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Functional connectivity changes in the brain of adolescents with internet addiction: A systematic literature review of imaging studies [1]

['Max L. Y. Chang', 'Child', 'Adolescent Mental Health', 'Department Of Brain Sciences', 'Great Ormond Street Institute Of Child Health', 'University College London', 'London', 'United Kingdom', 'Irene O. Lee', 'Behavioural Brain Sciences Unit']

Date: 2024-06 

Abstract Internet usage has seen a stark global rise over the last few decades, particularly among adolescents and young people, who have also been diagnosed increasingly with internet addiction (IA). IA impacts several neural networks that influence an adolescent’s behaviour and development. This article issued a literature review on the resting-state and task-based functional magnetic resonance imaging (fMRI) studies to inspect the consequences of IA on the functional connectivity (FC) in the adolescent brain and its subsequent effects on their behaviour and development. A systematic search was conducted from two databases, PubMed and PsycINFO, to select eligible articles according to the inclusion and exclusion criteria. Eligibility criteria was especially stringent regarding the adolescent age range (10–19) and formal diagnosis of IA. Bias and quality of individual studies were evaluated. The fMRI results from 12 articles demonstrated that the effects of IA were seen throughout multiple neural networks: a mix of increases/decreases in FC in the default mode network; an overall decrease in FC in the executive control network; and no clear increase or decrease in FC within the salience network and reward pathway. The FC changes led to addictive behaviour and tendencies in adolescents. The subsequent behavioural changes are associated with the mechanisms relating to the areas of cognitive control, reward valuation, motor coordination, and the developing adolescent brain. Our results presented the FC alterations in numerous brain regions of adolescents with IA leading to the behavioural and developmental changes. Research on this topic had a low frequency with adolescent samples and were primarily produced in Asian countries. Future research studies of comparing results from Western adolescent samples provide more insight on therapeutic intervention.

Citation: Chang MLY, Lee IO (2024) Functional connectivity changes in the brain of adolescents with internet addiction: A systematic literature review of imaging studies. PLOS Ment Health 1(1): e0000022. https://doi.org/10.1371/journal.pmen.0000022 Editor: Kizito Omona, Uganda Martyrs University, UGANDA Received: December 29, 2023; Accepted: March 18, 2024; Published: June 4, 2024 Copyright: © 2024 Chang, Lee. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Data Availability: All relevant data are within the paper and its Supporting information files. Funding: The authors received no specific funding for this work. Competing interests: The authors have declared that no competing interests exist.

Introduction The behavioural addiction brought on by excessive internet use has become a rising source of concern [1] since the last decade. According to clinical studies, individuals with Internet Addiction (IA) or Internet Gaming Disorder (IGD) may have a range of biopsychosocial effects and is classified as an impulse-control disorder owing to its resemblance to pathological gambling and substance addiction [2, 3]. IA has been defined by researchers as a person’s inability to resist the urge to use the internet, which has negative effects on their psychological well-being as well as their social, academic, and professional lives [4]. The symptoms can have serious physical and interpersonal repercussions and are linked to mood modification, salience, tolerance, impulsivity, and conflict [5]. In severe circumstances, people may experience severe pain in their bodies or health issues like carpal tunnel syndrome, dry eyes, irregular eating and disrupted sleep [6]. Additionally, IA is significantly linked to comorbidities with other psychiatric disorders [7]. Stevens et al (2021) reviewed 53 studies including 17 countries and reported the global prevalence of IA was 3.05% [8]. Asian countries had a higher prevalence (5.1%) than European countries (2.7%) [8]. Strikingly, adolescents and young adults had a global IGD prevalence rate of 9.9% which matches previous literature that reported historically higher prevalence among adolescent populations compared to adults [8, 9]. Over 80% of adolescent population in the UK, the USA, and Asia have direct access to the internet [10]. Children and adolescents frequently spend more time on media (possibly 7 hours and 22 minutes per day) than at school or sleeping [11]. Developing nations have also shown a sharp rise in teenage internet usage despite having lower internet penetration rates [10]. Concerns regarding the possible harms that overt internet use could do to adolescents and their development have arisen because of this surge, especially the significant impacts by the COVID-19 pandemic [12]. The growing prevalence and neurocognitive consequences of IA among adolescents makes this population a vital area of study [13]. Adolescence is a crucial developmental stage during which people go through significant changes in their biology, cognition, and personalities [14]. Adolescents’ emotional-behavioural functioning is hyperactivated, which creates risk of psychopathological vulnerability [15]. In accordance with clinical study results [16], this emotional hyperactivity is supported by a high level of neuronal plasticity. This plasticity enables teenagers to adapt to the numerous physical and emotional changes that occur during puberty as well as develop communication techniques and gain independence [16]. However, the strong neuronal plasticity is also associated with risk-taking and sensation seeking [17] which may lead to IA. Despite the fact that the precise neuronal mechanisms underlying IA are still largely unclear, functional magnetic resonance imaging (fMRI) method has been used by scientists as an important framework to examine the neuropathological changes occurring in IA, particularly in the form of functional connectivity (FC) [18]. fMRI research study has shown that IA alters both the functional and structural makeup of the brain [3]. We hypothesise that IA has widespread neurological alteration effects rather than being limited to a few specific brain regions. Further hypothesis holds that according to these alterations of FC between the brain regions or certain neural networks, adolescents with IA would experience behavioural changes. An investigation of these domains could be useful for creating better procedures and standards as well as minimising the negative effects of overt internet use. This literature review aims to summarise and analyse the evidence of various imaging studies that have investigated the effects of IA on the FC in adolescents. This will be addressed through two research questions: How does internet addiction affect the functional connectivity in the adolescent brain? How is adolescent behaviour and development impacted by functional connectivity changes due to internet addiction?

Methods The review protocol was conducted in line with the Preferred Reporting Items for Systematic Reviews and Meta-Analyses (PRISMA) guidelines (see S1 Checklist). Search strategy and selection process A systematic search was conducted up until April 2023 from two sources of database, PubMed and PsycINFO, using a range of terms relevant to the title and research questions (see full list of search terms in S1 Appendix). All the searched articles can be accessed in the S1 Data. The eligible articles were selected according to the inclusion and exclusion criteria. Inclusion criteria used for the present review were: (i) participants in the studies with clinical diagnosis of IA; (ii) participants between the ages of 10 and 19; (iii) imaging research investigations; (iv) works published between January 2013 and April 2023; (v) written in English language; (vi) peer-reviewed papers and (vii) full text. The numbers of articles excluded due to not meeting the inclusion criteria are shown in Fig 1. Each study’s title and abstract were screened for eligibility. PPT PowerPoint slide

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TIFF original image Download: Fig 1. Prisma flow diagram of study selection process. https://doi.org/10.1371/journal.pmen.0000022.g001 Quality appraisal Full texts of all potentially relevant studies were then retrieved and further appraised for eligibility. Furthermore, articles were critically appraised based on the GRADE (Grading of Recommendations, Assessment, Development, and Evaluations) framework to evaluate the individual study for both quality and bias. The subsequent quality levels were then appraised to each article and listed as either low, moderate, or high. Data collection process Data that satisfied the inclusion requirements was entered into an excel sheet for data extraction and further selection. An article’s author, publication year, country, age range, participant sample size, sex, area of interest, measures, outcome and article quality were all included in the data extraction spreadsheet. Studies looking at FC, for instance, were grouped, while studies looking at FC in specific area were further divided into sub-groups. Data synthesis and analysis Articles were classified according to their location in the brain as well as the network or pathway they were a part of to create a coherent narrative between the selected studies. Conclusions concerning various research trends relevant to particular groupings were drawn from these groupings and subgroupings. To maintain the offered information in a prominent manner, these assertions were entered into the data extraction excel spreadsheet.

Discussion The primary aim of this review was to present a summary of how internet addiction impacts on the functional connectivity of adolescent brain. Subsequently, the influence of IA on the adolescent brain was compartmentalised into three sections: alterations of FC at various brain regions, specific FC relationships, and behavioural/developmental changes. Overall, the specific effects of IA on the adolescent brain were not completely clear, given the variety of FC changes. However, there were overarching behavioural, network and developmental trends that were supported that provided insight on adolescent development. The first hypothesis that was held about this question was that IA was widespread and would be regionally similar to substance-use and gambling addiction. After conducting a review of the information in the chosen articles, the hypothesis was predictably supported. The regions of the brain affected by IA are widespread and influence multiple networks, mainly DMN, ECN, SN and reward pathway. In the DMN, there was a complex mix of increases and decreases within the network. However, in the ECN, the alterations of FC were more unilaterally decreased, but the findings of SN and reward pathway were not quite clear. Overall, the FC changes within adolescents with IA are very much network specific and lay a solid foundation from which to understand the subsequent behaviour changes that arise from the disorder. The second hypothesis placed emphasis on the importance of between network interactions and within network interactions in the continuation of IA and the development of its behavioural symptoms. The results from the findings involving the networks, DMN, SN, ECN and reward system, support this hypothesis (see Fig 5). Studies confirm the influence of all these neural networks on reward valuation, impulsivity, salience to stimuli, cue reactivity and other changes that alter behaviour towards the internet use. Many of these changes are connected to the inherent nature of the adolescent brain. There are multiple explanations that underlie the vulnerability of the adolescent brain towards IA related urges. Several of them have to do with the inherent nature and underlying mechanisms of the adolescent brain. Children’s emotional, social, and cognitive capacities grow exponentially during childhood and adolescence [57]. Early teenagers go through a process called “social reorientation” that is characterised by heightened sensitivity to social cues and peer connections [58]. Adolescents’ improvements in their social skills coincide with changes in their brains’ anatomical and functional organisation [59]. Functional hubs exhibit growing connectivity strength [60], suggesting increased functional integration during development. During this time, the brain’s functional networks change from an anatomically dominant structure to a scattered architecture [60]. The adolescent brain is very responsive to synaptic reorganisation and experience cues [61]. As a result, one of the distinguishing traits of the maturation of adolescent brains is the variation in neural network trajectory [62]. Important weaknesses of the adolescent brain that may explain the neurobiological change brought on by external stimuli are illustrated by features like the functional gaps between networks and the inadequate segregation of networks [62]. The implications of these findings towards adolescent behaviour are significant. Although the exact changes and mechanisms are not fully clear, the observed changes in functional connectivity have the capacity of influencing several aspects of adolescent development. For example, functional connectivity has been utilised to investigate attachment styles in adolescents [63]. It was observed that adolescent attachment styles were negatively associated with caudate-prefrontal connectivity, but positively with the putamen-visual area connectivity [63]. Both named areas were also influenced by the onset of internet addiction, possibly providing a connection between the two. Another study associated neighbourhood/socioeconomic disadvantage with functional connectivity alterations in the DMN and dorsal attention network [64]. The study also found multivariate brain behaviour relationships between the altered/disadvantaged functional connectivity and mental health and cognition [64]. This conclusion supports the notion that the functional connectivity alterations observed in IA are associated with specific adolescent behaviours as well as the fact that functional connectivity can be utilised as a platform onto which to compare various neurologic conditions. Limitations/strengths There were several limitations that were related to the conduction of the review as well as the data extracted from the articles. Firstly, the study followed a systematic literature review design when analysing the fMRI studies. The data pulled from these imaging studies were namely qualitative and were subject to bias contrasting the quantitative nature of statistical analysis. Components of the study, such as sample sizes, effect sizes, and demographics were not weighted or controlled. The second limitation brought up by a similar review was the lack of a universal consensus of terminology given IA [47]. Globally, authors writing about this topic use an array of terminology including online gaming addiction, internet addiction, internet gaming disorder, and problematic internet use. Often, authors use multiple terms interchangeably which makes it difficult to depict the subtle similarities and differences between the terms. Reviewing the explicit limitations in each of the included studies, two major limitations were brought up in many of the articles. One was relating to the cross-sectional nature of the included studies. Due to the inherent qualities of a cross-sectional study, the studies did not provide clear evidence that IA played a causal role towards the development of the adolescent brain. While several biopsychosocial factors mediate these interactions, task-based measures that combine executive functions with imaging results reinforce the assumed connection between the two that is utilised by the papers studying IA. Another limitation regarded the small sample size of the included studies, which averaged to around 20 participants. The small sample size can influence the generalisation of the results as well as the effectiveness of statistical analyses. Ultimately, both included study specific limitations illustrate the need for future studies to clarify the causal relationship between the alterations of FC and the development of IA. Another vital limitation was the limited number of studies applying imaging techniques for investigations on IA in adolescents were a uniformly Far East collection of studies. The reason for this was because the studies included in this review were the only fMRI studies that were found that adhered to the strict adolescent age restriction. The adolescent age range given by the WHO (10–19 years old) [65] was strictly followed. It is important to note that a multitude of studies found in the initial search utilised an older adolescent demographic that was slightly higher than the WHO age range and had a mean age that was outside of the limitations. As a result, the results of this review are biased and based on the 12 studies that met the inclusion and exclusion criteria. Regarding the global nature of the research, although the journals that the studies were published in were all established western journals, the collection of studies were found to all originate from Asian countries, namely China and Korea. Subsequently, it pulls into question if the results and measures from these studies are generalisable towards a western population. As stated previously, Asian countries have a higher prevalence of IA, which may be the reasoning to why the majority of studies are from there [8]. However, in an additional search including other age groups, it was found that a high majority of all FC studies on IA were done in Asian countries. Interestingly, western papers studying fMRI FC were primarily focused on gambling and substance-use addiction disorders. The western papers on IA were less focused on fMRI FC but more on other components of IA such as sleep, game-genre, and other non-imaging related factors. This demonstrated an overall lack of western fMRI studies on IA. It is important to note that both western and eastern fMRI studies on IA presented an overall lack on children and adolescents in general. Despite the several limitations, this review provided a clear reflection on the state of the data. The strengths of the review include the strict inclusion/exclusion criteria that filtered through studies and only included ones that contained a purely adolescent sample. As a result, the information presented in this review was specific to the review’s aims. Given the sparse nature of adolescent specific fMRI studies on the FC changes in IA, this review successfully provided a much-needed niche representation of adolescent specific results. Furthermore, the review provided a thorough functional explanation of the DMN, ECN, SN and reward pathway making it accessible to readers new to the topic. Future directions and implications Through the search process of the review, there were more imaging studies focused on older adolescence and adulthood. Furthermore, finding a review that covered a strictly adolescent population, focused on FC changes, and was specifically depicting IA, was proven difficult. Many related reviews, such as Tereshchenko and Kasparov (2019), looked at risk factors related to the biopsychosocial model, but did not tackle specific alterations in specific structural or functional changes in the brain [66]. Weinstein (2017) found similar structural and functional results as well as the role IA has in altering response inhibition and reward valuation in adolescents with IA [47]. Overall, the accumulated findings only paint an emerging pattern which aligns with similar substance-use and gambling disorders. Future studies require more specificity in depicting the interactions between neural networks, as well as more literature on adolescent and comorbid populations. One future field of interest is the incorporation of more task-based fMRI data. Advances in resting-state fMRI methods have yet to be reflected or confirmed in task-based fMRI methods [62]. Due to the fact that network connectivity is shaped by different tasks, it is critical to confirm that the findings of the resting state fMRI studies also apply to the task based ones [62]. Subsequently, work in this area will confirm if intrinsic connectivity networks function in resting state will function similarly during goal directed behaviour [62]. An elevated focus on adolescent populations as well as task-based fMRI methodology will help uncover to what extent adolescent network connectivity maturation facilitates behavioural and cognitive development [62]. A treatment implication is the potential usage of bupropion for the treatment of IA. Bupropion has been previously used to treat patients with gambling disorder and has been effective in decreasing overall gambling behaviour as well as money spent while gambling [67]. Bae et al. (2018) found a decrease in clinical symptoms of IA in line with a 12-week bupropion treatment [31]. The study found that bupropion altered the FC of both the DMN and ECN which in turn decreased impulsivity and attentional deficits for the individuals with IA [31]. Interventions like bupropion illustrate the importance of understanding the fundamental mechanisms that underlie disorders like IA.

Conclusion The goal for this review was to summarise the current literature on functional connectivity changes in adolescents with internet addiction. The findings answered the primary research questions that were directed at FC alterations within several networks of the adolescent brain and how that influenced their behaviour and development. Overall, the research demonstrated several wide-ranging effects that influenced the DMN, SN, ECN, and reward centres. Additionally, the findings gave ground to important details such as the maturation of the adolescent brain, the high prevalence of Asian originated studies, and the importance of task-based studies in this field. The process of making this review allowed for a thorough understanding IA and adolescent brain interactions. Given the influx of technology and media in the lives and education of children and adolescents, an increase in prevalence and focus on internet related behavioural changes is imperative towards future children/adolescent mental health. Events such as COVID-19 act to expose the consequences of extended internet usage on the development and lifestyle of specifically young people. While it is important for parents and older generations to be wary of these changes, it is important for them to develop a base understanding of the issue and not dismiss it as an all-bad or all-good scenario. Future research on IA will aim to better understand the causal relationship between IA and psychological symptoms that coincide with it. The current literature regarding functional connectivity changes in adolescents is limited and requires future studies to test with larger sample sizes, comorbid populations, and populations outside Far East Asia. This review aimed to demonstrate the inner workings of how IA alters the connection between the primary behavioural networks in the adolescent brain. Predictably, the present answers merely paint an unfinished picture that does not necessarily depict internet usage as overwhelmingly positive or negative. Alternatively, the research points towards emerging patterns that can direct individuals on the consequences of certain variables or risk factors. A clearer depiction of the mechanisms of IA would allow physicians to screen and treat the onset of IA more effectively. Clinically, this could be in the form of more streamlined and accurate sessions of CBT or family therapy, targeting key symptoms of IA. Alternatively clinicians could potentially prescribe treatment such as bupropion to target FC in certain regions of the brain. Furthermore, parental education on IA is another possible avenue of prevention from a public health standpoint. Parents who are aware of the early signs and onset of IA will more effectively handle screen time, impulsivity, and minimize the risk factors surrounding IA. Additionally, an increased attention towards internet related fMRI research is needed in the West, as mentioned previously. Despite cultural differences, Western countries may hold similarities to the eastern countries with a high prevalence of IA, like China and Korea, regarding the implications of the internet and IA. The increasing influence of the internet on the world may contribute to an overall increase in the global prevalence of IA. Nonetheless, the high saturation of eastern studies in this field should be replicated with a Western sample to determine if the same FC alterations occur. A growing interest in internet related research and education within the West will hopefully lead to the knowledge of healthier internet habits and coping strategies among parents with children and adolescents. Furthermore, IA research has the potential to become a crucial proxy for which to study adolescent brain maturation and development.

Acknowledgments The authors thank https://www.stockio.com/free-clipart/brain-01 (with attribution to Stockio.com); and https://www.rawpixel.com/image/6442258/png-sticker-vintage for the free images used to create Figs 2–4.

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[1] Url: https://journals.plos.org/mentalhealth/article?id=10.1371/journal.pmen.0000022

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