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Temporal Lobe Epilepsy: Clinical

Semiology and Neurophysiological Studies


María Rosa Querol Pascual, MD

Most partial epilepsy crises originate in the temporal lobe. Two main syndromes have been
described in temporal lobe epilepsy (TLE): mesial temporal epilepsy and neocortical tem-
poral epilepsy. In recent years, the number and types of drugs used to control the crises
have significantly increased, but almost 30% of patients do not have complete control of
their epilepsy. In those cases, surgery is an efficient therapeutic option, especially in the
case of mesial temporal sclerosis. Before surgery, wide and complex neurophysiological
studies are needed to precisely delineate the epileptogenic area. The clinical and neuro-
physiological aspects of TLE that may be useful for understanding this pathologic entity are
reviewed.
Semin Ultrasound CT MRI 28:416-423 © 2007 Elsevier Inc. All rights reserved.

T emporal lobe epilepsy (TLE) is a partial form of epilepsy


that originates in one or several of the anatomic locations
of the temporal lobe, and which can spread through a net-
video-electroencephalography), neuroimaging studies, and
neuropsychological evaluation.

work of neuronal interconnections to the adjacent brain tis-


sue.1
Ethiology of
Approximately 60% of all epilepsy patients suffer from Temporal Lobe Epilepsy
focal epilepsy; in a third of these cases, which are located Surgical treatment of epilepsy permits the realization of
mostly in the temporal lobe,2 there is not sufficient control anatomopathological studies of the cerebral cortex and iden-
following treatment with several antiepileptic drugs.3 tification of the lesions responsible for the epileptic seizures.
According to the classification4 of epileptic syndromes, Sclerosis of the hippocampus is the most frequent cause of
TLE is divided into two main groups: the first and most pharmacoresistant epilepsy originating in the mesial struc-
common is medial epilepsy, in which the crisis originates tures, and is the histopathological finding that most fre-
principally in the temporal medial structures such as the quently occurs following partial temporal lobectomy.3,9,10
hippocampus, entorhinal cortex, amygdala, and parahip- Other possible pathologies are: low-grade tumors, espe-
pocampal gyrus.5 The second type is lateral or neocortical cially in ganglioglioma, malformations of cortical develop-
epilepsy, in which the crisis affects the temporal neocortex, ment, traumatic, and infectious and vascular lesions3,9-11
which includes the superior, medial, and inferior temporal (Table 1).
circumvolutions, the temporal-occipital and temporal-pari- In 5% to 20% of the cases, temporal mesial sclerosis is
etal junctions, and the associative sensorial areas for hearing, associated with other structural lesions, in this case known as
visual, and language functions.1,6,7 dual pathology, and in most patients the second lesion is
Epilepsy surgery is an alternative and effective treatment usually associated with congenital alterations such as dysgen-
for carefully selected patients who undergo a wide range of esis or cortical heterotopia.9,10
presurgical studies, which include clinical history and careful From a clinical point of view a third type of temporal
neurological exploration,8 complex neurophysiological stud- epilepsy exists that does not show lesions in neuroimaging
ies (surface electroencephalogram, superficial, and invasive studies and may be of a hereditary nature.12,13

Department of Neurology, Infanta Cristina Hospital, Complejo Hospitalario


Clinical Semiology of
Universitario de Badajoz (CHUB), Badajoz, Spain. Temporal Lobe Epilepsy
Address reprint requests to: María R. Querol Pascual, MD, Infanta Cristina
Hospital, Avda de Elvas s/n, 06080 Badajoz, Spain. E-mail: rquerolp@ Epileptic seizures are the main clinical characteristics of epi-
hotmail.com leptic syndromes. Their symptoms and signs are produced by

416 0887-2171/07/$-see front matter © 2007 Elsevier Inc. All rights reserved.
doi:10.1053/j.sult.2007.09.004
Clinical semiology and neurophysiological studies 417

Table 1 Etiology of Temporal Epilepsies Of the types of auras that have been described in TLE, the
A. Temporal mesial sclerosis following are the most important.
B. Neocortical epilepsy Visceral-Sensory or Autonomous Auras
1. Defects of neuronal migration
These originate in the insular cortex and amygdala regions
a. Lamination alterations
b. Heterotopic neurons
that have wide interneuronal connections with other cerebral
c. Focal cortical dysplasia zones.17-19
2. Infections The most characteristic of the somatosensory auras, and
a. Bacterial meningitis probably the most frequent due to its high incidence in TLE,
b. Encephalitis is the abdominal sensation or epigastric rising sensa-
c. Cerebral abscess tion.7,14,16,20,21 This epigastric aura is more frequent in the
d. Parasitary infections subtype of temporal medial epilepsy than in temporal lateral
3. Cranial traumatisms epilepsy, although it is not exclusive of the temporal lobe.7,22
4. Tumors In all patients with abdominal aura followed by automatisms
a. Oligodendroglioma the epilepsy is located in the temporal regions.23
b. Astrocytoma
Other autonomous phenomena are: pallor, flushing, cya-
c. Meningioma
d. Glioblastoma
nosis, alterations in cardiac frequency and rhythm, vomiting,
e. Gangliocytoma urinary urgency, piloerection or pupillary alterations.16,21,24
f. Dysembryoplastic neuroepithelial tumor (DNT) Ictal vomiting may be the only manifestation of a partial
5. Vascular malformations simple seizure; it has been related with temporal crises of the
a. Cavernous angioma nondominant hemisphere25-27 and according to other au-
b. Artero-venous malformation thors with crises of the left dominant hemisphere.28,29
6. Cerebral infarction/Stroke Of the alterations of cardiac rhythm, sinus tachycardia is
7. Congenital malformations the most frequently associated with epileptic crises.14,18,21
a. Porencephalic cyst Bradycardia, which can become asystolic, is an uncommon
b. Arachnoid cyst phenomenon.30
c. Temporal encephalocele
C. Familiar temporal epilepsies Psychic or Experienced Auras
1. Dominant autonomous epilepsy with auditory This type of aura is characteristic of TLE and reflects the point
symptoms or lateral temporal dominant epilepsy of junction established between specific cerebral areas and
2. Medial familiar temporal epilepsy important neuropsychological aspects such as memory, re-
Reprinted from “Tratado de epilepsia” (“Treatise on Epilepsy”) by call, or lived experiences.21 In recent years, studies with deep
Asconapé and Gil-Nagel, McGraw-Hill-Interamericana, with per- electrodes have related the limbic structures of the temporal
mission from the publishers.49
lobe with this type of phenomenon.
In these auras the following are included:

the activation of determined cortical regions responsible for Dysmnesic phenomena. These consist of distortions of
generating or propagating these. Thus, through a detailed memory. The most characteristic is déjà vu, which is the
clinical description of the seizure in anamnesis, and studies sensation of having previously lived a determined situation,
with ictal and interictal electroencephalography (EEG) regis- and has been assigned a localizing value at the level of the
ters, different clinical patterns have been identified as char- anterior nondominant temporal lobe.16,31 Jamais vu is the
acteristic of each type of syndrome, and these offer lateraliz- inverse phenomenon, which consists in the inability to rec-
ing and even localizing information in many patients.6,14,15 ognize familiar surroundings.
TLE is characterized mainly by recurrent complex partial The feeling of presentiment is a very infrequent manifesta-
seizures (with loss of consciousness) preceded in a variable tion of temporal aura, and according to Sadler and Rathey it
percentage of cases by epileptic auras that represent simple may have lateralizing value.32
partial seizures.16
Cognoscitive phenomena. These are situations in which per-
We now present a description of the most frequent features
ception of internal or external reality is altered. The main
of both clinical types.
ones are: distortion of appreciation of time, sensation of un-
reality, of depersonalization, changes in body image, and
Epileptic Auras or Simple Partial Seizures what is known as forced thought, which consists of imposed
According to the Classification and Terminology Commis- and intrusive thoughts at the onset of crises.14,21,33
sion of the International League Against Epilepsy (ILAE), the
epileptic aura is a set of symptoms and signs that occur before Emotional phenomena. With regard to affective alterations,
loss of consciousness, of brief duration (between 5 and 30 the most frequent aura is fear associated with a rising epigas-
seconds), and for which memory is retained.4 It is a common tric sensation indicating a mesolimbic localization,7,14,17 and
phenomenon in temporal epilepsy, often of important local- in some cases is related with amygdalar atrophy.34 Panic at-
izing value, and may be the only comitial manifestation or tacks with autonomic and behavioral changes (agitation, pa-
previous symptom to a complex partial seizure. ralysis through terror, calls for help) have been described,
418 M.R. Querol Pascual

and deep EEG recordings have shown that the areas involved the other extremity, which always indicates contralaterality
are situated in orbital-prefrontal regions, in the anterior cin- to ictal discharge.25,40
gular gyrus and temporal limbic cortex, and most frequently Its origin has been attributed to propagation of the dis-
in the nondominant hemisphere.35 Other less frequent charge toward the basal ganglia.40-42
symptoms include sadness, pleasure, sexual emotions,
and anguish.33 Versive head-turning. The localizing and lateralizing value of
this is controversial. It is very frequent in temporal seizures, but
Illusions and hallucinations. Illusions or auditive, visual, or not exclusive to them.
vestibular hallucinations most often have lateral temporal There exists a general consensus on its localizing value
localization.7 when a clearly forced deviation occurs, with sustained and
The most frequent of these are visual hallucinations, which unnatural posturing of the eyes and head, for at least 10
represent up to 20% of patients with temporal lobe crises. seconds, followed by a generalized tonic-clonic convulsion.
They consist of deformations of size, shape, color, move- Origin is contralateral to the movement in more than 90% of
ment, or distance, and in general the right temporal lobe is cases.5,15,20,26 The phenomenon appears when epileptic activ-
most affected.21,31 ity extends to supra-Sylvian structures and involves the fron-
Auditive auras have been described as a buzzing, whis- tal lobe.5
tling, or whining noise, and reflect the activation of Heschl’s
gyrus7,21; they are common symptoms of hereditary temporal Postictal Period
epilepsy.12,13 Focal findings during the postictal period reflect the area of
Olfactory auras are usually unpleasant sensations associ- origin of the crisis, are independent of the region affected
ated, or not, with taste, and are known as uncinated crises. during the propagation of the attack,14,43 and therefore have
Their origin would seem to be in the temporal mesial region great localizing value.
near the amygdala, or in orbital-frontal regions.36 The most The postictal period is clearly related with a confusional
frequent subjacent pathology consists of localized tumors in state that can last several minutes. It is shorter if the epileptic
temporal regions.14,37 focus is located in the right hemisphere.26
Postictal aphasia is more frequent when the epileptic dis-
Complex Partial Crises charge is involved in the dominant hemisphere.5,7,26
In 70% of cases, after the aura there exists a loss of conscious- Less known are the psychiatric symptoms following an
ness associated with a variable neurological symptomatology epileptic seizure, which include depression, anxiety and irri-
with or without secondary generalization, which is followed tability, and even psychotic symptoms.5
by a period of postictal confusion.7 It is therefore possible to
distinguish in the epileptic crisis an ictal period and a postic-
tal period.
Neurophysiological Diagnostic
Tests in Temporal Lobe Epilepsy
Ictal Period
Automatisms. Between 40% and 80% of patients with tem- Detailed clinical history and neurological explorations are
poral epilepsy have stereotyped automatisms, especially oral essential for the initial study of the epileptic patient. Neuro-
alimentary and manual automatisms,7,14,16,38 during crisis. physiological and neuroimaging diagnostic tests are used to
The oral alimentary automatisms most frequently originate in confirm the pathology by attempting to identify the area of
the amygdala and anterior temporal region.7 the cortex where the epileptic discharge originates, known as
Automatisms are involuntary motor activities that in most the irritative zone, and to determine the presence or not of
cases occur with alterations of consciousness, although in 10% subjacent lesion.
of cases of attacks originating in the right hemisphere the patient Surgical treatment in pharmacoresistant epilepsy of the
remains reactive, usually with subsequent amnesia.38 temporal lobe requires an extensive presurgical study includ-
ing studies of classic electroencephalography with surface
Language alterations. These vary greatly in both the critical EEG, video-electroencephalography (VEEG) studies, and the
and the postcritical period. The presence during a crisis of use of more invasive methods with oval foramen, sphenoidal,
intelligible, well-articulated, linguistically correct language, or subdural electrodes, or, in very selected cases, intracranial
also known as ictal speech, is related to the onset of a crisis electrodes.
lateralized to the nondominant temporal lobe, in the supra- The presurgical study is completed with neuropsycholog-
marginal and angular circumvolutions.7,26,39 ical evaluation, and imaging tests such as magnetic resonance
Ictal aphasia and verbal automatisms are more frequent in and cerebral single-photon emission computed tomography
the dominant hemisphere26 in relation to limbic neocortical (SPECT) and positron emission tomography (PET).
structures.7,39

Unilateral dystonic posturing. This is a forced, unnatural Electroencephalography


posturing of a limb, maintained for more than 10 seconds, in Despite technological advances, EEG continues to be essential in
either flexion or extension, with rotation. Its localizing value the study of the epileptic patient. EEG records electrical activity
is very high especially when accompanied by automatisms of of the brain using different types of electrodes. Cerebral electri-
Clinical semiology and neurophysiological studies 419

Table 2 Electroencephalographic Findings in TLE


Electroencephalograph
(EEG) Temporal Medial Epilepsy Temporal Lateral Epilepsy
Ictal EEG Focal rhythmic activity in the theta range (5–9 Hz) Onset of seizure may have a wider
with maximum amplitude in the basal temporal distribution and has typical presence of
electrodes, preceded or not by bilateral irregular activity, polymorphic at 2–5 Hz
hypersynchronic slowdown. in inferior-temporal regions.
Interictal EEG Spike-wave interictal paroxystic alterations, Interictal paroxystic discharges in medium
normally located in the anterior temporal or posterior-temporal derivations.
region. Unilateral or bilateral in 40% of cases.

cal activity has its origin in the ionic currents derived from the ing capacity in 80% of cases, but low localizing capacity due
biochemical processes occurring on the cellular level.44 partly to the relative distance from the irritative zone, and
also to the fact that other anatomic structures are interposed
Surface Electroencephalography
between this zone and the electrodes.8,16 It is, however, a first
Surface EEG is a recording of 20-30 minutes made by applying
step in the assessment of epileptic patients and can guide
the electrodes directly on the scalp. During recordings certain
subsequent studies.47
maneuvers are carried out to provoke critical events such as
Table 2 shows the principal electroencephalographic fea-
hyperventilation or intermittent luminous stimulation. Routine
tures of the two main subtypes of TLE: mesial3,16,22,48-51 and
EEG studies on temporal epilepsy should be performed with the
neocortical or lateral.3,22,45
usual electrodes plus additional anterotemporal electrodes (T1,
T2), or temporal-basal electrodes, and should include record- Video-electroencephalography
ings made during wakefulness and sleep to facilitate reg- Video-electroencephalography (VEEG) monitoring consists
ister of intercritical epileptiform activity.45,46 of simultaneous EEG recording and video recording of the
The main indications for EEG to be performed are: patient’s behavior during a paroxystic event for a prolonged
1. Contribution to the identification of paroxystic events period (Fig. 1).
with clinical suspicion of epileptic crisis. The usefulness of VEEG recordings can be summarized in
2. Classification of the different types of epilepsy and ep- the following points:
ileptic syndromes.
1. They are helpful in the differential diagnosis of epileptic
3. Prognostic usefulness in recurrence of crisis.
crises. VEEG recordings have shown that in 20% to
Interictal activity registered in EEG studies has a lateraliz- 30% of patients the crisis was not epileptic.8,20,52

Figure 1 VEEG: image showing simultaneous video recording with EEG. The vertical line shows real time in EEG and
synchronizes both activities. (Color version of figure is available online.)
420 M.R. Querol Pascual

2. They classify and characterize the type of crisis.8,14,20,48 are electrodes placed in the oval foramen, in the epidural,
3. They quantify the crisis and assess triggering factors, subdural, or intraparenchymatous space.8,47
thus amplifying the interictal information obtained
through conventional EEG.48
4. They identify subtle crises that may go unnoticed by the Foramen Ovale Electrodes
patient and those around him or her. This technique, considered semi-invasive, was designed by
5. They provide presurgical assessment.11 Wieser and coworkers58 using flexible cylindrical electrodes
of between 4 and 8 contacts, which are introduced with
VEEG monitoring should be of sufficient duration to cap-
radioscopic control by puncturing the Gasser’s ganglion
ture a suitable number of crises similar to those habitually
through an oval hole to the ambiens cistern, below and at the
experienced by the patient; to achieve this, it may be neces-
level of the hippocampal gyrus. These studies provide infor-
sary to reduce partially or totally anticomitial treatment.8,11,14
mation on bilateral electric activity originating in the hip-
These prolonged VEEG studies require patients to be hos-
pitalized in specialized units. Some authors, however, pro- pocampal formation and in the circumvolution of the para-
pose the use of VEEG in outpatient clinics with a duration of hippocampus, and reduce the artifacts that are produced
30 minutes, or several hours in cases where patients have during the crisis with EEG recording47,58 (Fig. 2).
very frequent crises, or when the crises can be reproduced Foramen ovale electrodes have two main indications:
by other triggering factors; in these cases the time used is first, to determine whether the origin of the crisis is medial
considered sufficient to obtain a critical recording.8,53,54 basal or not, and second, to determine the laterality in
In these VEEG studies surface or noninvasive electrodes cases of dubious bilateral medial epilepsy, or with normal
may be used in addition to the conventional ones of the cerebral magnetic resonance imaging (MRI).59,60
International 10-20 System55 such as nasopharyngeal, sphe- Few side effects exist; 9% have pain or transitory sensitive
noidal, nasoethmoidal, and supraorbital electrodes, or inva- alterations in the trigeminus area, or infectious complica-
sisve or intracranial electrodes for the assessment of surgical tions, and in less than 1% of cases subarachnoid or intrapa-
candidates.56,57 Of this latter type the most frequently used renchymatous hemorrhage may exist.46,60

Figure 2 Recording during ictal episode. (A) Before seizure. (B) Patient begins to notice epigastric sensation. (C) Patient
also notices tachycardia. Bioelectric manifestations start with beta rhythm in right mesial temporal region (graphic),
and turn into a spike pattern. (Color version of figure is available online.)
Clinical semiology and neurophysiological studies 421

make a cartography by means of electric stimulation


before surgical resection.11
4. In other types of pharmacoresistant extratemporal
epilepsy.63

Subdural Electrodes
Subdural electrodes are the most frequently used. There are
two types: grids or strips, of varying size and configuration
(Fig. 3).
They must be placed by means of craniotomy or trepana-
tion depending on whether grids or strips, respectively, are
used, and are placed on the theoretically epileptogenic
zone.11,61,63 At least 4% of the patients implanted with these
Figure 3 Blanket of 64 subdural electrodes. (Color version of figure electrodes presented important complications, such as men-
is available online.) ingitis, bone infections, intracranial hypertension syndrome,
and subdural or intraparenchymatous hematoma.57
Study with Deep Electrodes
Intracranial electrodes are used exclusively in presurgical Intracerebral Electrodes
studies for assessing patients with pharmacoresistant epi- A variable number of these electrodes (between 5 and 15)
lepsy, as they are invasive and require the use of a complex with various contacts are implanted orthogonally to the ce-
and costly stereotaxic technique. The electrodes are placed rebral cortex in the three axes of the space following the
on or near the zone where the epilepsy is theoretically pro- stereotaxic Talairach atlas.64 The most frequent hemorrhage
duced. and infection complications affect 3% of the patients im-
The main indications for the use of intracranial electrodes are: planted61 (Fig. 4).
1. In patients presenting with clinical semiology, neu- Intracranial recordings should not be considered as an
roimaging studies (cerebral MRI, SPECT, PET), non- initial diagnostic technique, but rather should be seen as a
invasive neuropsychological and neurophysiological complement to the other tests, because they are not exempt
studies with insufficient or incongruous informa- from morbidity.
tion.11,57,59,61,62 In summary, a detailed clinical history combined with
2. In cases of dual pathology or possible neocortical tem- neurophysiological, neuroimaging (specific protocols) and
poral epilepsy.61 functional (PET and SPECT) studies must be carried out
3. In epileptogenic lesions close to the eloquent cortex prior to considering the surgical treatment of pharmacologi-
(motor zone, language area) in which it is necessary to cal-resistant epilepsy.

Figure 4 Deep electrodes.


422 M.R. Querol Pascual

Acknowledgment Clinical and electrographic manifestations of lesional neocortical


temporal lobe epilepsy. Neurology 49(3):757-763, 1997
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Ruber International Hospital, Madrid) for his kind collabo- abdominal aura and its evolution: a study in focal epilepsies. Neurology
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