"Supplementary motor area (SMA) seizure" rather than "SMA epilepsy" in optimal surgical candidates: a document of subdural mapping

PURPOSE: To clarify the relationship between epileptogenic zone and supplementary motor area (SMA) in patients who were regarded as the optimal surgical candidates for their intractable SMA seizures. METHODS: We analyzed the epileptogenic zone at/or adjacent to the SMA in four patients with clinical SMA seizures. All four patients had noninvasive presurgical evaluations (long-term video/EEG monitoring, MRI, and neuroimaging with radioisotopes), which provided convergent results between ictal semiology and the epileptogenic area, and thus, they had chronically implanted subdural electrodes, and finally had focus resection with a follow-up period of more than 2 years. RESULTS: Three patients had lesions shown by MRI outside the SMA, and one patient had a lesion within the SMA. Interictal epileptiform discharges were seen at/or outside the SMA. Ictal EEG pattern originated from the SMA in one patient, from the high lateral frontal area in two patients, and from the precuneus in one patient. In the latter three patients, the ictal EEG pattern immediately spread to the SMA. Those ictal onset zones were consistently localized within/or just adjacent to the lesions revealed by MRI. Only one patient had SMA resection, and three had the resection of epileptogenic zone by preserving the SMA. No neurological deficits developed and good seizure control was achieved. CONCLUSION: Among surgical candidates for intractable SMA seizures, frontal cortex other than SMA or even parietal cortex can be epileptogenic, and thus, the SMA itself may not necessarily have to be resected. This notion is clinically important when selecting surgical candidates as well as when planning presurgical invasive evaluation in patients with intractable SMA seizures.     

额叶癫痫的特点及手术治疗

目的 :分析额叶癫痫的临床特征、发作期及发作间期脑电图特点 ,探讨额叶癫痫手术治疗。方法 :应用视频脑电图对 9例额叶癫痫患者进行长程监测 ,并对其中 6例记录颅内脑电图。分析癫痫发作的临床表现及脑电图特点 ,定位致痫灶 ,行手术切除。结果 :额叶癫痫的发作特点为 :发作频繁而短暂 ,以睡眠期发作为主 ,常见过度运动 ,姿势性强直 ,发声等发作症状。发作期可见棘波节律 ,广泛低幅快活动 ,节律性慢波等特征性脑电活动。颅内电极记录可清晰显示异常脑电活动的发作起源及扩散情况 ,有助于定位致痫灶。手术切除病灶及致痫灶 ,效果满意。结论 :额叶癫痫是一组具有特征性的癫痫综合征 ,颅内电极记录有助于揭示其脑电活动变化。对于难治疗性额叶癫痫 ,准确定位致痫灶是手术成功的关键。     

Magnetoencephalography and diffusion tensor imaging in gelastic seizures secondary to a cingulate gyrus lesion

Gelastic seizures are relatively uncommon and rarely observed secondary to frontal lobe lesions. This report presents magnetoencephalography (MEG) and diffusion tensor imaging (DTI) findings in an adolescent with gelastic seizures secondary to a left anterior cingulate gyrus lesion. Ictal scalp video EEG showed bilateral frontal 4 Hz theta discharges. Interictal EEG showed left fronto-temporal spikes or sharp waves. Interictal MEG showed spike sources over bilateral temporal regions. DTI and tractography delineated slightly shifted corpus callosum posterior to the lesion, unaffected uncinate and inferior longitudinal fasciculi. The patient became seizure free for 12 months after surgical excision of a pleomorphic xanthoastrocytoma in the left anterior cingulate region. In our patient, MEG and EEG did not localize the deep-seated epileptogenic zone. The combination of DTI and neurophysiologic studies, however, possibly disclosed neuronal connections within the epileptic network and indicated that epileptic discharges propagated via the uncinate fibers from the primary epileptogenic zone in the anterior cingulate region to the mesial temporal region in this case with gelastic seizures secondary to a cingulate lesion.     

Alumina cream-induced focal motor seizures in cats. V. Unilateral lesions of the brain-stem reticular formation

The effect of unilateral mesencephalic (MRF) and pontine (PRF) lesions on EEG-EMG patterns of type B and C alumina cream induced focal motor seizures was studied on cats with chronically implanted electrode and cannula lesion systems. EEG patterns included number, amplitude and contralateral propagation of type B spikes and occurrence and duration of type C tonic-clonic discharges. EMG patterns included changes in muscular multiple unit activity (EMG-MUA) time locked to the onset of type B spikes and to the onset (tonic OTCD) and the end (clonic ETCD) of type C tonic-clonic EEG paroxysmal discharges. (1) MRF lesions ipsilateral to the cortical epileptogenic focus significantly increased number, amplitude and propagation of type B EEG spikes and the occurrence, but not the duration, of type C EEG tonic-clonic discharges. They also reduced amplitude of type B muscular jerks and blocked type C tonic contradversion with a significant decrease in EMG-MUA time locked to the onset of type B spikes and type C paroxysmal EEG discharges. (2) PRF lesions contralateral to the cortical epileptogenic focus produced an effect on muscular contractions of type B and C seizures similar to that produced by ipsilateral MRF lesions. PRF lesions, however, did not significantly change the EEG patterns of type B and C seizures. (3) Neither MRF lesions contralateral nor PRF lesions ipsilateral to the cortical epileptogenic focus produced significant changes on EEG and EMG patterns of types B and C epileptic seizures.     

An angiographically occult arteriovenous malformation in the medial parietal lobe presenting as seizures of medial temporal lobe origin

We present an unusual case of a patient who was diagnosed with temporal lobe epilepsy and whose seizures were reduced markedly after excision of an angiographically occult arteriovenous malformation (AVM) located in the left medial parietal lobe. A 38-year-old man had complex partial seizures characterized by motionless staring with oroalimentary and behavioral automatisms since the age of 15 years. Magnetic resonance imaging (MRI) demonstrated a small lesion extending from the left posterior cingulate gyrus to the precuneus. There was no MRI evidence of mesial temporal sclerosis. Intracranial EEG recordings showed ictal onset from the left medial parietal lobe propagating to the medial temporal lobes. Clinical signs appeared when these discharges reached the temporal lobes. After excision of the lesion (which was histologically confirmed as an AVM), together with the marginal cortex, seizures were reduced significantly. Careful diagnostic evaluation of lesions such as the this one may reveal an epileptogenic lesion (zone) far from the region where scalp ictal discharges seem to arise. In our case, we hypothesize that false localization was due to propagation of ictal discharges from the parietal focus through the limbic system.     

The neurobiological substrates of behavioral manifestations during temporal lobe seizures: A neuroethological and ictal SPECT correlation study

Ictal behavior coupled with SPECT findings during 28 seizures in patients with temporal lobe epilepsy (TLE) with unilateral hippocampal sclerosis (13 left; 15 right) was displayed as flowcharts from right-sided (RTLE) plus left-sided (LTLE) seizures. Ictal SPECT was classified blind to neuroethology. Behaviors were categorized as ipsilateral to the epileptogenic zone (IL), contralateral to the epileptogenic zone (CL), or bilateral. SPECT intensity and region were categorized as IL or CL to the epileptogenic zone. All patients developed automatisms and had hyperperfusion in their temporal lobes. Patients’ verbal responses to questions had statistical interactions in RTLE but not in LTLE sum. Most CL dystonic posturing was correlated to IL basal ganglia hyperperfusion. Basal ganglia activation occurred in seizures without dystonic posturing and CL manual automatisms, and lack of IL dystonic posturing and the presence of CL cerebellar hemispheric hyperperfusion were also observed. Coupling of neuroethology and SPECT findings reliably evaluates ictal behavior and functionality of associated brain areas.     

Successful epilepsy surgery with a resection contralateral to a suspected epileptogenic lesion.

We report on a case of frontal lobe epilepsy in an eight-year-old girl. Seizure semiology and EEG indicated an epileptogenic zone localized in the mesial frontal structures, without clear-cut lateralization. MRI showed a lesion in the right cingulate gyrus, initially regarded as a hamartoma. Ictal SPECT did not have a localization value. MR spectroscopy revealed two metabolic abnormalities: one in the area of the MRI lesion and a second contra-laterally. Invasive monitoring using subdural electrodes covering the convexity and mesial part of the right frontal lobe including mesial strips with bilateral contacts was used. The invasive monitoring failed to localize ictal onset in the right hemisphere; however, electric stimulation induced seizures from electrodes facing the left supplementary sensorimotor area ("through" the falx cerebri). We re-implanted the electrodes over the left frontal lobe and the second invasive monitoring clearly localized the ictal onset zone in the left supplementary sensorimotor area, which was subsequently resected. Histopathology found MRI-negative focal cortical dysplasia. The contralateral lesion was reassessed as nonspecific enlargement of perivascular spaces. The patient has been seizure-free for more than two years.[Published with video sequences].     

Successful hemispherotomy in two refractory epilepsy patients with cerebral hemiatrophy and contralateral EEG abnormalities

We describe two cases of refractory epilepsy with cerebral hemiatrophy and contralateral electroencephalographic (EEG) abnormalities, in which hemispherotomy of the atrophic hemisphere effectively controlled seizures. Case 1 was a 5-year-1-month-old girl with refractory bilateral asymmetrical tonic posturing seizures predominantly in the right arm. Magnetic resonance imaging showed left porencephaly corresponding to a left middle cerebral artery infarction. Case 2 was a 3-year-8-month-old boy with refractory bilateral asymmetrical tonic posturing seizures predominantly in the right arm due to atrophy of the left cerebral hemisphere after septic meningitis. Both patients had right hemiparesis and was incapable of pinching by the right hand. Contralateral interictal and ictal EEG abnormalities were observed. Interictal ^99mTc-ethyl cysteinate dimer (^99mTc-ECD) single photon emission computed tomography (SPECT) showed hypoperfusion and ictal ^99mTc-ECD-SPECT showed hyperperfusion within the left cerebral hemisphere. Left hemispherotomy was performed. Cases 1 and 2 remained seizure-free at the last follow-up 18?months and 15?months, respectively, after surgery, and contralateral interictal EEG abnormalities disappeared. In patients with cerebral hemiatrophy and contralateral EEG abnormalities, epilepsy surgery may be considered when the laterality of seizure semiology, functional imaging findings and motor deficits were concordant with the atrophic side. Ictal SPECT is effective to confirm the epileptogenic hemisphere.     

Startle epilepsy associated with gait-induced seizures: Pathomechanism analysis using EEG, MEG, and PET studies

We describe herein a girl who has had startle-induced seizures since she was 3 years old. These seizures were refractory to antiepileptic medications and worsened when the patient was 9 years old, following termination of phenytoin administration because of adverse effects. During this period she could walk only a few steps with support, and sudden drop attacks inevitably occurred. Interictal electroencephalography (EEG) revealed abundant spike–wave activity at the centroparietal midline areas, and ictal EEG of poststartle and gait-induced seizures revealed initial voltage attenuation followed by recruitment of vertex activity, which preceded a tonic or myoclonic–atonic phase. Magnetic resonance imaging (MRI) results were unremarkable, but magnetoencephalography (MEG) and positron emission tomography (PET) suggested the presence of an extensive epileptogenic zone in the bilateral pericentral gyri, and the bilateral paracentral and left precuneus lobules, including the primary motor, supplementary motor, and supplementary sensory areas. The pathophysiologic significance of these structures is discussed.     

Lateralizing value of early head turning and ictal dystonia in temporal lobe seizures: a video-EEG study.

To investigate early head turning, we retrospectively studied videotapes of 262 seizures from 82 patients who were seizure free after temporal lobectomy. Early head movements were arbitrarily classified into non-tonic turning, tonic turning, and absence of turning. Among the 222 seizures which showed early head turning, 168 (75.7%) had non-tonic turning and 54 (24.3%) had tonic turning. The direction of the first head turning was ipsilateral to the epileptogenic foci in 132 (78.6%) seizures with non-tonic turning and in 35 (64.8%) seizures showing tonic head turning. The proportion of seizures with turning towards the ipsilateral side in the presence of tonic and non-tonic head turning were significantly different (P= 0.04). Seventy-four seizures (28.2%) evolved to secondary generalization, more frequently found in seizures with early head turning (P= 0.0015) and especially those showing tonic turning (P< 0.0001). The direction of head turning immediately preceding secondary generalization was contralateral to the lesion side in 53 seizures (82.8%). Dystonic upper limb posturing occurred in 86 seizures (32.8%), exclusively contralateral to the seizure focus, whereas 65 (75.6%) were associated with initial head turning ipsilateral to the focus. In summary, temporal lobe seizures with tonic head turning tends to secondarily generalize and the direction of head turning before secondarily generalized was contralateral to the seizure foci. Earlier in the seizures the direction of non-tonic head turning tends to be towards the epileptogenic hemisphere. In addition, dystonic posturing of the extremities is a significant lateralizing sign to the contralateral hemisphere in temporal lobe seizures.     

Propagation of tonic posturing in supplementary motor area (SMA) seizures

We analyzed ictal motor symptoms in 10 patients diagnosed to have supplementary motor area (SMA) seizures based on ictal encephalographic (EEG) findings and ictal clinical semiology. Inclusion criteria were (1) EEG seizure pattern in the vertex for the scalp recording or in the area over and/or adjacent to SMA for epicortical recording and (2) ictal motor semiology characterized, as previously reported, by sudden and a brief tonic posturing of extremities and trunk mainly occurring during sleep without loss of consciousness. In 50% (5/10) of the patients, tonic posturing began in one part of the body and moved to other part(s) in 5-10s. Unlike Jacksonian march seen in seizures involving the primary sensorimotor area (S1-M1), it spread in no accordance with the somatotopy in S1-M1. The sequential propagation of tonic posturing may represent the somatotopic organization within the SMA proper.     

An infant with multiple cavernous angiomas presenting with frequent epileptic seizures - detection of epileptic focus by magnetoencephalography

We report on a six-year-old girl with frequent partial seizures secondary to multiple cavernous angiomas (CAs) since the age of 17 months. MRI showed two CAs in the left parietal and right frontal lobes. Ictal scalp video EEG demonstrated complex partial seizures of left hemispheric origin, indicating that the left parietal CA was the epileptogenic lesion. Ictal SPECT showed extensive hyper-perfusion in the left frontal and parietal lobes, indicating the left hemispheric focus. Magnetoencephalography (MEG) showed clustered equivalent current dipoles of interictal spikes in the left parietal cortex adjacent to the left parietal CA. We performed lesionectomy of the left parietal CA at 19 months old. The patient became seizure-free for four years. Postoperative MEG yielded no residual interictal spikes. Our study suggests that early surgical intervention of CA may prevent from further development of epileptic seizures. MEG can identify both the epileptogenic zone and lesion underlying the multiple CAs in the infants with catastrophic partial seizures.     

Ipsilateral blinking seizures during left fronto-temporal ictal pattern on scalp EEG.

We report an infant with left eye blinking seizures accompanying a left (ipsilateral) fronto-temporal scalp EEG ictal pattern. The epileptogenic lesion was a left frontal encephalomalacia along the ventriculo-peritoneal shunt tract. The shunt was inserted for treatment of communicating hydrocephalus. This case illustrates the lateralizing value of the ictal blinking. Review of the literature suggests that seizures with unilateral blinking are likely to be produced by activation of ipsilateral trigeminal fibers innervating subdural intracranial structures and pial vessels in temporal and frontal lobes. Ipsilateral blinking could also be produced by activation of the ipsilateral cerebellar hemisphere.     

Surgical treatment for musicogenic epilepsy

We report a patient with medically intractable musicogenic epilepsy (ME) who was treated with surgery. Using the non-invasive methods of ictal and interictal electroencephalography (EEG), MRI, interictal single photon emission computed tomography and clinical manifestations, we first localized the musicogenic seizures (MS). The ictal onset zone was then further localized using intracranial EEG to the middle part of the left superior temporal gyrus. Surgical resection of the epileptogenic zone was then performed. The patient had two seizures within 2 weeks post-operatively, but has then had no seizures during the following year (Engel class II). The results suggest that patients who have medically intractable ME combined with unilateral ictal onset zones should be considered for the surgical treatment of epilepsy.     

Ictal Contralateral Paresis in Complex Partial Seizures

Summary: Certain behaviors that occur during a complex partial seizure (CPS) are useful in lateralizing the side of seizure onset. In 5 (5.3%) of 94 consecutive patients with partial epilepsy, we observed ictal unilateral arm and hand paresis during 27 of 34 CPS. In all these seizures, this behavior occurred contralateral to an epileptogenic temporal lobe, as determined by video-EEG monitoring and surgical outcome. In 5 of the 27 seizures, an observer demonstrated that the paretic arm and hand were flaccid. None of these patients had postictal (Todd's) paralysis. In most of the seizures, the arm ipsilateral to seizure onset had simultaneous purposeful movements or automatisms, sometimes with awkward posturing. Ictal unilateral paresis is distinctly different from ictal dystonia or postictal paralysis and consistently lateralizes seizure onset to the contralateral temporal lobe. Recognition of this particular ictal behavior and comparison to other simultaneous behaviors can aid in the lateralization and possibly localization of the epileptogenic zone.     

Frontal Lobe Seizures: Electroclinical Syndromes

Summary: To define further the electroclinical manifestations of frontal lobe epilepsy (FLE), we studied 150 seizures manifested by 24 patients; 18 patients had subdural electrode arrays (SEA). The findings in these patients clearly overlapped presumably reflecting the interconnections between functionally related frontal zones; yet the manner in which the symptoms clustered and the sequence in which they occurred generally indicated the anatomic site of the epileptogenic zone. We divided the patients into three major groups: (a) those with supplementary motor seizures, (b) those with focal motor seizures, and (c) those with complex partial seizures (CPS, psychomotor seizures). Supplementary motor seizures began with tonic posturing of the extremities. Focal motor seizures generally began with conscious contralateral version or unilateral clonic focal motor activity; tonic posturing was noted only late in the seizure. CPS (psychomotor) began with unresponsiveness at onset, followed by staring or unconscious contraversion. We compared frontal lobe seizures with temporal lobe seizures reported previously; oral-alimentary automatisms, repetitive hand movements, or looking around, were more common in temporal lobe seizures, whereas tonic posturing and bicycling movements were more common in frontal lobe psychomotor seizures.     

Neck atonia with a focal stimulation-induced seizure arising from the SMA: pathophysiological considerations

A 28-year-old patient with pharmacoresistant non-lesional right frontal epilepsy underwent extra-operative intracranial EEG recordings and electrical cortical stimulation (ECS) to map eloquent cortex. Right supplementary motor area (SMA) ECS induced a brief seizure with habitual symptoms involving neck tingling followed by asymmetric tonic posturing. An additional feature was neck atonia. During atonia and sensory aura, discharges were seen in the mesial frontal electrodes and precentral gyrus. Besides motor signs, atonia, although rare and not described in the neck muscles, and sensations have been reported with SMA stimulation. The mechanisms underlying neck atonia in seizures arising from the SMA can be explained by supplementary negative motor area (SNMA) - though this was not mapped in electrodes overlying the ictal onset zone in our patient - or primary sensorimotor cortex activation through rapid propagation. Given the broad spectrum of signs elicited by SMA stimulation and rapid spread of seizures arising from the SMA, caution should be taken to not diagnose these as non-epileptic, as had previously occurred in this patient.     

Localising and lateralising value of ictal piloerection

BACKGROUND: Piloerection is a rare clinical symptom described during seizures. Previous reports suggested that the temporal lobe is the ictal onset zone in many of these cases. One case series concluded that there is a predominant left hemispheric representation of ictal cold. The aim of this study is to evaluate the localising and lateralising value of pilomotor seizures. METHODS: Medical records of patients who underwent video electroencephalogram (EEG) monitoring at the Cleveland Clinic between 1994 and 2001 were reviewed for the presence of ictal piloerection. The clinical history, physical and neurological examination, video EEG data, neuroimaging data, cortical stimulation results, and postoperative follow ups were reviewed and used to define the epileptogenic zone. Additionally, all previously reported cases of ictal piloerection were reviewed. RESULTS: Fourteen patients with ictal piloerection were identified (0.4%). Twelve out of 14 patients had temporal lobe epilepsy. In seven patients (50%), the ictal onset was located in the left hemisphere. Four out of five patients with unilateral ictal piloerection had ipsilateral temporal lobe epilepsy as compared with the ipsilateral side of pilomotor response. Three patients became seizure free after left temporal lobectomy for at least 12 months of follow up. An ipsilateral left leg pilomotor response with simultaneously recorded after-discharges was elicited in one patient during direct cortical stimulation of the left parahippocampal gyrus. CONCLUSIONS: Ictal piloerection is a rare ictal manifestation that occurs predominantly in patients with temporal lobe epilepsy. Unilateral piloerection is most frequently associated with ipsilateral focal epilepsy. No hemispheric predominance was found in patients with bilateral ictal piloerection.     

Fall related to epileptic seizures in the elderly

It is well known that both falls and epileptic seizures are very frequent and harmful in the elderly. Moreover, although seizures may cause falls, their relationship is poorly documented in this population. We report four women (mean age: 84.5 years) who presented falls with: late‐onset focal seizures of possible parietal (Case 1) or frontal localisation (Case 2), early onset with late aggravation of juvenile myoclonic epilepsy (Case 3), and generalised situation‐related myoclonic seizures (Case 4). Falls were presumably associated with tonic posturing of left (Case 1) or right (Case 2) hemibody, to bilateral and massive myoclonic jerks (Cases 3 and 4) with a loss of consciousness (Case 3). The diagnosis of seizures was difficult and routine EEG was unremarkable in Cases 1 and 2, requiring video‐EEG monitoring to capture the clinical events. Adequate treatment offered recovery from seizures and falls in all patients. Other mechanisms of seizure‐induced falls in older patients and their management are discussed. In conclusion, falls may be caused by different seizure types and appear to be underestimated due to difficulties in seizure diagnosis in the elderly. Recognizing falls related to seizures is important in geriatric practice, as it facilitates adequate management.     

Intracranial EEG findings in patients with lesional lateral temporal lobe epilepsy

PURPOSE: Intracranial EEG in patients with lesional lateral temporal lobe epilepsy is rarely reported. Therefore, the number of patients with seizures arising independently from ipsilateral mesial structures or contralateral hemisphere has not been clarified. We analyzed the intracranial EEG of cases with localized lesion in the lateral temporal cortex. METHODS: We studied 15 patients who satisfied the following criteria: (1) MRI depicted a lesion less than 4cm in diameter located lateral to the collateral sulcus and at least 3cm posterior to the temporal pole; (2) intracranial EEG with electrodes placed on bilateral temporal lobes captured at least one complex partial seizure; and (3) postoperative follow-up period of 2 years or longer. The mean age of seizure onset was 16.6 years (range, 11-25) and that at surgery was 26.7 years (range, 16-36). RESULTS: A total of 147 complex partial seizures, 51 simple partial seizures, 16 secondarily generalized seizures, and over 80 subclinical seizures were recorded. On the lesional side, many clinical seizures were recorded from the lateral cortex. Independent of the lateral temporal onset seizures, ictal discharges originating from the mesial temporal structures were recorded in 7 of 15 patients (47%). Moreover, onset of ictal discharges from the contralateral temporal lobe was recorded in 7 of 15 patients (47%). Interictal spikes from ipsilateral mesial structures were recorded in all patients. The presence of ipsilateral mesial onset seizures was not associated with hippocampal neuron losses. CONCLUSION: Intracranial EEG analysis revealed that approximately one-half of the patients with structural lesions in the lateral cortex showed independent epileptogenic areas in ipsilateral mesial structures. Although ictal discharges originating from the contralateral temporal lobe were recorded in a half of these patients, this finding does not constitute a contraindication of resective surgery. Interictal spike is not an indicator of whether mesial structures should be resected.