|Gi Jung Hyun1;Yong Wook Shin2;Bung-Nyun Kim3;Jae Hoon Cheong4;Seong Nam Jin1; and Doug Hyun Han1;
1;Department of Psychiatry, Chung Ang University Hospital, Seoul,
2;Department of Psychiatry, ASAN Medical Center, University of Ulsan College of Medicine, Seoul,
3;Department of Psychiatry, Seoul National University College of Medicine, Seoul,
4;Uimyung Research Institute for Neurosciecne, Samyook University, Seoul, Republic of Korea
The bulk of recent studies have tested whether video games change the brain in terms of activity and cortical volume. However, such studies are limited by several factors including cross-sectional comparisons, co-morbidity, and short-term follow-up periods. In the present study, we hypothesized that cognitive flexibility and the volume of brain cortex would be correlated with the career length of on-line pro-gamers.
Methods : High-resolution magnetic resonance scans were acquired in twenty-three pro-gamers recruited from StarCraft pro-game teams. We measured cortical thickness in each individual using FreeSurfer and the cortical thickness was correlated with the career length and the performance of the pro-gamers.
Results : Career length was positively correlated with cortical thickness in three brain regions: right superior frontal gyrus, right superior parietal gyrus, and right precentral gyrus. Additionally, increased cortical thickness in the prefrontal cortex was correlated with winning rates of the pro-game league. Increased cortical thickness in the prefrontal and parietal cortices was also associated with higher performance of Wisconsin Card Sorting Test.
Conclusion : Our results suggest that in individuals without pathologic conditions, regular, long-term playing of on-line games is associated with volume changes in the prefrontal and parietal cortices, which are associated with cognitive flexibility.
On-line game;Cortical thickness;Frontal cortex;Cognitive flexibility.
Correspondence: Doug Hyun Han, MD, PhD, Department of Psychiatry, Chung Ang University Hospital, 102 Heukseok-ro, Dongjak-gu, Seoul 156-755, Republic of Korea
Tel: +82-2-6299-3132, Fax: +82-2-6299-1114, E-mail: email@example.com
ㅔRecent studies have examined whether video games change the brain in terms of activity and cortical volumes.1,2,3 Erickson et al.1 have reported that dorsal striatal volume predicts the level of accomplishment achieved in video games in healthy volunteers. Hubert-Wallander et al.2 and Lee et al.3 have also suggested that visual attention training using video games leads to improvement in brain activation of prefrontal cortex and visuo-spatial attention in individuals with playing game. Further, Zhou et al.4 have reported that adolescents with internet addictions have less gray matter volume in the cingulate gyrus compared to healthy controls. However, there are several limitations in interpreting these results including comorbidity in the samples, ambiguous playing game time (How much time and duration), and genre of game.
ㅔAs reported in our previous study,5 pro-gamers may be a type of sample that closely parallels the characteristics of patients with an on-line gaming addiction. Pro-gamers typically play on-line games for over 10 hours/day, similar to those with an on-line gaming addiction. However, pro-gamers do not show any addiction symptoms such as a disrupted daily life structure and sleep-wake cycle, high impulsivity, or other comorbidities. Pro-gamers appear to be unique subjects that show brain changes in response to long-term, on-line game play without underlying comorbidities. In one voxel-based morphometry study,5 pro-gamers versus general on-line game users show increased brain volume in the prefrontal cortex. Among various on-line games, StarCraft is a well-known, real-time strategy games that is thought to require much executive functioning and spatial attention for complex visual targets.5,6 With the specific group of pro-gamers (Regular, long-term playing unified genre of on-line games in individuals without pathologic conditions), we hypothesized that cortical volume of the brain and cognitive flexibility would be correlated with the career length of pro-gamers.
Subjects and measurements
ㅔTwenty-three pro-gamers (all male and mean age=19.8±1.7 years) from two StarCraft pro-game teams were assessed at Chung Ang University Medical Center. All pro-gamers were members of the Korea eSports Association (KeSPA). Exclusion criteria were: 1) disrupted behaviors or distress due to excessive on-line game play, 2) Beck Depression Inventory scores >19, 3) other axis I psychiatric disorders including attention deficit hyperactivity disorder, major depressive disorder, and substance abuse, and 4) history of head injury or trauma. No pro-gamers met any of the exclusion criteria.
ㅔAll pro-gamers were screened with the Structured Clinical Interview for DSM-IV and the Beck Depression Inventory (BDI).7 The impulsiveness of pro-gamers was assessed using the Barratt Impulsiveness Scale-Korean version (BIS-K).8,9 Additionally, a psychiatrist (D.H.H) interviewed all pro-gamers to rule out other psychiatric disorders. The protocol used in the current study was approved by the Institutional Review Board at Chung Ang University Hospital. Written informed consent was provided by all pro-gamers.
ㅔExecutive function involving cognitive flexibility was estimated with a computerized version of the Wisconsin Card Sorting Test (WCST) (CNT4.0, Maxmedica Inc).10 The cards in WCST contained colored shapes considering one of three possible rules (color, shape, and number). If the chosen sorting rule was correct, pro-gamers observed the feedback
"correct" for a placed card. After several correct trials, the sorting rule abruptly changes without notice. Thus, pro-gamers received the feedback information
"wrong" for changing their response for choosing a relevant sort in next trial. Scores are recorded along several dimensions, with the number of categories achieved (TCC), the number of total errors (TE) and the number of perseverative errors (PE) committed the most commonly measured category.
ㅔThe education level of the pro-gamers was 12.0±0.8 years. The average career length of the pro-gamers was 4.0±1.9 years. Seventeen pro-gamers graduated from high school or university. Three pro-gamers were student gamers with the permission of chairman in school, which is similar to a student athlete. Three pro-gamers quit high school to become a pro-gamer with the consent of parents. Pro-gamers played StarCraft an average of 9.2±1.6 hours/day and used the Internet (except for game playing) an average of 1.8±0.9 hours/day. The mean Young Internet Addiction Scale Score (YIAS) score of pro-gamers was 40.9±13.5. The mean BDI score of pro-gamers was 7.2±4.9. The mean total BIS-K score was 50.2±5.7.
MR imaging processing and data analysis
ㅔAll MR imaging was performed on a 1.5 Tesla Espree MRI scanner (SIEMENS, Erlangen, Germany). 3D T1-weighted magnetization-prepared rapid gradient echo (MPRAGE) data were collected with the following parameters: TR=1500 ms; TE=3.00 ms; Inversion time=1100 ms; FOV=256×256 mm; Flip angle=15°; 128 slices; 1.0×1.0×1.33 mm voxel size. Cortical thickness was measured using FreeSurfer 5.1 (http://surfer.nmr.mgh.harvard.edu). The standard protocol of the package uses intensity normalization, white matter segmentation, tessellation of the gray/white matter junction, inflation of the folded surface with correction of topological defect, and the measurement of the cortical thickness as defined by the distance between the grey-white matter junction and the pial surface. All images were aligned to 1-mm isotropic stereotaxic standard space (Montreal Neurological Institute, MNI 305 template) and smoothed with a Gaussian kernel of 15 mm full-width at half maximum (FWHM).
ㅔFor each hemisphere, a general linear model estimated the effects of career length as pro-gamer on cortical thickness. The statistical analysis was done on the surface data that included vertices and their Cartesian coordinates. The ages of the subjects were included as covariates of no interest. Results represented by log of p were mapped onto the average brain and considered significant at uncorrected p<0.005 with a cluster extent threshold of 50
mm2. Partial correlations between career length of pro-gamer and total/sub-scale scores of Wisconsin Card sorting Test were analyzed with Pearson correlations, controlling for age. For all statistical analyses, the α level for significance was set at 0.01 (0.05/5) and all analyses were performed using Statistica 6.0.
ㅔCareer length was positively correlated with cortical thickness in three brain regions: right superior frontal gyrus [Talairach coordinates: 8.7, 36.9, 40.1; maxima=3.2 log of p value; size
(mm2)=292.1], right superior parietal gyrus (27.1, -56.0, 62.6; 3.1 log of p value; 137.23), and right precentral gyrus (40.9, -7.5, 57.6; 2.7 log of p value; 50.2) (Figure 1 and 2). Controlling for age, cortical thickness in the right superior frontal gyrus was positively correlated with rate of winning in the Korea StarCraft pro-game league (r=0.51, p=0.02). There was no significant correlation between cortical thickness of other areas and winning rate. Controlling for age, career length was negatively correlated with total trials needed to complete six categories (TCC) (r=-0.58, p<0.01) and total number of errors (TE) (r=-0.44, p<0.01) of WCST. Controlling for age, cortical thickness in the right superior frontal gyrus was negatively correlated with TCC (r=-0.64, p<0.01), TE (r=-0.64, p<0.01) and PE (r=-0.59, p<0.01). Controlling for age, cortical thickness in the right superior parietal gyrus was also negatively correlated with TCC (r=-0.59, p<0.01) and TE (r=-0.56, p<0.01). There was no significant correlation between cortical thickness in the precentral gyrus and any subscale of the WCST.
ㅔThe current research examined the unique subject group of StarCraft pro-gamers. As mentioned before, pro-gamers in current research have played same game 10 hours/day, about four years. However, they have no pathologic conditions. StarCraft on-line game requires executive and spatial cognitive functions. Putting those results of several studies together, current research may contribute to the argument of the effect of on-line game on the brain change.
ㅔWe found that the career length of pro-gamers was associated with increased cortical volume in the frontal cortex, parietal cortex, and precentral gyrus. In addition, increased volume in the prefrontal cortex was positively correlated with the rate of winning. Increased volume in the prefrontal and parietal cortices was also positively associated with higher functioning as assessed by the WCST.
ㅔThe right medial superior frontal cortex was thicker in the pro-gamers with longer career length and higher winning rate. This cortical region is known to be involved in attention shifting,11 executive function,12 or inhibitory control of action,13 which are all contributing to cognitive flexibility necessary for playing on-line games. Recent studies have reported that video game training changes activation in the dorsolateral prefrontal gyrus and improves cognitive flexibility.2,3 In an fMRI study, Lee et al.3 reported that game training produced less activation in the dorsolateral prefrontal cortex with greater performance improvement in visuo-spatial attention and goal-directed motor planning. Hubert-Wallander et al.2 reported that action-based video games can improve selective attention and spatial distribution of vision. First-person shooter game players also show superior cognitive flexibility relative to individuals with little or no video game playing experience.14 Bonilha et al.15 reported that decreased gray matter volume in the prefrontal cortex is associated with difficulties set-shifting and mental inflexibility in patients with schizophrenia. Decreased cortical thickness in the right medial superior frontal gyrus was found in the patients with attention deficit hyperactivity disorder and it was correlated with severity of inattention and impulsivity.16 In our study, increased volume of prefrontal cortex was associated with career length of pro-gamers. Moreover, the increased volume was correlated with a higher winning rate and better cognitive flexibility (lower TCC and TE). We cautiously suggest that long-term, on-line game playing can increase cortical volume in the prefrontal cortex and associated cognitive functioning.
ㅔIn addition to the prefrontal cortex, we also found that the parietal cortex was associated with career length and cognitive functioning (lower TCC and TE). The parietal cortex is part of the brain network that controls movement and is also thought to be associated with the spatial attention required for processing complex visual targets.17 The posterior parietal cortex is thought to be associated with processing execution and preparation signals.18 Moreover, those signals may reflect behavior shifting induced by internal and external trigger.18 The superior parietal cortex is implicated in working memory representations assessed with the WCST.19 Interestingly, the left hand utilized often during StarCraft game playing. In response to error mismatch during right/left hand presentation experiments, unexpected left hand stimulation provoked activation in the right superior parietal cortex.20 Increased volume of right parietal cortex may reflect the trained left hand of StarCraft pro-gamers. The increased cortical thickness in the right precentral gyrus could be viewed in the same context. The plasticity of cortical gray matter volume has been reported after motor practices21,22 and also after practices on visual-spatial tasks23 including playing video-games.18,19 In our study, increased gray matter volume of prefrontal, parietal and prefrontal cortices was associated with career length of progamers. Moreover, the increased volume in the prefrontal and parietal cortices was correlated with a higher winning rate and better cognitive flexibility. We cautiously suggest that long-term, on-line game playing can increase cortical volume in the prefrontal and parietal cortices and associated cognitive func-tioning.
ㅔThere were several limitations in the current study. First, because pro-gamers are a very specific group, readers should be cautious in generalizing these results to other types of on-line gamers. In future study, more characteristics of pro-gamers such as personality and coping style should be assessed.
ㅔSecond, because the current study has no control group, research design is strict enough to show meaningful correlation. A more informative study including other comparison groups should be done in the future.
ㅔConclusively, regular long-term playing of on-line games of individuals without pathologic conditions may change brain volume in the prefrontal and parietal cortices, which are associated with cognitive flexibility.
Erickson KI, Boot WR, Basak C, Neider MB, Prakash RS, Voss MW, et al. Striatal volume predicts level of video game skill acquisition. Cereb Cortex 2010;20:2522-2530.
Hubert-Wallander B, Green CS, Sugarman M, Bavelier D. Changes in search rate but not in the dynamics of exogenous attention in action videogame players. Atten Percept Psychophys 2011;73:2399-2412.
Lee H, Voss MW, Prakash RS, Boot WR, Vo LT, Basak C, et al. Videogame training strategy-induced change in brain function during a complex visuomotor task. Behav Brain Res 2012;232:348-357.
Zhou Y, Lin FC, Du YS, Qin LD, Zhao ZM, Xu JR, et al. Gray matter abnormalities in Internet addiction: a voxel-based morphometry study. Eur J Radiol 2011;79:92-95.
Han DH, Lyoo IK, Renshaw PF. Differential regional gray matter volumes in patients with on-line game addiction and professional gamers. J Psychiatr Res 2012;46:507-515.
Blizzard. StarCraft. 2012.
Beck AT, Ward CH, Mendelson M, Mock J, Erbaugh J. An inventory for measuring depression. Arch Gen Psychiatry 1961;4:561-571.
Barratt ES. Factor analysis of some psychometric measures of impulsiveness and anxiety. Psychol Rep 1965;16:547-554.
Patton JH, Stanford MS, Barratt ES. Factor structure of the Barratt impulsiveness scale. J Clin Psychol 1995;51:768-774.
Kim SW, Shin IS, Kim JM, Yang SJ, Shin HY, Yoon JS. Association between attitude toward medication and neurocognitive function in schizophrenia. Clin Neuropharmacol 2006;29:197-205.
Nagahama Y, Okada T, Katsumi Y, Hayashi T, Yamauchi H, Sawamoto N, et al. Transient neural activity in the medial superior frontal gyrus and precuneus time locked with attention shift between object features. Neuroimage 1999;10:193-199.
Taylor SF, Welsh RC, Wager TD, Phan KL, Fitzgerald KD, Gehring WJ. A functional neuroimaging study of motivation and executive function. Neuroimage 2004;21:1045-1054.
Floden D, Stuss DT. Inhibitory control is slowed in patients with right superior medial frontal damage. J Cogn Neurosci 2006;18:1843-1849.
Colzato LS, van Leeuwen PJ, van den Wildenberg WP, Hommel B. DOOM'd to Switch: Superior Cognitive Flexibility in Players of First Person Shooter Games. Front Psychol 2010;1:8.
Bonilha L, Molnar C, Horner MD, Anderson B, Forster L, George MS, et al. Neurocognitive deficits and prefrontal cortical atrophy in patients with schizophrenia. Schizophr Res 2008;101:142-151.
Almeida LG, Ricardo-Garcell J, Prado H, Barajas L, Fernandez-Bouzas A, Avila D, et al. Reduced right frontal cortical thickness in children, adolescents and adults with ADHD and its correlation to clinical variables: a cross-sectional study. J Psychiatr Res 2010;44:1214-1223.
Granek JA, Gorbet DJ, Sergio LE. Extensive video-game experience alters cortical networks for complex visuomotor transformations. Cortex 2010;46:1165-1177.
Kamigaki T, Fukushima T, Miyashita Y. Neuronal signal dynamics during preparation and execution for behavioral shifting in macaque posterior parietal cortex. J Cogn Neurosci 2011;23:2503-2520.
Lie CH, Specht K, Marshall JC, Fink GR. Using fMRI to decompose the neural processes underlying the Wisconsin Card Sorting Test. Neuroimage 2006;30:1038-1049.
Stefanics G, Czigler I. Automatic prediction error responses to hands with unexpected laterality: an electrophysiological study. Neuroimage 2012;63:253-261.
Draganski B, Gaser C, Busch V, Schuierer G, Bogdahn U, May A. Neuroplasticity: changes in grey matter induced by training. Nature 2004;427:311-312.
Driemeyer J, Boyke J, Gaser C, Buchel C, May A. Changes in gray matter induced by learning--revisited. PLoS One 2008;3:e2669.
Haier RJ, Karama S, Leyba L, Jung RE. MRI assessment of cortical thickness and functional activity changes in adolescent girls following three months of practice on a visual-spatial task. BMC Res Notes 2009;2:174.