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Seizure Semiology

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104 views

Seizure Semiology

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kashif mansoor
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© © All Rights Reserved
We take content rights seriously. If you suspect this is your content, claim it here.
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Review

Eur Neurol 2010;63:3–10 Received: August 7, 2009


Accepted: September 30, 2009
DOI: 10.1159/000258634
Published online: November 14, 2009

Seizure Semiology:
An Overview of the ‘Inverse Problem’
Andrea O. Rossetti a Peter W. Kaplan a, b
a
Service de Neurologie, Centre Hospitalier Universitaire Vaudois and University of Lausanne, Lausanne, Switzerland;
b
Department of Neurology, Johns Hopkins Bayview Medical Center, Baltimore, Md., USA

Key Words The inverse problem is commonly referred to as the


Ictal manifestations ⴢ Postictal manifestations ⴢ process of identifying the brain source of the discharges
Focal seizures ⴢ Lateralization ⴢ Localization ⴢ Epilepsy recorded on the scalp surface. Furthermore, in correlat-
ing the ictal source with the clinical expression or presen-
tation of epilepsy, the description of focal seizure mani-
Abstract festations is commonly made with reference to an in-
In clinical practice, a classification of seizures based on clini- volved side or lobe. Usually, however, the anatomic origin
cal signs and symptoms leads to an improved understand- of particular seizure signs or symptoms is often not
ing of epilepsy-related issues and therefore strongly contrib- known at initial presentation. Therefore, one may also
utes to a better patient care. The inverse problem involves postulate an inverse problem for the issue of anatomo-
inferring the anatomical brain localization of a seizure from clinical correlation, i.e., how to infer the epileptogenic (or,
the scalp surface EEG, a concept we apply here to correlate in a less favorable case, the symptomatogenic) focus from
seizure origin with seizure semiology. The spheres of senso- the analysis of seizure semiology.
rium, motor features, consciousness changes and autonom- A seizure classification based exclusively on semiology
ic alterations during ictal and postictal manifestations are (i.e., independently from other ancillary information,
reviewed, including several subdivisions used to better cat- such as EEG or neuroimaging) is believed to improve and
egorize particular features. Particular attention is given to complement the clinical information data needed for pre-
behavioral features, as well as to features occurring in idio- surgical evaluation, as it has been pointed out by the
pathic generalized epileptic syndromes and psychogenic ‘Cleveland School’ [1, 2]. Indeed, four spheres have been
nonepileptic spells. Copyright © 2009 S. Karger AG, Basel identified: sensorial (auras), motor, consciousness, and
autonomic; special categories may be added if none of the
preceding sphere applies. Seizures affecting conscious-
ness may be labeled as ‘dialeptic’ in order to avoid confu-
sion with syndromes (e.g., absence). Motor seizures are
divided into simple and complex (hyper- and automotor).
This paper is dedicated to the memory of Edward B. Bromfield, MD Finally, atonic, astatic, hypomotor (when consciousness
(1951–2009). is not testable), akinetic, negative myoclonic and aphasic

© 2009 S. Karger AG, Basel Dr. Andrea O. Rossetti


0014–3022/10/0631–0003$26.00/0 Service de Neurologie, CHUV-BH07
Fax +41 61 306 12 34 CH–1011 Lausanne (Switzerland)
E-Mail [email protected] Accessible online at: Tel. +41 21 314 1220, Fax +41 21 314 1290
www.karger.com www.karger.com/ene E-Mail andrea.rossetti @ chuv.ch
manifestations may also occur as special manifestations in seconds, and may be contra- or ipsilateral [7]. SMA
[1]. involvement elicits diffuse contralateral or bilateral tin-
Here we review current knowledge regarding ictal and gling, and a sensation of movement [3, 9], the semiology
postictal manifestations of focal seizures, focusing first is thus very similar to S2 involvement.
on symptoms and signs, and then inferring seizure ori- A lateralized ictal headache is usually ipsilateral to a
gin. While several items reflect the reviews by the Cleve- temporal or occipital focus [3], whereas preictal headache
land group, to which we refer for further reading [1, 2], has been reported in up to 11% of pharmaco-refractory
we add some recently analyzed features, such as gusta- patients with localization-related epilepsy; it may result
tory sensations, multiple auras, several psychic and be- from increased blood perfusion, or release of neuropep-
havioral manifestations, hyperkinetic and gyratory sei- tides [10]. Postictal headache, conversely, is relatively fre-
zures, nonclonic ictal hand motions, and changes in car- quent, and of no localizing value, apart from the idio-
diac rhythm. We conclude by reviewing data regarding pathic focal epilep-sies of childhood, where, again, it
idiopathic generalized epilepsy (IGE) and psychogenic points to a posterior focus.
nonepileptic seizures. A systematic description of the dif- Gustatory auras are also related to the insular region
ferential diagnosis towards nonepileptic disorders and [7, 11]; they often display a metallic-rubbery character,
the phenomenology of peri-ictal psychosis are beyond the and occur with other sensory changes related to S2 in-
scope of this paper. volvement, or unpleasant sensations of the pharynx: the
early combination of visceral, somatosensory and motor
signs, especially if involving the buccopharyngeal region,
Sensory Phenomena has recently been described to suggest an insular focus
[12]. Visual phenomena of elementary colorful character,
Auras are ictal sensory phenomena occurring at the but also including amaurosis, arise from the contralat-
beginning of a focal seizure and with preserved con- eral occipital lobe, and present a more formed character
sciousness, and are reported by 22–83% of the patients if involving the associative cortex located more rostrally
[3]; the longer the subsequent seizure, the higher the like- [3, 13]. Elementary auditory manifestations are produced
lihood of forgetting the aura. Furthermore, auras seem to in the primary auditory cortex [14]; if unilateral, these
be less prevalent after seizures arising from the dominant phenomena point to the contralateral hemisphere [3, 15],
temporal lobe as compared to the nondominant, and in since most auditory fibers cross within the brainstem.
seizures occurring during sleep [4]. An aura is the result Complex auditory auras arise from the temporoparietal
of the first involved symptomatic region, and needs to be junction. Musicogenic seizures may have an acoustic
differentiated from nonspecific prodromes. The latter, aura: two types of events have been described. One aris-
characterized mainly by headache, vague nonascending ing from the laterotemporal regions (auditory cortex), the
and long-lasting abdominal sensations or dysphoria, may other from the mesiotemporal structures (emotional
precede (focal) seizures by many minutes (usually 15) [5]; component) [16]. The delay between the auditory trigger
up to 17% of the patients with epilepsy may report them and the seizure onset suggest that these events are due to
[5]. In contrast, auras are generally experienced immedi- involvement of auditory association areas, rather than
ately prior to the loss of consciousness. Interestingly, sen- being simple reflex seizures occurring from the primary
sory auras are invariably recognized as pseudohallucina- auditory cortex [17]. Olfactory sensations are the result of
tions by patients [3], meaning that their unreal character activation of the anterior mesiotemporal lobe (‘uncinate
is readily identified. fits’), and are nearly always unpleasant, consisting of
Somatosensory phenomena most often arise from the smells of burning or rotten nature [3]. Vertigo might be
parietal lobe (primary somatosensory cortex, S1) [6], or elicited by the insular-parietal-temporal junction [6, 18];
more rarely from the posterior insula-parietal operculum it appears to be a very rare symptom and needs to be dif-
(supplementary somatosensory area, S2) [7, 8]; they may ferentiated from the much more frequently reported, un-
also occur during supplementary motor area (SMA) sei- specific prodromal ‘dizziness’. Viscerosensory manifes-
zures [3]. Localization can be inferred according to the tations are often characterized by stereotypical feelings
following features: auras related to S1 are well localized, of nausea, ascending sensations, and occasionally pain,
discriminatory, and spread relatively slowly (like a sort of and occur shortly before the rest of the seizure. Although
‘jacksonian march’), whereas symptoms arising from S2 these are most often encountered in mesiotemporal sei-
are ill-defined, often accompanied by pain, spread with- zures, especially at the onset, similar manifestations may

4 Eur Neurol 2010;63:3–10 Rossetti /Kaplan


be elicited after stimulation of the insula, SMA, and the Mouth deviation also shows a high PPV of 92% (contra-
thalamus [3]. lateral), especially if accompanying forced head version
Although patients reporting several different experi- [29].
ences preceding a loss of consciousness may raise con- Nonversive head turning (seemingly purposeful) is
cerns about possible nonepileptic seizures, the pattern of less common, occurring in about 25%, and has an 80%
multiple auras was recently observed in 0.4% of subjects PPV for ipsilateral lateralization mostly within the tem-
undergoing long-term EEG monitoring [19]. Interesting- poral lobe [29], often occurs at the beginning of mesio-
ly, a strong predominance of nondominant hemispheric temporal seizures, and is practically never followed by a
lateralization was found, mostly involving the temporal generalization [31]; it is probably the consequence of the
or posterior regions, probably leading to more accurate involvement of basal ganglia, and, if arising from the
reporting following the relative preservation of language frontal lobe, has been described in orbitofrontal, fronto-
in these cases. polar or dorsofrontal seizures [31]. Ipsilateral version may
also be observed at the end of a generalized convulsion
[30]. Of note, one possible source of confusion are sei-
Psychic Manifestations zures originating form the SMA, where the head may
turn in either direction as compared to the focus [9].
This group of symptoms has also been defined rather Focal clonic or tonic activities also have an excellent
as being part of ‘complex internal’ sensory manifesta- lateralizing value, since these are almost invariably con-
tions, since ‘psychic’ may be perceived as an ambiguous tralateral to the triggering hemisphere; the movements
term [20]. These manifestations are dominated by experi- arise after involvement of the motor cortex in the frontal
ence of déjà-vu, which points to a mesiotemporal origin lobe [29].
without lateralizing value [21]; this is however not spe- Hyperkinetic seizures arise from the orbital or mesial
cific of epilepsy. Another interesting symptom is forced regions of the frontal lobe, where they tend to occur in
thinking, which has been reported to be related to frontal brief and frequent attacks, often out of sleep [32]; how-
(more verbal character) or mesiotemporal (more emo- ever, they may be also observed in seizure arising from
tional features) regions of the dominant hemisphere [22]. the temporal lobe, when the discharges reach the frontal
Ictal fear has been related to involvement of the amyg- lobe [33], as well as from the anterior insula [34]. In this
dala and is a relatively frequent reported symptom; rarer context, seizures with violent behavioral manifestations
phenomena are ecstatic auras, which are also related to and fear tend to arise from the ventromesial frontal re-
the amygdala [23, 24]. None of these phenomena have gions, whereas relatively mild, horizontal movements
clear lateralizing values. These have to be differentiated coupled with dystonia are mostly seen when the mesial
from an orgasmic aura, also an uncommon feature aris- premotor cortex is involved [35]. Gyratory seizures have
ing for the nondominant mesiotemporal, or more rarely been reported to result from activation of the contralat-
parasagittal parietal regions, and possibly with female eral frontotemporal region if heralded by forced head
predominance [25, 26]. Ictal autoscopy, an exceptional turning, and ipsilateral if presenting with an en bloc ver-
phenomenon characterized by the sight of the patient’s sion of the body [36]; furthermore, rotations around the
body from outside it, has been linked to the nondominant horizontal body axis seem to be predictive of a mesial
parietal lobe [27, 28]. frontal origin [37].
Asymmetric termination of the clonic phase has a pre-
dictive value of around 80%: the last cloni are ipsilateral
Head and Limb Movements to the seizure onset in both temporal and frontal lobe sei-
zures [38]. Postictal paresis (Todd’s phenomenon) is an-
Head version is probably the most frequently encoun- other excellent lateralizing sign [39]: it is consistently con-
tered sign in focal seizures [15, 29], occurring in 35–40%. tralateral to the seizure onset, with a median duration of
Forced and sustained (15 s) head and eyes deviation has only 3 min, and without a difference between temporal
a positive predictive value (PPV) of 94% for contralateral and frontal seizure origin [40]. It has been mainly associ-
localization, mostly in the temporal or frontal lobes, ris- ated with unilateral dystonia and ictal limb immobility.
ing to 100% if accompanied by neck extension and im- The latter is actually a rare phenomenon [41], suggesting
mediately followed by generalization [15, 29]. It is thought an active inhibitory process, described in lesions of the
to arise from the involvement of the frontal eye field [30]. primary somatosensory area [42], the temporal lobe [41],

Seizure Semiology, an Overview of the Eur Neurol 2010;63:3–10 5


‘Inverse Problem’
or the prefrontal cortex [43]. Accordingly, the ipsilateral involvement of the midbrain reticular formation during
head turn and the resulting variant of gyratory seizure dominant temporal lobe seizures as compared to non-
could possibly be interpreted as a consequence of a con- dominant [52]. Postictal nose wiping has an excellent lat-
tralateral neglect. eralization value (190%) to the ispilateral side (temporal
lobe more than frontal lobe) [15]; it could be the conse-
quence of a contralateral postictal paresis. Different from
Eye and Eyelid Movements automatisms are rhythmic ictal, nonclonic hand motions,
in the form of low-amplitude milking, grasping, or pill-
Unless accompanying a headturn (see above), isolated rolling movements [53]; they have been described as an
sustained eye movements are relatively uncommon. Iso- early contralateral sign in temporal lobe epilepsy, preced-
lated eye deviation per se does not seem to have a lateral- ing dystonic posturing, and occurring in about 10% of
izing value, especially in young children [39]. Unilateral them.
blinking points to an ipsilateral, mostly temporal or fron-
tal seizure focus [44], but might also be encountered in
occipital seizures [45]. Ictal nystagmus is the consequence Behavioral and Phasic Manifestations
of a contralateral hemisphere seizure, either in the re-
gions responsible for contralateral saccades, or in the lo- Ictal speech has been described in up to 10–20% of
cations inducing ipsilateral smooth pursuit [39, 46, 47]. complex-partial seizures, and shows a PPV of about 80%
pointing to the nondominant temporal lobe [29], whereas
postictal dysnomia, encountered in roughly the same
Dystonic Posturing percentage, has a 100% PPV for the dominant hemisphere
[29]. Ictal vocalizations are mostly seen during frontal
Unilateral limb dystonia occurs in about 20–37% of lobe seizures, especially from the orbitofrontal and para-
focal seizures, and has a PPV of 93% for a contralateral sagittal regions [45], but may also present as a loud scream
focus [15, 29]; it is more often encountered in temporal at the beginning of generalized seizures.
than frontal lobe seizures, probably after involvement of Behavioral arrest and consciousness impairment are
the basal ganglia. A variant is the sign of four [48], in characteristic for seizures arising from the temporal lobe,
which the extended arm is contralateral to the seizure the cingulum or the orbitofrontal region [45]; when the
onset. Tonic limb posturing is not exclusively seen in temporal lobe is involved, this semiology suggests a lat-
temporal lobe epilepsy, but is also a feature of frontal lobe eralization towards the dominant side [54]. Late loss of
and SMA seizures. In the latter case, the lateralizing val- contact (1 40 s into the seizure) is observed in mesiotem-
ue is very poor, according to the tight interhemispheric poral seizures as opposed to laterotemporal seizures, hav-
connections at this level [49]. A fencing posture has been ing an early onset of consciousness impairment [18]. In
described by Penfield and Welch [50], although in its clas- this context, seizure duration may also help to differenti-
sical form it is not frequently encountered [9]; more often, ate mesio- from laterotemporal onset, the former often
one observes a head turn with asymmetric posturing of having longer seizures with rare generalizations (up to
the upper limbs: the most extended limb suggests a focus 2/year) [18]. If the SMA is primarily involved, conscious-
in the contralateral hemisphere, especially if accompa- ness may be preserved. The same, despite bilateral motor
nied by unilateral clonic activity. manifestations, also occurs in insular seizures, [7] or as
exceptional phenomenon in laterotemporal lobe seizures
[55].
Automatisms Rarely, ictal humming or singing may be observed;
they are reported in about 1% of patients admitted to an
Unilateral automatisms occur in about 25% of focal epilepsy unit [56]; anatomically, temporal lobe and pre-
seizures, showing a 100% PPV for ipsilateral focality, frontal cortex have been implicated, as part of the net-
mostly in the temporal lobe, or the limbic structures and work underlying musical processing and without clear
the orbital regions of the frontal lobe [29, 45]. Interest- lateralization.
ingly, ictal automatisms with preserved consciousness, a
rare phenomenon, point to the nondominant, mesiotem-
poral lobe [51]. This might be explained by a preferential

6 Eur Neurol 2010;63:3–10 Rossetti /Kaplan


Autonomic Manifestations atisms and lateralizing signs, especially in temporal lobe
epilepsy [71]. This likely reflects dynamic brain matura-
A very rare but intriguing sign is represented by pilo- tion across different ages.
motor phenomena. If unilateral, they point to an ispilat-
eral focus with temporal lobe involvement, probably fol-
lowing activation of the amygdala, the insula, or the pos- Focal Signs in Generalized Epilepsies
terior hypothalamus [57].
Ictal tachycardia is very frequent and has no localizing It is important to bear in mind that the discussed signs
value, conversely, ictal bradycardia or asystole are very are not specific for focal seizures: focal phenomena may
rare phenomena [58]. They are related to temporal lobe occur in IGE, and thus represent potentially misleading
foci, with no lateralizing value, as they are probably in- features. In a retrospective study, focal EEG signs were
duced by bilateral activation of mesiotemporal and in- reported to occur in 35% (7/20) of mostly medically re-
sular regions [59, 60]. Dyspnea is also linked to the in- fractory IGE patients, and clinical signs pointing to a fo-
sula [7]. cal origin also occurred in 35% (7/20, 2 patients had both
Ictal spitting has been related to the nondominant EEG and clinical focal features), including the figure of
temporal lobe [61]. Although the same region has been four, nose wiping, unilateral dystonia, head version, and
implicated in cases of vomiting [62], ictal nausea and postictal hemiparesis [72]. In another observation, forced
vomiting probably occur following activation of the an- ictal head version was found in 5/20 subjects with IGE,
terior insula [63]. and 2 of them had version to the other side in other sei-
Ictal laughing (gelastic seizures) classically occurs in zures [37]. Even gyratory seizures have been described
children with hypothalamic hamartoma, but may be ob- [37, 73]; again, the rotation sense may change from one
served in temporal or, more rarely, frontal (cingulus) sei- seizure to the other. Recently, asymmetric termination of
zures in adults [64], no lateralization value is recognized. the tonic phase has also been described in about 20% of
As a rule, it is not accompanied by emotional perception primarily generalized seizures [38]. It has also been re-
of happiness, but temporal foci may rarely induce laugh- ported that patients with IGE may mention auras in the
ter with mirth; furthermore, hypothalamic gelastic sei- seconds or minutes before a seizure, with a prevalence (up
zures are generally brief. Ictal smiling (without laugh- to 70%) similar to that of subjects suffering from localiza-
ing) is probably more frequent, having been reported in tion-related epilepsy [74]; as compared with the latter, pa-
up to 6–11% of patients undergoing long-term monitor- tients with IGE tend to perceive their warnings in the
ing [65, 66]. It is most often encountered in nondomi- midline of the body and to have a less discriminatory
nant, posterior (temporo-parieto-occipital) localiza- (precise) anatomical character. Visual auras are also de-
tions. Ictal weeping (dacrystic seizures), again with no scribed, and they tend to occur as very brief flashing sen-
particular accompanying feelings, has been rarely de- sations [75]. All these falsely localizing signs might reflect
scribed in mesiotemporal seizures without a clear later- the occurrence of – mostly nonspecific – structural brain
alization [67, 68]. abnormalities, which have been described in up to 1 in 4
Other autonomic manifestations, such as mydriasis patients with IGE and, again, seem to correlate with the
and flushing, have no specific localizing value, as they degree of EEG focal features [76], a not uncommon oc-
may be associated with mesiotemporal, insular and fron- currence in this diagnostic group [72, 77].
tal (parasagittal, orbitofrontal) lobe involvement [45].
The same applies for urinary incontinence [69], which
seems more common after convulsions (probably follow- Psychogenic Nonepileptic Seizures
ing a sudden rise in intra-abdominal pressure). Inconti-
nence is also encountered in seizures arising from the Patients with psychogenic nonepileptic seizures
parasagittal portion of the fontal lobe [45]. (PNES) account for about 20% of admissions in a long-
It is important to underscore that an age-dependent term monitoring EEG unit [78], and about 10% have con-
occurrence of localizing manifestations seems to occur, current epileptic seizures [79]. Characteristic clinical fea-
paralleling brain maturation. Seizure in pre-school sub- tures suggesting PNES are a very gradual onset or termi-
jects tend to be shorter and to show fewer localizing signs nation of the events, often not followed by a postictal
than those occurring in older children [70]; furthermore, state; discontinuous, irregular, asynchronous motor ac-
as compared to children, adults more often show autom- tivity with a waxing and waning intensity, side-to-side

Seizure Semiology, an Overview of the Eur Neurol 2010;63:3–10 7


‘Inverse Problem’
Table 1. Overview of some ictal or postictal clinical features with regard to anatomical origin and their reliability

Clinical feature Anatomical origin Lateralization Reliability

Well-defined somatosensory symptoms parietal (primary sensory cortex) contralateral high


Unilateral elementary visual phenomena occipital contralateral high
Ascending visceral feelings mesiotemporal, insula, supplementary motor area none moderate
Forced thinking frontal or mesiotemporal dominant hemisphere moderate
Ictal fear amygdala, hippocampus none high
Forced head version frontal, temporal contralateral high
Nonversive head turning temporal ispilateral moderate
Focal clonic activity frontal (primary motor cortex) contralateral high
Unilateral dystonia temporal or frontal (basal ganglia) contralateral high
Nystagmus frontal eye field or parieto-temporal junction contralateral to fast component high
Ictal laughing hypothalamus, temporal, mesiofrontal none moderate
Ictal eye closure nonepileptic seizure none high
Asymmetric termination of cloni temporal, frontal ipsilateral (to the last cloni) high
Postictal paresis frontal, temporal contralateral high
Postictal nose wiping temporal, frontal ipsilateral high
Postictal aphasia/dysnomia frontal, temporal, parietal dominant hemisphere high

head movement, pelvic thrusting, opisthotonic postur- Chvostek sign on gentle percussion of the facial nerve
ing, and preserved awareness during bilateral motor ac- during the spell; furthermore, generally there is no inter-
tivity [80] (table 1). It should be noted that bilateral arm vening cyanosis even after prolonged convulsions of non-
movement with preserved consciousness can occur with epileptic origin. While oral lacerations (including tongue
myoclonic seizures in juvenile myoclonic epilepsy, and bites), and, to a lesser extent, urinary incontinence have
with SMA seizures, and exceptionally in temporal lobe been shown to be highly suggestive of epileptic seizures,
seizures [55]. Ictal eye closure [81], resistance to eye open- or less frequently of syncope, since these signs are only
ing and to the passive release of one arm onto the face are rarely seen after PNES [69], at times patients with PNES
also frequently encountered in PNES and are rather spe- may be hurt during their spells. It is therefore strongly
cific, as is ictal stuttering, although this occurred in only advisable not to rely solely on these features in diagnosing
9% of PNES patients in a one series [82]. However, cata- nonepileptic seizures: in this context, ictal semiology
lepsy (such as when the elevated arm does not fall when alone shows a rather low inter-rater agreement even
released) can occur with complex partial status epilepti- among experienced epileptologists [85]. PNES diagnosis
cus [83]. The postictal breathing pattern is deep, slow and should always be formulated based on video-EEG analy-
loud after epileptic seizures, and superficial and fast after sis of typical events integrated with clinical history, neu-
nonepileptic spells [84]. In our experience, it is not rare rological and psychiatric examinations. Table 1 gives an
to observe concomitant hyperventilation with a positive overview of the most important described features.

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