The extratemporal lobe epilepsies in the epilepsy monitoring unit.

Extratemporal lobe epilepsies (ETLE) are characterized by the epileptogenic foci outside the temporal lobe. They have a wide spectrum of semiological presentation depending upon the site of origin. They can arise from frontal, parietal, occipital lobes and from hypothalamic hamartoma. We discuss in this review the semiology of different types of ETLE encountered in the epilepsy monitoring unit.

Introduction

Extratemporal lobe epilepsies (ETLE) are characterized by the epileptogenic foci outside the temporal lobe. They have a wide spectrum of semiological presentation depending on the site of origin. They can arise from frontal, parietal, occipital lobes. We discuss in this review the semiology of different types of ETLE encountered in epilepsy monitoring unit.

Semiology of Frontal Lobe Epilepsy (FLE)

FLE is the second most common epilepsy syndrome in adults. Approximately 18% of patients referred to tertiary care centers for pharmacoresistant focal epilepsy have FLE.[1] Frontal lobe seizures are challenging to diagnose and can be mistaken for non-epileptic events, such as psychogenic seizures, parasomnias and movement disorders. The clinical manifestations are extremely diverse but certain features suggest ictal origin from the frontal lobe. According to the specific part of frontal lobe affected semiology will differ.

General Features of Seizures Originating from Frontal Lobe

Auras are relatively less often reported in patients with FLE. Palmini and Gloor examined experiential phenomenon in seizure patients and found that auras were found in 93% of patients with temporal lobe onset versus only 61% with frontal lobe onset.[2] Non-specific auras have been reported in patients with seizure foci in the frontal lobe. Patients usually report non-specific, unexplainable feeling, often localized to the head (“cephalic aura”).[3] Asymmetric tonic seizures originating in the supplementary motor area are often preceded by a somatosensory aura. Autonomic auras like nausea or palpitations as well as emotional auras such as fear are also reported from seizure arising from the frontal lobe.

The duration of seizures are significantly shorter in the frontal lobe seizure compared those originating from temporal lobes and usually last less than 1 min. Secondary generalization occurs in 70% of patients with FLE. Nocturnal preponderance and a significant association with sleep-wake cycle have been reported[4] Consciousness is usually preserved in seizures originating from the frontal lobe. Even if consciousness is impaired, it is for a very brief period. If seizures of frontal lobe onset spread to the temporal lobes, postictal confusion, as typical for temporal lobe seizures, can also be observed. Clustering of seizures is also frequent in FLE. Convulsive and non-convulsive status epilepticus are frequently observed in FLE.

Clonic activity and asymmetric tonic posturing are typical of frontal seizures and of all the possible frontal seizure symptoms and signs, motor manifestations remain the most frequent and important, observed in 90% of patients.[5] Complex motor automatisms, including bicycling and thrashing movements, sexual automatisms, laughter and vocalizations, may result in misdiagnosis as psychogenic seizures and when present early in the attack, seem to be particularly characteristic of certain types of FLE.[6]

Kotagal et al. compared the behavior in patients with mesial temporal lobe epilepsy to patients with FLE and found that repetitive, proximal upper extremity movements, complete loss of consciousness, complex motor and hypermotor (large repetitive movements of the proximal musculature, i.e., bicycling movements) activity were more common in the frontal lobe seizures.[7]

Division of Frontal Lobe

FLE can be further subdivided into:

Dorsolateral frontal

Mesial frontal

Basifrontal.

Semiology of Dorsolateral Frontal Lobe Seizures

Dorsolateral frontal lobe can be further divided into central lobe, prefrontal and premotor cortex.

Central lobe

Somatosensory auras, which include unilateral paresthesia restricted to the hand, face, tongue or foot, have specific localizing value to the contralateral central lobe. Unilateral myoclonic and or clonic seizures affecting the distal parts of the body like the face or tongue also suggest involvement of contralateral central lobe. In a seizure emanating from central lobe the typical evolution pattern will be: (i) Focal clonic seizures with Jacksonian march without secondary generalization, usually accompanied by ipsilateral head version and followed by postictal paresis; and (ii) somatosensory aura often followed by tonic posturing and head version or clonic seizures. They are characterized by preservation of consciousness.[8]

Premotor cortex

Seizures originating from premotor cortex are characterized by version followed by motor manifestation like automatism. The version of the head and eyes is due to involvement of the frontal eye fields. Studies show that forced head deviation is contralateral to the frontal lobe seizure focus in >90% of patients.[9] The direction of version is not a consistently reliable guide to lateralization of the seizure. There could be associated speech arrest if the brocas area is involved. 90% of patients had prolonged postictal aphasia in patients with seizure originating from dominant frontal lobe and spreading to the ipsilateral temporal lobe.[10]

Prefrontal cortex

The seizures originating from the prefrontal cortex are the least well-characterized of all frontal seizures. The semiology in such patients is diverse and extremely complex. Bancaud and Talairach have reported differences in semiology in seizures emanating from ventromedial prefrontal cortex from dorsolateral prefrontal cortex (DLPF).[11]

Ventro-medial prefrontal cortex

There is intense reaction to fear, with a frightened facial expression, screaming and abrupt agitation. This is distinct from the subtle feeling of fearfulness felt in temporal lobe epilepsy. Motor manifestations include bizarre gestures, repetitive movements, bicycle peddling, pelvic thrusting and shouting, often charged with emotional and aggressive features. Associated autonomic signs such as mydriasis, tachycardia and facial flushing are common.

Dorso-lateral prefrontal cortex

Tonic deviation of eyes preceding version along with gestural automatism directed toward the direction of gaze suggests involvement of the dorslateral prefrontal seizures. Associated compulsive forced acting component is often seen complex motor patterns like semirhythmic tapping of the hands or feet or grasping motions along with asymmetrical tonic or dystonic posturing of upper and/or lower limbs.

Vocalization may occur; unlike the pattern seen in medioventral seizures, this often does not appear to have an initial emotional modification. Such vocalizations may be non-verbal (e.g. groaning) or verbal (e.g. palilalia, jargon, swearing and singing). Visual hallucinations may also be reported in seizures from this region; these can include dimming or blurring of vision and more rarely actual hallucinations, either simple, such as coloured shapes, or what have been described as “psychical” illusions. “Forced thinking” may occur, consisting of a recurrent intrusive thought or an overwhelming impulse to perform a certain act (e.g. to open the eyes, or to grab something).

Another form of seizure reported from DLPF is “frontal absence.” The patient loses contact with his environment, but may still respond to his surroundings in a slow and inappropriate way. These seizures can be brief and distinct, but longer episodes lasting hours have also been reported. Associated partial or completely amnesia for events occurring during the episode is seen. The ictal electroencephalogram (EEG) pattern consists of generalized disorganized spike-wave activity, a pattern similar to that described for absence status in adults.

Mesial Frontal Epilepsy

The mesial surface area can be further divided into primary motor cortex for the lower limb, the supplementary sensorimotor area (SSMA), the anterior cingulate cortex and the prefrontal cortex. Of these, the anterior cingulate cortex and the SSMA have been most extensively studied in terms of focal epilepsy.

The seizures arising from the SSMA are generally frequent, occurs in clusters and are more common during the non-rapid eye movement Stage I and II of sleep. These seizures typically present with abrupt onset with bilateral, asymmetric, tonic posturing of the extremities lasting 10-30 s along with facial grimacing, with vocalization or speech arrest and absence of postictal confusion.[12] The tonic posturing may be unilateral with involvement of a single limb but predominantly involves the proximal and axial musculature. Penfield and Jasper described “the arm being raised and the head and eyes turned as though to look at hand” which is called the “fencing posture.”[13] Ajmone-Marsan and Ralston created the term “M2e” to describe tonic abduction and external rotation of the shoulder with flexion of the elbow.[14] Before tonic posturing, a somatosensory aura consisting of “tingling” or a feeling of tension, pulling or heaviness in a limb or the impression of impending movement of the limb may precede the tonic seizure. The sensation may be relatively focal, involving a portion of a limb, lateralized with both upper and lower limbs involved simultaneously and a poorly defined bilateral sensation in the head. Postictal manifestations are absent or mild and short-lived. Their shorter duration, stereotypical nature, occurrence in sleep, and the presence of a tonic contraction of the abducted upper extremities distinguish SSMA seizures from non-epileptic attacks. These postures are often accompanied by vocalizations and preserved awareness.

Other semiologies may also be associated with mesial frontal lobe onset, including: hypermotor seizures, dialeptic seizures, focal clonic seizures of the lower limb and negative myoclonus.

Absence type seizures are characterized by altered consciousness and minimal motor manifestations. The patient loses contact with his environment. He may still respond to his surroundings to some degree but in a slow and inappropriate way. These seizures can be brief and distinct, but they may also last hours or even days. These episodes, when prolonged, can present like a type of non-convulsive status epilepticus. Although this condition has also been called “spike-wave stupor,” this term is somewhat misleading because of the great variability in the level of altered consciousness from a barely perceptible change to bland unresponsiveness. For example, during prolonged episodes of this type of non-convulsive status, patients may seem normal but complain of being mildly confused. They may also be partially or completely amnestic for events occurring during the episode despite appearing alert. The ictal EEG pattern consists of generalized disorganized spike-wave activity, a pattern similar to that described for absence status in adults. It is, therefore, important to differentiate this type of frontal lobes seizure from idiopathic generalized absence seizures, as they may be clinically and electrographically similar.

Hyperkinetic seizures usually begin abruptly, almost explosively, with the onset of complex behavioral automatisms. Patients may jump around, thrash, rock to-and-fro, pound on objects or rock back and forth. Bicycling movements or stepping movements are frequently described. Along with the motor manifestations there is extensive vocalization with screaming, yelling, shouting, humming, grunting, laughing, or barking. The patient may swear and produce understandable speech. The prominent motor features distinguish them from the automatisms seen in temporal lobe seizures and have been called “hypermotor automatisms.” Hyperkinetic seizures further can be divided into two types.[15] The first, manifests with marked agitation with body rocking, kicking, or boxing and associated with a facial expression of fear and is associated with ictal foci in the ventromesial frontal cortex, The second variety manifests with mild agitation with either horizontal movements or rotation of the trunk and pelvis and usually accompanied by tonic or dystonic limb posturing was seen primarily in seizures arising from the mesial premotor cortex, mesial intermediate frontal cortex and dorsal anterior cingulate cortex. Hyper kinetic seizures have been reported to be also associated with the origin in the orbitofrontal or anterior cingulate areas, frontopolar and dorsal frontal origin.[16]

Cingulate gyrus epilepsy frequently present with complex stereotypic movements, in particular thrashing, kicking, grasping and running with or without vocalization. Behavioral disturbances such as motor or verbal aggression, paranoid delusions and personality changes including autistic, obsessive-compulsive and self-mutilating behavior have been described. Fear with or without a matching facial expression and laughter without mirth may be an early manifestation in mesial frontal lobe seizures.

Basal frontal lobe epilepsy

Unpleasant olfactory auras can occur with activation of the orbitofrontal part of the gyrus rectus. Autonomic seizures in the form of objective evidence of autonomic change including cardiovascular (tachycardia, bradycardia, asystole, arrhythmia), respiratory (hyperventilation, apnea, dyspnea and stridor), gastrointestinal (epigastric aura, vomiting, spitting, defecation), cutaneous (piloerection, pallor, flushing), papillary (mydriasis, miosis) or urogenital (urinary urge, sexual/orgasmic aura, genital aura, sexual and genital automatisms) manifestations. To establish that such an event is a seizure simultaneous EEG recording is required.

Semiology of Occipital Lobe Seizures

Occipital lobe epilepsy (OLE) appears to account for 2-13% of extratemporal epilepsies.[1718] Ictal clinical symptoms of the occipital lobe seizures are subjective, objective, or both.[1920] The signs and symptoms of OLE can be divided into.

Signs and symptoms due to discharge from the occipital lobe itself or

Signs and symptoms due to discharge propagation outside occipital lobe.

Visual Hallucinations

Visual hallucination is considered one of the hallmark of the occipital lobe seizures but occur only in 47-85% of patients.[21] Subjective visual hallucinations can be positive (seeing objects) or negative (not seeing objects). Different type of visual hallucinations have been reported. Elementary visual hallucinations are the most common, characteristic and well-defined ictal symptoms of the occipital lobe seizures. Most common patterns in ictal elementary hallucinations are generally multicolored. Shapes vary and can be circular, square, triangular and rectangular. Their location at the onset is usually unilateral, mainly in the temporal visual hemifield. They may appear in a normal, blind, or damaged hemifield. Central or undefined localization occurs in 10-30% of patients. Elementary visual hallucinations that may be limited to the contralateral hemifield occur in 50-60% of cases.[22] If they appear in the upper quadrant, the seizure discharge is below the calcarine fissure. Symptoms in the inferior quadrant have an analogous anatomical relationship. The visual hallucination may move horizontally, usually from the side contralateral to the seizure focus. The side of unilateral elementary visual hallucinations is contralateral to the epileptogenic focus. Conversely, this is ipsilateral to the epileptogenic focus for unilateral visual hallucinations, moving horizontally toward the other side.[23]

Complex visual hallucinations

Complex visual hallucinations are less commonly seen in the occipital lobe origin than temoral lobe origin.[24] These may take the form of persons, animals, objects, figures or scenes. They may be familiar, friendly or frightening and may appear in a small or large area of a hemifield, or in the center or whole of the visual field, may be static or move horizontally. When compared with the hallucinations of temporal lobe seizures, occipital seizures do not have the emotional component to it.[25]

Ictal amaurosis

Ictal amarousis has been reported to be the second most common symptom of OLE.[22] They may be missed if not questioned for specifically. Visual loss is usually bilateral, but homonymous hemianopsia contralateral to the seizure discharge can also occur. Ictal amaurosis usually consists of a blackout, but whiteouts or diffuse perceptions of color can occur. Ictal amaurosis can be prolonged and represent status epilepticus amauroticus.

Visual illusions

Visual illusions can present when seizure origin is from the occipital-temporoparietal junction. Simple illusions are where objects appear distorted and seem to have changed in size (macropsia or micropsia), shape (metamorphopsia), illumination, color or clarity. Lines may appear wavy (dysmorphopsia), objects may appear inclined (plagiopsic) and there may be a loss of color (achromatopsia). Complex illusions are where objects appear disorientated in distance (macroproxiopia, microtelepsia), appear to be distant and minute (teleopsia), appear to have a loss or enhancement of stereoscopic vision, or are persistent or recurrent (palinopsia).

Motor phenomenon

Seizures arising from the occipital lobe can also present with ocular motor signs and symptoms such as forced eye blinking, eyelid flutter, nystagmus, eye movement sensation and ocular deviation.

The sensation of eye movement in the absence of detectable movement has been reported as a sign of occipital seizure.[26] Examination of patient during the ictus may pick up subtle signs such as eye deviation, epileptic nystagmus and eyelid blinking and flutter. Tonic deviation of the eyes with or without head deviation is frequently reported in seizures beginning in the occipital lobe.[1727] The ictal focus is almost always contralateral to the movement of the head and eyes. Nystagmus as a manifestation of epileptic discharges has been reported repeatedly, but there is no consensus regarding its lateralizing value.

Up to 50% of patients have forced blinking or eye fluttering with occipital lobe seizures.[26] Visual seizures develop rapidly within seconds and they are usually brief, lasting from a few seconds to 1-3 min, rarely longer. Exceptionally, they last for more than 30 min constituting focal visual status epilepticus.[2829]

Clinical Presentation Due to Propagation

Owing to the unique topographical location of the occipital lobe, it allows multiple possible propagation patterns.[15] The seizures can spread above or below the sylvian fissure, medially or laterally, ipsilateral or contralateral to the side of the origin. The occurrence of complex visual hallucinations following elementary visual hallucination, suggest propagation to the limbic or neocortical structures.[23] Automatisms, which suggest typical temporal lobe origin occur if the spread is to temporal lobe. Suprasylvian spread results in various focal tonic and clonic motor manifestations. Postictal headache occurs in >50% of cases and can be confused with migraine. Ictal vomiting, eye deviation and autonomic features also point toward occipital lobe origin and are seen classically in the benign childhood seizure susceptibility syndrome described by Panayiotopoulos.[30] Table 1 summarizes objective and subjective signs of OLE.

Table 1

Semiology of seizures arising from occipital lobe

Semiology of Seizures Originating from Parietal Lobe

Parietal lobe epilepsy (PLE) accounts for a very small percentage of extratemporal epilepsies. Clinical semiology is difficult to study as much of the parietal lobe is silent with respect to clinical seizure manifestations. There is also dearth of literature because less frequent involvement of this lobe. In addition, some aspects of seizure-induced parietal lobe dysfunction might not be apparent without specific testing like testing of various cortical somatosensory functions.

These seizures emanating from the parietal lobe are mainly simple focal events that manifest with subjective symptoms, such as somatosensory, somatic illusions, vertiginous, visual illusions or complex visual hallucinations, receptive or conductive linguistic disturbances, in the order of prevalence. These clinical seizure manifestations are usually related to the epileptogenic location, anterior or posterior, of the dominant or the non-dominant parietal lobe. Onset with simple sensorimotor manifestation is usually associated with anterior parietal lobe foci, whereas more complex symptomatology emanates from the posterior regions.

Subjective Signs

Patients with PLE most commonly experience somatosensory auras. These include various types of paresthetic, dysesthetic and painful sensations.

Paresthesia

Paresthesia is the most common sensory phenomenon experienced in PLE. They are usually lateralized contralateral to the side of seizure onset. These include a feeling of numbness, “pins and needles” sensation and sometimes an unpleasant crawling sensation. They remain localized although in 40% of patients they may exhibit a march similar to Jacksonian motor seizure.

Ictal pain

Ictal pain is rare, and is usually suggest parietal lobe seizure origin. The pain usually consists of a burning, unpleasant dysesthesia with lateralization and distribution characteristics similar to those described for paresthesias.

Alien hand phenomenon

Another rarely encountered symptom is the sensation that a body part, usually a hand, does not belong to the person.[31]

Vertigo

Vertigo and other vertiginous sensations or illusion of rotatory body movement are reported in about 10% of the parietal lobe seizures and are elicited predominantly from the temporal-parietal border.

Sensations of movement

During vertiginous seizures, the environment may appear to move. In addition, the sensation of a body part movement without observable movement has been reported as a symptom of the parietal lobe seizure activity. Disturbances of body image and somatic illusions are the second most common ictal symptom of PLE. They include illusions of distorted posture, limb position or movement, a feeling that an extremity or a body.

Objective Signs

Parietal lobes are primary responsible for processing sensory information and thus very few objective ictal signs are reported.[22] Demonstrable language dysfunction and abnormal reactions to unpleasant stimuli, such as severe pain have been reported. Inhibitory motor or paralytic seizures can be associated with parietal lobe seizure origin. Ictal hemiballism has been associated with seizure onset in the inferior parietal lobule or the parietal operculum.

Signs and Symptoms of Seizure Propagation

Semiological manifestation depends on the direction of spread of seizure. Anterior spread to frontal lobes results in unilateral clonic activity, asymmetric tonic posturing or contralateral version. Posterior propagation to occipital cortex results in a patient experiencing elementary visual hallucinations or ictal amaurosis. Anterior spread can produce focal clonic motor activity. Posterior parietal lobe seizure origin is most often associated with spread to the temporal lobes. Propagation to temporal lobe produces alteration in consciousness and automatism. In a series of 82 patients with PLE, 57%presented with unilateral clonic activity (spread to precentral cortex), 28% with tonic posturing (SMA involvement) and 17% with oral or gestural automatism and 4% had complex automatisms.[26]

Semiology of Seizures Originating From Hypothalamic Hamartomas

The prototypical seizure type associated with hypothalamic hamartoma is the gelastic seizures. They are usually the first seizure type and occur very early in life. The gelastic seizures are usually very brief (duration < 20 s) and frequent (usually with multiple gelastic seizures per day). They mimic true laughter but more often are peculiar and mirthless even to the casual observer, and may incorporate behavioral elements of grimacing or crying (dacrystic seizures). They may or may not be associated with altered consciousness, which is often difficult to determine in infants. Other additional types of seizures develop in 80% of patients. Complex partial seizure, and other generalized seizure types can include tonic-clonic, tonic, atonic, or even absence can be seen along with the classic gelastic seizures.

Table 2 summarizes the different localizing and lateralizing signs seen in ETLE.

Table 2

Lateralizing and localizing features of extratemporal lobe epilepsy