Impaired social reward processing in individuals with Internet gaming disorder and its relationship with early face perception

The last decade has witnessed the swift development of wireless networks and smart devices, driving rapid growth in the Internet gaming industry, which has gradually become one of the most popular forms of recreation and entertainment among adolescents and even adults. Although online games have provided immense enjoyment, they also present challenges. Notably, Internet gaming disorder (IGD) has garnered significant attention from the research community. The prevalence of IGD is notably high in East Asia, where it ranges between 10 and 15 percent, with males exhibiting a higher rate than females (Li et al., 2020, Wang et al., 2018, Yu et al., 2021; for a meta-analysis, see Liao et al., 2022). Given this, unraveling the neurocognitive mechanisms underpinning the emergence and sustenance of IGD is crucial.

The loss of interest in other social activities and impairment of social function due to excessive gaming activity is one of the main symptoms and the core diagnostic basis of IGD (American Psychiatric Association, 2013). For example, previous studies showed that compared with healthy gamers, individuals with IGD have lower academic motivation and poorer academic performance (Eichenbaum et al., 2015), compromised empathy (Jiao et al., 2017), lower real-world social motivation (Haagsma et al., 2013), less real-world social support (Tham et al., 2020), and are more likely to lose their jobs (Jiang, 2014). However, these social impairments of IGD have completely different manifestations in game-related social contexts. For example, studies have found that individuals with IGD have higher social motivation (Király et al., 2022) and have more social support (Tham et al., 2020) in games. This difference is also manifested in the cognitive neural processing of facial expressions. For instance, the N170 elicited by real faces in individuals with IGD was significantly reduced compared with healthy controls, but this effect was only shown in left hemispheres (He et al., 2011). A recent study found that the P100, P200, and mismatch negativity elicited by game-related faces in individuals with IGD were significantly larger than those in healthy controls (He et al., 2019). However, this study did not find a difference between the real face N170 and the game-related face N170 in individuals with IGD.

It is evident that the impaired social functioning of individuals with IGD has distinct behavioral and neural differences in real and game-related social contexts. According to the Social Motivation Theory, the behavioral manifestations of humans’ social motivation are of at least three kinds (Chevallier et al., 2012): social orienting (objects with social importance are prioritized by attention, for instance, human faces; Fletcher-Watson et al., 2008, Ro et al., 2001); social seeking and liking (social interactions are rewarding, social signals are incentive; Hayden et al., 2007, Fehr and Camerer, 2007); and social maintaining (interpersonal behaviors are influenced by the desire to maintain and enhance relationships; Leary & Allen, 2010). Meanwhile, the theory also proposes that the social motivational deficits have downstream effects on the development of social cognition. This argument is supported by numerous pieces of evidence (e.g., Gossen et al., 2014, Burnside et al., 2018, Hayward et al., 2018, Martin et al., 2023, Dziura et al., 2023). That is to say, the impairment of an individual’s social cognition may be caused by dysfunctional of social reward. If individuals derive limited pleasure from social activities, then they might gradually lose their motivation for them, which will lead to impairment of social cognition function. Therefore, the impairment of social cognition function in individuals with IGD may be related to their social reward dysfunction.

Social rewards are a broad set of stimuli, which instigate positive experiences involving other people, including a vast repertoire of verbal and non-verbal behaviors, gestures, and feelings such as a smile, praise, a thumbs-up, the acquisition of a good reputation, etc. (Matyjek et al., 2020, Gu et al., 2020). Social rewards have the function of guiding individual social behavior response strategies and shaping social behavior patterns (Matyjek et al., 2020). Research paradigms centered on social reward were mainly adapted from research paradigms of monetary reward, such as the social judgement task and the social incentive delay task. A common research paradigm of social reward is the social judgment task (Somerville et al., 2006), developed based on the doors task (Hajcak et al., 2005, Hajcak et al., 2007, Weinberg et al., 2012, Weinberg et al., 2014, Weinberg et al., 2015), which is a guessing task that requires obtaining a photo of the participants before the experiment and informing them that the photo will be evaluated by a group of peers. In the formal experiment, participants are presented with photos of two peers and informed that one of the two peers gave his/her photo an evaluation of “like” and the other one gave a “dislike”. They must then deduce which peer viewed them favorably, after which feedback is provided (Wang et al., 2020, Wang et al., 2020). The social incentive delay task was another common research paradigm of social reward, modified based on the monetary incentive delay task, which mainly includes three stages: cue presentation, target stimulus response, and feedback (Martins et al., 2021). During the cue presentation, participants are signaled that the target stimulus is about to be presented, prompting them to prepare for a response. The participants need to respond as soon as possible when the target stimulus is presented. Social reward or punishment feedback is given based on the cue type and reaction time after the response (Cremers et al., 2015, Goerlich et al., 2017, Martins et al., 2021). Studies using these paradigms have found that social rewards can activate brain regions similar to monetary rewards, such as the ventral striatum, orbitofrontal cortex, and amygdala (Rademacher et al., 2017, Gu et al., 2019).

Electrophysiologically, with the aid of ERP technology, social rewards can also elicit the reward positivity (RewP) that is sensitive to monetary rewards (Wang et al., 2020, Wang et al., 2020). RewP, which is induced 200 to 300 ms after the presentation of feedback stimuli, is a relatively more positive component of reward feedback ERP compared to punishment feedback ERP. It is usually calculated using difference waves, mainly distributed in the central frontal region. This component is sensitive to both feedback valence (reward vs. punishment) and reward degree and is a reliable indicator for investigating the reward processing mechanisms of individuals (Proudfit, 2015). There have been nuanced findings while using RewP as an indicator, some studies showed similar activations for social rewards and monetary rewards (Nelson & Jarcho, 2021), while several other studies found that the two may have distinct relationships (Ethridge et al., 2017, Pegg et al., 2021, Rappaport et al., 2019). Research has also found that the induction of RewP is related to the activation of the medial prefrontal cortex, cingulate gyrus, and striatum under reward conditions (Becker et al., 2014).

To date, the study of the social reward processing of individuals with IGD had not been reported. However, relevant studies have found that there is an impairment of social reward processing in individuals with substance use disorder (SUD). For example, Preller et al. (2014) utilized a social interaction paradigm in tandem with fMRI technology to reveal individuals with cocaine use disorder displayed reduced emotional evolvement and impaired activation of the ventromedial orbitofrontal cortex compared with healthy controls for social interaction. This impairment of activation was correlated with a smaller social circle, indicating that the neural sensitivity to social reward of individuals with cocaine use disorder is significantly reduced relative to healthy controls. Similarly, Tobler et al. (2016) used functional neuroimaging in cocaine users to investigate social reward as modeled by agreement of music preferences with music experts and found that, compared to healthy controls, there is a significantly decreased activation of the ventromedial prefrontal cortex for social reward in individuals with cocaine use disorder compared with healthy controls. Wei et al. (2020) recorded the ERPs of individuals with methamphetamine use disorder performing a social incentive delay task, which used thumbs up as a social reward and thumbs down as a social punishment. They found that the feedback-related negativity component elicited by social incentives in the healthy controls was larger than that in the individuals with methamphetamine use disorder. Wei et al. concluded that individuals with methamphetamine use disorder have a blunted neural response to the processing of social incentives. Quednow (2017) reviewed the literature regarding social cognition and reward function in individuals with stimulant use disorder and concluded that the dysfunction of social reward may contribute to the social problems and the decay of social relationships in stimulant-addicted individuals. Meanwhile, Quednow suggests that training in social reward might improve social functioning and enhance treatment success in stimulant addiction.

In summary, previous studies found that individuals with SUD have social reward dysfunction and explored its neurocognitive mechanisms, whereas there is still a lack of evidence in the domain of IGD. In addition, there are differences between SUD and IGD; for example, online gaming and related social activities can provide rich social rewards for individuals with IGD (Arbeau et al., 2020), who can easily get social rewards in a game-related context. This may lead to the weakening of their real-life social reward function and the enhancement of their game-related social reward function. Therefore, the impairment of social reward processing and its neurocognitive mechanism in individuals with IGD may present distinct characteristics compared with individuals with SUD. Thus, the primary objective of this study is to explore the neurocognitive mechanisms of impaired social reward processing in individuals with IGD. Meanwhile, according to the Social Motivation Theory (Chevallier et al., 2012, Blinka and Mikuška, 2014, Quednow, 2017), social motivation and reward dysfunction may be the preceding factors of social cognition dysfunction. Previous studies found that the face perception cognition of individuals with IGD was impaired. Therefore, investigating the social reward function among individuals with IGD and whether it is related to face cognition is the second purpose of this study. Finally, this study also intends to examine whether the severity of IGD symptoms is related to the degree of social reward function impairment.

In order to address the above three study purposes, this study will use a social judgement task combined with ERP technology and take the RewP component that related to social reward processing and the N170 component that related to early face perception as the neural indicators to explore the neurocognitive mechanism of social reward impairment and its relationship with face cognition in individuals with IGD. The social judgement task was chosen in this study because it can simultaneously evaluate social reward and face cognition functions. This study hypothesized that: (1) compared with healthy gamers, the individuals with IGD would show significantly larger game-related social reward RewP and significantly smaller real-life social reward RewP; (2) similarly, compared with healthy gamers, the individuals with IGD might exhibit significantly larger game face N170 and significantly smaller real face N170, and N170 would be correlated with RewP. (3) The game-related social reward RewP is expected to positively correlate with the symptoms severity of IGD. Finally, as He et al. (2011) only observed a reduction in real faces N170 in individuals with IGD in the left hemispheres, this study will also investigate whether there is a lateralization effect in the N170 components.

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