The EEG in Selected Generalized Seizures

REVIEW ARTICLES

Richard A. Hrachovy*‡ and James D. Frost Jr.*†

activity that are bilaterally synchronous and symmetric Abstract: This article reviews the ictal and interictal EEG findings (Penry et al., 1975; Holmes et al., 1987). These bursts are associated with a select group of generalized seizures. These include absence seizures, myoclonic seizures seen in juvenile myoclonic usually frontocentral dominant; however, in some patients the epilepsy, idiopathic generalized tonic clonic seizures, infantile bursts are restricted to, or maximally expressed in, the occip- spasms, and atypical absence, tonic, and atonic seizures associated ital regions. The discharges appear and disappear suddenly. with the Lennox Gastaut syndrome. The frequency of the spike-and-wave complexes frequently varies slightly during the burst. The first few complexes of Key Words: Electroencephalography, Ictal, Interictal, Generalized the burst may occur at a frequency of 3.5 to 4 Hz, whereas, seizures, Epilepsy. the last few may slow to 2.5 Hz (Niedermeyer, 1972; Daly, (J Clin Neurophysiol 2006;23: 312–332) 1990; Fig. 2). Some of the bursts of spike-and-slow wave activity may be followed by brief runs of rhythmic 2.5 to 3.5 Hz activity in the frontal leads bilaterally (ringing effect). As he purpose of this article is to briefly describe the inter- soon as the 3 Hz spike-and-wave bursts stop, the background Tictal and ictal EEG patterns associated with a select group EEG activity immediately returns to the baseline state, with of generalized seizures. A detailed description of the clinical no postictal depression or slowing except for the ringing manifestations of the seizures is beyond the scope of this effect just mentioned. Three Hz spike-and-wave activity discussion. usually becomes more frequent with hyperventilation (Sato et al., 1983) and may be induced by photic stimulation (Wolf and Goosses, 1986). IDIOPATHIC GENERALIZED EPILEPSIES During sleep, the spike-and-wave complexes become Of the various idiopathic generalized seizures, absence, more fragmented, and bursts of polyspike-and-wave activity myoclonic and generalized tonic-clonic seizures will be dis- may appear (Niedermeyer, 1965; Ross et al., 1966; Sato et al., cussed. 1973). The frequency of the complexes may slow to 1.5 to 2.5 Hz. In some patients, the bursts consist of only single spike- ABSENCE SEIZURES and-wave complexes that may be low in voltage. These fragmentary bursts may occur in a generalized fashion or may Interictal EEG Findings lateralize to one hemisphere. The location of maximal ex- The background activity is usually normal, although pression of these fragmentary complexes often shifts from some degree of slowing of the background rhythms may be burst to burst and, in an occasional patient, these fragments seen in up to one third of patients (Sato et al., 1983; Holmes seem to arise consistently from one region or hemisphere et al., 1987). Paroxysms of rhythmic slow wave activity with (Fig. 3). Such fragmentary bursts may be misinterpreted as a frequency of 2.5 to 3.5 Hz may occur in a generalized representing focal epileptiform abnormalities. The amount of fashion or may be restricted to the occipital derivations (Fig. epileptiform activity increases with the onset of slow wave 1). This rhythmic slow activity is generally symmetric and sleep and then waxes and wanes in close relationship to the usually blocks with eye opening. It may occur in isolated sleep wake cycle. In most patients, REM sleep is associated runs or may be coupled with the bursts of generalized with an attenuation or cessation of the spike-and-wave activ- spike and wave activity described below (Dalby, 1969; ity (Kellaway and Frost, 1983; Fig. 4). In a small number of Holmes et al., 1987). absence seizure patients, the interictal EEG may exhibit The interictal EEG in patients with absence seizures benign centrotemporal spikes (Fig. 5). typically demonstrates brief bursts of 3 Hz spike-and-wave

*Peter Kellaway Section of Neurophysiology, Department of Neurology and ICTAL EEG FINDINGS the †Department of Neuroscience, Baylor College of Medicine, Houston, Texas and ‡Michael E. Debakey VA Medical Center, Houston, Texas. Both simple and complex absence seizures are associated Address correspondence and reprint requests to Dr. Richard A. Hrachovy, with bursts of generalized 3 Hz spike-and wave activity, which Peter Kellaway Section of Neurophysiology, Department of Neurology, generally last less than 30 seconds in duration (Fig. 6). Clinical MS NB302, One Baylor Plaza, Houston, Texas 77030; E-mail: manifestations of bursts lasting less than 2.5 seconds in duration [email protected] Copyright © 2006 by the American Clinical Neurophysiology Society are difﬁcult to detect, although specialized measurements of ISSN: 0736-0258/06/2304-0312 reaction times of patients with 3 Hz spike-and-wave activity

312 Journal of Clinical Neurophysiology • Volume 23, Number 4, August 2006 Journal of Clinical Neurophysiology • Volume 23, Number 4, August 2006 EEG in Selected Generalized Seizures

FIGURE 1. Occipital rhythmic in- termittent delta activity (ORIDA) in a 7-year-old patient with absence seizures.

FIGURE 2. Modulation of the frequency of the spike and slow wave complexes during a burst of 3 Hz spike-and-wave activity. The first few complexes occur at frequency Ͼ3 Hz whereas the frequency of the later complexes slows to Ͻ3 Hz.

FIGURE 3. NREM sleep in a 7-year-old patient with absence seizures demonstrating a burst of polyspike-and-wave activity (A) and fragmentary bursts of spike-and- wave activity (B).

FIGURE 4. Time modulation of 3 Hz spike and wave activity. Note the marked attenuation of the spike-and-wave activity during the REM sleep periods.

FIGURE 5. Centro-temporal spikes recorded during NREM sleep in a 9-year-old patient with absence seizures.

FIGURE 6. Burst of fronto-central dominant generalized 3 Hz spike-and-wave activity recorded during hyperventilation in a 9-year-old patient with absence seizures. Clinical manifestations observed during the burst of spike-and-wave activity included a behavioral arrest, staring, blinking, and unresponsiveness.

FIGURE 7. Bursts of 3.5 to 5 Hz spike-and-wave and polyspike-and-wave activity in a 12-year-old patient with juvenile myoclonic epilepsy.

FIGURE 8. Photoparoxysmal response in a 14-year-old patient with juvenile myoclonic epilepsy.

316 Copyright © 2006 by the American Clinical Neurophysiology Society Journal of Clinical Neurophysiology • Volume 23, Number 4, August 2006 EEG in Selected Generalized Seizures have shown that, regardless of its duration, 3 Hz spike-and-wave are often restricted to the frontal regions. Typical 3 Hz spike- activity impairs performance (Mirsky and Van Buren, 1965; and-wave activity may occur in JME patients and such patients Goode et al., 1970; Porter et al., 1973; Browne et al., 1974). usually also exhibit clinical absence seizures. Thus, in the clinical setting, the number of absences occurring During sleep, the bursts of spike-and-wave and polyspike- daily is often difﬁcult to determine, and a precise count requires and-wave activity may decrease, particularly during deep slow the use of long-term video/EEG monitoring. wave sleep, and the bursts are markedly diminished, or absent, during REM sleep. Fragmentary bursts are frequently seen MYOCLONIC SEIZURES-JUVENILE MYOCLONIC during sleep. Arousal from sleep is an extremely potent activator EPILEPSY of spike-and-wave and polyspike-and-wave discharges (Tou- chon, 1982). In some patients, this may be the only time The EEG ﬁndings associated with myoclonic seizures epileptic activity is seen during a routine 30 to 60 minute vary depending on the underlying epileptic syndrome. In this EEG recording. Likewise, clinical seizures often occur on section, only the EEG features associated with the myoclonic awakening. Hyperventilation may increase or induce epilep- seizures seen in patients with juvenile myoclonic epilepsy tic discharges (Janz, 1985) and approximately one third of (JME) will be discussed. JME patients are photosensitive (Wolf and Goosses, 1986; Janz, 1990; Fig. 8). INTERICTAL EEG FINDINGS As with other idiopathic generalized epilepsies, the background EEG activity is usually normal. There are bursts of ICTAL EEG FINDINGS frontocentral dominant generalized spike-and-wave and The myoclonic jerk seen in JME is typically associated polyspike-and-wave activity. The frequency of these bursts with a burst of 3 to 4 Hz polyspike-and-wave activity (Janz, tends to be more irregular than the typical 3 Hz spike-and-wave 1957; Delgado–Escueta and Enrile–Bascal, 1984). The jerk bursts and varies between 3 and 5 Hz (Janz 1957, 1985, 1989, occurs simultaneously with the burst of spikes which usually 1990; Tsuboi, 1977; Delgado–Escueta and Enrile–Bascal, 1984; have a frequency of 10 to 16 Hz. The spikes are followed by Fig. 7). The polyspikes may occur without the aftercoming slow slow waves occurring at a frequency of 2.5 to 5 Hz (Fig. 9). wave. Frequently these bursts are fragmentary in appearance and The polyspike-and-wave pattern, which often persists beyond

FIGURE 9. Polyspike-and-wave complex associated with a myoclonic seizure. This complex was recorded shortly after arousal from sleep in a 14-year-old patient with juvenile myoclonic epilepsy.

FIGURE 10. Burst of 4 to 5 Hz spike-and-wave and polyspike-and-wave activity in a 42-year-old patient with juvenile myoclonic epilepsy. Myoclonic jerks were associated with the first few spike-and-wave complexes. the termination of the myoclonic jerk, may last up to several patients whose EEG shows abortive generalized spike-and-wave seconds (Fig. 10). The myoclonic jerks may occur in iso- activity will experience clinical seizures. lation or repetitively. As mentioned above, the arousal As with most primary generalized seizures, the bursts of mechanism is a potent activator of the myoclonic seizures spike-and-wave activity observed interictally in patients with seen JME. idiopathic generalized tonic-clonic seizures typically become more frequent with the onset of slow wave sleep. The transition IDIOPATHIC GENERALIZED TONIC-CLONIC period from wakefulness to drowsiness is particularly important SEIZURES because, in some patients, this is the only time spike-and-wave activity may appear in a routine EEG. Thus, it is imperative that Interictal EEG Findings a sleep EEG be obtained in all patients in whom the diagnosis of Since idiopathic generalized tonic-clonic seizures may seizures is being considered and that the awake-sleep transition occur with any of the primary generalized seizure disorders, the period be recorded. Fragmentary bursts of spike and wave interictal EEG ﬁndings associated with these seizures are vari- activity are also common during sleep in this condition. able (see above). However, in all patients with idiopathic generalized tonic-clonic seizures, the interictal background EEG activity is usually normal, and the EEG may show brief bursts of ICTAL EEG FINDINGS generalized 2.5 to 3.5 Hz spike-and-wave and/or polyspike-and- In the usual clinical setting, the background EEG activity wave activity. In most patients, these bursts last less than 2.5 is obscured by high voltage myogenic artifact during a primary seconds, and such bursts are frequently referred to as “abortive” generalized seizure. Digital high frequency ﬁltering of the mus- spike-and-wave activity. It should be remembered that only cle artifact allows for adequate visualization of the EEG activity about one half of patients with primary generalized tonic-clonic in some patients. The most informative data concerning the ictal seizures will demonstrate spike-and-wave activity on a routine EEG changes associated with primary generalized tonic-clonic EEG. Conversely, it is also important to realize that not all seizures has been obtained from patients paralyzed with muscle

FIGURE 11. Photoparoxysmal response followed by a generalized tonic clonic seizure in a 9-year-old patient with a history of absence seizures. (A) Burst of 3 hz spike and wave activity elicited by photic stimulation. The patient exhibited staring and unresponsiveness during the burst. (B) The spike-and-wave activity is replaced by rhythmic generalized alpha frequency activity (recruiting rhythm) which is associated with tonic posturing. (C) The recruiting rhythm persists for several seconds and then the background activity becomes obscured by myogenic artifact.

FIGURE 11. Continued.

FIGURE 12. Myoclonic seizures followed by a generalized tonic-clonic seizure in a 12-year-old patient with juvenile myoclonic epilepsy. (A) Burst of spike-and-wave and polyspike-and-wave activity associated with myoclonic jerks. (B) Bursts of spike-and-wave and polyspike-and-wave activity followed by the appearance of rhythmic generalized alpha frequency activity (recruiting rhythm) which is associated with tonic posturing. (C) The recruiting rhythm persists for several seconds and then the background activity becomes obscured by myogenic artifact.

FIGURE 12. Continued. relaxants. As the seizure begins, there may be recurrent high voltage rhythmic generalized 10 to 12 Hz activity. This rhythmic alpha polyspike-and–wave bursts which are associated with myoclonic frequency activity progressively increases in amplitude over the jerks and/or a cry. Then, the EEG typically shows generalized next 8 to 10 seconds and is associated with the tonic phase of the voltage attenuation with superimposed low voltage fast activity seizure. Thereafter, the EEG shows generalized slower activity, (20–40 Hz). This attenuation and superimposed fast activity may which increases in amplitude but slows in frequency from 7 to 8 to not be seen at the onset of all generalized tonic-clonic seizures. The 1 to 2 Hz. When the frequency of these waves reaches 4 to 5 Hz, the attenuation lasts a few seconds and is followed by the appearance of waves become mixed with polyspikes and these polyspike-and-

FIGURE 13. Hypsarrhythmia in a 23-month-old infant. (Reprinted from Hrachovy and Frost, 2003, with permission.)

FIGURE 14. Hypsarrhythmia with increased interhemispheric synchronization in a 22-month-old infant. (Reprinted from Hrachovy and Frost, 2003, with permission.)

FIGURE 15. Asymmetric hypsarrhythmia in a 13-month-old infant. (reprinted from Hrachovy and Frost, 2003, with permission.)

FIGURE 16. Suppression burst variant of hypsarrhythmia in a 3-month-old infant. (Reprinted from Hrachovy and Frost, 2003, with permission.)

FIGURE 17. Two variants of hypsarrhythmia. The suppression burst variant and a consistent focus of abnormal discharge (characterized by recurrent electrical seizure discharges in the right temporo-central region). (Reprinted from Hra- chovy and Frost, 2003, with permission.)

Copyright © 2006 by the American Clinical Neurophysiology Society 323 R. A. Hrachovy and J. D. Frost, Jr. Journal of Clinical Neurophysiology • Volume 23, Number 4, August 2006 wave complexes are associated with myoclonic jerks. As the seizure (i.e., atypical absence, atonic, and tonic) will be discussed in continues, the bursts of polyspike-and-wave activity become inter- this section. mittent and between bursts the background EEG activity is sup- pressed. Following the last burst of polyspike-and-wave activity, the INFANTILE SPASMS EEG shows a generalized voltage attenuation lasting several seconds. This attenuation is followed by irregular low voltage delta Interictal EEG Findings activity which gradually increases in frequency and amplitude (Gastaut and Broughton, 1972; Gastaut and Tassinari, 1975; Nied- The most common interictal EEG pattern associated with ermeyer, 2005). The time required for the EEG to return to the infantile spasms is hypsarrhythmia. This pattern consists of baseline state is highly variable from patient to patient. The onsets generalized high voltage, generally asynchronous, slow waves of two generalized tonic-clonic seizures are shown in figures 11 and mixed with random high voltage multifocal spikes and sharp 12. waves. At times, the spikes and sharp waves occur in a gener- In conclusion, although each of the idiopathic gen- alized fashion, but they do not occur in rhythmic, repetitive eralized seizures is associated with a specific ictal EEG sequences such as the slow spike slow wave discharges seen in pattern, all of the seizures share two major interictal the Lennox Gastaut Syndrome (Vazquez and Turner, 1951; features: the background EEG activity is usually normal Gastaut and Remond, 1952; Kellaway, 1952; Alva–Moncayo et and there are bursts of synchronous and symmetric 2.5 to al., 2002; Frost and Hrachovy, 2003). Figure 13 illustrates the 3.5 Hz spike-and-wave and/or polyspike-and-wave activ- typical hypsarrhythmic pattern. However, in many infantile ity. Thus, when a routine EEG shows these two interictal spasms patients, variations of this prototypical pattern are seen features, it can be strongly suggested that the findings are (Hrachovy et al., 1984; Frost and Hrachovy, 2003; Hrachovy consistent with a diagnosis of an idiopathic generalized and Frost, 2003): epilepsy. 1. Hypsarrhythmia with increased interhemispheric synchronization (Fig. 14). In this variant, the diffuse asynchronous slow wave activity and the multifocal spike and sharp wave CRYPTOGENIC OR SYMPTOMATIC activity are mixed with activity that exhibits a significant degree GENERALIZED EPILEPSIES of interhemispheric synchrony and symmetry. Most commonly The EEG features of infantile spasms and three com- this activity takes the form of synchronous rhythmic frontal or mon seizures associated with the Lennox Gastaut syndrome occipital dominant delta activity or synchronous frontal domi-

FIGURE 18. Hypsarrhythmia comprised of high voltage slow wave activity with little spike or sharp wave activity. (Reprinted from Hrachovy and Frost, 2003, with permission.)

324 Copyright © 2006 by the American Clinical Neurophysiology Society Journal of Clinical Neurophysiology • Volume 23, Number 4, August 2006 EEG in Selected Generalized Seizures nant slow spike and slow wave activity. This synchronous wave sleep, however, in some patients they occur in a continu- activity usually occurs intermittently throughout the record. ous, unremitting fashion. In this latter instance, the pattern is Most infants with hypsarrhythmia will show some degree of referred to as the suppression burst variant of hypsarrhythmia. synchronization of the background activity if the disorder per- The electrodecremental episodes are also one of the ictal EEG sists for many months, particularly those that transition to the patterns associated with infantile spasms. Lennox Gastaut syndrome. 4. Hypsarrhythmia with a consistent focus of abnormal 2. Asymmetric hypsarrhythmia (Fig. 15). This pattern discharge (Fig. 17). In this variant, a consistent focus of spike is characterized by the presence of hypsarrhythmia, with a or sharp wave activity is superimposed on a hypsarrhythmic consistent voltage asymmetry between hemispheres. The pat- background. In some patients, focal electrographic seizure tern is also referred to as hemihypsarrythmia or unilateral discharges may occur which do not disrupt the ongoing hypsarrhythmia. This pattern is associated with an underlying hypsarrhythmic activity. structural lesion of the brain and may be expressed over either 5. Hypsarrhythmia with little or no spike or sharp wave the more normal or abnormal hemisphere. activity (Fig. 18). This is the least common of the variants and 3. Hypsarrhythmia with episodes of generalized or later- consists of asynchronous and synchronous high voltage gen- alized voltage attenuation (Fig. 16). This variant is characterized eralized slow activity with little or no spike/sharp transients. by a hypsarrhythmic pattern that is interrupted by recurrent In addition to these variants, transient alterations occur in episodes of generalized or lateralized voltage attenuation. Such the hypsarrhythmic pattern throughout the day. During slow episodes of attenuation are most commonly seen during slow wave sleep, the voltage of the background activity usually

FIGURE 19. REM sleep modulation of the hypsarrhythmic pattern. The awake tracing reveals an asymmetric hypsarrhythmic pattern. During REM sleep, the hypsarrhythmic pattern disappears. (Reprinted from Hrachovy and Frost, 2003, with permission.)

FIGURE 20. One of the most common ictal changes associated with infantile spasms: a period of generalized voltage attenuation with superimposed fast activity. (Reprinted from Hrachovy and Frost, 2003, with permission.)

FIGURE 21. Burst of 1.5 to 2 Hz slow spike-and-wave activity in a 15-year-old patient with the Lennox-Gastaut syndrome. 326 Copyright © 2006 by the American Clinical Neurophysiology Society Journal of Clinical Neurophysiology • Volume 23, Number 4, August 2006 EEG in Selected Generalized Seizures

FIGURE 22. Attenuation episodes during NREM sleep in an 11-year-old patient with the Lennox-Gastaut syndrome.

FIGURE 23. Bursts of generalized fast activity during NREM sleep in a 13-year-old patient with the Lennox-Gastaut syndrome. Such bursts of fast activity may be associated with tonic seizures. increases and often there is a grouping of the multifocal sharp rhythmic pattern is frequently markedly reduced or abolished wave and spike activity, resulting in a quasi-periodic pattern and this change may last from seconds to many minutes. (Hrachovy et al., 1981, 1984; Watanabe et al., 1993). As noted Finally, the hypsarrhythmic pattern may also disappear or be previously, episodes of generalized voltage attenuation fre- greatly reduced during a cluster of spasms, only to return quently occur during slow wave sleep. Conversely, during immediately after cessation of the spasms (Hrachovy et al., REM sleep there is a marked reduction or total disappearance 1984). of the hypsarrhythmic pattern (Hrachovy et al., 1981, 1984, Although hypsarrhythmia and its variants are the most Fig. 19). Furthermore, on arousal from sleep, the hypsar- common patterns seen with infantile spasms, other interictal

FIGURE 24. Burst of frontal dominant 2 to 2.5 Hz slow spike-and-wave activity associated with an atypical absence seizure, during which time the patient stared and was nonresponsive to name calling. patterns may be seen. These include diffuse slowing, focal with superimposed fast activity; (8) a period of attenuation slowing, focal or multifocal spikes and sharp waves, parox- with rhythmic slow activity; (9) fast activity only; (10) a ysmal slow or fast activity, slow spike-and-wave activity, and sharp and slow wave complex followed by a period of continuous fast and spindling. These patterns may occur in voltage attenuation with superimposed fast activity; and isolation or in various combinations. In rare instances, the (11) a period of voltage attenuation with superimposed fast interictal EEG may be normal. This situation is most often activity followed by rhythmic slow activity. The most encountered when hypsarrhythmia disappears following common ictal pattern seen is a period of generalized treatment, although clinical spasms may continue. However, voltage attenuation (Fig. 20). The duration of the ictal normal interictal background may be seen shortly after the events can range from less than a second to more than 100 onset of the disorder. In such instances, hypsarrhythmia will seconds. There is no close correlation between specific usually be seen on subsequent EEG recordings. types of clinical events (e.g., flexor, extensor, or mixed spasms) and specific ictal EEG patterns. Also, as noted ICTAL EEG FINDINGS above, episodes of voltage attenuation frequently occur Video/EEG monitoring studies have identified 11 during slow wave sleep in the absence of clinical spasms. different ictal EEG patterns that occur with infantile Also, no significant correlation has been found between the spasms (Kellaway et al., 1979; Yamatogi and Ohtahara, various ictal EEG patterns and underlying cause, response 1981; King et al., 1985; Donat and Wright, 1991, Fusco to therapy, or long term developmental outcome (Haga et and Vigevano, 1993; Haga et al., 1995a, 1995b; Wong and al., 1995a, 1995b). However, as with the asymmetric Trevathan, 2001). These include: (1) a high voltage, fron- hypsarrhythmic pattern, an asymmetric ictal EEG pattern tal dominant, generalized slow wave transient; (2) a gen- does correlate with focal or lateralized structural lesions. eralized sharp and slow wave complex; (3) a generalized Asymmetric spasms frequently occur in association with sharp and slow wave complex followed by a period of asymmetric ictal patterns (Donat and Lo, 1994; Gaily et voltage attenuation; (4) a period of voltage attenuation al., 1995, 2001). only (electrodecremental episode); (5) a generalized slow The ictal discharges frequently occur in clusters near the wave transient only; (6) a period of voltage attenuation end of REM sleep periods. If the patient awakens from REM with superimposed fast activity; (7) a generalized slow sleep during this cluster, the ictal complexes may become wave transient followed by a period of voltage attenuation associated with clinical spasms (Hrachovy et al., 1981).

FIGURE 25. Generalized voltage attenuation associated with a tonic seizure in a 15-year-old patient with the Lennox-Gastaut syndrome.

FIGURE 26. Generalized voltage attenuation with superimposed fast activity associated with a tonic seizure in a 3-year-old patient with the Lennox-Gastaut syndrome.

FIGURE 27. Generalized voltage attenuation associated with head drops (atonic seizures) in a 4-year-old patient with the Lennox- Gastaut syndrome. The asynchronous slow wave transients occurring during the attenuation episodes represent movement artifacts.

FIGURE 28. Polyspike-and-wave activity followed by a brief period of generalized voltage attenuation in a 3-year-old patient with a history of atonic and generalized tonic-clonic seizures. This complex was associated with a drop attack (atonic seizure).

LENNOX GASTAUT SYNDROME Atypical Absence Seizures Atypical absence seizures are accompanied by bursts of (Atypical Absence, Tonic And Atonic Seizures) high amplitude generalized 1.5 to 2.5 Hz activity basically Interictal EEG Findings indistinguishable from that seen interictally (Markand, 1977; The EEG usually shows moderate to severe slowing of Fig. 24). Less commonly, bursts of fast activity (10-20 Hz) have the background activity (Gastaut et al., 1966; Chevrie and been reported to accompany atypical absence seizures (Blume et Aicardi, 1972; Markand, 1977, 2003; Bauer et al., 1983). The al., 1973, Markand, 2003). In general, the impairment of con- characteristic interictal EEG pattern in the Lennox Gastaut sciousness that occurs with atypical absence seizures is progres- syndrome is the slow spike-and-wave discharge. Although sive and not abrupt like that which occurs with 3 Hz spike-and- the frequency of this discharge may vary from 1 to 4 Hz, the wave activity. Likewise, recovery of consciousness at the end of typical frequency is 1.5 to 2.5 Hz (Blume et al., 1973; the seizure is gradual. Thus, in severely retarded individuals, the Markand, 1977, 2003; Fig. 21). The frequency, amplitude, detection of atypical absence seizures at bedside may be ex- distribution, and morphology often vary between bursts and tremely difficult. The occurrence of drooling, changes in pos- during bursts of slow spike-and-wave activity. Shifting asym- tural tone and myoclonus of the eyelids or perioral musculature metries of the discharge are common. If patients have large may aid in the clinical identification of the seizures. However, in unilateral hemispheric lesions, the slow spike-and-wave ac- many patients, long runs of slow spike-and-wave discharges tivity is generally higher over the good hemisphere with frequently occur without any apparent change in the patient’s corresponding suppression of the background activity over clinical state. the abnormal hemisphere (Markand, 1977, 2003). There is a marked variation in the duration of the slow Tonic Seizures spike-and-wave bursts between patients and across serial The EEG during tonic seizures may show generalized EEGs in a given patient. Bursts may last only a few seconds voltage attenuation or so-called electrodecremental change, or they may occur in long runs. In some patients, the dis- bursts of rhythmic fast activity (15-25 Hz), or attenuation charge may be virtually continuous and it is often difficult to followed by rhythmic fast activity (Gastaut and Tassinari, determine in such patients whether the discharge is associated 1975; Markand, 1977; Horita et al. 1987; Figs. 25, 26). A generalized slow spike-and-wave complex may precede these with a clinical seizure (Gastaut et al., 1966; Blume et al., ictal patterns. Following the ictal event, the EEG may show 1973; Markand, 1977, 2003). generalized delta activity for several seconds before returning Slow spike-and-wave activity is generally not influ- to the baseline state (Markand, 2003). As mentioned previ- enced by hyperventilation or photic stimulation. However, ously, bursts of fast activity frequently occur during slow slow wave sleep dramatically increases the number of wave sleep and may or may not be associated with clinical bursts and duration of the discharges and the slow-spike- seizure activity. Some of the clinical seizures occurring and-slow-wave complexes frequently become intermixed during sleep are subtle (e.g., eye opening and minimal up- with polyspikes. Electrodecremental periods lasting from 2 wards eye deviation) and may be easily missed without to 4 seconds may occur during slow wave sleep and, if video/EEG monitoring. prominent, may produce a suppression burst pattern (Gastaut et al., 1966; Blume et al., 1973; Markand, 1977; Atonic Seizures Fig. 22). Also common in Lennox Gastaut syndrome Atonic seizures have been associated with a variety of patients is the presence of bursts of fast activity during ictal EEG patterns (Markand, 2003) including generalized slow wave sleep (Gibbs and Gibbs, 1952; Brenner and spike-and-wave activity, generalized polyspike-and-wave ac- Atkinson, 1982; Beaumanoir and Dravet, 1992; Markand, tivity, generalized voltage attenuation (Fig. 27), and runs of 2003; Fig. 23). The frequency of this fast activity is 10 to low or high voltage fast activity. These patterns can occur 25 Hz, and it is typically generalized, although it is usually alone or in various combinations (Fig. 28). maximally expressed in the frontal and central regions. These bursts of fast activity may last up to 10 seconds and may be associated with tonic seizures (see below). During REFERENCES REM sleep, the bursts of slow spike-and-wave activity are Alva-Moncayo E, Diaz-Leal MC, Olmos-Garcia de Alba G. Electroencepha- greatly diminished (Blume et al., 1973; Amir et al., 1986; lographic discoveries in children with infantile massive spasms in Mexico. Rev Neurol. 2002;34:928–32. Horita et al. 1987). Amir N, Shalev RS, Steinberg A. Sleep patterns in the Lennox-Gastaut In addition to the generalized slow spike-and-wave dis- syndrome. Neurology. 1986;36:1224–6. charges, focal, or multifocal spike and sharp wave discharges Bauer G, Aichner F, Saltuari L. Epilepsies with diffuse slow spikes and may be seen (Blume et al., 1973; Markand, 1977, 2003). waves of late onset. Eur Neurol. 1983;22:344–50. Beaumanoir A, Dravet C The Lennox-Gastaut syndrome. In: Roger, J, Bureau M, Dravet C, Dreifuss FE, Perret A, Wolf P, eds. Epileptic Ictal EEG Findings syndromes in infancy, childhood and adolescence. London: John Patients with Lennox Gastaut syndrome experience Libbey, 1992:115–32. multiple seizure types, both generalized and focal. The ictal Blume WT, David RB, Gomez MR. Generalized sharp and slow wave complexes: associated clinical features and long-term follow-up. Brain. EEG changes associated with three generalized seizures com- 1973;96:289–306. monly encountered (atypical absence, tonic, and atonic) are Brenner RP, Atkinson R. Generalized paroxysmal fast activity: electroen- briefly discussed here. cephalographic and clinical features. Ann Neurol. 1982;11:386–90.

Browne TR, Penry JK, Porter RJ, Dreifuss FE. Responsiveness before, Janz D Juvenile myoclonic epilepsy. In: Dam M, Gram, L, eds. Comprehen- during, and after spike-wave paroxysms. Neurology. 1974;24:659–65. sive epileptology. New York: Raven Press, 1990;171–85. Chevrie JJ, Aicardi J. Childhood epileptic encephalopathy with slow spike- Janz D. Juvenile myoclonic epilepsy: Epilepsy with impulsive petit mal. wave: a statistical study of 80 cases. Epilepsia. 1972;13:259–71. Cleve Clin J Med. 1989;56(Suppl. 1):S23–33. Dalby MA. Epilepsy and 3 per second spike-and-wave rhythm. Acta Neurol Janz D, Christian W. Impulsiv-Petit mal: Dtsch Z Nervenheilk 1957;176: Scand Suppl. 1969;45:1–183. 348–86. Daly DD Epilepsy and Syncope. In: Pedley, TA, Daly DD, eds. Current Kellaway P. Myoclonic phenomena in infants. Electroencephalogr Clin nd practice of clinical electroencephalography,2 edition. New York: Neurophysiol. 1952;4:243. Raven Press, 1990:269–334. Kellaway P, Frost JD Jr. Biorhythmic modulation of epileptic events. In: Delgado-Escueta AV, Enrile-Bacsal F. Juvenile myoclonic epilepsy of Janz. Pedley, TA, Meldrum BS, eds. Recent advances in epilepsy. Churchill- Neurology. 1984;34:285–294. Livingstone: Edinburgh, 1983;139–54. Donat JF, Lo WD. Asymmetric hypsarrhythmia and infantile spasms in West Kellaway P, Hrachovy RA, Frost JD Jr., Zion T. Precise characterization and syndrome. J Child Neurol. 1994;9:290–6. quantification of infantile spasms. Ann Neurol. 1979;6:214–8. Donat JF, Wright FS. Unusual variants of infantile spasms. J Child Neurol. King DW, Dyken PR, Spinks IL Jr., Murvin AJ. Infantile spasms: ictal 1991;6:313–8. phenomena. Pediatr Neurol. 1985;1:213–8. Frost JD Jr., Hrachovy RA. Infantile spasms. Boston: Kluwer Academic Markand ON. Lennox-Gastaut syndrome childhood epileptic encephalopa- Publishers, 2003. Fusco L, Vigevano F. Ictal clinical electroencephalographic findings of thy. J Clin Neurophysiol. 2003;20:426–41. spasms in West syndrome. Epilepsia. 1993;34:671–8. Markand ON. Slow spike-wave activity in EEG and associated clinical Gaily E, Liukkonen E, Paetau R, et al. Infantile spasms: diagnosis and features: often called “Lennox” or “Lennox-Gastaut” syndrome. Neu- assessment of treatment response by video-EEG. Dev Med Child Neu- rology. 1977;27:746–57. rol. 2001;43:658–67. Mirsky AF, Van Buren JM. On the nature of the absence in centrencephalic Gaily EK, Shewmon DA, Chugani HT, Curran JG. Asymmetric and asyn- epilepsy. Electroencephalogr Clin Neurophysiol. 1965;18:334–48. chronous infantile spasms. Epilepsia. 1995;36:873–82. Niedermeyer E Epileptic seizure disorders: In: Niedermeyer, E, Lopes Da Gastaut H, Broughton, R. 1972. Epileptic seizures. Springfield, IL: Charles Silva F, eds. Electroencephalography: Basic principles, clinical appli- C. Thomas. cations and related fields,5th edition. Philadelphia: Lippincott Williams Gastaut H, Remond A. Etude electroencephalographique des myoclonies. and Wilkins, 2005:505–619. Rev Neurol. 1952;86:596–609. Niedermeyer E. The generalized epilepsies. Charles C. Thomas, Springfield, Gastaut H, Roger J, Soulayrol R, et al. Childhood epileptic encephalopathy IL, 1972. of children with diffuse slow spike-waves (otherwise known as “petit Niedermeyer E. Sleep electroencephalograms in petit mal. Arch Neurol. mal variant”) or Lennox syndrome. Epilepsia. 1966;7:139–79. 1965;12:625–30. Gastaut H, Tassinari CA. The Ictal and Interictal EEG in different types of Penry JK, Porter RJ, Dreifuss FE. Simultaneous recording of absence epilepsy. In: Handbook of electroencephalography and clinical neuro- seizures with videotape and electroencephalography. A study of 374 physiology, vol. 13A: The epilepsies. Amsterdam: Elsevier, 1975:1–104. seizures in 48 patients. Brain. 1975;98:427–40. Gibbs FA, Gibbs EL. Atlas of electroencephalography, vol. 2. Epilepsy. Porter RJ, Penry JK, Dreifuss FE. Responsiveness at the onset of spike-wave Cambridge, MA: Addison-Wesley, 1952. bursts. Electroencephalogr Clin Neurophysiol. 1973;34:239–45. Goode DJ, Penry JK, Dreifuss FE. Effects of paroxysmal spike-wave on Ross JJ, Johnson LC, Walter R. Spike and wave discharges during stages of continuous visual-motor performance. Epilepsia. 1970;11:241–54. sleep. Arch Neurol. 1966;14:399–407. Haga Y, Watanabe K, Negoro T, et al. Do ictal, clinical, and electroencepha- Sato S, Dreifuss FE, Penry JK. The effect of sleep on spike-wave discharges lographic features predict outcome in West syndrome? Pediatr Neurol. in absence seizures. Neurology. 1973;23:1335–45. 1995a;13:226–9. Sato SS, Dreifuss FE, Penry JK, et al. Long-term follow-up of absence Haga Y, Watanabe K, Negoro T, et al. Ictal electroencephalographic findings seizures. Neurology. 1983;33:1590–5. of spasms in West syndrome. Psychiatr Clin Neurosci. 1995b;49: Touchon J. Effect of awakening on epileptic activity in primary generalized S233–4. myoclonic epilepsy. In: Sterman, MB, Shouse MN, Passouant P, eds. Holmes GL, McKeever M, Adamson M. Absence seizures in children: clinical and electroencephalographic features. Ann Neurol. 1987;21: Sleep and epilepsy. New York: Academic Press, 1982. 268–273. Tsuboi T. Primary generalized epilepsy with sporadic myoclonias of myo- Horita H, Kumagai K, Maekawa K. Overnight polygraphic study of Lennox- clonic petit mal type. Stuttgart: Thieme, 1977. Gastaut syndrome. Brain Dev. 1987;9:627–35. Vazquez HJ, Turner M. Epilepsia en flexion generalizada. Arch Argent Hrachovy RA, Frost JD Jr. Infantile Epileptic Encephalopathy with Hypsar- Pediatr. 1951;35:111–41. rhythmia (Infantile spasms/West syndrome). J Clin Neurophysiol. 2003; Watanabe K, Negoro T, Aso K, Matsumoto A. Reappraisal of interictal 20:408–25. electroencephalograms in infantile spasms. Epilepsia. 1993;34: Hrachovy RA, Frost JD Jr., Kellaway P. Hypsarrhythmia: variations on the 679–85. theme. Epilepsia. 1984;25:317–25. Wolf P, Goosses R. Relation of photosensitivity to epileptic syndromes. Hrachovy RA, Frost JD Jr., Kellaway P. Sleep characteristics in infantile J Neurol Neurosurg Psychiat. 1986;49:1368–91. spasms. Neurology. 1981;31:688–93. Wong M, Trevathan E. Infantile spasms. Pediatr Neurol. 2001;24:89–98. Janz D. Epilepsy with impulsive petit mal (juvenile myoclonic epilepsy). Yamatogi Y, Ohtahara S. Age-dependent epileptic encephalopathy: a longi- Acta Neurol Scand. 1985;72:449–59. tudinal study. Folia Psychiatr Neurol Jpn. 1981;35:321–32.