The Effect of Video-Game Software in Video-Game Epilepsy
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1 Epilepsia, 4O(Suppl. 4):3-37, Lippincott Williams & Wilkins, Inc., Philadelphia International League Against Epilepsy The Effect of Video-Game Software in Video-Game Epilepsy Stefan Ricci and *Federico Vigevano Epilepsy Center, Department of Neurological Sciences, University of Rome La Sapienza; and *Section of Child Neurology, Bambino Gesd Children s Hospital I.R. C. C.S., Rome, Italy Summary: Purpose: The individual role of video-game (VG) programs in VG activation is still unclear. Strict relations between VG seizures and photo- and pattern sensitivity suggest that programs per se may have a role in seizure activation. Methods: We tested a series of 2 commercially available VG programs in 3 subjects aged 7-2 years; test protocol comprised intermittent photic stimulation (IPS), pattern stimulation, and a game session with 2 programs, each played for 5 min, delivered from a 5-Hz screen. Results: Activation was observed in 7 subjects; marked differences were observed between different games: two programs activated 3 subjects; one program did not provoke activation. High variability between scenes makes it impossible to define mean brightness for the whole program. Activation correlated with steady maximal brightness (SMB) within a program; SMB is defined as the brightness in lux of the brightest scene steadily present in a program. SMB varied between and 35 lux in tested programs. Difference in activation between different games was statistically significant (p <.). Pattern sensitivity is strictly correlated with the probability of VG activation (p <.). Conclusions: Our study demonstrates a strong variation in activation between different game programs and a strict relation between VG activation and pattern sensitivity. Programs with SMB >lo lux should be regarded as potentially dangerous; programs with SMB <5 lux may be considered relatively safe. Key Words: Epilepsy-Photosensitivity-Pattern sensitivity-occipital cortex-video games. The importance of video game (VG) playing in seizure induction has increased progressively during the last 2 years, together with the diffusion and development of electronic devices. The number of VG programs also increased constantly, in parallel with increased market availability and growing software complexity. A further impulse in the evolution of VG software recently is the product of hardware development, particularly computer processors (central processing unit, CPU) and video cards. It is still not demonstrated that VG programs have a role in seizure activation. However, given the close relation of photosensitivity with seizure activation by television (TV) and VGs, it is highly probable that such a relation exists; for example, undoubtedly a brighter image has a higher probability of provoking discharges than a darker one; flashing lights are present in some VG scenes; moreover, it has been reported that activation increases in relation to the presence of geometric patterns (-3). Seizure activation by VGs may result from nonvisual activating factors, such as cognitive or decision- Address correspondence and reprint requests to Dr. F. Vigevano at Department of Child Neurology, Bambino Gesh Children s Hospital, IRCCS, Piazza S. Onofrio 4, 5 Rome, Italy. obg-irccs.rm.it making factors, sleep deprivation, emotional excitement, or hand movements (4-). A VG program is computer software. The software generates different images in response to interactions between the player and the computer; the interactions are related to the contents of the image. The interface between the player and the computer requires an input and an output. The joystick or the keyboard (usually a dedicated keyboard with buttons and arrows, which allows continuous.movements as well as sudden actions: for example, punching or jumping or launching missiles) represents the motor-output interface; the video screen represents the visual-input interface. Motor inputs and visual outputs are managed by the CPU; the VG software generates video images running under precise relations between inputs and ouputs. VGs may have different visual aspects: some are abstracted or semiabstracted (for example, Tetris and his clones), but the majority are figured and represent scenes and subjects; among the figured games, some are reality shaped, and some are fantastic. The variability is as extreme as the fantasy of the designers. It is well known that VGs may also act in the psychological sphere; VGs are said to be related to aggressiveness, cardiovascular changes, and addictive behavior (7- ). The emotional content of the VG program is strictly related to psychological effects. 3
2 32 S. RICCI AND F. VIGEVANO The use of VGs is related to sex, age, and personality of the player. In a study in 357 students in the United States, it was reported that the majority of boys played frequently in arcade rooms, whereas the majority of girls played mainly at home. Boys play longer than girls. Half of the games preferred by boys were classified as violent (); the majority of tested subjects preferred VGs classified as fantasy violence and sports. Given the close relation between VG seizures and photosensitivity, some authors tested the patients by VG scenes isolated from the context, with the purpose of identifying visual patterns related to epileptic activation (,2). However, patients who experienced VG seizures while playing with VG software were not playing with VG scenes isolated from the context. A VG program is a unitary software that is purchased and played separately from other similar programs. In arcade multigame rooms, each VG machine is dedicated to a single software. The program also generates sounds and music that are part of the game. To study the response in a realistic way, reflecting normal situations encountered during the play, activation should be studied during a full-playing session. We tested a series of 2 VG programs to identify the potential risk for each game program and to verify the EEG and clinical response. CONTENT-RELATED CLASSIFICATION OF VG PROGRAMS There are so many VG programs on the market that testing and classifying all the types of programs is impossible. We selected a series of 2 programs commonly available for home consoles in 5, all playable on a normal TV screen. There are different ways to classify VG programs. A classification of VG programs according to the meaning of the game is used commercially by producers; its importance is related to some characteristics of the programs (for example, characters and background movements, rapidity of movements required of the player). Other classifications are strictly related to violence and type of violence (). With a classification according to the character s actions, the VGs we used may be grouped into six categories: Platform: The character moves on one or more platforms, walking or jumping, fighting the enemies. In this series of games, movement is prevalently horizontal, generally brief (the designers are conditioned by the size of the screen and the longer horizontal axis). The prototype of this type of game is represented by Super Mario and his numerous variations. Shoot em up: These are prevalently space games with spaceships. Background movement (scrolling) is usually one-directional. Sport games present sport competitions (for example, tennis, basketball, soccer, rugby, golf). The action and the character s movements are conditioned by the sport being simulated in the game. Beat em up: The character fights the enemies at high speed. These are often fast and violent games. Beat em up games are very popular and generally show a struggle between one or more contenders. Driving: The character (or the player himself, who is often not visible in the scene, except for his hands) drives a moving vehicle, generally cars, but also go-karts, airplanes, or fantasy vehicles. Puzzle: This category contains widely different games, which are characterized by strategic decisions. Puzzle games can require fast or slow action. Other categories, not included in our study, include Arcade Adventure, Role Playing, Strategy and Simulation, and Card programs. Programs based on virtual reality were not available in 5 for home consoles. INTERACTIONS BETWEEN SUBJECT AND VIDEOGAME Factors responsible for triggering TV and VG-induced seizures can be grouped in four categories: Patient-dependent factors are related only to the state of the subject. These include flicker andor pattern sensitivity, type of sensitivity (occipital, generalized), drug therapy and antiepileptic drug (AED) levels, lowest and highest threshold for flicker, threshold for pattern, somnolence, and previous sleep deprivation. Visual factors (conditions influencing the transmission of visual stimuli to retinal receptors) as well as central pathways also may influence the response. Other patient-dependent factors may influence the response to screens, for example, exogenous andor endogenous toxic substances, non-aeds, and neurologic diseases. Last, other patient-dependent factors, not part of our study, do exist. These are related to the psychological context and include affective and behavioral responses, pleasant-positive or unpleasant-negative sensations, and aggressiveness and addictive behavior. Screen-dependent factors include screen type (flicker frequency, number of lines) and screen size; for computers, screen characteristics, with particular regard to refresh frequency, screen size, brightness and contrast. Other factors to consider in this category are distance from screen and surrounding lights. Image-dependent factors are related to visual contents of the image, such as brightness, contrast, col- Epilepsia, Vol. 4, Suppl. 4,
3 VIDEO-GAME SOFWARE IN VIDEO-GAME EPILEPSY 33 ors, lines (e.g., presence of flashing lights or patterns), movement of objects and backgrounds. Sojhvare-dependent factors are conditions implying a changing relation between the subject and the screen or between the subject and the contents of the image (visual-motor interactions). These are particularly related to the possibility of the subject to modify the image by using a joystick, a keyboard, or a mouse. PATIENTS AND METHODS The study protocol was administered to 3 patients, 3 male and 7 female subjects; age ranged from 7 to 2 years (mean age, 5 years; Table ). Test protocol included 5 min of EEG at rest, with eyes open, followed by intermittent photic stimulation (IPS) delivered in trains of 5 s at frequencies between 2 and Hz in three conditions (eyes open, eye closure, eyes closed) by a Grass PS 33 Plus photic stimulator (.44 Joules/flash, 3-cm distance nasion-lamp), followed by pattern stimulation delivered by vertical and horizontal disks subtending visual angles of, 5, 2, 3, 4, and degrees, with black and white stripes with a 5% duty cycle and spatial frequency of 2 cycleddegree, which were illuminated by a 5-W white spot placed behind the patient. All sub- TABLE. Responses to ILS and pattern stimulation Photosensitivity range Eye Eyes Eyes Pattern Patient Sex Age (yr) closure closed open sensitivity M 2 M F M M 2 F 3 M 3 M M M 3 F 4 M F 5 F M 4 F 2 M 25 F 2 F 2 F F F F 4 F 7 F F 7 F 2 F M 2 F so SO so C IN jects were investigated by polygraphic recording [ EEG channels, vertical and horizontal electrooculogram (EOG), two electromyogram (EMG) channels from deltoid muscles, electrocardiogram (EKG)]. Video-EEG was obtained by a dedicated three-way video-eeg that simultaneously records the EEG, the image of the patient while playing, and the VG image delivered from the screen, which is digitally compressed and inserted in a part of the VHS picture. The analysis of the interactions between player and VG and recording of ictal manifestations is reported in another article ( ). Each patient received a series of 2 VG programs (Table 2) delivered from a fixed distance of m, each for 5 min. All programs were produced by Nintendo (Nintendo International, Kyoto, Japan). Players used a dedicated keyboard with buttons for fast actions and arrows for direction of movements; programs were allocated in cartridges running in a dedicated console. The television set was a Philips 25 SL55/2 (Philips International, Eindhoven, The Netherlands, PAL system, 25 lines, refresh frequency, 5 Hz), with a diagonal of 2 cm, which subtends a visual angle of 3 degrees. When generalized discharges appeared or myoclonic jerks were observed, VGs were stopped by turning off the screen. The sequence of game programs was random. EEG activation is defined as the appearance of generalized discharges or occipital spikes with a spread to anterior regions clearly different from the EEG recorded at rest. The programs tested varied markedly in visual characteristics (Fig. ): dominant colors, contrast, presence and orientation of geometric components, color areas in the screen, scrolling directions and speed, and type and speed of character s movements are different from game to game, and in the same game, from scene to scene, depending on the player s ability to reach different game levels. High variability between one scene and another in the same game, which influences the observed response, prevented us from assigning mean brightness values to each game program. For example, in a single program ( Nintendo Super Mario World ), brightness can change repeatedly between a minimum near zero lux (black passages between a play action and that following) and a maximum of 2 lux (bright scenes with dominant green); these changes are unpredictable, because they depend on game results and are different from player to player and with a given player in subsequent pert-ormances. The most reliable visual characteristic of a VG program is the steady maximal brightness (SMB), which is defined as the brightness of the brightest scene steadily present in a program (>lo s). SMB varied between a minimum of and a maximum of 32 lux in our series of games (Table 2). Photometric data were obtained by a screen-devoted color analyzer, Minolta CRT Color Analyzer CA-; the instrument was leaned at direct con- Epilepsia, Vol. 4, Suppi. 4,
4 34 S. RICCI AND F. VIGEVANO TABLE 2. Classification and visual characteristics of the programs used Steady Brightness (lux) maximum Videogame program Classification and features Dominant color minimum-maximum brightness Super Mario World Platform, horizontal scrolling Bright green, bright blue Super Mario Kart Driving (fantasy), vertical split-screen Bright green I7&35 35 Biometal Shoot em up, horizontal scrolling Dark grey 5 Super Strike Gunner Shoot em up, vertical scrolling Grey Donkey Kong Country Platform, horizontal scrolling Brown Kick Off Sport (soccer), horizontal scrolling Green Street Fighter Beat em up, fast character movements Orange, bright red Super Bomberman Puzzle with fast actions, geometric components Green Super Mario All Stars Platform, horizontal scrolling Green, bright blue 2G2 2 Nigel Mansell s World Driving (realistic) Grey, bright blue Championship Super Aleste Shoot em up, vertical scrolling Blue, bright blue The Magical Quest Platform, horizontal scrolling Bright blue -3 3 tact to the center of screen and measured a restricted circular area with a diameter of 5 cm. This measurement is insensitive to brightness of periphery of the screen. However, the games we tested were characterized by limited variability between different screen areas, so that the center of the picture corresponds to 275% of the whole image. RESULTS All subjects selected for this study were photosensitive to IPS, the photosensitivity ranges (minimal and maximal frequency) for each eye condition are displayed in Table ; (33.3%) subjects also were pattern sensitive. Sensitivity to VG programs was observed in 7 (5.%) subjects. Sensitivity to VG programs varied widely between different programs (Fig. 2) and different scenes in a single game. The majority of sensitive subjects were activated by six to nine programs of the series (Table 3). The most activating games were those with a bright background (>2 lux SMB), in particular those with dominant bright green or bright blue. In particularly sensitive subjects, discharges may be observed even with less bright scenes. Threshold varied among subjects; however, scenes <lo lux were scarcely or nonactivating. One of the programs tested ( Super Bomberman, with an SMB of 3 lux) was particularly dangerous, because it activated generalized convulsive seizures in two patients. As demonstrated in another article, this program is also responsible for a particular type of EEG activation characterized by repeated absences that may precede the seizures ( ). Activation differs widely between different programs. Games characterized by a dim background (low SMB) were scarcely or nonactivating; games characterized by bright backgrounds (high SMB) were the most activating. Table 3 shows activation for each game program; two programs (SMW and SMK) activated 3 subjects each; activation decreased progressively up to BMET, which did not provoked activation in any subject. The difference observed between game programs is statistically significant (two-tailed x2 test, p <.). All the patients in our series were IPS sensitive; subjects who did not have IPS sensitivity were excluded from this study. In our series, the presence of pattern sensitivity is strictly correlated with VG sensitivity. Between VG-sensitive subjects, non-pattern-sensitive subjects responded to 2.2 programs, whereas patternsensitive subjects responded to 5. programs. The probability for IPS- and pattern-sensitive subjects to be sensitive to any VG program is statistically higher than for IPS-sensitive subjects who are not pattern sensitive (two-tailed x2 test, p <.). DISCUSSION Our study confirms the hypothesis that the type of VG program influences the response and the risk of seizures in screen-sensitive subjects. Activation related to TV and VG is the result of many factors, which added together result in increased risk: genetic factors, age, neurologic or metabolic diseases, type of photosensitivity (types of manifestations provoked by IPS or flashing lights), and pattern sensitivity. Screen characteristics, in particular screen type regarding refresh frequency (2), screen size, distance, and screen type were the object of detailed studies, as well as other factors such as the brightness of the surroundings ( 3). The attention of the media to the importance of the image delivered by the screen in epileptic activation reached a maximum when, on December, 7, -7 children in Japan had seizures simultaneously, while watching a cartoon called Pokemon (Pocket Monsters) (4,5); most of those children never had experienced seizures before. The reason for this extreme activation is presumed to be the presence of red flickering light in the cartoon (particularly in the background), which has been Epilepsia, Vol. 4, Suppl. 4,
5 FIG.. Typical scenes of the 2 programs tested. Starting from top left, row : Super Mario World, Super Mario Kart, Biometal, Super Strike Gunner ; row 2: Donkey Kong Country, Kick Off, Street Fighter It, Super Bomberman It ; row 3: Nigel Mansell s World Championship, Super Aleste, The Magical Quest, Super Mario All Stars.
6 3 S. RICCI AND F. VIGEVANO SMW SMK SFII SBII TMQ SMAS SAL DUG KOFF NMAN SSG BMET FIG. 2. Histogram of activation. Ordinates: number of patients activated. SMW, Super Mario World; SMK, Super Mario Kart ; SFII, Street Fighter ; SBII, Super Bomberman ; TMQ, The Magical Quest ; SMAS, Super Mario All Stars ; SAL, Super Aleste ; DKC, Donkey Kong Country ; KOFF, Kick Off ; NMAN, Nigel Mansell s World Championship ; SSG, Super Strike Gunner ; BMET, Biometal. TABLE 3. Individual responses to 2 programs Programs No. of activating Patients S.M.W. S.M.K. BIOMET. S.S.G. D.K.C. K.OFF S.F. S.B. S.M.A.S. N.MAN S.AL. T.M.Q. programs No. of pts. activated 3 Percentage 43.3% Epilepsia, Vol. 4, Suppl. 4,
7 VIDEO-GAME SOFTWARE IN VIDEO-GAME EPILEPSY 37 proved to be extremely activating. In our series of games, flickering lights were absent; a bright red background was present in some scenes of Street Fighter, which was one of the most activating programs ( subjects of 7 activated, corresponding to 4%); however, activation was higher with other two programs, Super Mario World and Super Bomberman. According to recent studies, the incidence of photosensitivity is estimated to be -% of all new epilepsy cases in the age range 7- years (), considered the peak age for photosensitivity (7,). The annual incidence of first seizures provoked by games played on video screens is presumed to be -.5 new cases/,, which represents 3% of all new epilepsy cases in this age range (). Seizures triggered by VGs received extensive attention from the media, because VG play is one of the most common amusement activities of daily living during late childhood and adolescence, and because VG seizures are dramatic events when they occur in subjects not previously known to be screen sensitive. There are many reasons for identifying potentially safer as well as particularly dangerous VG programs. Safer VG programs may decrease the probability of seizures related to VG exposure; diffusion of safer VG programs may decrease the overall risk of seizures in general population in this age range. On the contrary, VG programs known to be potentially dangerous should be avoided by subjects at risk. To reproduce the conditions most frequently encountered during VG play both at home and in public places (arcade rooms), we tested our patients with a 5-Hz screen, which is far more activating than -Hz screens. In previous studies it was demonstrated that -Hz TV screens are extremely effective in reducing screen activation (2,2). However, -Hz TV screens are still expensive and much less common than 5-Hz ones; therefore probably 5-H~ screens will remain the most common screens for years. As a consequence, the classification of VG programs into potentially risky and probably harmful will continue to be important. Our data confirm a previous observation, that a close link between screen activation and pattern sensitivity does exist (2,22). Therefore testing pattern sensitivity is a fundamental part of EEG examination to determine the individual risk for VG seizures. Subjects who have both IPS and pattern sensitivity should avoid VGs because of very high risk. As a conclusion of our study, we propose that safer VG programs (those with a SMB never exceeding 5 lux under all possible playing conditions) could be labeled relatively safe program, and that those with a higher SMB (>I lux) should be labeled potentially dangerous program, with a warning discouraging the use by known sensitive subjects and those subjects whose photosensitivity is not known. Acknowledgment: This work was supported by a Nintendo Grant for Videogame-induced seizures. We thank Philips Italy for technical assistance. We are grateful to Vincenzo Di Ciommo and Gaetano Di Liso for statistical calculations. REFERENCES. Harding GFA, Jeavons PM, Edson AS. Video material and epilepsy. Epilepsia 4;35: Maeda Y, Kurokawa T, Sakamoto K, Kitamoto I, Ueda K, Tashima S. Electroclinical study of video-game epilepsy. Dev Med Child Neurol ;32: Graf WD, Chatrian GE, Glass ST, Knauss TA. Video game-related seizures: a report on patients and a review of the literature. 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Ricci S, Vigevano F, Manfredi M, Kasteleijn-Nolst TrenitC DGA. Epilepsy provoked by television and videogames: safety of Hz screens. Neurology ;5:7&3. 3. Binnie CD, Darby CE, De Korte RA, Veldhuizen R, Wilkins AJ. EEG sensitivity to television: effects of ambient lighting. Electroencephalogr Clin Neurophysiol I;5:32-3 I 4. Takahashi T. Action needed to prevent Pokemon seizures. Asahi Evening News, January, p.. 5. Ishida S, Yamashita Y, Matsuishi T, et al. Photosensitive seizures provoked while viewing pocket monsters, a made-for-television animation program in Japan. Epilepsia ;3: Quirk JA, Fish DR, Smith SJM, Sander JWAS, Shorvon SD, Allen PJ. Incidence of photosensitive epilepsy: a prospective national study. Electroencephalogr Clin Neurophysiol 5;5:2&7. 7. Harding GFA, Jeavons PM. Photosensitive epilepsy: New edition. London: Mc Keith Press, 4.. Kasteleijn-Nolst Trenitk DGA. Photosensitivity in epilepsy: electrophysiological and clinical correlates. Acra Neurol Scand ;(S 25).. 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