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Epilepsy & Behavior 15 (2009) 22–33

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Epilepsy & Behavior


journal homepage: www.elsevier.com/locate/yebeh

Review

The role of EEG in epilepsy: A critical review


Soheyl Noachtar *, Jan Rémi
Epilepsy Center, Department of Neurology, University of Munich, Marchioninistrasse 15, 81377 Munich, Germany

a r t i c l e i n f o a b s t r a c t

Article history: Electroencephalography (EEG) is the most specific method to define epileptogenic cortex. Its sensitivity
Received 18 February 2009 and specificity depend on several factors such as age and recording procedures, for example, sleep record-
Accepted 19 February 2009 ings and activation procedures (hyperventilation, photic stimulation). EEG reveals characteristic findings
Available online 25 February 2009
in several epilepsy syndromes. Rarely, epileptiform discharges are recorded in healthy, particularly young
individuals. Ictal video/EEG recording is considered to be critical in localizing the epileptogenic zone. A
Keywords: careful analysis of the first clinical signs and symptoms of a seizure and of the evolution of the seizure
EEG
symptomatology can provide important localizing clues. Although surface EEG recordings are less sensi-
Epilepsy
Epileptiform discharges
tive than invasive studies, they provide the best overview and, therefore, the most efficient way to define
Invasive EEG the approximate localization of the epileptogenic zone. Invasive recordings are used in patients in whom
EEG-video-monitoring the epileptogenic zone either cannot be located with noninvasive diagnostic methods or is adjacent to
eloquent cortex. The most commonly used invasive electrodes are stereotactically implanted depth elec-
trodes and subdural strip or grid electrodes. Foramen ovale and epidural electrodes are of intermediate
invasiveness, but less sensitive. Invasive electrodes are subject to sampling errors if misplaced and should
be used only after exhaustive noninvasive evaluations have (1) failed to localize the epileptogenic zone
and (2) led to a testable hypothesis regarding this localization. Invasive EEG studies are associated with
additional risks that are justifiable only if there is a good chance of obtaining essential localizing infor-
mation and on a potentially resectable area.
Ó 2009 Elsevier Inc. All rights reserved.

1. Introduction Spikes
Sharp waves
Electroencephalography (EEG) is the most useful diagnostic Benign epileptiform discharges of childhood
procedure for epilepsy, and with the advent of more sophisticated Spike–wave complexes
methods of imaging structural damage, epilepsy is now actually Slow spike–wave complexes
one of the few common clinical problems routinely demanding 3-Hz spike–wave complexes
EEG evaluation [1]. EEG can answer three main questions in the Polyspikes
diagnostic workup of patients suspected of having epilepsy [1]: Hypsarrhythmia
Seizure pattern
Does the patient have epilepsy? Status pattern
Where is the epileptogenic zone?
How good is therapy? There is no difference in the diagnostic information between
sharp waves and spikes [4] (Fig. 1). Rarely, the electroencephalo-
gram of a normal individual shows IEDs. No epileptiform dis-
2. Does the patient have epilepsy? charges were seen in a study with 100 healthy volunteers [5]. A
study in more than 13.000 young male candidates for aircrew per-
Interictal epileptiform discharges (IEDs) in EEG help to differen- sonnel showed IEDs in 0.5% (in 58% of these only during photic
tiate between epileptic and other nonepileptic paroxysmal attacks. stimulation) [6]. Forty-three of these individuals were followed
The following EEG patterns are considered epileptiform [2,3]: up to 29 years and only one person developed epilepsy. The
authors conclude that the chance of developing epilepsy in healthy
individuals with IEDs on EEG is 2–3% [6]. IEDs are more common in
normal children between 1 and 15 years of age (about 1–2%) [7].
* Corresponding author. Fax: +49 89 7095 6691.
Mostly they are so-called benign focal epileptiform discharges of
E-mail address: noa@med.uni-muenchen.de (S. Noachtar). childhood and may occur in the occipital, centrotemporal, and

1525-5050/$ - see front matter Ó 2009 Elsevier Inc. All rights reserved.
doi:10.1016/j.yebeh.2009.02.035
S. Noachtar, J. Rémi / Epilepsy & Behavior 15 (2009) 22–33 23

Fig. 1. Left temporal sharp wave with a negative sharp component at electrodes F7 and T7 in a bipolar longitudinal recording during light sleep. This 32-year-old patient had
left temporal lobe epilepsy due to mesial left temporal sclerosis.

Fig. 2. Right central benign epileptiform discharges of childhood in a bipolar longitudinal recording. This 8-year-old child had rare generalized tonic–clonic seizures during
sleep that were preceded by left face clonic seizures.

frontal regions [8] (Fig. 2). Younger children more often display sensitivity of EEG. EEG including wake and sleep following partial
occipital discharges. Only about 8% of these children develop epi- sleep deprivation showed IEDs in about 50% of patients with a
lepsy [9]. About 2% of patients with neurological disorders but no clinically likely diagnosis of epilepsy, in whom routine EEG
epilepsy have IEDs [10]. Depending on age and epileptogenicity, including stage II sleep did not reveal any IEDs [15]. However,
epileptiform discharges occur in up to 98% of patients with epi- the value of routine EEG after a first unprovoked seizure has been
lepsy [11]. debated. Some authors would not start therapy following a first
Initially, EEG may be normal in 12–50% of patients with epi- seizure [16]. Others emphasize that the risk of seizure relapse is
lepsy [12,13]. Repeated EEG, however, increases the diagnostic increased if EEG shows IEDs [17]. The decision for antiepileptic
yield [14]. Long-term recordings likewise increase the chance of therapy clearly depends on the etiology of the epilepsy and the
recording IEDs. Activation procedures such as hyperventilation, individual seizure relapse risk, rather than on a general rule to
photic stimulation, and sleep deprivation enhance the diagnostic start therapy after a first or second seizure.
24 S. Noachtar, J. Rémi / Epilepsy & Behavior 15 (2009) 22–33

There is no objective definition of IEDs [3]. Even experienced Table 2


electroencephalographers sometimes disagree on the diagnosis of Typical interictal epileptiform discharges on the EEGs of patients with characteristic
epilepsy syndromes or etiologies.
IEDs, and, therefore, EEG interpretation is hampered by poor inter-
observer reliability [18]. Normal sharp transients have to be differ- EEG pattern Epileptic syndrome/etiology
entiated from epileptiform discharges to avoid misinterpretation of Anterior temporal spikes Mesial temporal lobe
the EEG recording. Some EEG patterns that are not epileptic may be epilepsy
overinterpreted, leading to a misdiagnosis of epilepsy [1]. Table 1 Generalized 3-Hz spike–wave complexes Absence epilepsy
>4-Hz spike–wave complexes, generalized Juvenile myoclonic epilepsy
summarizes several sharp variants (wickets, spikes, 14- and 6-Hz polyspikes
positive spikes, etc.) and their characteristics which can be easily Generalized slow spike–wave complexes Lennox–Gastaut syndrome
confused with epileptiform discharges (Fig. 3). The polarity of Regional (extratemporal) polyspikes Focal cortical dysplasia
sharp transients is important for interpretation; the sharp compo- Hypsarrhythmia West syndrome
nent of epileptiform discharges is typically negative (Fig. 1) [3]. Po-
sitive spikes are rare and can be found in patients who have
undergone resective brain surgery [19]. to differentiating between ictal and interictal EEG findings. How-
ever, although this distinction is clinically important, it is very
3. Where is the epileptogenic zone? arbitrary. It is easy if, for instance, a clonic seizure is observed dur-
ing an EEG discharge, but it may be difficult to assess the level of
Several characteristic EEG patterns are associated with well-de- consciousness during an epileptiform discharge [20]. A continuum
fined epilepsy syndromes (Table 2). EEG, thus, helps to define cer- between the interictal and ictal states for both focal and general-
tain epilepsy syndromes, which is important for selection of ized epilepsies is clinically more likely than a clear-cut border line
therapy and assessment of prognosis of the epilepsy. We are used (Fig. 4). A reaction time task during EEG (klicker test) helps to bet-

Table 1
Sharp transients that represent normal EEG variants and can be easily confused with epileptiform discharges.

Rhythmical temporal Wicket spike Small sharp spike 14- and 6-Hz 6-Hz ‘‘spike and wave” SREDA
theta of drowsiness positive ‘‘spikes”
Frequency (Hz) 4–7 6–12 Sporadic (about 14 and 6 5–7 5–6
50 ms)
Localization Temporal Temporal Frontal maximum Lateral to posterior Generalized Generalized
temporal
Waveform Notched, rhythmic Monophasic,similar Amplitude <50 lV Monophasic Diphasic, small spike Sudden onset and
to l waves duration <50 ms and large wave sudden end
Level of Relaxed wake sleep Wake sleep stage 1 Relaxed wake, sleep Wake sleep stages 1 Sleep stage 1 Wake sleep stage 1/
consciousness stage 1 stages 1 and 2 and 2 hyperventilation
Age Young adults Adults Adults Adolescents, adults Adolescents, adults Elderly
Duration 10 s 0.5–2 s Single discharges <1 s <1 s 40–80 s
Characteristics Synonym: Modulated, similar to Synonym: benign 6- and 14-Hz ‘‘Phantom” spike and Subclinical rhythmic
psychomotor variant sleep spindles epileptiform components may wave. Occipital or electrographic
transients of sleep occur separately frontal maximum discharge of adults
(‘‘BETS”)

Fig. 3. Wicket spikes (arrow) in the left temporal region in a bipolar longitudinal recording during wakefulness. This patient had migraine without aura.
S. Noachtar, J. Rémi / Epilepsy & Behavior 15 (2009) 22–33 25

lamotrigine, topiramate), whereas other AEDs may lead to deterio-


Status ration of the condition (carbamazepine, tiagabine) (Fig. 5). Several
EEG seizure pattern
epilepticus generalized epilepsy syndromes are associated with typical epilep-
tiform discharges (Table 2). Generalized SWCs with a repetition
rate of 3 Hz are typically associated with clinical absence seizures
Clinical symptoms

Ictal EEG seizure pattern if the discharge lasts longer than 4 seconds (Fig. 5) [24]. However,
selected patients may still be able to respond, though more slowly
than normal (Fig. 6). Other patients may already not respond to
auditory stimuli during SWCs of 1–2 seconds’ duration (Fig. 7). A
Subclinical EEG seizure pattern standardized reaction test to auditory or visual stimuli is manda-
tory to assess responsiveness during IEDs and is frequently re-
quired to assess the driving capacity of patients with absence
epilepsy [21].
Interictal Interictal epileptiform discharges
Generalized polyspikes are common in patients with juvenile
myoclonic epilepsy (JME). These patients are more likely to be pho-
time tosensitive (30%) than patients with other generalized idiopathic
epilepsies such as absence epilepsies [25]. About 30–60% of pa-
Fig. 4. Continuum between the interictal state and ictal state in patients with
epilepsy. tients with idiopathic generalized epilepsies display regional IEDs
and slowing in some EEG recordings on long-time follow-up
(Fig. 7) [26,27]. Thus, regional IEDs in the presence of generalized
ter assess responsiveness during epileptiform discharges (Fig. 5) IEDs do not exclude the diagnosis of idiopathic generalized epi-
[21]. This information is clinically important, for instance, to eval- lepsy. Sleep modulates IEDs in these patients as more irregular
uate a patient’s ability to drive a car. SWCs and polyspikes were recorded than during waking periods.
Sometimes EEG seizure patterns are recorded in clinically Generalized slow spike–wave complexes (SSWCs) are typical of
asymptomatic patients. These are called subclinical seizures and patients with Lennox–Gastaut syndrome, which has a poor prog-
are probably the case when the epileptic seizure discharge involves nosis (Fig. 8) [28,29]. EEG during sleep is more likely to show gen-
only asymptomatic cortex or when the clinical testing does not eralized SSWCs than EEG during waking, and typically, generalized
cover the cortical function that is altered [22] (Fig. 4). Spread of polyspikes also occur during sleep in these patients. Some of these
the epileptic activity into symptomatogenic cortex eventually patients had West syndrome at an earlier age. The typical EEG
leads to clinical symptoms. recording of West syndrome is hypsarrhythmia.

3.1. Generalized epilepsies 3.2. Focal epilepsies

Generalized 3-Hz spike–wave complexes (SWCs) are the hall- The precise localization of the epileptiform discharges is crucial
mark of absence epilepsy [23], which has a very good prognosis to the localization of the epileptogenic zone, particularly in pa-
and responds well to certain antiepileptic drugs (AEDs: valproate, tients considered for resective epilepsy surgery [30]. In the early

Fig. 5. Generalized spike–wave complexes in a 25-year-old patient with childhood absence epilepsy who had a seizure relapse after being seizure free off medication for
8 years. This bipolar longitudinal recording demonstrates that the patient is able to respond to an auditory stimulus to push a button at the onset of the discharge, but fails to
respond to later stimuli. At the end of the discharge a delayed response was recorded.
26 S. Noachtar, J. Rémi / Epilepsy & Behavior 15 (2009) 22–33

Fig. 6. Generalized spike–wave complexes in an ipsilateral ear reference recording during wakefulness in a 19-year-old patient with juvenile absence epilepsy. Note the
higher amplitude in the left frontal region at onset of the discharge. Generalized spike–wave complexes typically have a shifting maximum between left and right frontal
regions. Despite the generalized spike–wave complexes, the patient was initially able to respond to the auditory stimuli. The response time, however, gradually increased
with the duration of the discharge. At the end of the discharge, the patient failed to respond to the last stimulus.

Fig. 7. Generalized polyspikes and spike waves in a 39-year-old patient with juvenile absence epilepsy who never was free of absence seizures. Generalized tonic–clonic
seizures ceased about 20 years ago. This bipolar longitudinal recording shows generalized polyspikes and spike waves in the left part of the figure. The patient fails to respond
to auditory stimuli during the discharge (klicker), but he is able to do so after the discharge. In the right part of the figure, left temporal spike waves were recorded (arrow).

days of EEG, it was recognized that anterior temporal IEDs were the etiology of epilepsy in many patients and to consider surgical
frequently associated with temporal lobe epilepsy (TLE) [31]. The treatment, as the majority of these patients are not controlled with
advent of MRI enabled us to identify mesial temporal sclerosis as medical treatment only [32]. The use of anterior temporal and
S. Noachtar, J. Rémi / Epilepsy & Behavior 15 (2009) 22–33 27

Fig. 8. Generalized slow spike–wave complexes in a 22-year-old patient with idiopathic Lennox–Gastaut syndrome. Note the slow repetition rate (<2.5 Hz) of the spike–wave
complexes in an ipsilateral ear reference montage.

sphenoidal electrodes increases the yield of EEG in patients with extratemporal epilepsies [43]. Surface ictal EEG adequately local-
mesial temporal epilepsy [33,34]. Patients with TLE frequently ized onsets in 72% of cases, more often in temporal than extratem-
have IEDs independently in both temporal lobes. The occurrence poral epilepsy. Lateralized ictal onsets were seen in 57% of seizures
of strictly unilateral temporal IEDs has an excellent predictive va- and were most common in mesial temporal lobe epilepsy (MTLE),
lue for successful resective epilepsy surgery in TLE [35]. The pre- lateral frontal lobe epilepsy (LFLE), and parietal lobe epilepsy,
dominance of IEDs in the mesial or lateral temporal regions whereas lateralized onsets predominated in neocortical temporal
points to a mesial or lateral TLE as evidenced by MRI lesion or inva- lobe epilepsy and generalized onsets in mesial frontal lobe epilepsy
sive EEG [36]. Patients with mesial TLE as a result of hippocampal (MFLE) and occipital lobe epilepsy [43]. Approximately two-thirds
sclerosis who show frequent IEDs have a poorer prognosis for of seizures were localized, 22% generalized, 4% lateralized, and 6%
resective epilepsy surgery (28.6% seizure free) than patients with mislocalized/lateralized. False localization/lateralization occurred
rare IEDs (80.5% seizure free) [37]. in 28% of occipital and 16% of parietal seizures. Rhythmic temporal
Mesial temporal spikes do not, however, necessarily indicate theta at ictal onset was seen exclusively in temporal lobe seizures,
TLE. EEGs in patients with extratemporal epilepsies also have a whereas localized repetitive epileptiform activity was highly pre-
tendency to exhibit temporal IEDs. Despite this tendency, typically dictive of LFLE. Seizures arising from the lateral convexity and me-
the IEDs are located predominately in the epileptogenic lobe. How- sial regions were differentiated by a high incidence of repetitive
ever, some patients with extratemporal epilepsies do not show any epileptiform activity at ictal onset in the former and rhythmic the-
IEDs [38]. EEGS in patients with central (46.7%) and frontal (17.8%) ta activity in the latter. With the exception of MFLE, ictal record-
lesions more often lack interictal spiking than patients with tem- ings are very useful in the localization/lateralization of focal
poral (4.2%) or parieto-occipital (7.0%) lesions (p < 0.01). IEDs were seizures. One limitation of ictal EEG is the potential for false local-
found exclusively in the lesioned lobe in 45.6% of temporal, 31.3% ization/lateralization in occipital and parietal lobe epilepsies [43].
of central, 25% of frontal, and only 5% of parieto-occipital lesions Regional slowing of EEG activity is not specific for epilepsy and,
(p < 0.01). Ictal EEG changes in the lesioned lobe occurred more therefore, does not support the diagnosis of epilepsy. However,
commonly in temporal (58%), frontal (43.8%), and central (42.1%) rhythmic slowing may assist in localization of the epileptogenic
than in parieto-occipital (28.9%) lesions (p < 0.05). The occurrence zone once the diagnosis of epilepsy is established. Interictal rhyth-
and localization of ictal and interictal epileptiform EEG discharges mic slowing in the temporal regions (temporal intermittent rhyth-
in patients with clearly defined lesions on MRI differ depending on mic delta activity, TIRDA) occurs in patients with focal epilepsies
the lesioned lobe. In patients with temporal lesions, the EEG [44]. Rhythmical midline theta (RMT) activity not related to drows-
changes are most congruent with the location of the lesion, and iness or mental activation is significantly more common in patients
parieto-occipital lesions have the least congruent changes on with frontal (48.1%) than with temporal (3.7%) lobe epilepsy [45].
EEG. Regional polyspikes seem to provide a useful etiological as- Controls without epilepsy did not have this kind of RMT activity.
pect mainly for extratemporal epilepsy, as they occur significantly This finding is in clear contrast to the initial description of the pat-
more commonly in patients with cortical malformations than in tern which was attributed to TLE [46]. However, it was later
those with other etiologies [39]. pointed out that drowsiness leads to the same EEG pattern which
Ictal EEG recordings have the highest diagnostic yield, particu- was not clearly excluded in the early description, and one has to
larly if accompanied by simultaneous video recordings of the pa- consider that localization of the epileptogenic zone relied on sei-
tient. Therefore, most centers include ictal recordings in their zure semiology and interictal EEG only; imaging studies (CT, MRI,
diagnostic evaluation of patients considered for epilepsy surgery PET, SPECT) or video/EEG monitoring were not available at that
[40–42]. The localizing yield of ictal EEG is higher in TLE than in time. The localizing value of RMT activity is even more important
28 S. Noachtar, J. Rémi / Epilepsy & Behavior 15 (2009) 22–33

in those patients with FLE who do not have any IEDs at all (24%), Subdural
which is more frequently the case than in TLE. RMT was observed electrodes
in the majority of these patients with FLE (62%) [45]. Interictal RMT
Epidural
activity is, thus, common and has a localizing value in patients electrodes
with FLE, provided that conditions such as drowsiness and mental
activation as confounding factors for RMT activity are excluded
[45].

3.3. Invasive EEG recordings

In most patients who are referred to an epilepsy surgery center


today, noninvasive methods are sufficient to evaluate the patients
before surgical resection [30,47]. This is especially the case when Stereotactically
findings from imaging studies (MRI, PET) are congruent with the implanted
electroclinical and neuropyschological findings and when the epi- depth electrodes
leptogenic zone is in one mesial temporal lobe. Invasive EEG
recordings are used only when noninvasive methods do not allow
sufficient localization of the epileptogenic zone or when the epi- Foramen-ovale
leptogenic zone is anatomically too close to eloquent cortex electrodes
[30,48]. The use of invasive electrodes and with it the risk of com-
Fig. 9. Schematic representation of different invasive electrode types.
plications [49] are justified only when noninvasive methods (MRI,
video/EEG monitoring, FDG-PET, and ictal SPECT) deliver evidence
that the epileptogenic zone is potentially resectable. Invasive EEG- patients achieved seizure freedom after a unilateral anterior tem-
recording is therefore based on the following criteria: poral lobe resection [51]. In another third of these patients, inva-
sive EEG demonstrated an extratemporal origin of the seizure
There exists a clear hypothesis on the epileptogenic zone. pattern, which is congruent with more recent studies [52].
The hypothesis can be tested with the chosen electrodes. Interictal epileptiform discharges contralateral to the lobe
The suspected epileptogenic zone is potentially resectable. where seizure patterns were recorded reduce the chance for sei-
There is a low risk of possible complications. zure freedom after resection, but are in themselves not an indica-
tion for invasive EEG diagnostics when the other findings (MRI,
The typical electrodes are illustrated in Fig. 9. ictal EEG, neuropsychological findings, FDG-PET, ictal SPECT) are
consistent with unitemporal epilepsy [35].
3.3.1. Advantages of invasive electrodes
Invasive electrodes have several advantages that justify their 3.3.2.2. Unilateral temporal versus extratemporal. Another common
use. The signal-to-noise ratio is considerably better with invasive part of presurgical evaluation is determination of the hemisphere
EEG than with surface EEG. An invasive EEG derivation may al- in which the seizure pattern originates. The temporal and frontal
ready show a seizure pattern while the surface EEG seems still lobes are the most common regions to be evaluated in that respect
undisturbed. The higher sensitivity of foramen ovale electrodes [30]. Determining the epileptogenic zone is more difficult when
as compared with surface EEG is illustrated in Fig. 10. Electromyo- there is no lesion on MRI on which the location of the invasive elec-
graphic artifacts from muscle activity or ballistic movement arti- trodes can be based. The development of new imaging techniques
facts can disturb surface EEG in typical patterns. The artifacts are (FDG-PET, flumazenil-PET, ictal SPECT) further limited the use of
considerably reduced with ictal invasive EEG recordings (Fig. 11). invasive EEG recordings [53–55]. Despite some reservations over
In the following, the typical constellations and questions in the the specificity of functional imaging findings, which naturally can
use of invasive EEG electrodes are discussed. display only the secondary results of epileptic activity [56], and
can be misleading because of spread phenomena, they are helpful,
3.3.2. Constellations for the use of invasive EEG electrodes in our experience, in narrowing down results and finding the right
Invasive electrodes may help to determine the extent of the epi- placement for invasive electrodes. In some cases, the number of
leptogenic zone and to distinguish the epileptogenic zone from le- invasive electrodes and, thus, the risks of complications of the
sions identified with imaging studies and from eloquent cortex. implantation can be reduced.
The epileptologic constellations where EEG electrodes are used Fig. 12 is an ictal invasive EEG-recording of a patient with right
can be summed up as follows: frontal focal cortical dysplasia. It demonstrates a focal seizure on-
set at one electrode overlying the cortical dysplasia. The spread of
Unitemporal versus bitemporal seizure activity from mesial temporal to ipsilateral frontal regions
Unilateral temporal versus unilateral extratemporal is captured with depth electrodes implanted in both lobes (Fig. 13).
Unilateral extratemporal versus bifocal/multifocal The semiology of hypermotor seizures had been very suggestive of
frontal lobe epilepsy [57], but the invasive recording may demon-
strate seizure activity beginning at the amygdala and subsequently
3.3.2.1. Unitemporal versus bitemporal. The most common task spreading rapidly to the ipsilateral frontal lobe (Fig. 13).
accomplished with invasive electrodes is distinguishing unilateral
from bilateral temporal lobe epilepsy. In one study, for a large per- 3.3.2.3. Unilateral extratemporal versus bifocal or multifocal. Invasive
centage (77%) of the patients with temporal lobe epilepsies in diagnostic procedures are more complex when the contralateral
whom lateralization was not achieved with noninvasive methods, hemisphere also has to be investigated. Typical questions are
seizure patterns from only one temporal lobe were obtained in whether the epileptogenic zone is located frontally or temporally
invasive EEG studies [50]. The interictal and ictal EEG findings in on one or on both sides. A given patient is a good candidate for epi-
that study did not allow for lateralization. Almost a third of these lepsy surgery only if an epileptogenic zone in one hemisphere
S. Noachtar, J. Rémi / Epilepsy & Behavior 15 (2009) 22–33 29

Fig. 10. Synchronous EEG recording with foramen ovale (upper part of the tracing) and scalp electrodes. An EEG seizure pattern can be recorded in electrode Fo8 which is not
reflected in the scalp electrodes.

Fig. 11. Synchronous EEG recording with epidural (upper part of the tracing) and scalp electrodes, which were implanted through single bore holes [59]. While the surface
EEG is obscured from the strong ictal muscle activity of a bilateral tonic seizure, the epidural electrodes demonstrate a left frontopolar (FP1) seizure pattern that spreads to
the adjacent epidural electrodes in a typical fashion.
30 S. Noachtar, J. Rémi / Epilepsy & Behavior 15 (2009) 22–33

Fig. 12. This selection of a multichannel EEG recording with subdural electrodes in a referential montage to the subdural reference electrode A1 shows a focal seizure onset in
electrode A16, which was overlying the right lateral frontal cortex (arrow, see radiograph). This patient had right frontal lobe epilepsy due to focal cortical dysplasia (see MRI).

Fig. 13. This selection of a multichannel EEG recording with stereotactically implanted depth electrodes in the amygdala (AM), anterior hippocampus (AH), posterior
hippocampus (PH), and orbitofrontal (OF) and mesial frontal (MF) regions demonstrates rapid spread of seizure onset in the amygdala (electrode AM2) to the frontal regions.
The patient had hypermotor seizures that were rarely preceded by abdominal auras. At the time the clinical semiology was a hypermotor seizure; the seizure pattern had
already spread to the left frontal lobe, which could be shown with the depth electrodes. The radiograph demonstrates electrode positioning.

(even when the focus is in more than one lobe) can be identified. or stereotactically implanted into the brain parenchyma. Fig. 9
Patients with epileptogenic zones in both hemispheres will most illustrates the most common electrode types. Epidural and fora-
likely not benefit from a surgical approach. Callosotomy as a palli- men ovale electrodes are sometimes referred to as ‘‘semi-invasive”
ative approach has been performed in some of these patients. because their placement is less invasive than that of subdural or
However, the results from several centers differ considerably depth electrodes [60–63].
[58,59]. The decision on which electrode type to use depends on the
brain region and the question to be answered, on the one hand,
3.3.3. Invasive electrodes and the experience and common practice at the different epilepsy
For the most part, the aforementioned invasive electrodes are centers, on the other hand. The advantages and disadvantages of
either placed subdurally on the cortex (strip or grid electrodes) each electrode type are discussed next.
S. Noachtar, J. Rémi / Epilepsy & Behavior 15 (2009) 22–33 31

3.3.3.1. Depth electrodes. Depth electrodes are stereotactically im- discharges than invasive EEG recordings, they do give the best
planted, and the technique has considerably improved from angi- overview and allow estimation of the epileptogenic zone.
ography and ventriculography toward less invasive and safer Invasive electrodes can only derive a signal in close proximity to
three-dimensional MRI coordinate acquisition. The final placement the electrode, typically a few millimeters, so an epileptogenic zone
of the electrodes can now be determined within the range of a few that is just millimeters further away may be missed. In these cases
millimeters. The placement trajectories are chosen to avoid dam- the invasive electrodes will show the spread of the seizure pattern
age to important brain structures or blood vessels. and not the actual origin. When invasive electrodes do not cover
Depth electrodes are most commonly used in the temporal lobe. the cortical area where the seizure originates, the electrodes may
The electrodes can either be implanted from the lateral face toward show the spread pattern after the clinical seizure begins.
the mesial structures or from occipital positions toward mesial Invasive EEG recordings lead in 1–4% of patients to complica-
temporal structures in a sagittal trajectory. The former allows dis- tions (hemorrhages or infections with consecutive hemiparesis,
tinguishing between mesial and lateral temporal activity; the latter hemianopsia, or aphasia) [49,66], which are mostly temporary,
can identify parieto-occipital spread patterns. Basal frontal or me- but should only be accepted as risks when a clear gain in informa-
sial frontal and parietal areas can be investigated very well with tion on seizure localization is expected. Invasive electrodes should
depth electrodes, whereas the placement of subdural electrodes therefore be used only after extensive noninvasive EEG studies
can be technically challenging in these locations. The approach have been performed and did not localize the epileptogenic zone
should be guided by the clinical question. Depth electrodes can well enough, but they were the grounds on which a testable
also be used in patients where dura and cortex may be attached hypothesis of the seizure onset zone could be built [30].
after bacterial meningitides, hemorrhages, or trauma.
3.3.4. Electrocorticography
3.3.3.2. Subdural strip or grid electrodes. Subdural strip electrodes Intraoperative electrocorticography (ECoG) was introduced sev-
can be implanted through bore holes to investigate the basal, me- eral decades ago to determine the extent of resection, mostly in
sial, and lateral temporal cortical surface. They can also be im- partial temporal lobe resections. The resection could be enlarged
planted in the interhemispheric surface after trepanation. if epileptiform activity could still be recorded from the remaining
Subdural grid electrodes also require a craniotomy. Subdural grid tissue. As for intraoperative electrical stimulation, ECoG has strict
electrodes are especially valuable because large, connected areas time constraints and is usually limited to less than 30 minutes of
can be examined and exact cortical mapping is possible (Figs. 5 recording. The importance of resecting areas with interictal epilep-
and 8). One of their disadvantages is that the cortex in deep sulci tiform activity is not well studied, and the zone from which inter-
may not be covered. Only spread out of the sulcus will be visible ictal epileptiform activity can be recorded is typically far larger
in the electrode derivations. Also, after trauma, hemorrhages, or than the actual seizure onset zone. ECoG most likely does not con-
infections, the dura and cortex may be inseparable and the implan- tribute much to standardized procedures like an anterior temporal
tation of subdural electrodes may not be possible. lobe resection, but may be helpful in determining the extent of
resection in more diffuse pathologies such as focal cortical dyspla-
3.3.3.3. Epidural electrodes. A less invasive method to locate the epi- sia [67]. Some ECoG findings that were thought to be specific to fo-
leptogenic focus employs epidural electrodes [61]. Epidural elec- cal cortical dysplasia [67] were obtained in other pathologies [68]
trodes are placed on the dura through bore holes. Typically, and, therefore, seem not to be as specific as previously thought.
penlike or mushroom-shaped electrodes are used. Some centers
use strips with several electrodes that are epidurally inserted 4. How good is therapy?
through a bore hole. The mushroom-shaped electrodes require
one bore hole per electrode. Epidural electrodes were used to cover Where the usefulness of EEG as an aid to diagnosis of seizure
larger areas of the convexity, but mesial cortex areas could not be disorders is established, its role as a guide to monitoring treatment
investigated and basal temporal cortex could be investigated only is much less certain [69]. The EEG may reflect unspecific central
with epidural strip electrodes. Their use has steadily declined since nervous side effects of the standard AEDs such as carbamazepine,
the advent of functional imaging studies (PET, ictal SPECT) and the valproate, phenytoin, benzodiazepines, and phenobarbital [70].
improvement of MRI techniques [61]. Their disadvantages are that All standard AEDs may result in slowing of the dominant rhythm
they cannot be used for electrical stimulation of the cortex and that and increased slow activity. Carbamazepine, in particular, is often
their signal-to-noise ratio is not as favorable compared with that of associated with apparent deterioration of background activity,
subdural electrodes. even in the face of clinical improvement. Less information is avail-
able on the newer AEDs [71]. Benzodiazepines and barbiturates re-
3.3.3.4. Foramen ovale electrodes. Foramen ovale electrodes come to sult in increased fast activity [69]. Intravenous benzodiazepines
rest in the cisterna ambiens and ideally receive their electrical sig- and phenytoin result in both acute seizure control and suppression
nal from the parahippocampal gyrus and neighboring areas. They of IEDs.
were introduced to reduce the risk of intraparenchymal depth elec- There is a very close correlation between control of clinically
trodes [64]. The implantation closely follows the method used for detected seizures and EEG events for patients with absence epi-
blocking the stellate ganglion in patients with trigeminal neuralgia. lepsy and 3-Hz SWCs [69]. In some, but not all, patients with other
Foramen ovale electrodes can record signals from the mesial tem- seizure disorders, there is a positive correlation between number
poral lobe areas and are an alternative to depth electrodes, which of seizures and amount of IEDs. For seizures other than absences,
are implanted in the brain parenchyma [60]. They are used to lat- and AEDs given in the medium and long term, there is generally
eralize temporal lobe epilepsies. In extratemporal epilepsies they not a clear relationship between control of seizures and IEDs
can be used to document the spread to the temporal lobe. Compli- [69]. In studies of children whose epilepsy is in remission, persis-
cations are described to be low, even in patients with previous sur- tent IEDs have been associated with a higher risk of seizure relapse
gery [65]. should AEDs be discontinued, but in adults the relevance of persis-
tent IEDs appears to be much less certain. The risk for seizure re-
3.3.3.5. Disadvantages and risks of invasive electrodes. Even though lapse is increased if the EEG showed the slowing prior to
surface EEG recordings are less sensitive in detecting epileptiform medication withdrawal (relative risk = 2.4) [72].
32 S. Noachtar, J. Rémi / Epilepsy & Behavior 15 (2009) 22–33

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