4 EEG and Noninvasive Electrophysiological Monitoring
The goal of epilepsy surgery is to locate and resect the epileptic focus without losing any cortical function. The purpose of the presurgical evaluation is to lateralize and localize this focus using a combination of data: the semiology of the clinical seizure, neuroimaging, and electroencephalography (EEG). Initial EEG recording is noninvasive, with scalp surface recording, and presurgical data determine whether further invasive monitoring with intracranial recording electrodes is needed. This chapter reviews the interictal and ictal EEG data used to identify the epileptic focus and discusses pitfalls in lateralization and localization with seizure semiology and noninvasive EEG.
Seizures are classified by their initial site of cortical origin—focal or generalized1 —determined by the seizure semiology and surface, noninvasive EEG. The seizure has several phases: the onset, or aura, that begins the ictal phase; the continuation of the ictal phase during which the discharge may spread, activating additional neurons; and the postictal phase. A focal seizure without altered awareness is called a simple partial seizure; one with altered awareness is called a complex partial seizure (CPS).
Interictal data are important, but the gold standard is to capture the habitual seizure during time-locked video-EEG monitoring and to analyze its clinical sequence along with the electrographic manifestations. This requires prolonged EEG recordings, referred to as long-term monitoring. The spatial and temporal relationships of the clinical manifestations (semiology) to the electrographic seizure are important, because the electrographic seizure may begin in one area but spread to another before any clinical manifestations are noted. The term inverse solution applies to using the seizure semiology and ictal surface EEG data to predict the cortical location of the epileptic focus.2
The concept of an epileptogenic zone is a practical method used to identify the epileptic focus. Data from the various modalities reviewed in Chapter 2 are used to identify its constituents. An in-depth discussion of the epileptogenic zone and its constituents can be found in several articles, especially the article by Rosenow and Lüders.3–6
The epileptogenic zone is the theoretical cortical area indispensable to generating a clinical seizure, and its complete removal is needed to control seizures.7 It consists of the following constituent zones:
The irritative zone is the cortical area generating epileptiform activity, defined by interictal spikes and sharp waves. This irritative zone is usually larger than the actual epileptogenic zone and can be thought of as all areas in which the epileptic focus may potentially be located. Interictal spikes may spread more in children.
The symptomatogenic zone is the cortical area producing the actual ictal symptoms, when activated. It may be the origin of the epileptic discharge or may be secondarily activated by the propagation of a discharge from the ictal onset zone (seizure onset zone).
The ictal onset zone is the area in which the seizure is actually generated, and if the ictal onset zone is located in a silent cortical area (noneloquent cortex), there are no associated clinical manifestations.
The epileptogenic lesion is the neuroradiological lesion that causes epilepsy. Therefore, neuroimaging, usually magnetic resonance imaging (MRI), is an important modality, but not all MRI lesions seen are necessarily in the cortical area from which seizures originate.
The functional deficit zone is the cortical region abnormal in the interictal period. This zone may be either focal or diffuse and is defined by several modalities: the neurological examination, the neuropsychological examination, and the EEG or functional neuroimaging [typically a single photon emission computed tomography or positron emission tomography (PET) scan]. The EEG shows slowing in the functional deficit zone but not epileptiform activity. A functional deficit zone may not be present in every patient. This zone may be focal or generalized, if there is diffuse dysfunction.
Eloquent cortex refers to cortex in which a defined clinical function is located. For the purposes of epilepsy surgery, eloquent cortex refers to primary motor, primary sensory, language, or memory functions. It is sometimes referred to as the silent cortex. However, the term silent cortex is a misnomer because every cortical area has some function, but it may not be possible to specifically identifyits function.
Seizure semiology (see Table 2.6 on page 11) and the ictal surface EEG are important in localizing the epileptic focus, and combining these modalities improves lateralization.8 Using these data to infer the cortical location of the epileptic focus is referred to as the inverse problem. The symptomatogenic zone is identified by the clinical manifestations, whereas the ictal onset zone is identified by the electrographic discharge. The exact temporal relationship between the clinical onset and the electrographic seizure must be determined. This is done by close inspection of the videotape of the recorded seizure, noting the time of the clinical onset as “Time 0” and then relating the electrographic seizure onset to this Time 0. The ictal onset and symptomatogenic zones are certainly interrelated. Ideally, these would be located in the same or contiguous cortical areas, and a focal resection removes both. But the ictal onset may occur in an area of silent cortex, causing no symptoms until it propagates and activates the symptomatogenic zone.
EEG Interpretation
EEG records the electrical activity generated by cortical neurons, consisting of the summation of excitatory and inhibitory postsynaptic potentials, which spread to the scalp surface where the recording electrode is placed. All structures between the generator and the electrode attenuate these signals, especially the skull, which is a high-frequency filter. Surface EEG electrodes are placed in a standard array, a montage, as designated by the American Clinical Neuro-physiologic Society. A standard 10/20 International Distribution is used for diagnostic EEG, with electrode positions related to the underlying brain.9 When localizing for epilepsy surgery, additional scalp electrodes may be required, using a 10/10,10 or even a 10/5 array,11 which vary by how closely spaced the scalp electrodes are ( Fig. 4.1 ). Closely spaced electrodes are more precise when localizing for epilepsy surgery12 High-density EEG recording may better localize an epileptic focus.
Both interictal and ictal EEG are analyzed, starting with the interictal EEG background: continuity symmetry and the individual components in the waking and sleep states ( Fig. 4.2 ). Subtle background asymmetries may be important for lateralization and localization, especially without an epileptogenic lesion ( Table 4.1 ). Slow wave activity, one component of the functional deficit zone, and epileptiform activity (spikes and sharp waves), which defines the irritative zone, are identified and locations noted.
Analyzing the habitual seizures is important to determine that they are originating from one location or, in some cases, to exclude nonepileptic seizures. Even if a lesion is present, ictal recordings confirm that the seizures arise from the lesion or are not multifocal. We prefer to capture at least three habitual seizures. In a study of ictal 259 EEGs in 183 children, the seizure type was confirmed in 101 seizures, ictal EEG aided in the classification in 101 seizures, errors in classification were corrected in 37 seizures (detected 11 nonepileptic seizures), and previously undetected seizures were found in 20 seizures. Eleven children had no interictal spikes.13 Ictal onset patterns include discharges with rhythmic frequencies (α, θ, δ), paroxysmal fast activity, suppression of activity (electrodecremental response), repetitive epileptiform activity, arrhythmic activity, or may stay obscured. The initial ictal rhythm is more predictive of the seizure origin.7
Anterior temporal spikes (F7/F8) are the most commonly encountered epileptiform feature in temporal lobe epilepsy (TLE). Focal sharp waves; spike and wave discharges; and slowing (especially polymorphic 5 activity) or independent, synchronous, or time-locked (a time lag) bitemporal discharges may be seen. Synchronous bitemporal spikes indicate a generating source propagating to the two temporal lobes, whereas time-locked bitemporal discharges indicate transcallosal propagation. Generalized discharges may occur.14 Frequent interictal discharges were present in symptomatic TLE patients and in mesial temporal sclerosis cases but in only one third of these cases they were strictly temporal.15 In the Miami series, unilateral temporal discharges occurred in 22 EEGs (36%), unilateral multilobar or poorly localized abnormalities occurred in 23 patients EEGs, bilateral abnormalities occurred in 12 patients EEGs, and no abnormality occurred in 3 patients EEGs.16 Spikes in the waking state or during active sleep provide the best localizing data, and sleep typically activates anterior temporal lobe discharges.17
For TLE, Ebersole and Pacia defined three seizure types: regular 5- to 9-Hz rhythm, irregular 2- to 5-Hz rhythm, and no distinct ictal discharge. Type 1 seizures likely originate in hippocampus. Type 2 seizures likely have a neocortical origin.18 In children, two types of ictal discharges were seen: a rhythmic 5–8 pattern progressively increasing in amplitude, followed by a rhythmic monomorphic 8 and initial temporal flattening (an electrodecrement) with a progressive appearance of fast activity, frequently spreading to surrounding areas, and finally postictal slowing with a temporal predominance15 ( Fig. 4.3 ).
The largest series after a temporal lobectomy is from Toronto, with 126 children.19 The interictal EEG showed lateralization in only 68/126 (54%); 26 children had ipsilateral diffuse epileptiform discharges, 7 children had bitemporal discharges, 8 children had generalized activity, and 17 children had a normal interictal EEG. Ictal EEG showed ipsilateral localization in 72 children, and 3 children had a generalized pattern. Nineteen children had either no seizures or had a normal EEG. In the Miami series, a unilateral and well-localized ictal onset was seen in 33 children (54%); a lateralized but poorly localized or multilobular discharge occurred in 23 children; and an independent or a synchronous, bilateral onset was seen in 3 children.16
In frontal lobe epilepsy (FLE), the frontal lobe is a large area with much of its cortex inaccessible to scalp electrodes: mesial, inferior, and orbitofrontal regions. Seizures originating from the dorsolateral convexity demonstrated interictal activity, whereas seizures originating from the mesial frontal region either had no interictal or multifocal activity.20 A younger age is also associated with discordant discharges.21 Discharges from the mesial areas may be detected in the vertex electrodes: Fz, Cz, and Pz electrodes. In a series from Alberta, the interictal EEG was normal in 18 of 21 children.22 Ictal recordings showed a frontal onset in 9 children and a bifrontal onset in 13 children. Generalized discharges may predict surgical failure.23 The absence of interictal spikes with documented seizures suggests extratemporal epilepsy.24
In FLE, three patterns were reported by Battaglia et al: high-amplitude sharp transients followed by low-voltage fast activity, rhythmic fast activity/decremental activity followed by slow waves with admixed spikes, and repetitive localizedq activity with spike waves25 ( Fig. 4.4 ).
In a study of supplementary sensory-motor seizures in children, the interictal EEG was normal in 49%, and generalized slowing or background disorganization was the only finding in 19%.26 Interictal EEG abnormalities included midline spikes; both negative and positive sharp waves; and slowing that could spread unilaterally or bilaterally to the frontal, temporal, or parietal areas—all more frequent in sleep. The actual ictal EEG findings may be subtle: an abrupt attenuation of background activity (electrodecrement) accompanied by diffuse p activity followed by semirhythmic 8 or 5 activity in the frontal or frontocentral regions or by generalized rhythmic slowing, maximal in the midline. These may be misdiagnosed as pseudoseizures.27
Most of the pediatric focal resections done in the posterior cortex are on patients with a documented lesion. The surface EEG localizes poorly to the parietal lobe; only 10% of parietal lobe seizures have localized EEG changes.28 The interictal EEG may be normal; show focal slowing; or have unilateral or bilateral parietal spikes, central spikes, or temporal synchronous or independent discharges, with a more posterior spreading, bifrontal, or even widespread discharges.29 In a large series of all ages in both children and adults from Montreal, only 9 of 66 patients (14%) had interictal parietal spikes, and ictal discharges were predominantly lateralized, but a localized parietal onset occurred in only four.30 The ictal EEG may show diffuse suppression at onset, followed by sharp waves over the parietal areas, or these may spread to other areas, especially the frontal and mesial frontal regions.29 In a series of children from Alberta with posterior resections, nine children had parietal lobe surgery and all has lesions except for one.31 Only two had epileptiform activity limited to the parietal lobe, one had frontal activity, five had ipsilateral diffuse activity, and one had slowing.
The surface EEG may also be misleading in occipital epilepsy, showing posterior temporal activity or bilateral, independent, or synchronous occipital spikes or sharp waves, with a lower amplitude on the contralateral side; diffuse posterior spikes or sharp waves; or involvement of the bilateral frontal, posterior temporal, or parietal regions.29 Surface EEG may show regionalized patterns over the ipsilateral occipital lobe in 50%, with less than 20% showing focal ictal patterns.28 Results vary; one study showed that the most active interictal area correctly identified the epileptic focus in 15 of 19 patients32; another study revealed that only 18% of patients had spikes limited to the occipital areas, with posterior temporo-occipital spikes seen in 46%.33 The number was similar for ictal data (80%). There were six occipital patients in the Alberta series; one each had epileptiform activity localized to the occipital area or to the parietooccipital region, three had hemispheric activity, and one had generalized slowing.31
Computerized techniques for dipole mapping (source analysis) are now available and are used to identify the epileptic focus. These can be done on both ictal and interictal data.34,35