Do video games evoke specific types of epileptic seizures?

Epilepsy & Behavior 7 (2005) 524–530 www.elsevier.com/locate/yebeh

Do video games evoke specific types of epileptic seizures? Marta Piccioli a, Federico Vigevano b,*, Carla Buttinelli a, Dorothe´e G.A. Kasteleijn-Nolst Trenite´ c a

Neurology Division, II Faculty of Medicine, University of Rome La Sapienza, Rome, Italy b Neurophysiology Section, Bambino Gesu` ChildrenÕs Hospital, IRCCS, Rome, Italy c Department of Medical Genetics, University Medical Center, Utrecht, The Netherlands Received 9 June 2005; revised 21 July 2005; accepted 23 July 2005 Available online 27 September 2005

Abstract We determined whether epileptic clinical manifestations evoked by playing video games (VG) differ from those evoked by intermittent photic stimulation (IPS) or striped patterns (P). We exposed nine children who had TV- and VG-evoked seizures in daily life to 12 VG after standardized photic stimulation and pattern stimulation. Their EEGs were recorded continuously, analyzed, and then correlated with a video of their behavior. Similar types of clinical signs were seen during VG, P, and IPS, but the signs we observed were more subtle during the VG. Eight patients showed a clear lateralization. A new observation was the lowering of the eyelids to a state of half-closed. Our study suggests that the type of visual stimulus provoking a photoparoxysmal response or seizure is not particularly relevant. The children belonged to different epilepsy groups, and our findings add to the discussion on the boundaries of the epilepsy types. Ó 2005 Elsevier Inc. All rights reserved. Keywords: Video games; Epilepsy; Photoparoxysmal response; Clinical symptomatology; Classification; Epileptiform discharges; Electroencephalogram; Children

1. Introduction Epileptic signs related to playing video games (VG) have been recognized since the early 1980s, with the first definitions being ‘‘Space Invader epilepsy,’’ ‘‘Dark Warrior epilepsy,’’ and ‘‘Nintendo epilepsy’’ [1–3]. Epileptic seizures can also be provoked by playing other video games. VG sensitivity is, in the majority of cases, connected with sensitivity to intermittent photic stimulation (IPS) and patterns (P) as demonstrated in laboratory studies [4,5]. Nevertheless, in a recent follow-up study in 73 P-sensitive patients (11% not IPS-sensitive) only 7% had a history of VG seizures [6]. VG seizures are more common in male patients, while photosensitivity is found predominantly in females [7]. VG playing is a combination of visual stimuli (flickering screen, color, patterns and brightness of the program and influence of scanning of the screen) and other *

Corresponding author. Fax: +39 06 68592463. E-mail address: [email protected] (F. Vigevano).

1525-5050/$ - see front matter Ó 2005 Elsevier Inc. All rights reserved. doi:10.1016/j.yebeh.2005.07.022

factors like praxis and mental activity. VG playing might thus indeed evoke different seizure types in different types of patients, compared with a rather simple visual stimulus like looking at white flickering light. Epileptic signs provoked by IPS and by P stimulation are absences, myoclonic jerks, tonic–clonic seizures, and focal, mainly occipital, seizures, with or without secondary generalization [6,8–10]. Patterns have been shown to provoke epileptiform activity (EA) with a maximum over the posterior temporal and parietal scalp area, instead of the occipital area as is usual in IPS [11]. It is therefore plausible that VG, containing many patterned images, evoke a different type of seizure when studied in great detail. However, our knowledge of the clinical and electroencephalographic signs provoked by playing VG remains very limited, especially since VG playing is difficult to perform in a routine EEG clinical setting because of the length of play time normally involved [7,12]. It is unknown if there are differences in phenomenology between IPS- and VG-evoked clinical signs and symptoms in the same patients. Furthermore, it

a VPA, valproic acid; CBZ, carbamazepine; CLB, clobazam; TV, television; VG, video games; disco, discotheque; FL, fluorescent lighting; IPOE, idiopathic photosensitive occipital epilepsy; TLE, temporal lobe epilepsy; IGE, idiopathic generalized epilepsy; FC, febrile convulsions; S, sister; F, brother; P, father.

— — Yes — Yes — — Yes — — — Yes Yes — Yes Yes — Mild developmental delay — Mild developmental delay — — — Mild developmental delay 9a; 8 9c; 8 9a 9c; 8 3a; 7; 8 7; 5 7; 8 7; 8 IPOE IPOE IPOE TLE IPOE IGE IGE IGE TV + VG + Game Boy + arcade TV + VG TV + VG + sunlight + pattern TV + VG + disco TV TV TV + VG TV + VG + FL Clomipramine 10 VPA 600 (75) VPA 600 (22) CBZ 600 (8) CLB 30 VPA 800 (53) VPA 500 (62) — VPA 500 (37) M M F M F F F F 2 3 4 5 6 7 8 9

10 11 13 14 15 10 12 10

Yes — — 5; 9c IPOE TV M 1

Age (years) Sex Patient

Long-term polygraphic EEG recording (16 EEG channels, vertical and horizontal EOG (electro-oculogram), two EMG channels for the deltoid muscles, ECG) with simultaneous video recording was performed for all children. After a resting EEG, the children were visually stimulated with flashing white light (IPS) and black-and-white striped patterns (P) before they started playing the VG. IPS was performed according to the standard European protocol [13]. A Grass PS-33 photic stimulator (1.44 J/ flash) was used with 5-second flashes between 2 and

Table 1 Clinical characteristics of patientsa

3. Methods

Medication in mg (blood level mg/L)

Reason for investigation of ‘‘provoked seizures’’

Type of epilepsy

Type of seizure (see Appendix A)

Remarks

Febrile convulsions

Out of a cohort of 29 patients with a history of visually induced seizures (mainly TV and VG) (12 boys, 17 girls; average age 14.7 years ± 5.1; range 7–28 years), we selected those with generalized epileptiform discharges of at least 0.5-second duration during VG provocation: 8 boys and 7 girls. We had several reasons to select only those patients who had primary or secondary generalized epileptiform discharges during VG provocation: (1) we wanted to be able to compare symptoms evoked by VG and IPS, as IPS is a strong stimulus that evokes mainly generalized epileptiform discharges in children; (2) generalized epileptiform discharges are more likely to be accompanied by clinical symptomatology; (3) we wanted to exclude false-positive reactions by selecting true VG-positive children; (4) we could investigate not only the onset (origin) of the EA, but also possible differences in spreading between the two modalities. Nine of these 15 patients underwent continuous EEG and video monitoring while playing the same number and type of commercially available VG (4 boys, 5 girls; average age 11.9 years; range 10–15 years). These nine patients were considered suitable for comparing the clinical manifestations, both within and between patients, evoked by VG with those evoked by P and IPS. All nine children appeared to have a clinical history of TV (3)- or VG (6)-evoked seizures. Six patients had a history of tonic–clonic seizures (GTCSs) while watching TV. Three patients had idiopathic generalized epilepsy (IGE), five had idiopathic photosensitive occipital epilepsy (IPOE), and one had temporal lobe epilepsy (TLE). Three children were mildly developmentally delayed. Table 1 lists their clinical characteristics in detail. See also Appendix A [10].

—

2. Subjects

12

Migraine complaints

Family history of seizures

is still unclear if different VG provoke different types of EEG and clinical phenomena and whether prolonged playing, in particular, might evoke seizures. We therefore decided to identify the clinical manifestations related to playing a series of VG and compare these with the manifestations associated with standard IPS and P stimulation.

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S: focal seizure, IPS positive 2 FC (third degree) — FC (third degree) — F: IPS positive — P: FC 3 FC (third degree)

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60 Hz, and the lower and upper thresholds, for each eye condition (eyes open, eye closure, eyes closed) were determined. The distance between the eyes (nasion) and the lamp was 30 cm. Pattern stimulation was performed as described by Wilkins [14] with six disks of black-and-white stripes of increasing diameter subtending visual angles of 10°, 15°, 20°, 30°, 40°, and 60°, with a Michelson contrast of 0.8, a duty cycle of 50%, and spatial frequency of 2 cycles/degree. The patterns were illuminated by a 500-W white spot and presented for 10 seconds [14]. Each patient was exposed to a standard series of 12 commercially available VG; they were asked to play each game for 5 minutes (total exposure, 1 hour). The VG were shown at a distance of 1 m on a TV set (Philips 25 SL550/20; PAL system, 625 lines, refresh frequency 50 Hz, and diagonal screen measurement of 62 cm subtending a visual angle of 36°). Each line forming the screen picture subtended a visual angle of about 2 minutes of arc. The following games, all produced by Nintendo International, Kyoto, Japan, were used: Super Mario World, Super Mario Kart, Street Fighter II, Super Bomberman II, The Magical Quest, Super Mario All Stars, Super Aleste, Donkey Kong Country, Kick Off, Nigel MansellÕs World Championship, Super Strike Gunner, and Biometal. The visual characteristics of the games are listed in Table 2. The players used a dedicated keyboard with buttons for fast action and arrows for direction of movements. The screen was turned off as soon as clear myoclonic jerks were repeatedly observed. Nevertheless, major events were recorded in two patients (numbers 3 and 6) due to the unexpected provocativeness of one of the games (Super Bomberman II) (see Table 3). A dedicated three-way video system simultaneously recorded the EEG, the patientÕs behavior, and the VG image itself. The EEG recordings were first analyzed separately to describe the types of discharges, localization, spreading, and duration.

The localization and spreading of epileptic EEG abnormalities (sharp waves, spikes, spike–waves, and/or polyspikes–wave complexes) were evaluated in the available bipolar EEG recordings. Half a second (time lag) was used to establish a difference between spreading and generalization from the start in the longitudinal montage. Analyzing the three-way tape then led to the exact relationship between the patientÕs behavior, EEG pattern, and simultaneous play action. All discharges were taken into account. The EEG traces and video tapes were analyzed separately but by the same investigators. The study was conducted according all applicable laws. After having been well informed about the procedures of the study and the possible risks involved, the childrenÕs parents gave their signed consent. 4. Results 4.1. EEG data 4.1.1. Provocative factors, types of discharge, localization, and spread of epileptiform activity All patients showed exclusively generalized epileptiform activity either spontaneously (three patients, resting with eyes closed) or evoked by IPS (all nine), by P (four), and by playing VG (all). The majority reacted to 4 or 5 of the 12 VG tested, while Super Mario World was provocative in all nine patients. Patient 2 had clear bisynchronous generalized EA from the start, evoked by both IPS and VG, while in the other eight patients, a local onset or clear lateralization could always be found. The minimum duration of the discharges appeared to be 0.5 second regardless of the type of stimulus; the maximum for the pattern stimulation was 5 seconds, for IPS up to 12 seconds, and for VG playing up to 36 seconds. Seven patients were sensitive in all three eye conditions, while two exhibited EA only during eye closure. See Table 3 for details.

Table 2 Classification and visual characteristics of the video games used Video game

Classification and features

Dominant colors

Brightness (lux) min max

Steady maximum brightness (lux)

Super Mario World Super Mario Kart Biometal Super Strike Gunner Donkey Kong Country Kick Off Street Fighter II Super Bomberman IIa

Platform, horizontal scrolling Driving (fantasy), vertical split-screen Shoot Ôem up, horizontal scrolling Shoot Ôem up, vertical scrolling Platform, horizontal scrolling Sport (soccer), horizontal scrolling Beat Ôem up, fast character movements Puzzle with fast actions, geometrical components Platform, horizontal scrolling Driving (realistic) Shoot Ôem up, vertical scrolling Platform, horizontal scrolling

Bright green, bright blue Bright green Dark gray Gray Brown Green Orange, bright red Green

250–280 170–305 56–160 6–10 4–305 120–240 93–290 114–300

280 305 60 6 210 240 290 300

Green, bright blue Gray, bright blue Blue, bright blue Bright blue

120–280 74–225 32–225 199–310

280 225 225 300

Super Mario All Stars Nigel MansellÕs World Championship Super Aleste The Magical Quest a

Super Bomberman II proved to be the most provocative video game.

L P-O SW 1 0.5 15° LO SW 12 9 — — 2–40 T-P-O SW — — 9

7 8

5 6

4

3

1 2

a

EA, generalized epileptiform activity; Irr, irregular; SW, spike–waves; R, right; L, left; C, central; P, parietal; T, temporal; O, occipital; Gen, generalized; IPS, intermittent photic stimulation; VG, videogames; PPR, photoparoxysmal response; SMW, Super Mario World; SMK, Super Mario Kart; SFII, Street Fighter II; SBII, Super Bomberman II; TMQ, The Magical Quest; SMAS, Super Mario All Stars; SAL, Super Aleste; DKC, Donkey Kong Country; KO, Kick Off; ST, Super Strike Gunner. Note that all EA appeared to be generalized.

2 2

18 10 0.5 0.5 SW Irr SW 8–60 12–60 T-O T-P SW Irr Poly SW — —

— —

8–60 12–60

8–60 12–60

1 1

5 8

SW —

1 — 30° — Gen —

4 —

R R>L occipital R > L T-O R = L T-P — — — — 8–15 8–40 O O Polyspikes Irr Polyspikes R T-O — Irr SW —

8–60 10–40

12–60 14–40

1 0.5

5 7

— —

— —

— —

Irr SW Irr SW

SMW, TMQ SFII, KO, ST, SBII, SMW TMQ, SMW

6 10 0.5 1

12 0.5 0.5 6–60 Gen Irr SW L Irr SW

6–60

6–60

0.5

5

Irr SW

10°

3

Irr SW

R=L occipital L T-O 2 30° 18–40 O Irr SW — —

—

—

1

2

Irr SW

R=L occipital R P-O

5

Irr SW

SMW, SMK, SFII, SBII, SAL ST, SMK, SMW, SFII SBII, SMW, SMK, SFII

32 0.5

3 36 1 2 L R=L — — — — 10–50 8–30 Gen Gen Polyspikes Polyspikes — Irr SW

— R C-P

10–40 10–30

14–30 25–25

1 2

8 8

— —

— —

— —

Irr SW Irr SW

SMW SBII, SMAS, SMW, SAL, DKC SBII, SMW, SFII

Max Min Onset Type of EA Max Min Size Type of EA Max Min Eyes closed Eye closure Onset Type of EA Onset Type of EA

PPR range (Hz) IPS Rest, eyes closed Patient

Table 3 Electroencephalographic findings in the nine patientsa

Eyes open

Duration of EA (s)

Pattern

Onset

Duration of EA (s)

Video game

Provoking game

Duration EA (s)

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4.2. Ictal manifestations See Table 4 for details of signs and symptoms observed during the IPS and VG playing. 4.2.1. IPS Myoclonus was observed in all patients: eyelid myoclonia was observed in all; many also exhibited myoclonus of the head, arms, or body (see Table 4). Loss of consciousness was noted in three patients (33%). Subjective sensations were reported by three (33%) and loss of vision and visual aura by two; tears were observed in the eyes in two patients. Six (67%) showed asymmetrical signs, and three manifested both right- and left-sided signs. Although clinical signs could be observed in nearly all the IPS-evoked discharges (99%), some of the EA 1, 2, and 5 seconds in duration, respectively, was asymptomatic. 4.2.2. Patterns Myoclonus of the eyelids and head was observed in three of the four P-sensitive patients (duration of EA between 0.5 and 5 seconds). The fourth showed deviation of the eyes and head to the left, corresponding with a right parieto-occipital beginning and subsequent spreading of EA (max, 3 seconds) to all other areas. 4.2.3. Video games Myoclonus was seen in all patients: eyelid myoclonia and myoclonus of the body in all patients, and of the arms in five (see Table 4). Eight children had episodes in which they had their eyes half-closed. Loss of consciousness, confusion, and making mistakes were observed in eight of the nine players. Six (67%) showed asymmetrical signs, which were inconsistently right- and left-sided. The duration of evoked EA was between 0.5 and 36 seconds with a median of 2 seconds. Although clinical signs could be seen in the majority (80%) of VG-evoked discharges, those ranging from 0.5 to 7 seconds and one 12 seconds in duration went without any noticeable signs. The two patients having the longer-lasting seizures (clonic movement of the head, eyelid myoclonia with loss of consciousness, loss of consciousness in the first one; with tonic movement of the eyes and head to the left followed by generalized tonic–clonic movements in the second one) were both playing Super Bomberman II when their seizure started. 4.3. Symptoms Six patients (67%) reported symptoms during IPS and VG playing, with visual disturbances—aura and amaurosis—occurring in four of them. 4.4. Comparison of subtle ictal signs and symptoms evoked by the various stimuli IPS, P, and VG evoked myoclonus of the eyelids in all the patients. Other common symptoms were myoclonus

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Table 4 Signs and symptoms in the nine patients Sign

Myoclonus Eyelid Arms Body Hemifacial Eyes half-closed Eye movement Top/right/left Fixation Opening of mouth Oral automatism Head deviation right/left Elevation of arms Swallowing Verbal automatism Dysphasia Confusion Loss of consciousness Tonic–clonic seizure Symptoms Tears in eyes Amaurosis Visual aura Visual discomfort

IPS

VG

1

2

3

4

5

6

7

8

9

1

2

3

4

5

6

7

8

9

* * *

*

*

*

*

*

*

*

* * *

* * *

*

*

* * *

*

*

* * *

*

*

* * *

*

*

* * * *

* *

* *

*

*

*

*

*

*

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*

*

*

*

*

* *

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*

* *

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* *

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*

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*

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*

*

*

*

*

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*

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*

*

*

* * *

* * * *

* * *

* *

*

* *

*

* *

* *

* *

*

*

*

* *

* * * *

* *

* *

*

*

*

of the body and deviation of the head. Exclusively during VG, we noted opening of the mouth and oral automatisms in four patients. Focal signs were observed in nearly all the patients (eight of nine). Furthermore, in both VG and IPS, most signs were independent of the duration of EA; only loss of consciousness, confusion, and, obviously, the generalized tonic–clonic movements were observed in longer-lasting generalized EA (longer than 10 seconds). Six patients had various complaints either during IPS alone (one), during VG alone (three), or during both types of stimulation (two). No complaints were mentioned during pattern stimulation. See Table 4 for details. 5. Discussion All VG-sensitive patients were also IPS-sensitive, and they all showed clinical signs during the generalized epileptiform discharges evoked by VG and IPS. This is 25% higher than in a previous, similar type of study performed with only IPS in patients with a generalized photoparoxysmal response (PPR) outlasting the photic stimulus series [15]. Because our study was based on repeated and detailed analysis of the three-way video tapes and not only on observations during the patientÕs stimulation, we were able to detect subtle and less evident phenomenological signs, such as eyelid myoclonias and changes in eye movements. The video tapes also revealed the patientsÕ stereotyped behavioral patterns during EA and especially during the VG.

*

*

*

A new finding was the lowering of the eyelids to a state of half-closed eyes. This phenomenon occurred especially during VG (eight patients) and can possibly be considered a negative myoclonus, but, of course, polygraphic recordings are necessary to confirm this [16]. Although VG playing is different from IPS and P, both in duration and in type of stimulation, in the majority of cases, IPS and VG evoked similar types of clinical signs. The signs were often less intense than during IPS, which had to be interrupted because of the myoclonic jerks, whereas VG playing was not stopped because the signs were less noticeable in the same session. Not surprisingly, the likelihood of polyspikes was higher during IPS than during VG playing maybe because the light flashes are of very high intensity and delivered repetitively (1.44 J/flash). The children did not complain about any jerks or other signs while playing VG, apart from being annoyed about the mistakes they made during the EA. Because these subtle signs are easily missed, the children continued playing, with a high risk of GTCSs occurring, as did in two of our patients. It is therefore important to warn parents and children about the subtle signs that may appear during VG playing and might lead to a GTCS. Unlike TV viewing, in VG, the player is generally closer to the TV set, and playing has also been shown to be more provocative than watching [17]. The patients all proved to be sensitive to 25-Hz IPS, which is the frequency of the change in lines of the TV screen (refresh frequency). Thus, the flickering of the TV screen must at least add to the provocative effect, but because the maximum number of provocative games seen for any child was

M. Piccioli et al. / Epilepsy & Behavior 7 (2005) 524–530

5 of 12, the TV screen alone cannot be held responsible for all the symptoms observed. Some games were more provocative than others in terms of amount of EA evoked, depending on their level of brightness and combination of colors and flashing lights [5,18]. In our study, the longer-lasting seizures with loss of consciousness and generalized tonic–clonic movements occurred during Super Bomberman II, a game with one of the highest levels of brightness. Unlike the other games, in this one, the screen does not automatically go dark after a mistake has been made. In our children it is therefore possible that, in this particular game, the provoked EA that led to mistakes did not interrupt the visual stimulus and thus stop the EA, as occurred in the other games. A combination of factors, such as tiredness, prolonged visual stimulation, and game content, could lead to tonic–clonic seizures, as this is the classic history in children with VG-induced seizures [19]. Why the repeated bursts of generalized EA did not lead to a GTCS in seven of the nine children investigated is unclear: they did not differ with respect to EEG phenomena, type of seizures, type of epilepsy, medication, or duration of stimulation. As observed in the European study on video games, TV- and VG-sensitive children continue playing their games even though they are bothered by making mistakes due to the EA or have had a history of evoked GTCSs [17]. Eye deviation, lowering of the eyelids, fixation, and oral signs are observed especially during VG playing. Eye deviation and oral signs can be considered focal signs, and lowering of the eyelids and fixation as generalized tonic and atonic phenomena. Nevertheless, the type of more subtle symptoms evoked by the various games did not differ. Only a minority of our patients were P-sensitive, and although P sensitivity is highly correlated with TV and VG sensitivity, this does not seem to be a condition sine qua non. One of the P-sensitive patients clearly showed a deviation of the eyes and head to the left, corresponding to a right parieto-occipital beginning and subsequent spreading of EA (max, 3 seconds) to all other areas. This is in line with the observations of Darby at al. [11] and Radhakrishnan et al. [6] in P-sensitive patients. Surprisingly, in this selected group of children, based on generalized EA during VG playing, many (six of nine) had a partial type of epilepsy (IPOE or TLE), and even those with an IGE showed focal signs (two of three). The visual cortex is the seat of the primary epileptogenic process, and thus the evoked seizures may be regarded as partial with secondary generalization [9,20]. Our study confirms the hypothesis of Hennessy and Binnie [9], and Nicolson et al. [20] that this occurs more often than expected. Eye deviation to the right and left sides, often both independently within the same patient, was very common and can be well related to the involvement of the temporal lobe (eight of nine) [21]. This has also been described in patients with visual seizures both with and without IPS sensitivity [22]. That IPS and TV can provoke partial seizures (occipital seizures with visual aura) has been recognized since

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1960 and 1989, respectively [8–23], and often reported since then [7,9,24–26]. There could, however, be an overlap between IPOE and the more ‘‘usual’’ PSE and IGE; even in patients with non-photosensitive occipital epilepsy, rapid eyelid blinking was found to be an initial seizure manifestation [27]. As far as we know, no such data on VG playing have been published. The children in our study did not complain much. Apart from some visual manifestations and ocular discomfort, no other symptoms were reported. In P-sensitive patients at the Mayo Clinic [5], up to 34% reported subjective symptoms such as ocular discomfort and headache. Unlike Maeda et al. [7], we did not find headaches to be related to VG epilepsy, but headache during VG playing was a selection criterion in their population. In our patients with visually evoked occipital epilepsy, one would have expected complaints of headache and nausea during VG playing, but this was not the case. However, four of the patients did have more general complaints of headache. Our findings confirm that in visually sensitive patients, stimuli like IPS, P, and VGs, all trigger EA in the occipital striate and prestriate as well as infratemporal and posterior parietal brain regions [12,28]. Spreading of the EA, especially during variations in intensity and content of the visual stimuli as occur during VG playing, could very well determine the variability in signs within patients. It is still unclear why evoked generalized EA in the same patient does not always lead to visible clinical signs or why the clinical signs often seem to be independent of the total duration of EA. No differences were observed between males and females in type of symptomatology or any EEG feature. IPS-sensitive patients are predominantly female, in P-sensitive patients the sex difference is less clear, and in VG-sensitive patients males predominate. Our selection of VG-sensitive patients reflects this: five girls and four boys, with four of them P-sensitive. Two children were sensitive to IPS in the eye closure condition only. If this had not been tested, the VG-sensitive patients would have been considered non-photosensitive. This stresses the importance of performing IPS in a standardized manner [13]. It does not, however, rule out the possibility of praxis-induced seizures or seizures evoked by the cognitive content of the VG in non-photosensitive patients. Although linkage has recently been found in photosensitive patients, whether specific genes are related to a specific PPR phenotype or to a specific epilepsy type is still unresolved [29]. Another issue is the possible interaction between genes: either between PPR genes or between a PPR gene and one or more genes coding for an epilepsy phenotype. It is, in any case, necessary to take both the EEG phenomena (PPR) and the seizure types and syndromes involved into account in further genetic studies of photosensitivity. From this study it seems plausible that the type of visual stimulus that provokes a PPR or a seizure is not particularly relevant.

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Overall there were no major differences in clinical manifestations or EEG phenomena between the patients during the EEG or video recording. Nevertheless, because our patients have different types of epilepsy according to the official classification of epileptic syndromes and seizures [30] and subclassification of visually sensitive patients [10], this report can add to the general discussion on the boundaries of the epilepsy types [31] and subsequent pathophysiology of epilepsy [32,33]. Acknowledgments This article is based on work started by Stefano Ricci, M.D., who died in January 2000 and, unfortunately, was not able to see the final results. We thank Maria Angela Pinna for technical support and Jackie Senior for editing the text. This work was supported by a grant from the Japanese Organization for Epilepsy. Appendix A. Supplementary data Supplementary data associated with this article can be found, in the online version, at doi:10.1016/ j.yebeh.2005.07.022. References [1] Rushton DN. ‘‘Space Invader’’ epilepsy. Lancet 1981;1:501. [2] Daneshmend TK, Campbell MJ. Dark Warrior epilepsy. Br Med J 1982;284:1751–2. [3] Hart EJ. Nintendo epilepsy. N Engl J Med 1990;322:1473. [4] Harding GFA, Jeavons PM, Edson AS. Video material and epilepsy. Epilepsia 1994;35:1208–16. [5] Ricci S, Vigevano F. The effect of video-game software in video-game epilepsy. Epilepsia 1999;40(S4):31–7. [6] Radhakrishnan K, St. Louis EK, Johnson JA, McClelland RL, Westmoreland BF, Klass DW. Pattern-sensitive epilepsy: electroclinical characteristics, natural history, and delineation of the epileptic syndrome. Epilepsia 2005;46:48–58. [7] Maeda Y, Kurokawa T, Sakamoto K, et al. Electroclinical study of video-game epilepsy. Dev Med Child Neurol 1990;32:493–500. [8] Naquet R, Fegersten L, Bert J. Seizure discharges localized to the posterior cerebral regions in man, provoked by intermittent photic stimulation. Electroencephalogr Clin Neurophysiol 1960;12:305–16. [9] Hennessy MJ, Binnie CD. Photogenic partial seizures. Epilepsia 2000;41:59–64. [10] Kasteleijn-Nolst Trenite´ DGA, Guerrini R, Binnie CD, Genton P. Visual sensitivity and epilepsy: a proposed terminology and classification for clinical and EEG phenomenology. Epilepsia 2001;42:692–701. [11] Darby CE, Park DM, Smith AT, Wilkins AJ. EEG characteristics of epileptic pattern sensitivity and their relation to the nature of pattern stimulation and the effects of sodium valproate. Electroencephalogr Clin Neurophysiol 1986;63:517–25. [12] Graf WD, Chatrian GE, Glass ST, Knauss TA. Video game-related seizures: a report on 10 patients and a review of the literature. Pediatrics 1994;93:551–6.

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