibility for their in-game behavior, and suspend their enjoyment in the virtual environment (<xref ref-type="bibr" rid="B47">47</xref>). This reduced need for self-inhibition is also very appealing, can generate strong psychological rewards, and ultimately, in vulnerable users, lead to transition from habitual gaming to compulsive gaming.</p></list-item>
</list></p>
</sec>
<sec id="S3">
<title>IGD and the Impulsive Brain System (System 1)</title>
<p>In the course of addiction, the sensitivity to cues related to the addictive substance or behavior is progressively increased, and responses become more automatic after continuous exposure to addiction stimuli (<xref ref-type="bibr" rid="B48">48</xref>). This process could easily shift goal-directed behaviors to compulsive behavior, in which the action becomes independent of the current value of the goal, and result with impulsive behavior (<xref ref-type="bibr" rid="B49">49</xref>). Previous research indicates that impulsivity is associated with increased novelty seeking and poor decision-making and can lead to negative consequence such as monetary losses or social failures; thus, it underlies the development and maintenance of state compulsivity (<xref ref-type="bibr" rid="B50">50</xref>).</p>
<p>Recent studies found that the striatal-cortical system is a central one for acting prematurely without foresight (<xref ref-type="bibr" rid="B51">51</xref>). This system includes the striatum (dopaminergic systems) and the amygdala, which are key structures that form the impulsive system, and mediate reward seeking and compulsion, through sensitization (<xref ref-type="bibr" rid="B17">17</xref>). Accordingly, the amygdala has been repeatedly reported to be involved in risk-taking behavior; lower density of gray matter in the amygdala has been found in many substance addiction cases (<xref ref-type="bibr" rid="B52">52</xref>, <xref ref-type="bibr" rid="B53">53</xref>) and may be perceived as indicative of making the amygdala-striatal system more efficient (<xref ref-type="bibr" rid="B28">28</xref>, <xref ref-type="bibr" rid="B29">29</xref>).</p>
<p>Research has also pointed to the role of the amygdala-striatal system in IGD development and maintenance. The structures of the impulsive system have changed during the transition from goal-directed to compulsive behaviors (<xref ref-type="bibr" rid="B54">54</xref>). For instance, excessive play of Internet games was associated with specific aspects of synaptic structure plasticity in both striatal regions. A positron emission tomography study found that, after prolonged Internet use, the level of dopamine D2 receptor and transporters availability in subdivisions of the striatum has been reduced compared with controls (<xref ref-type="bibr" rid="B55">55</xref>, <xref ref-type="bibr" rid="B56">56</xref>). Voxel-based morphometry research suggested that frequent Internet game playing is associated with higher volumes in the left striatal and right caudate compared with infrequent game players (<xref ref-type="bibr" rid="B57">57</xref>, <xref ref-type="bibr" rid="B58">58</xref>), but the bilateral amygdala had a lower gray matter density in IGD cases compared to controls (<xref ref-type="bibr" rid="B59">59</xref>). Moreover, through the repetition of online gaming experience and exposure to gaming-related information, players learn to associate gaming with reward, and progressively become hypersensitive to gaming-related cues (<xref ref-type="bibr" rid="B60">60</xref>). This process can establish linkage between gaming-related cues and positive mood, which can increase dopaminergic activity and dopamine levels (<xref ref-type="bibr" rid="B61">61</xref>).</p>
<p>Moreover, a person who presents IGD symptoms can become hypersensitive to gaming-related cues; that is, develop attentional bias toward game-related cues (<xref ref-type="bibr" rid="B62">62</xref>), which can manifest in issues such as time distortion (<xref ref-type="bibr" rid="B63">63</xref>). Human behavior is determined by two aspects of cognition, implicit cognition, which includes memory association and situational circumstance, and explicit cognition, which includes cognitions amenable to introspection and deliberate decision-making (<xref ref-type="bibr" rid="B64">64</xref>). According to the implicit association test, which is used to asses implicit associations, players with IGD have a positive motivational implicit response to screenshots of games (<xref ref-type="bibr" rid="B65">65</xref>), including in cases of first-person shooter and racing games (<xref ref-type="bibr" rid="B66">66</xref>). These findings indicate a strong association between implicit cognition and uncontrolled gaming behavior. Implicit cognition not only represents an automatic appetitive response to a specific substance but can also impact specific behaviors, such as playing online videogames. Because implicit cognitions play an important role in addictive behavior through the generation of automatic approach tendencies, and these cognitions are often mediated <italic>via</italic> the amygdala&#x02013;striatal system, the modulation of this system can be associated with addictive behaviors (<xref ref-type="bibr" rid="B67">67</xref>, <xref ref-type="bibr" rid="B68">68</xref>), including the presumed-to-be addictive and problematic use of technologies (<xref ref-type="bibr" rid="B6">6</xref>, <xref ref-type="bibr" rid="B20">20</xref>, <xref ref-type="bibr" rid="B28">28</xref>, <xref ref-type="bibr" rid="B29">29</xref>, <xref ref-type="bibr" rid="B69">69</xref>, <xref ref-type="bibr" rid="B70">70</xref>, <xref ref-type="bibr" rid="B71">71</xref>).</p>
<p>fMRI studies also point to differences between brain activity of the impulsive system of presumed IGD and non-IGD cases. Both arterial spin-labeling perfusion and functional magnetic resonance imaging found differences during resting state: IGD subjects showed significantly higher global cerebral blood flow in the left parahippocampal and amygdala (<xref ref-type="bibr" rid="B72">72</xref>) and revealed reduced functional connectivity with fronto-striatal circuits (<xref ref-type="bibr" rid="B73">73</xref>, <xref ref-type="bibr" rid="B74">74</xref>). Studies using the cue-reactivity paradigm indicated higher activation of the striatum among IGD subjects, compared to controls (<xref ref-type="bibr" rid="B26">26</xref>, <xref ref-type="bibr" rid="B75">75</xref>). They further suggested functional differences between dorsal and ventral striatal subdivisions. After presenting game-related stimuli and neutral stimuli, the left ventral striatum activity of IGD cases showed negative correlation with cue-induced craving, but dorsal striatal activation was positively associated with duration of IGD. Hence, the transition from ventral to dorsal striatal processing of addiction-related cues may occur among IGD individuals (<xref ref-type="bibr" rid="B76">76</xref>).</p>
<p>Overall, continuously playing online can build a strong association between reward and behavior schema, and this association is mainly mediated by the amygdala-striatal system (<xref ref-type="bibr" rid="B77">77</xref>); impairment of this system can be associated with addictions in general (<xref ref-type="bibr" rid="B17">17</xref>) and specifically IGD (<xref ref-type="bibr" rid="B26">26</xref>, <xref ref-type="bibr" rid="B27">27</xref>). The impairment of the impulsive system may be similar across addictions and problematic behaviors (<xref ref-type="bibr" rid="B78">78</xref>). Hence, it is not surprising to see structural, functional and connectivity abnormalities in this system in presumed-to-be IGD cases.</p>
</sec>
<sec id="S4">
<title>IGD and the Reflective Brain System (System 2)</title>
<p>The reflective system can be conceived as a controller of the motivation toward addiction related reward and the impulsive behavior that is produced by impulsive system. The reflective system forecasts the result of current behavior and allows more flexible pursuit of long-term goals. This system consists of two sets of neural systems: a &#x0201C;cool&#x0201D; system (elicited by relatively abstract, decontextualized problems, and refers to basic working memory operations, inhibition of prepotent impulsions, and mental set shifting) and a &#x0201C;hot&#x0201D; system (involved in triggering somatic states from memory, knowledge, cognition, and activates numerous affective/emotional (somatic) response that conflict with each other) (<xref ref-type="bibr" rid="B79">79</xref>).</p>
<p>Studies indicated that the cool executive functions are mainly dependent on the lateral inferior and dorsolateral prefrontal cortices, and the anterior cingulate cortex, and that they are involved in several kinds of psychological reaction, such as shifting between multiple tasks and the updating or maintaining of working memory (<xref ref-type="bibr" rid="B79">79</xref>). In contrast to the cool executive functions, the orbitofrontal cortex (OFC) and ventromedial prefrontal cortex (VMPFC) form the main structure of hot executive functions. These are involved in the interaction between affective/emotional responses and somatic states that produce overall positive or negative signals related to behavioral choices (<xref ref-type="bibr" rid="B79">79</xref>).</p>
<sec id="S4-1">
<title>IGD and Hot Executive Function</title>
<p>The disruption of hot executive function in addiction has been initially demonstrated in clinical research of patient populations with damage in frontal lobe regions. These studies showed that hot executive function disruption delineates similar result to those obtained in cases of impairment to the frontal cortex (<xref ref-type="bibr" rid="B80">80</xref>, <xref ref-type="bibr" rid="B81">81</xref>). The Iowa Gambling Task (IGT) has been typically applied in such addiction studies, to examine decision-making abilities under ambiguity (<xref ref-type="bibr" rid="B82">82</xref>). This paradigm was introduced as a tool to measure &#x0201C;risk-anticipation,&#x0201D; which involves probabilistic learning <italic>via</italic> monetary rewards and punishments (<xref ref-type="bibr" rid="B83">83</xref>). Results of IGT studies demonstrated a reduced decision-making ability compared to controls during the task; they also show that presumed IGD cases made more disadvantageous decisions and performed worse than healthy controls (<xref ref-type="bibr" rid="B40">40</xref>, <xref ref-type="bibr" rid="B84">84</xref>, <xref ref-type="bibr" rid="B85">85</xref>). Excessive game playing that results in addiction-like symptoms, therefore, may be associated with deficient ability to integrate previous emotional/affective experiences of rewards or punishments, to motivate and engage in inhibition as well as to trigger somatic responses.</p>
<p>According to the somatic marker hypothesis, somatic response is multidimensional and the emotional experience caused by the reward or punishment under a decision-making situation, would change with the somatic state (<xref ref-type="bibr" rid="B86">86</xref>). Adapting this view, one can argue that IGD may be associated with impaired reward and punishment expectation and processing functions. Support for this view has been given in a study on the underlying neural mechanisms of disadvantageous risky decision-making in IGD cases. During the Balloon Analog Risk Task (BART), a significant interaction effect between risk level and activation of the bilateral ventral medial prefrontal cortex (PFC) has been shown (<xref ref-type="bibr" rid="B87">87</xref>). Another study, which used a modified delay-discounting task, also suggested that IGD cases prefer the probabilistic or risky options; it also showed that there is a positive correlation between activation of inferior frontal gyrus and probability discounting rates (<xref ref-type="bibr" rid="B88">88</xref>).</p>
<p>In contrast, evidence from First Person or Ego-Shooters players suggests that excessive videogame playing may enhance the performance on an IGT compared to controls (<xref ref-type="bibr" rid="B89">89</xref>), while experience with First Person or Ego-Shooters games was positively correlated with impulsivity, and experience with strategy games was negatively correlated with impulsivity (<xref ref-type="bibr" rid="B85">85</xref>). One reasonable interpretation is that First Person or Ego-Shooters games include many violent elements, which could arouse the impulsive system (<xref ref-type="bibr" rid="B90">90</xref>, <xref ref-type="bibr" rid="B91">91</xref>). The most popular type of game, Multiplayer Online Role Playing game, can also contain violent scenes (<xref ref-type="bibr" rid="B92">92</xref>). Indeed, studies suggest relation between IGD and aggression (<xref ref-type="bibr" rid="B91">91</xref>), which may manifest from deficits in the hot inhibition/control brain system. In other words, after prolonged exposure to violent games, IGD cases may develop higher aggression than healthy subjects, which would promote their risk-taking intentions and behaviors (<xref ref-type="bibr" rid="B93">93</xref>).</p>
<p>Several studies have also reported that structural impairment in the orbital frontal cortex in IGD cases. These impairments include abnormal glucose metabolism, abnormal of cortical thickness, and white matter fiber consistency (<xref ref-type="bibr" rid="B94">94</xref>&#x02013;<xref ref-type="bibr" rid="B96">96</xref>). Moreover, compared to the neutral pictures, gaming pictures activated the OFC, right nucleus accumbens and bilateral Anterior Cingulate Cortex (ACC) (<xref ref-type="bibr" rid="B26">26</xref>). These results demonstrate that the orbital frontal cortex is involved in the modulation of reactive aggression; simply put the orbital frontal cortex fails to &#x0201C;inhibit&#x0201D; reactive aggression in response to social cues present in the environment (<xref ref-type="bibr" rid="B97">97</xref>).</p>
<p>Distinguishing it from other addictive substances and behaviors, video gaming provides different kinds of scenes and environments that can constantly stimulate use, rewards, violence and arousal. This emotional aspect that is apparent especially in violent games can lead to mood changes and disrupt the integration of emotional and cognitive inputs in the orbital frontal cortex (<xref ref-type="bibr" rid="B98">98</xref>). This process can also increase impulsivity, tendency for risk-taking and ignoring negative effects while seeking further rewards. The antisocial behavior among IGD cases suggests an association between aggression and excessive play of violent videogames (<xref ref-type="bibr" rid="B99">99</xref>). Overall, excessive play of online games can disrupt the hot executive system in two ways. First, the dysfunction of the ventral medial PFC impacts the value evaluation of rewards and punishments (<xref ref-type="bibr" rid="B100">100</xref>). Second, game-related cues arouse the mood with aggression, and this can affect the integration of emotional inputs into decision-making. The somatic state would be influenced by the aggression, and as a result, IGD cases develop impulsive tendencies as manifested in impairments to the orbital frontal cortex and the balance mediated by the orbital and ventral medial cortices is infringed upon.</p>
</sec>
<sec id="S4-2">
<title>IGD and Cold Executive Function</title>
<p>The ability to suppress automatic and pre-potent response behaviors is critical to the prevention of addictive behaviors. Accordingly, IGD cases showed impairment of inhibition control across many studies (<xref ref-type="bibr" rid="B58">58</xref>, <xref ref-type="bibr" rid="B101">101</xref>). Reduction in inhibition of pre-potent responses may essentially make incentive habits more powerful and increase their status to become a &#x0201C;default&#x0201D; automatic habit system (<xref ref-type="bibr" rid="B102">102</xref>). This happens because impaired response inhibition could lead to abnormal salience attribution toward gaming-related cues in IGD cases.</p>
<p>Through the paradigms of stop-signal (<xref ref-type="bibr" rid="B102">102</xref>) and go/no-go tasks (<xref ref-type="bibr" rid="B103">103</xref>), researchers could measure the ability to inhibit advantage response irrelevant to the current task or topic. Subjects were required to withhold response while a particular stop signal (stop-signal task) or stimuli occurs (go/no-go tasks). IGD cases showed impaired inhibition control while they performed relevant go/no-go tasks (such as responding faster to stimuli pictures than to neutral pictures and making more false responses than healthy subjects did) (<xref ref-type="bibr" rid="B104">104</xref>&#x02013;<xref ref-type="bibr" rid="B107">107</xref>). A similar picture emerged from studies based on the stop signal task (<xref ref-type="bibr" rid="B108">108</xref>, <xref ref-type="bibr" rid="B109">109</xref>). Considering the characteristics of online games, which include many well-designed stimuli (e.g., arousing scenes or pictures), the video-game-special go/no-go task is deemed suitable for videogame addiction research.</p>
<p>Results from recent brain imaging studies suggested that IGD can be associated with a disruption of brain circuits involved in motor response inhibition. Excessive gaming experience is associated with increased gray matter in the right hippocampal formation, dorsolateral PFC, and bilateral cerebellum (<xref ref-type="bibr" rid="B110">110</xref>, <xref ref-type="bibr" rid="B111">111</xref>). Resting state studies find decreased functional connectivity in the PFC&#x02014;striatal circuit in IGD cases (<xref ref-type="bibr" rid="B112">112</xref>). Using the go/no-go task, a significantly hyperactive left superior medial frontal and right anterior cingulate cortex during no-go trials was found (<xref ref-type="bibr" rid="B105">105</xref>). Using gaming-related picture as cues, healthy controls increased brain activation in the right dorsolateral PFC in comparison with the IGD cases (<xref ref-type="bibr" rid="B113">113</xref>). Moreover, 6&#x02009;months therapy of Bupropion, which is used in the treatment of substance disorders, reduced relevant activations in response to the game-related cues, in IGD cases (<xref ref-type="bibr" rid="B114">114</xref>). These results point to possible abnormalities in presumed IGD cases in terms of cold executive function. They show that prolonged playing, sensitizes the impulsive brain systems and when coupled with deficits in executive control (<xref ref-type="bibr" rid="B115">115</xref>), it can lead to difficulty to inhibit prepotent game cues and to the emergence of addiction-like symptoms (<xref ref-type="bibr" rid="B116">116</xref>).</p>
</sec>
</sec>
<sec id="S5">
<title>The Interoceptive Processes (System 3)</title>
<p>Previous research has suggested that an interoceptive system can modulate the balance between the impulsive and reflective systems, and that the exacerbated imbalance can help maintaining addictions (<xref ref-type="bibr" rid="B20">20</xref>). The main function of interoceptive processes is sensing psychological and physical imbalances and mediating response signals in the form of disgust, craving, urge, etc. as a means to signal the need to restore homeostasis. In the case of addiction, this system mediates anticipation for rewards by translating somatic sensory signals into one&#x02019;s subjectively experience of a desire to engage in the behavior (<xref ref-type="bibr" rid="B117">117</xref>&#x02013;<xref ref-type="bibr" rid="B119">119</xref>). This process mainly depends on the structure of bilateral insular cortex (<xref ref-type="bibr" rid="B120">120</xref>).</p>
<sec id="S5-1">
<title>The Insula and IGD</title>
<p>Studies have shown that the insular cortex plays an important role in substance dependence and seeking (<xref ref-type="bibr" rid="B121">121</xref>, <xref ref-type="bibr" rid="B122">122</xref>). This happens because the translating of somatic signals into subjective experience of craving increases sensitivity toward addiction-related cues and can reduce inhibition resources availability (<xref ref-type="bibr" rid="B118">118</xref>, <xref ref-type="bibr" rid="B120">120</xref>). Indeed, the activation of the insular cortex has been implicated in a wide range of conditions and behaviors, such as anticipating the future results about monetary gains (<xref ref-type="bibr" rid="B123">123</xref>) or losses (<xref ref-type="bibr" rid="B124">124</xref>). Accordingly, the thickness of insular cortex was negatively associated with cigarette exposure response (<xref ref-type="bibr" rid="B125">125</xref>), while damage to the insular cortex could disrupt cigarette smoking; smokers with damage to insula quit smoking easily and show a higher rate of cessation from smoking which is nearly 100 times more than this of smokers without damage to insula (<xref ref-type="bibr" rid="B126">126</xref>).</p>
<p>The formation of interoceptive system representation through insular cortex activation is crucial for decision-making regarding prepotent cues (<xref ref-type="bibr" rid="B118">118</xref>). Considering the position of the insular cortex in the brain, it can be seen as a bridge between ventromedial and OFC and the impulsive system regions. As such, the insula has been suggested to act as a connector that translates somatic signals and triggers bodily states (<xref ref-type="bibr" rid="B118">118</xref>). The co-activation pattern between the insula and the ventromedial frontal cortex has been revealed during the process of generating somatic markers that involved reference judgments (<xref ref-type="bibr" rid="B127">127</xref>). By working in tandem with the vmPFC, the insula could map the relationship between external objects and internal somatic sensory states, and invoke bodily states.</p>
<p>Recent studies also suggest that the insula plays an important role in IGD. They revealed decreased functional connectivity between the insula and the motor/executive cortices (such as dlPFC, OFC, cingulated cortex) in IGD cases (<xref ref-type="bibr" rid="B128">128</xref>, <xref ref-type="bibr" rid="B129">129</xref>). This finding revealed weaken connections between the insula and the reflective system among IGD individuals, which might explain loss of control in such cases. As such, in IGD cases the insula can be presumed to have abnormal abilities to communicate with the executive system. While exposed to game-related pictures, the insula has been activated and the activation was positively correlated with self-reported gaming urge stimulated by the pictures (<xref ref-type="bibr" rid="B26">26</xref>, <xref ref-type="bibr" rid="B27">27</xref>). This may reveal that the insula is related to the relationship between rewarding cues and the craving level one subjectively experience.</p>
<p>Evidence from co-activation research also suggested strong association between the insula and the impulsive and reflective systems; in the presence of game-related cues, co-activation patterns in orbital frontal cortex, insula, anterior cingulate cortex, and dorsolateral cortex have been observed (<xref ref-type="bibr" rid="B26">26</xref>). These findings provide further support to the hypothesis that the key role of the insula is to serve as a hub mediating craving production through communication with impulsive and reflective brain systems.</p>
<p>The insula also plays an important role in the development and maintenance of addiction; it integrates the interoceptive effects of addictive substances or behaviors into conscious awareness, memory, or executive functions (<xref ref-type="bibr" rid="B130">130</xref>). In support of this view, research has indicated that deficit in response inhibition is pronounced during periods of heightened motivational state of drug intake (<xref ref-type="bibr" rid="B131">131</xref>) or drinking alcohol (<xref ref-type="bibr" rid="B132">132</xref>). These deficits are triggered by the high subjective state during the stage of abstinence while the affective stimuli related to the addiction substance consume enormous attentional resources and result in the disruption of inhibitory control. Under such overload of attentional resources, the attraction caused by the stimuli may encourage relapse and make it difficult to overcome tempting addictive behaviors (<xref ref-type="bibr" rid="B131">131</xref>, <xref ref-type="bibr" rid="B132">132</xref>). In other words, insula-mediated interoceptive representations have the capacity to &#x0201C;hijack&#x0201D; the cognitive resources necessary for exerting inhibitory control to resist the temptation to smoke, use drugs, or use social media impulsively (<xref ref-type="bibr" rid="B20">20</xref>) by disabling activity of the prefrontal (control/reflective) system. The anterior insula has bidirectional connections to the amygdala, ventral striatum, and OFC. The insula integrates the interoceptive state into conscious feelings and into decision-making processes that involve certain risks and rewards; it presents decreased cortical thickness in IGD cases (<xref ref-type="bibr" rid="B94">94</xref>, <xref ref-type="bibr" rid="B133">133</xref>). This structural abnormality of the interoceptive system may also hamper self-awareness, which could take the form of failure to recognize an illness (<xref ref-type="bibr" rid="B134">134</xref>). Young adults with high levels of IGD often also present depression, anxiety, aggression, or social phobias symptoms (<xref ref-type="bibr" rid="B135">135</xref>). Such symptoms may also be associated with dysfunction of the translation of interoceptive signals emerging from somatic and emotional states (<xref ref-type="bibr" rid="B136">136</xref>). Moreover, deprivation interoceptive signals (e.g., when one cannot play videogames even if he or she strongly desires to do do) may also hamper metacognitive abilities in addicts (<xref ref-type="bibr" rid="B137">137</xref>). This abnormal degree of dissociation in addicted people, between the &#x0201C;object&#x0201D; level and the &#x0201C;meta&#x0201D; level, raises the possibility that poor metacognition lead to action and decision-making monitoring and adjustment (<xref ref-type="bibr" rid="B138">138</xref>). Hence, when metacognitive judgment becomes exceedingly disrupted, the repetition of addictive behaviors may be heightened by an underestimation of addiction severity.</p>
<p>The tripartite view that includes three systems of IGD that emerges from this review is presented in Figure <xref ref-type="fig" rid="F1">1</xref>.</p>
<fig id="F1" position="float">
<label>Figure 1</label>
<caption><p>A schematic tripartite neurological model illustrating the key systems that may underlie IGD, (1) gaming related cues excite the impulsive system, which mainly depend on the amygdala and striatum, and activates cue-action links through mental associations, (2) the reflective system mainly depends on the structure of the prefrontal cortex (PFC) and inhibits the impulsions toward an Internet game, (3) the interoceptive awareness systems plays a key role in modulating the equilibrium between system 1 and system 2. Through translating interoceptive signals, the insular cortex maintains craving for an Internet game. The activity of the insular cortex increases the drive to play the Internet game and weakens the inhibition abilities regarding this action. The excessive and problematic play of online games can also invoke changes in the relevant brain regions, and by so doing exacerbate or help expressing other mental health problem.</p></caption>
<graphic xlink:href="fpsyt-08-00285-g001.tif"/>
</fig>
</sec>
</sec>
<sec id="S6" sec-type="discussion">
<title>Discussion</title>
<p>In this article, we reviewed the neurocognitive processes that may underlie presumed IGD. This is important as many young adults (but not all) lose the ability to resist the reward and pleasure from virtual gaming worlds. That is, for some heavy gamers, an inability to resist unreal rewards emerges, despite mounting monetary, social and performance losses leading to personal, familial, financial, professional, and legal negative consequences. This loss of control that is termed IGD, we argue, may be sub-served by a tripartite network of brain systems.</p>
<p>Specifically, the review we provide in this paper suggests that the continuous engagement in videogame playing in IGD cases can be explained by increased automatic motivational response directed at gaming-related behaviors coupled with a lowered efficiency of impulse control and self-reflective processes, and that this imbalance may be further accentuated by abnormal interoceptive awareness processes. This tripartite view of the brain systems involved in addictive disorders (<xref ref-type="bibr" rid="B20">20</xref>) as applied to IGD cases here, has received support in various studies; albeit such studies have typically provided a disjointed view regarding the three involved systems. They specifically show that failure to self-control is associated with dysfunction of the impulsive and reflective brain systems (functionally and structurally) and that this dysfunction can be regulated by insular activity, the dysfunction of which can augment the imbalance between reflective and impulsive brain processes. The translation of interoceptive signals in the insula disrupted this balance by changes in somatic states that were aroused by addiction-related stimuli (videogame cues in our case). In addition, impairment in the interoceptive awareness system leads IGD cases to often ignore the negative effects of excessive playing. This increases the probability of relapse in IGD cases. Overall, online gaming provides many rewards to users and can have positive effects on many children (<xref ref-type="bibr" rid="B139">139</xref>). However, these same rewards can exploit brain deficits in the impulsive, reflective, and interceptive brain systems and create dysfunctions in learning, motivation, an assessment of the salience of a video game-related stimuli, to such an extent that the vulnerable individual develops addiction-like symptoms in relation to videogame playing.</p>
<p>Previous research has proposed several models of IGD, which are also in line with the framework we present here, but put different emphasis or ignore interoceptive awareness processes. Davis (<xref ref-type="bibr" rid="B140">140</xref>) argued that there are differences between generalized pathological Internet use (GIU) and specific Internet use (SIU) and suggested a cognitive behavior model to explain such differences. According to this model, maladaptive cognition of the external environment drives a series of internal responses such as negative emotions and increases the use of specific rewarding application over the Internet (e.g., online gaming, pornography). This model provides support for the assumptions in our model as both allude to the idea that maladaptive cognitions may underlie IGD; our model points to brain regions that are likely involved in developing and maintaining such cognitions.</p>
<p>On the basis of this research, neurocognitive models have been developed and emphasized the importance of executive function in SIU (<xref ref-type="bibr" rid="B18">18</xref>). These overlap with regions we discussed: the VMPFC and dorsolateral lateral PFC are suggested to be most likely involved in development and maintenance of addictive use of Internet applications. Again, this model overlaps some aspects of our model, but our model puts stronger emphasis on interoceptive awareness processes. Similarly, Dong and Potenza (<xref ref-type="bibr" rid="B141">141</xref>) proposed a cognitive behavior model for IGD. The model contains three key cognitive domains of IGD: motivational drive and reward-seeking, behavioral control and executive control, and decision-making as related to the long-term negative consequence of current behavioral choices. This model also emphasizes the importance of seeking motivation and the state of craving, and suggests that the state of craving may contribute to the IGD process. This is similar to our model in terms of components but does not specifically focus on the regions involved in craving generation. Similarly, a process model called Person-Affect-Cognition-Execution (I-PACE) suggests that addiction may result from increasing exposure to addiction-related cues and may involve deficits in the personal, affective, cognition, and execution domains. This model is also aligned with our neurocognitive model as personal, affective, cognition and execution domains can be mapped onto the tripartite view we present.</p>
<p>According to our review of neuro-cognitive studies, the dysfunction of brain structure and activations that sub-serves IGD may be similar to this in cases of substance and behavioral addictions. The impairment of the impulsive and reflective processes showed that IGD shares common mechanisms with substance addictions. They showed that prolonged excessive playing can be associated with structural and connectivity abnormalities in relevant brain regions. Importantly, such studies hint at ways through which IGD can be treated; though such approaches should be further examined in future research. First, several studies suggest the bupropion could reduce the craving and urge for video gaming (<xref ref-type="bibr" rid="B114">114</xref>, <xref ref-type="bibr" rid="B142">142</xref>). This can be a viable treatment option, but future research should examine its efficacy given different profiles of comorbidity that are plausible in IGD cases.</p>
<p>Second, cognitive behavioral therapy has been most widely used for IGD treatment. It aims at moderating the impulsive processes or at boosting reflective resources such that IGD cases learn to better cope with their inability to resist gaming. For instance, after recognize the inappropriateness of their behavior, IGD cases may learn to adjust their behavioral patterns and choices (<xref ref-type="bibr" rid="B143">143</xref>). Such approaches should also be further studied, especially since they assume relatively intact prefrontal brain regions. This seems to be the case in mild to medium addiction levels (<xref ref-type="bibr" rid="B28">28</xref>, <xref ref-type="bibr" rid="B69">69</xref>), but in severe IGD cases, there may be abnormalities in prefrontal regions that will not allow successful cognitive behavioral therapy. This idea merits future research.</p>
</sec>
<sec id="S7" sec-type="author-contributor">
<title>Author Contributions</title>
<p>LW, OT, AB, and QH were responsible for the study conception and design; LW and SZ wrote the first draft of the paper. SZ, OT, and QH also contributed to the writing of the paper. LW, SZ, OT, AB, and QH made the critical revision of the article. All authors gave the final approval of the article.</p>
</sec>
<sec id="S8">
<title>Conflict of Interest Statement</title>
<p>The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.</p>
</sec>
</body>
<back>
<fn-group>
<fn fn-type="financial-disclosure">
<p><bold>Funding.</bold> QH was supported by research grants from the National Natural Science Foundation of China (31400959), Entrepreneurship and Innovation Program for Chongqing Overseas Returned Scholars (cx2017049), Fundamental Research Funds for the Central Universities (SWU1509422, 15XDSKD004), Open Research Fund of the Key Laboratory of Mental Health, Institute of Psychology, Chinese Academy of Sciences (KLMH2015G01), and the Research Program Funds of the Collaborative Innovation Center of Assessment toward Basic Education Quality at Beijing Normal University (2016-06-014-BZK01, SCSM-2016A2-15003).</p></fn>
</fn-group>
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