Short Term Exposure to a Violent Video Game InducesChanges in Frontolimbic Circuitry in Adolescents

Yang Wang & Vincent P. Mathews & Andrew J. Kalnin &

Kristine M. Mosier & David W. Dunn &

Andrew J. Saykin & William G. Kronenberger

Received: 16 September 2008 /Accepted: 18 December 2008 /Published online: 9 January 2009# Springer Science + Business Media, LLC 2009

Abstract Despite evidence of effects of violent video gameplay on behavior, the underlying neuronal mechanismsinvolved in these effects remain poorly understood. Wereport a functional MRI (fMRI) study during two modifiedStroop tasks performed immediately after playing a violentor nonviolent video game. Compared with the violent videogame group, the nonviolent video game group demonstrat-ed more activation in some regions of the prefrontal cortexduring the Counting Stroop task. In contrast to the violentvideo game group, significantly stronger functional con-nectivity between left dorsolateral prefrontal cortex(DLPFC) and anterior cingulate cortex (ACC) was identi-fied in the nonviolent video game group. During anEmotional Stroop task, the violent video game groupshowed more activity in the right amygdala and lessactivation in regions of the medial prefrontal cortex(MPFC). Furthermore, functional connectivity analysisrevealed the negative coupling between right amygdalaand MPFC in the nonviolent video game group. Bycontrast, no significant functional connectivity betweenright amygdala and MPFC was found in the violent videogame group. These results suggest differential engagementof neural circuitry in response to short term exposure to aviolent video game as compared to a nonviolent videogame.

Keywords Functional magnetic resonance imaging .

Prefrontal cortex . Amygdala . Video game .Media violence

Introduction

The relationship between media violence exposure andaggressive behavior has been the subject of social, political,and scientific attention for decades. There is considerableempirical evidence suggesting that media violence exposurehas effects on aggressive behavior, aggressive cognition,aggressive affect, physiological arousal, and adolescenthostility (Anderson 2004; Anderson and Bushman 2001,2002; Gentile et al. 2004; Kronenberger et al. 2005a;Kronenberger et al. 2005b; Sigurdsson et al. 2006).However, the mechanisms by which exposure to violentmedia increases aggressive behavior are still poorlyunderstood. One leading theory for the media violenceexposure-aggression relationship, the General AggressionModel (GAM) (Anderson and Bushman 2001; Carnagey etal. 2007a), proposes that repeated exposure to violent mediacan increase aggressive behavior by influencing aspects ofa person’s internal state such as arousal, cognition, andaffect. Although GAM has received empirical support incorrelational and experimental studies (Carnagey et al.2007a), knowledge about the underlying neural substrateremains elusive.

An emerging body of research has been conducted toidentify areas of brain functioning that may be affected bymedia violence exposure. Studies of neuroimaging andelectrophysiology have found links between abnormalfrontal or temporal lobe functioning and aggressive/violentbehavior (Anderson et al. 2006; Bartholow et al. 2006;Bufkin and Luttrell 2005; Mathews et al. 2005), althoughthese studies have relied on correlational methods which

Brain Imaging and Behavior (2009) 3:38–50DOI 10.1007/s11682-008-9058-8

Y. Wang (*) :V. P. Mathews :A. J. Kalnin :K. M. Mosier :A. J. SaykinDepartment of Radiology, Indiana University School of Medicine,950 W. Walnut St., R2 E124,Indianapolis, IN 46202, USAe-mail: ywang1@iupui.edu

D. W. Dunn :W. G. KronenbergerDepartment of Psychiatry, Indiana University School of Medicine,Indianapolis, IN 46202, USA

cannot fully account for potential confounding variables(Browne and Hamilton-Giachritsis 2005). It has beenproposed that impulsive aggression and violence may be aconsequence of dysfunction in the neural circuitry ofemotion regulation (Davidson et al. 2000). Research onthe neural circuitry of emotion regulation could suggestnew avenues of intervention for such at-risk populations(Davidson et al. 2000).

Functional neuroimaging studies illustrate that emotionregulation depends upon interactions between prefrontalcontrol systems and emotion-generative systems includingthe amygdala (Ochsner and Gross 2005). Cognition andemotion are intricately interrelated. Information associatedwith danger, for example, may be especially likely tocapture or engage attention (Compton 2003; Compton et al.2003). To evaluate areas of brain functioning associatedwith cognitive and emotional functions, researchers haveused a variant of the classic Stroop tasks, such as CountingStroop and Emotional Stroop tasks. The Counting Strooptask generates cognitive interference similar to the tradi-tional Stroop test, using numbers and counting in place ofreading and color-naming (Bush et al. 1999; Mathews et al.2005). Our previous study using a Counting Stroopparadigm found differences in prefrontal function relatedto past media violence exposure (Mathews et al. 2005). TheEmotional Stroop effect refers to the fact that latencies toname the ink colors of emotional words are typically longerthan latencies to name the ink colors of matched neutralwords (Compton et al. 2003; Mohanty et al. 2005; Phaf andKan 2007). The Emotional Stroop task has proved to be anexcellent tool for elucidating the nature of cognitiveprocessing of emotional information in various clinicaland subclinical populations (e.g., anxious individuals) inwhich the content of the emotion words matches theparticular concerns of the participant sample (Mohanty etal. 2005; Phaf and Kan 2007). One behavioral study usingthe Emotional Stroop task found that violent video gameplayers showed greater emotional interference than nonvi-olent game players (Kirsh et al. 2005). Again, little isknown about the underlying psychological and neuralmechanisms associated with these findings.

A recent functional MRI (fMRI) study found that short-term viewing of televised violence recruits a network ofbrain regions involved in the regulation of emotion, arousal,and attention (Murray et al. 2006). Another fMRI reportobserved increased activation of the dorsal anterior cingu-late cortex (ACC) and reduced activation of the amygdalaregion during play of a first person shooting game (Mathiakand Weber 2006). In response to tailored violent videogame stimuli, fMRI demonstrated activation in severalareas including the ventromedial prefrontal cortex andamygdala (King et al. 2006). However, these fMRI reportsdiffered in methodological details that may account for the

apparently discrepant findings. Furthermore, these studiesinvestigated brain activation during violent game play, asopposed to following game play. It is unclear whether theseeffects persist beyond the immediate exposure and whetherthere are specific changes suggesting functional adaptationto violent stimuli. It is possible that activation followinggame play will differ from that observed during game play.

To better understand the causal effects of mediaviolence, attention has been devoted to experimentalstudies. After random assignment to two groups playingeither a violent or nonviolent game for 10–20 min, twostudies found that violent video game playing subjectsendorsed aggressive thoughts and behaved more aggres-sively (Bartholow et al. 2005; Uhlmann and Swanson2004). These findings demonstrated a short term behavioreffect of violent video game play, and also highlight theusefulness of experimental design for such research. In thepresent study, we used an experimental design with randomassignment of subjects, in order to investigate the shortterm neurocognitive effects of exposure to violent vs.nonviolent video games, using established fMRI probetests. Immediately after playing a violent or nonviolentvideo game for 30 min, fMRI data were acquired during aCounting Stroop task and an Emotional Stroop task. Wetested the hypothesis that brief exposure to violent videogame play induces short term alterations in brain function-ing as compared to exposure to nonviolent video gameplay, specifically in the prefrontal cortex and amygdala,regions associated with executive control and affectiveregulation.

Materials and methods

All subjects (age 13–17) were screened with a basic set of theDSM-IV criteria using the Adolescent Symptom Inventory-4(Gadow and Sprafkin 1998). Subject exclusion criteriaincluded a history of neurologic or psychiatric disorders(including history of significant aggressive outbursts). Thestudy was approved by the local Institutional Review Board,and written informed consent was obtained from subjectsand their parents. A total of 44 adolescents were included inthis report, 22 per group playing a nonviolent or violentvideo game. These two groups did not differ significantly onage (15.0±1.1 vs. 14.8±1.2), IQ (110±13 vs. 108±7), orgender (male/female, 15/7 vs. 18/4) (p>0.05).

Experimental procedures

The experimental procedure consisted of two study visits.The first visit involved consent, administration of psycho-logical tests, and training in the assigned video game.Subjects and parents completed the Media Exposure

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Measure (MEM) (Kronenberger et al., 2005a), a semi-structured interview (completed by the adolescent) andquestionnaire (completed by the parent) measure of theadolescent’s television viewing and video game playinghabits over the past week and year. MEM scores areaggregated into a single variable reflecting total mediaviolence exposure. Subjects were then randomly assignedand taught to play one of two video games: Need for Speed(NfS, an exciting, nonviolent car driving video game) orMedal of Honor (MoH, a violent first-person shootergame). Adolescents spent approximately 30 min learningand practicing the assigned game during the first visit sothat they would have sufficient proficiency to playindependently during the second visit, prior to the fMRI.At the end of video game practice, subjects completed theVideo Game Rating Index (VRI), a brief questionnaireconsisting of 13 items asking about characteristics of theassigned video game such as familiarity, excitement, fun,difficulty, experience, expertise, and violence, as well asexperience and expertise with video games in general.Within 4 weeks of the first visit, subjects attended a secondstudy visit for the fMRI procedure. After training for thefMRI tasks, every subject played the assigned video game(NfS or MoH) for 30 min, immediately (within 10 min)before the fMRI scan.

fMRI procedure

Imaging data were acquired on a 3T Siemens Trio MRscanner equipped with an 8 channel head coil (Siemens,Erlangen, Germany). Immediately after localizer andhigher-order shimming, functional scanning was conductedusing a T2* weighted 2D gradient-echo echo planarsequence with parameters: TR/TE=2,000/30 ms; thirty-three contiguous axial slices with isotropic voxel size of3.5 mm. Three-dimensional high resolution magnetizationprepared rapid gradient echo (MPRAGE) images wereacquired after functional scans for each subject to serve asan anatomical reference. Head immobilization was estab-lished by foam pads within the head coil.

Two Stroop variant tasks were designed in an event-related manner and consisted of incongruent and congruentconditions. The Counting Stroop task required subjects topress one of three buttons to indicate the number ofdisplayed objects. X’s in groups of 1, 2 or 3 X’s werepresented as congruent events. For incongruent events, oneto three identical numerals were shown, in which thenumerals did not correspond to the number of numerals inthe group, e.g. 3, 11, 222. Every stimulus was presented for800 ms. There were 120 trials for each condition, jittered ina pseudorandom order. The interstimulus interval (ISI)ranged from 1,200 ms to 11,200 ms, with a mean ISI of4,400 ms. During the Emotional Stroop task, subjects were

instructed to press one of three different buttons to indentifythe ink color of the visually presented word. Wordsindicating violent actions (e.g. hit, harm) were interspersedamong the non-violent action words (e.g. run, walk) in apseudorandom order. Each word was presented for1,600 ms. ISI ranged from 400 ms to 14,400 ms, withaverage of 2,400 ms. A total of 40 violent and 40nonviolent words were generated based on a review ofreferences in various thesauruses and texts. All words wereverbs. There was no difference between two word lists forword usage (p=0.82), but as intended the lists differedmarkedly for ratings of violence/aggression (p<0.001).Colors (red, green, or blue) were randomly assigned towords, such that each color occurred at the same frequencyin each word list.

Data analysis

All statistical analyses of behavioral data were carried outusing SPSS 14.0 for Windows (SPSS Inc., Chicago, IL).Based on a larger sample of 100 adolescents participating inmedia violence studies (which included the 44 subjects inthe present study), principal components analysis withPromax rotation of components with eigenvalues > 1 wasapplied to the Video Game Rating Index (VRI) to derivefour subscales: Interest/Fun/Challenge, Violence, SpecificGame Expertise, and General Game Expertise (detailedresults of this analysis are available from the authors). Thereaction time during fMRI tasks was analyzed using amixed two-way analysis of variance (ANOVA) with onebetween group factor (nonviolent game vs. violent game)and one within subject factor (incongruent vs. congruentcondition for the Counting Stroop task and violent vs.nonviolent words for the Emotional Stroop task). Theaveraged Stroop interference time was calculated as thedifference in reaction time (in milliseconds) betweenconditions for each task. Paired samples t-test was appliedfor comparison of reaction time between conditions withineach group. The response accuracy was analyzed nonpara-metrically employing the Mann-Whitney U test for testingdifferences in both Stroop tasks between groups and withthe Wilcoxon test for differences between conditions.

Imaging data were analyzed using the AFNI softwarepackage (Cox 1996) (Robert Cox, National Institute forMental Health, Bethesda, MD). Following image recon-struction, the first eight volumes of each functional scanwere discarded from subsequent analyses to allow the MRsignal to reach steady state. All time-series data wereslice-timing corrected and motion-corrected using 3Dvolume registration least-squares alignment of threetranslational and three rotational parameters. Spatialsmoothing of functional data was conducted using FWHMof 5 mm. The estimation of the impulse response function

40 Brain Imaging and Behavior (2009) 3:38–50

(IRF) for each voxel was performed using a deconvolutiontechnique (Glover 1999). Using multiple regressiontechniques (with nuisance motion regressors included),this procedure calculates the IRF (i.e., the average best-fitting “shape”) that follows each event. The area underthe IRF curve was converted into percent signal changesfrom the baseline and was used as an index ofhemodynamic response for each type of event. Ageneral linear test was performed to create individualfunctional maps of each condition compared to thebaseline, as well as contrast maps between twoconditions for each task. Each subject’s functional mapswere coregistered to the anatomical imaging, thenspatially normalized into the Talairach stereotaxiccoordinate system with isotropic voxel size of 2 mm(Talairach and Tournoux 1988). Using MEM and generalvideo game experience / expertise scores as covariates,mixed-effect model ANCOVA (group as fixed effect,subject as random effect) was performed. To calculatethe significance level, Monte Carlo simulations were runto estimate the likelihood of detecting false positives overmultiple comparisons. It was determined that an individualvoxel threshold of p<0.05 and a minimum cluster sizethreshold of 25 voxels provided a corrected overall alphaof p<0.05 (Forman et al. 1995). Due to the specific natureof our research question regarding the response ofamygdala during the Emotional Stroop task, we conducteda small volume correction (Worsley et al. 2002) in theamygdala region based upon the Talairach atlas labelsimplemented in AFNI (Lancaster et al. 2000). The smallvolume correction resulted in a cluster size threshold of 5voxels in this region, rather than the 25 required whenconsidering the entire brain.

Functional connectivity was assessed using psycho-physiological interaction (PPI) analysis, evaluating howregional network activity covaries in relation to a sourceregion during task performance (Foland et al. 2008;Gitelman et al. 2003; Williams et al. 2006). Seed regionswere delineated as 6-mm sphere radius around the peak ingroup difference fMRI activation maps within the leftdorsolateral prefrontal cortex (DLPFC) for CountingStroop task and within the right amygdala for EmotionalStroop task, respectively. First, the drift effect wasextracted from time series using AFNI 3dSynthesize, andthen the temporal trend was removed. After that, averagedtime series of each seed region were deconvolved with agamma variant model to generate the first regressor for thePPI analysis (Gitelman et al. 2003). A general linearmodel was then constructed for each subject using threeregressors: (1) the physiological variable, represented bythe deconvolved bold signal from the seed region, (2) thepsychological variable, represented by the task conditiontype encoding and (3) the interaction term between the

first and the second regressor. Contrasts for this interactionterm revealed brain regions considered to covary as afunctional network with the seed region for each individ-ual subject (Gitelman et al. 2003; Williams et al. 2006).These subsequent connectivity contrasts were then takenthrough to a group based, mixed-effect model ANCOVA,as described above.

Results

Behavioral findings

The MEM total score indicating past violent media exposurewas not significantly different between the nonviolent andviolent video game groups [−1.25±2.81 vs. −0.14±2.25, F(1,42)=2.092, p=0.16]. Additionally, no significant differenceswere found in ratings between the violent game (MoH) vs.the nonviolent video game (NfS) groups on the VRI in termsof interest, fun, and challenge [23.59±4.56 vs. 24.36±4.10,F(1,42)=0.349, p=0.56]. As expected, the MoH game wasrated significantly higher than NfS in terms of violence[9.13±1.08 vs. 2.91±1.23, F(1,42)=317.606, p=3.38e−21]on the VRI. Although both groups of players had equivalentVRI-rated specific expertise with their assigned video game[5.50±1.90 vs. 5.59±1.65, F(1,42)=0.029, p=0.87], subjectswho had just finished playing the violent game rated theirgeneral expertise with video games as slightly but notsignificantly higher than subjects who played the nonviolentvideo game [12.59±2.97 vs. 11.09±2.72, F(1,42)=3.029,p=0.09]. Although it is possible that this latter finding wasdue to chance (especially in light of the lack of difference inpast media violence exposure between groups on the MEM),it may be the case that violent game play increased the senseof competitiveness and efficacy, causing individuals in theviolent game play group to inflate their general video gamecompetence and experience. To account for this possibilityand to rule out the potential confounding effects of long termviolent media exposure in the past, MEM scores and VRIgeneral video game expertise scores were applied ascovariates in further image analyses.

Task performance

The two-way ANOVA revealed a significant main effect ofcondition on reaction time in both Stroop tasks [CountingStroop task: F(1,42)=84.6, p=12.78E-11; Emotional Strooptask: F(1,42)=11.3, p=0.0016], indicating an interferenceeffect (represented as slower performance) in the incongru-ent condition for the Counting Stroop task and also in theviolent words condition for the Emotional Stroop (seeTables 1 and 2). The difference in reaction time betweenconditions was calculated as the Stroop interference time.

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Both groups showed significant Counting Stroop interfer-ence time (p<0.001) but no difference between groups wasevident [F(1,42)=0.067, p=0.80]. Despite the comparableinterference reaction time elicited by the Counting Strooptask in both groups, the violent game group demonstrated atrend toward less accurate performance on the CountingStroop task in both congruent and incongruent conditions(p=0.06 and p=0.08 respectively; Table 1).

A statistically significant Emotional Stroop interfer-ence time was found only for violent video gameplayers [t(1,21)=−2.928, p<0.01], whereas nonviolentvideo game players demonstrated a similar trend [t(1,21)=−1.806, p=0.08]. The difference between groupswas not significant [F(1,42)=0.813, p=0.37]. The in-creased latency in the violent word task of the EmotionalStroop indicates that it took longer to ignore taskirrelevant violent distracters, as noted previously in otherEmotional Stroop studies (Compton et al. 2003; Etkin etal. 2006; Phaf and Kan 2007). Although violent gameplayers responded more slowly to violent words than tononviolent words, comparable performance accuracy wasobserved in both the violent and nonviolent wordsconditions (Z=−0.98, p=0.33) in the violent video gamegroup. By contrast, nonviolent game subjects performedless accurately processing violent words compared tononviolent words (Z=−2.43, p=0.016).

Functional MRI findings

To identify differences in brain activation after short termviolent vs. nonviolent video game play, we first examinedactivity within each group separately for each task, and thenwe contrasted these neural activation patterns between thetwo groups for each task. To determine whether adifferential network of regional connectivity emerged as aconsequence of these changes in fMRI activation, wefurther identified brain areas showing significant functionalconnectivity with key regions revealed from task activation.

Counting Stroop task

Comparing the incongruent condition to the congruentcondition, the nonviolent video game group demonstratedactivation in the anterior cingulate cortex (ACC) thatextended into pre-supplementary motor area (pre-SMA),right pre-motor area, bilateral dorsolateral prefrontal cortex(DLPFC), bilateral ventrolateral prefrontal cortex (VLPFC)and inferior parietal lobule (IPL) (p<0.05, corrected), asshown in Fig. 1 and summarized in Table 3. The violentvideo game group showed activation in the ACC, pre-SMA, bilateral DLPFC, left VLPFC and left IPL (p<0.05,corrected). Overall, the nonviolent video game group hadmore activation in the prefrontal cortex area than the violent

Table 1 Counting Stroop task performance

Reaction Time (ms) Response Accuracy Rate (%)

CongruentCondition

IncongruentCondition

withingroup

CongruentCondition

IncongruentCondition

Withingroup

Nonviolent GameGroup

640.4±76.4 670.1±81.4 P<0.001* 94.5±6.3 89.0±7.1 P<0.001*

Violent Game Group 629.7±63.6 661.1±69.0 P<0.001* 91.2±6.9 83.6±10.9 P<0.001*Between groups P=0.61 P=0.69 P=0.06 P=0.08

Results are presented as mean ± standard deviations in the table. For both nonviolent and violent game groups, reaction time was significantlylonger in incongruent condition than congruent condition, while response accuracy rate was much less in incongruent condition. Violent gamegroup demonstrated less response accuracy in both congruent and incongruent conditions. There were no statistically significant differencesbetween groups while differences between conditions were significant within both groups.* indicates significant difference (p<0.05)

Table 2 Emotional Stroop task performance

Reaction Time (ms) Response Accuracy Rate (%)

Nonviolent Words Violent Words within group Nonviolent Words Violent Words Within group

Nonviolent Game Group 734.8±123.5 748.3±126. P=0.08 96.2±4.1 94.4±4.3 P<0.05*Violent Game Group 722.0±94.1 745.2±108.1 P<0.01* 94.5±5.2 93.8±4.6 P=0.33between groups P=0.70 P=0.93 P=0.20 P=0.60

Results are presented as mean ± standard deviations in the table. For both nonviolent and violent game groups, reaction time was longer forviolent words than nonviolent words, while response accuracy rate was less for the violent words than nonviolent words. There were nostatistically significant differences between groups. * indicated significant difference (p<0.05)

42 Brain Imaging and Behavior (2009) 3:38–50

video game group. In the direct comparison betweengroups, the nonviolent video game group showed signifi-cantly more activation (p<0.05, corrected), mainly in theleft DLPFC (Fig. 1 and Fig. 2), as well as in pre-SMA, rightpre-motor area, and also in right IPL. Our previous studyshowed abnormal activity in left DLPFC and ACCassociated with long term high media violence exposure(Mathews et al. 2005). Thus, the peak region of groupdifference within the left DLPFC was selected as the seedregion for functional connectivity analysis. Relative to theviolent game group, significantly stronger functionalcoupling was identified in the nonviolent game groupbetween left DLPFC and dorsal ACC (p<0.05, corrected)(Fig. 1 and Table 4). These regions are important inimplementation and top down modulation of behavioralresponses (Botvinick et al. 2004; Cole and Schneider2007). The nonviolent game group also demonstratedsignificantly more negative connectivity between the left

DLPFC and right IPL and right lingual gyrus, while theviolent game group demonstrated more negative connec-tivity with the left striatum.

Emotional Stroop task

Comparing the violent word condition to the nonviolentword condition, nonviolent video game playing subjectsdemonstrated increased activations in the medial prefrontalcortex (MPFC), left VLPFC, left middle temporal gyrus,precuneus and cuneus, and right lingual gyrus (p<0.05,corrected), as depicted in Fig. 3 and Table 5. By contrast,violent video game players demonstrated increasedactivation in the bilateral VLPFC, right amygdala andright lingual gyrus (p<0.05, corrected). Whereas violentwords elicited significant activation in the right amygdalaand right VLPFC in the violent video game group,deactivation in the right amygdala was observed in

Fig. 1 fMRI regions of significant activation and functional connectivity during the Counting Stroop task (Note: G0 = nonviolent video gamegroup; G1 = violent video game group, DLPFC = dorsolateral prefrontal cortex)

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nonviolent video game group (Fig. 4a, b). In the directcontrast between groups, the violent video game playingsubjects demonstrated significantly greater activation inthe right amygdala (p<0.05, corrected). Although thenonviolent game players showed several regions ofactivation during the Emotional Stroop task, no differ-ences were found between video game groups in thoseregions using a threshold of p<0.05 (corrected). Since theamygdala is believed to play a crucial role in theinteraction and integration of cognitive affective processes(Phelps 2006) and the video game groups demonstratedopposite responses in right amygdala activation, weselected the peak region of group difference in the rightamygdala as the source region for further connectivityanalysis. Nonviolent game playing subjects demonstratedsignificant negative connectivity with the MPFC andpositive connectivity with dorsal ACC (Fig. 3 and Table 6)(p<0.05, corrected), which are akin to previously reportedconnections in amygdala pathways associated with con-scious fear (Williams et al., 2006). The nonviolent gamegroup also showed significantly more positive connectiv-ity with right DLPFC, right superior temporal gyrus(STG), cuneus and precuneus. In contrast, only signifi-cantly more positive connectivity with left VLPFC wasevident in the violent game group.

Fig. 2 Group average impulse response functions of left DLPFCduring the Counting Stroop task. Both groups showed similarresponse patterns to incongruent stimuli relative to the congruentstimuli, while the nonviolent video game group demonstrated higherresponse amplitude compared with the violent video game group.(Note: DLPFC = dorsolateral prefrontal cortex; G0 = Nonviolentvideo game group; G1 = Violent video game group; ON = Responseto incongruent stimuli; OFF = Response to congruent stimuli)

Table 3 Regions of significant fMRI activation of the Counting Stroop task

Contrast Region (BA) Talairachcoordinate

Z-score

Cluster size(mm3)

X Y Z

Nonviolent Game Group (ON>OFF ) ACC (32/24) 1 9 39 3.557 3,440pre-SMA (6) 8 −2 56 4.412 5,088L. DLPFC (9/46) −38 40 25 4.193 5,808L. VLPFC (44/45)

−46 7 23 3.334 2,856

L. IPL (40) −40 −43 40 3.938 7,040R. DLPFC (9/46) 34 45 28 3.539 2,648R. VLPFC (44) 48 8 19 3.174 2,160R. pre-motor (6) 21 −3 55 4.077 3,464R. IPL (40) 39 −45 43 3.683 3,064

Violent Game Group (ON>OFF ) ACC (32/24) −1 14 34 3.283 3,688pre-SMA (6) −3 4 51 3.156 2,008L. DLPFC (9/46) −40 21 26 3.815 3,280L. VLPFC (44/45)

−42 4 25 3.772 1,944

L. IPL (40) −34 −50 40 4.145 5,744R. DLPFC (9/46) 39 31 21 3.162 2,016

Nonviolent Game Group (ON>OFF ) vs. Violent Game Group(ON>OFF)

pre-SMA (6) 8 −8 58 2.852 1,256L. DLPFC (9) −36 42 27 4.596 2,392R. pre-motor (6) 21 0 54 3.629 1,272R. IPL (40) 58 −33 24 3.511 1,968

ON incongruent condition, OFF congruent condition, BA Brodmann’s area, L left side, R right side, ACC anterior cingulate cortex, pre-SMA pre-supplementary motor area, DLPFC dorsolateral prefrontal cortex, VLPFC ventrolateral prefrontal cortex, IPL inferior parietal lobule

44 Brain Imaging and Behavior (2009) 3:38–50

Discussion

Video games have become one of the favorite activities ofAmerican children and adolescents. According to a 2004survey (Roberts and Henry 2005), children ages 8–18 spenton average between 14–49 min a day playing video games.Violent video games can increase the likelihood ofaggressive and violent behavior in both short– and long–term contexts (Anderson 2004; Anderson and Dill 2000;Bartholow et al. 2006; Bartholow et al. 2005; Browne andHamilton-Giachritsis 2005; Bushman and Huesmann 2006;Carnagey et al. 2007b; Funk et al. 2004; Gentile et al. 2004;Sigurdsson et al. 2006; Uhlmann and Swanson 2004). Tothe best of our knowledge, this is the first fMRI study usingrandom assignment and an experimental design to investi-gate effects immediately after short-term violent videogame play on neural functioning, as opposed to behavioralor psychological changes. Because of random assignmentand experimental control, differences in brain functionbetween groups (playing violent or nonviolent videogames) can be attributed to the experimental condition(type of video game played).

Our previous study demonstrated a relationshipbetween executive dysfunction and violent media expo-sure, using correlational methods (Kronenberger et al.2005a; Mathews et al. 2005). In the present study, violentvideo game players compared to nonviolent video gameplayers showed reduced activity in some regions of the

prefrontal cortex, specifically in the left DLPFC, as wellas less functional connectivity between left DLPFC anddorsal ACC. These prefrontal regions have been reportedas key components recruited during executive and cogni-tive control processing, such as selective attention andresponse inhibition (Botvinick et al. 2004; Cole andSchneider 2007). The present research advances previousfindings by using a prospective, experimental design todemonstrate functional changes in the prefrontal regionduring a Counting Stroop task following short-termviolent vs. nonviolent video game play.

We found a differential pattern of activation andfunctional connectivity during the Emotional Stroop taskbetween violent and nonviolent video game players.Deactivation of the amygdala in the nonviolent video gamegroup during the Emotional Stroop task may reflect amechanism of emotional regulation, in which cognitiveprocessing, including prefrontal engagement, regulatessubstrates of emotions. This is consistent with a previousreport using an Emotional Stroop task with negative wordsin normal subjects (Compton et al. 2003). The greater rightamygdala activation in the violent game group shares somesimilarities with results from psychiatric patients complet-ing an Emotional Stroop task (Mohanty et al. 2005), whichmay suggest a mechanism for dysregulation in the face ofaversive stimuli (Davidson et al. 2000). The role of theright amygdala in negative emotion regulation is alsosupported in part by lesion studies (Adolphs et al. 2001).

Table 4 Regions found to be functionally connected with the response of the left DLPFC during the Counting Stroop task

Region (BA) Talairach coordinate Z-score Cluster size (mm3)

X Y Z

Positive functional connectivityNonviolent Game Group Dorsal ACC (24) 5 −7 38 3.068 1,080

L. STG (38) −39 8 −19 3.710 2,744Violent Game Group L. MTG (21) −61 −41 −9 3.643 1,920

L. Angular gyrus (39) −38 −62 29 3.705 1,264R. Precentral gyrus (1) 55 −17 44 3.264 3,504

Nonviolent Game Group vs. Violent Game Group Dorsal ACC (24) 4 −4 36 3.288 1,304Violent Game Group vs. Nonviolent Game Group L. MTG (21) −62 −38 −5 3.284 1,192

R. Precentral gyrus (1) 50 −4 46 3.067 1,304Negative functional connectivityNonviolent Game Group R. IPL (40/39) 37 −67 36 2.617 1,432

R. Lingual gyrus (18) 17 −85 −10 4.357 2,016Violent Game Group L. pre-motor (6) −43 −8 45 3.232 2,680

L. Striatum −18 7 5 2.883 2,000R. Lingual gyrus (18) 9 −80 −3 2.95 1,088

Nonviolent Game Group vs. Violent Game Group R. IPL (40) 51 −48 43 3.086 1,928R. Lingual gyrus (18) 17 −88 −10 4.297 1,240

Violent Game Group vs. Nonviolent Game Group L. Striatum −17 6 8 3.663 3,640

BA Brodmann’s area, L left side, R right side, ACC anterior cingulate cortex, STG superior temporal gyrus, MTG middle temporal gyrus, IPLinferior parietal lobule

Brain Imaging and Behavior (2009) 3:38–50 4545

Table 5 Regions of significant fMRI activation of the Emotional Stroop task

Contrast Region (BA) Talairachcoordinate

Z-score

Cluster size (mm3)

X Y Z

Nonviolent Game Group (VW > NVW ) MPFC (9/32) 5 46 25 2.775 1,216L. VLPFC (45/47) −46 22 6 4.087 2,720L. MTG (21) −52 −22 −6 3.504 3,376Precuneus (7) −1 −65 37 3.010 1,768Cuneus (17/18) −3 −88 21 3.586 1,544R. Lingual gyrus (18) 14 −73 −6 3.214 1,472

Violent Game Group (VW > NVW) L. VLPFC (44/45) −40 11 22 2.820 2,168R. VLPFC (47) 47 23 −3 2.941 3,544R. Amygdala 24 −5 −16 3.400 920*R. Lingual gyrus (18) 23 −89 2 3.058 2,744

Violent Game Group (VW > NVW) vs. Nonviolent Game Group(VW > NVW)

R. Amygdala 22 −6 −20 2.829 296*R. Lingual gyrus (18) 33 −87 −3 3.195 1,552

VW violent words stimuli, NVW nonviolent words stimuli, BA Brodmann’s area, L left side, R right side, MPFC medial prefrontal cortex, VLPFCventrolateral prefrontal cortex, MTG middle temporal gyrusThe symbol (*) indicates that this cluster was indentified through a small volume correction

Fig. 3 fMRI regions of significant activation and functional connectivity during the Emotional Stroop task (Note: G0 = nonviolent video gamegroup; G1 = violent video game group)

46 Brain Imaging and Behavior (2009) 3:38–50

Furthermore, metabolism has been found to be significantlyelevated in the right amygdala region in impulsiveaggressive individuals (Raine et al. 1997). The role of theprefrontal cortex in the regulation of emotion is wellestablished (Northoff et al. 2004; Quirk and Beer 2006).The MPFC has been characterized as important in thegeneral processing of emotion (Phan et al. 2002). There is

evidence suggesting the existence of a medial inhibitorysystem capable of controlling amygdala responsiveness andexpression of negative emotion (Northoff et al. 2004; Quirkand Beer 2006; Williams et al. 2006). The MPFC isengaged when an individual must select between taskrelevant responses and emotion-based action preparation asin the Emotional Stroop task (Compton et al. 2003). In thepresent study, the significant activation of MPFC, couplednegatively with activity in the right amygdala, as demon-strated in the Emotional Stroop task by nonviolent gameplayers, is consistent with the notion that MPFC plays acrucial role in emotional conflict monitoring and is alsoinvolved in top-down inhibition of amygdala activity inresolution of emotional conflict during the EmotionalStroop task (Etkin et al. 2006; Williams et al. 2006).Reduced amygdala-MPFC coupling is also associated withanxiety and related arousal states, which are commonlyseen in individuals following violence exposure (Andersonet al. 2003). On the other hand, the right VLPFC activity inviolent video game playing individuals in this study may beconsistent with a greater effort to inhibit strongly interferingemotional stimuli in an effort to achieve normal behavioralperformance. Activation in this region has been produced innegative high arousal versus negative low-arousal words inthe Emotional Stroop task (Compton et al. 2003), negative-neutral word subtraction (Kuchinke et al. 2005), or viewingsad films (Goldin et al. 2005). Studies that have specificallyassociated the right VLPFC with the inhibition of negativeemotions suggest that greater activity in this region reflectsenhanced inhibitory processes engaged to control theimpact of distracting negative emotions (Dolcos andMcCarthy 2006; Ochsner et al. 2004).

Despite the considerable differences between the contentof the Counting Stroop and the Emotional Stroop tasks,common left prefrontal activation was found in both tasks.This is likely due to attentional demands, in view of the factthat both tasks involve selective attention while suppressingresponse to distracting task irrelevant information. Ourresults are in concert with evidence that the left lateralprefrontal cortex is involved in maintaining attentional setin the Stroop task whether or not the challenging task-irrelevant information is emotional (Brass and von Cramon2004; Compton 2003; Compton et al. 2003).

It is important to place the findings of this study in thecontext of findings from behavioral studies of mediaviolence exposure and aggressive behavior in children andadolescents. The psychological processes that may linkchildren’s exposure to violence with subsequent increasesin children’s aggressive behaviors can be divided into thosethat produce more immediate short term effects and thosethat produce more delayed long term effects (Bushman andHuesmann 2006). The potential short-term effects ofexposure to violent video games are thought to include

Fig. 4 Group average impulse response functions of the rightamygdala during the Emotional Stroop task a and group averagepercent signal change of the right amygdala during nonviolent wordand violent word conditions in the Emotional Stroop task b. Only theviolent video game group demonstrated pronounced positive impulseresponse to violent words. Conversely, the nonviolent video gamegroup showed decreased activation responding to violent words in theright amygdala relative to nonviolent words. (Note: R–Amygdala =Right Amygdala; G0 = Nonviolent video game group; G1 = Violentvideo game group; ON = Response to violent words; OFF = Responseto nonviolent words)

Brain Imaging and Behavior (2009) 3:38–50 4747

increases in emotional arousal stimulated by the observa-tion of violence, coupled with disinhibition of controls overaggressive behavioral responses (Bushman and Huesmann2006). The present results provide evidence consistent withthis interpretation by showing that short-term violent videogame play evokes increased activity in brain regionsassociated with arousal, anxiety, and emotional reactivity,as well as decreased activation in prefrontal regionsassociated with emotion regulation and executive control.

The long-term effects of exposure to media violence arethought to include desensitization, in the form of a“reduction in distress-related physiological reactivity toobservations or thoughts of violence” (Anderson 2003).This reduction in physiological reactivity/arousal occurs asa result of repeated exposure to violence, which initially (inthe short-term) causes significant arousal that is graduallyattenuated as time, duration, and frequency of violenceexposure increases. In other words, the initial (short-term)increase in arousal is a precondition for eventual desensi-tization following repeated (long-term) exposure. Althoughthe present study addressed only the issue of increasedarousal after short-term exposure to video game violence,one hypothesis for sustained/long-term effects of violentvideo game play is that people become desensitized toviolence after prolonged exposure to it, leading to reductionof normal inhibition against aggression and makingindividuals less responsive to the pain and suffering

experienced by victims of violence (Bartholow et al.2005; Bushman and Huesmann 2006; Carnagey et al.2007b; Funk et al. 2004). Although our findings held evenafter controlling for prior (long term) media violenceexposure and general experience with video games, thisstudy focused on short-term effects of violent video gameplay, and we did not directly examine long-term/sustainedeffects.

In addition to investigating long-term/sustained effectsof violent video game play on brain functioning, futureresearch should address potential moderating factors forshort-term and long-term effects of video game violenceexposure. These include underlying personality, genetic,and experiential characteristics of individuals, which mayattenuate or exacerbate media violence effects (Bushman1995). Additionally, gender differences in media violenceexposure type and effects should receive additional atten-tion. Our study did not address gender differences (whichcan affect video game preferences, video game experience,and fMRI results), and (like most video game studies) oursample was largely male. Hence, while the current study isan essential first-step in demonstrating short-term effects ofvideo game violence on brain functioning, additionalresearch is needed to better understand the specifics ofthese effects.

Our current study extends recent media violence expo-sure findings by demonstrating differential activation in

Table 6 Regions found to be functionally connected with the response of the right amygdala during the Emotional Stroop task

Region (BA) Talairach coordinate Z-score Cluster size (mm3)

X Y Z

Positive functional connectivityNonviolent Game Group ACC (32) 6 12 42 3.937 1,600

R. DLPFC (9) 32 21 38 3.149 1,464R. STG (39) 45 −52 13 3.266 1,104Precuneus (7) 9 −61 31 3.036 3,576Cuneus (7/31) −13 −63 24 2.999 1,568

Violent Game Group L. VLPFC (44/45) −46 12 20 3.843 2,736Nonviolent Game Group vs. Violent Game Group ACC (32) 12 16 35 3.534 1,328

R. DLPFC (9) 31 22 37 3.146 1,584R. STG (39) 46 −53 14 4.071 1,656Precuneus (7) 10 −55 26 3.608 4,304Cuneus (7/31) −12 −61 22 3.224 1,136

Violent Game Group vs. Nonviolent Game Group L. VLPFC (44/45) −44 10 26 4.219 2,736Negative functional connectivityNonviolent Game Group MPFG (9) −4 47 24 3.481 1,336

L. DLPFC (9) −45 6 43 3.404 1,336L. Lingual gyrus (18/17) −3 −86 5 3.819 3,368

Violent Game Group L. Lingual gyrus (18/17) −5 −63 12 3.143 3,088Nonviolent Game Group vs. Violent Game Group MPFG (9) −12 48 25 3.145 2,160

BA Brodmann’s area, L left side, R right side, ACC anterior cingulate cortex, DLPFC dorsolateral prefrontal cortex, STG superior temporal gyrus,VLPFC ventrolateral prefrontal cortex, MPFC medial prefrontal cortex

48 Brain Imaging and Behavior (2009) 3:38–50

brain areas associated with executive function and emotionregulation following violent vs. nonviolent video game playin a controlled experimental setting. It will be important toreplicate these findings using a longitudinal design tofurther determine if this effect extends to long-term differ-ences in brain activation.

Acknowledgements This work was supported by a grant from theCenter for Successful Parenting, Carmel, Indiana.

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