Neocortical Temporal Lobe Epilepsy

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1 INVITED REVIEW Jeffrey D. Kennedy and Stephan U. Schuele Summary: Neocortical temporal lobe epilepsy (NTLE) comprises a heterogeneous group of epilepsies with focal seizures characterized by auditory, somatosensory, or psychic auras followed by motionless staring, early contralateral clonic activity often secondarily generalizing. Neurophysiologic findings in NTLE are typically a predominance of lateral temporal interictal epileptiform activity (IEA) and an ictal onset pattern consisting of irregular, hemispheric delta slowing. Advanced neurophysiologic techniques such as EEG and magnetoencephalography source imaging can help to determine the area generating the initial and propagated interictal and ictal activities and may limit the number of patients requiring long-term invasive recordings before epilepsy surgery. Key Words: Neocortical, Temporal, EEG, Epilepsy, Neurophysiology. (J Clin Neurophysiol 2012;29: ) reflect involvement of the insular and opercular regions with nausea, palpitation, bilateral or contralateral sensory symptoms, or pain (Ebner, 2008). A rising epigastric sensation is less frequent than in MTLE but still represents one-third of the auras in NTLE. Olfactory, gustatory, or fearful sensations, however, are rare and indicative of a mesial onset (Gil-Nagel and Risinger, 1997). Motionless staring and unresponsiveness are typically the first objective clinical symptoms in NTLE (Pacia et al., 1996), often followed by early contralateral clonic movements (Gil-Nagel and Risinger, 1997). Automatisms, contralateral dystonic posturing, searching head movements, body shifting, hyperventilation, postictal cough, or sigh are more frequently seen in MTLE (Foldvary et al., 1997). Patients with NTLE tend to generalize earlier than patients with MTLE particularly if the onset is from the posterior temporal neocortex (Lee et al., 2006). DEFINITION Temporal lobe epilepsy is typically divided into mesial and NTLE (Walczak, 1995). A distinct electroclinical constellation associated with a specific cause is rare for NTLE but has been described for patients with autosomal dominant temporal lobe epilepsy presenting with focal seizures with prominent ictal auditory phenomena, negative magnetic resonance imaging and usually a good response to antiepileptic medications (Michelucci et al., 2009). The majority of NTLEs, however, are characterized by their etiologic heterogeneity and electroclinical features less typical for the more common mesial temporal lobe epilepsy (MTLE) yet not necessarily specific for NTLE. CLINICAL FEATURES The mean age of onset for NTLE is during early adolescence (Pfander et al., 2002) with a wide range depending on the underlying cause that includes malformations of cortical development, benign tumors such as gangliogliomas, dysembryoplastic neuroepithelial tumors or neurocytomas, vascular malformations (mostly cavernomas), or remote trauma (Lahl et al., 2003). A history of febrile seizures, central nervous system infections, perinatal complications, or head injury is less common than in MTLE and a lucid interval between initial insult and habitual seizures atypical for NTLE (Foldvary et al., 1997). Around two-thirds of seizures are preceded by an aura, which can present with symptoms indicating neocortical temporal involvement such as auditory phenomena, psychic experiences of deja and jamais vu, visual distortions, vertiginous symptoms, aphasia; or From the Department of Neurology, Comprehensive Epilepsy Center, Feinberg School of Medicine, Northwestern University, Chicago, Illinois, U.S.A. Address correspondence and reprint requests to Stephan U. Schuele, MD, MPH, Department of Neurology, Feinberg School of Medicine, Northwestern University, Abbott Hall # 1425, 710 North Lake Shore Drive, Chicago, IL 60611, U.S.A.; s-schuele@northwestern.edu. Copyright Ó 2012 by the American Clinical Neurophysiology Society ISSN: /12/ NEUROPHYSIOLOGIC CHARACTERISTICS Ipsilateral IEA is seen in 80% to 90% of NTLE (Pfander et al., 2002). A unilateral predominance of IEA (defined as.65% of discharges) over the ipsilateral anterior-mesial temporal electrodes was seen in one-third of patients with NTLE, compared with two-thirds of patients with MTLE (Pfander et al., 2002). Twenty-two percent of patients with NTLE had IEA predominance over the lateral temporal electrode derivations on EEG, which was not encountered in the MTLE group (Pfander et al., 2002). However, other studies did not find a significant difference in the interictal surface EEG findings distinguishing neocortical from mesial TLE (O Brien et al., 1996). The ictal pattern in NTLE tends to consist of an irregular, polymorphic delta slowing with lateralized rather than focal temporal distribution at onset (Foldvary et al., 1997). This can be preceded by repetitive spiking or followed by a more rhythmic theta or alpha activity (Ebersole and Pacia, 1996). Patients with NTLE develop more often (55% vs. 26%) and earlier (23 vs. 74 seconds) bilateral ictal changes compared with MTLE (O Brien et al., 1996). By combining scalp with intracranial recordings, Pacia and Ebersole (1997) demonstrated that the more regular 5- to 9-Hz subtemporal and temporal scalp EEG pattern associated with MTLE requires the recruitment of adjacent inferolateral temporal neocortex. These authors also demonstrated a regional attenuation or low voltage fast followed by irregular 2 to 4 Hz activity in seizures with a lateral temporal propagation. The authors concluded that EEG patterns of temporal lobe seizures are not a direct reflection of cortical activity at seizure onset but rather an expression of the ictal evolution, propagation, and synchronization and hence have a limited specificity for the actual seizure onset zone. ADVANCED CLINICAL NEUROPHYSIOLOGY Source Localization Electric source imaging and magnetic source imaging have become important noninvasive techniques not only to understand 366 Journal of Clinical Neurophysiology Volume 29, Number 5, October 2012

2 Journal of Clinical Neurophysiology Volume 29, Number 5, October 2012 FIG. 1. Interictal sharp wave, regional left temporal phase reversing at the right sphenoidal electrode (FP2). Displayed in longitudinal bipolar montage (sensitivity 10 mv, LF 1 Hz, HF 70 Hz). the neurophysiologic and anatomical substrate of the scalp EEG but also an important additional step in the investigation of candidates for epilepsy surgery. The EEG dipole modeling is a useful addition to the surface localization of the EEG field potential, and it has been demonstrated that the orientation of the EEG dipole is often a better predictor of the involved anatomical structure than the location of the absolute maximum (Ebersole, 2000). Spikes characterized by a vertex positivity and an inferior temporal negative maximum are generated by the inferior-basal cortex and are typically associated with MTLE. Spikes presenting with a horizontal or radial orientation typically reflect involvement of the temporal neocortex. Source imaging can be applied to the ictal discharges as well and shows a similar preponderance of basal activity for MTLE and lateral source activity for NTLE (Assaf and Ebersole, 1997). Magnetoencephalography offers head modeling, which is less distorted by the skull and has a higher spatial accuracy combined with higher sensitivity for tangential sources (and reduced sensitivity for radial source; Ebersole and Ebersole, 2010). Combining EEG and magnetoencephalography source analysis is therefore more likely to model the full extent of the radial and tangential vectors. A lateral maximum of IEA suggests a neocortical epilepsy or a more extensive epileptogenic zone, often warranting further invasive EEG evaluations (Iwasaki et al., 2002). Not only the maximum but also the preceding propagation of a source dipole should be taken into consideration. A source with an early component over the lateral cortex with a maximum field over the inferior-basal region is likely neocortical, whereas a source with the opposite evolution may have started in the mesial structures. The absence of magnetoencephalography activity in a patient with a lateral EEG source and limited FIG. 2. Scalp electroencephalographic seizure. At seizure onset, semirhythmic delta activity is seen over the right hemisphere, maximum temporal, evolving in amplitude. Displayed in longitudinal bipolar montage (sensitivity 10 mv, LF 1 Hz, and HF 70 Hz, 20-second page). Copyright Ó 2012 by the American Clinical Neurophysiology Society 367

3 J. D. Kennedy and S. U. Schuele Journal of Clinical Neurophysiology Volume 29, Number 5, October 2012 FIG. 3. Magnetoencephalography (MEG) source imaging. The MEG localized the interictal epileptiform activity in the right basal midtemporal lobe with anterior propagation. The left panels show the recorded MEG and electroencephalographic (EEG) activities. Left upper panel: MEG and EEG channels; left lower panel: magnetic (left) and electric (right) field distribution map. The right panels demonstrate the magnetic source coregistered to the patient s magnetic resonance imaging (MRI). Right upper panel: three-dimensional head model; right lower panel: coronal, sagittal and axial volume acquisition MRI. Note the anterior and inferior-lateral propagation of the magnetic field on the 3D model (courtesy of Dr. John Ebersole). change in dipole orientation from onset to peak suggests a lateral neocortical onset from a radial source. Invasive Encephalography Intraoperative electrocorticography (ECoG) has been available since 1935 and continues to be used for recording afterdischarges during electrical cortical stimulation in patients with dominant NTLE requiring awake language mapping. Intraoperative ECoG can also be helpful in delineating the extent of the irritative cortex surrounding an epileptogenic neocortical temporal lesion, particularly in patients in whom the suspected pathologic etiology on imaging does not necessarily match the borders of the epileptogenic cortex (e.g., focal cortical dysplasia). Intraoperative ECoG is limited in terms of sampling time, the effects of anesthesia on the EEG, the potential of recording lateral surface spike propagation from a mesial focus, and the often widespread involvement of epileptiform discharges that may be devoid of clinical significance (Schwartz et al., 1997). Stereotactic EEG (Stereo-EEG) was the first invasive method used to systematically record the ictal onset in patients with focal epilepsy. The stereotactic placement of the electrodes allows targeting of brain areas otherwise poorly accessible for subdural electrodes, for example, the insular cortex, and the recording of larger epileptogenic networks within the temporal lobe. Around one-third of patients with TLE demonstrate concurrent onset of ictal activity in the mesial temporal and neocortical temporal regions or the insula (Bartolomei et al., 1999; 2010), warranting in some patients more extended surgical resections and in others exclusion from surgery (Kahane and Bartolomei, 2010). Long-term subdural recordings are typically offered to nonlesional epilepsy surgery candidates with clinical or electrophysiologic findings that suggest neocortical temporal involvement. The goal of the invasive ictal recording is to distinguish temporal from pseudotemporal lobe seizure onset (Andermann, 2003), the involvement of mesial versus neocortical structures and to perform functional mapping of language in the dominant hemisphere. In patients who underwent neocortical temporal resections after subdural invasive recordings, a focal or sublobar onset in the anterior temporal region and a slow ictal propagation time were associated with good outcome, which was overall seen in 66.7% (21 out of 31) patients (Jung et al., 1999). Epilepsy Surgery An estimated 20% of temporal lobe epilepsy surgeries involve neocortical resections sparing mesial structures according to a larger series of 610 patients (Ebner, 2008). A significant difference in the outcome between mesial and NTLE has not been demonstrated 368 Copyright Ó 2012 by the American Clinical Neurophysiology Society

4 Journal of Clinical Neurophysiology Volume 29, Number 5, October 2012 FIG. 4. Intraoperative electrocorticography (ECoG). Spikes were recorded over mesial, anterior basal temporal lobe (2 6 grid: involving electrodes B1 3, B 7 8). Stereotactically placed depth electrodes in the head (AH) and body of the hippocampus (MH) were spared as was the 4 8gridoverthe lateral temporal surface (not shown). Parameters used were sensitivity 200 mv, LF 1 Hz, and HF 70 Hz. except in patients with an incomplete resection (Burgerman et al., 1995; O Brien et al., 1996). Patients with lesional and nonlesional temporal lobe epilepsy can benefit from surgery (Engel et al., 2003; Fong et al., 2011). The underlying cause plays probably the major factor in the prognosis of NTLE surgery (Spencer and Huh, 2008). Benign tumors and cavernous angioma are associated with a better outcome than focal cortical dysplasia or trauma or patients with nonlesional TLE (Janszky et al., 2006; Lee et al., 2006). The presence of electroclinical features typical of MTLE and congruent with functional imaging findings can obviate the need for further invasive recordings (Bell et al., 2009; Immonen et al., 2010; Jeha et al., 2006; LoPinto-Khoury et al., 2012). This approach bears the risk of failing to identify patients with NTLE that present with clinical and neurophysiologic findings that suggest MTLE. Depending on the extent of the neocortical involvement, a standard anterior temporal resection may fail to resect the complete epileptogenic area. A staged surgical approach has been recently described in patients with TLE and nonlesional magnetic resonance imaging (Luther et al., 2011). The small study demonstrated that the eight patients with interictal discharges on ECoG limited to the mesial structures uniformly showed mesial ictal onset on subsequent invasive monitoring and did well with anterior temporal resections. It was only patients with mesial and lateral or exclusively lateral epileptiform discharges during intraoperative ECoG in whom invasive implantation and ictal recording provided additional information. Illustrative Case A 39-year-old right-handed woman with a history of epilepsy since age 33 presented to our center for evaluation. Her seizures were described as an aura of a rising gastric sensation and nausea followed by an unaccounted period of time lasting 1 to 2 minutes during which she was noted to be unresponsive and staring. She reported a frequency of 6 to 15 seizures monthly despite taking multiple combinations of 5 antiepileptic drugs. Epilepsy protocol magnetic resonance imaging with volume acquisition sequences and coronal FLAIR was normal. Neuropsychologic evaluation showed a high average full scale IQ and no evidence of neurocognitive impairment. During epilepsy monitoring unit evaluation, five of her typical seizures were captured. Scalp EEG during prolonged video-eeg monitoring revealed sharp waves localizing to the right anterior temporal region, with phase reversals at the right sphenoidal electrode maximal at T8 (Fig. 1). Seizures clinically began with an aura of nausea and tingling of her arms and legs followed by diminished responsiveness with chewing and lip smacking and left arm dystonic posturing. She was able to follow simple commands and name objects during her automatisms but did not recall testing after the seizure resolved. Additionally, during the second and fourth seizures she displayed ictal kissing behavior. The ictal EEG was similar for all five seizures captured. Approximately 5 to 10 seconds after the clinical onset, there was an attenuation of the posterior dominant background with a rhythmic 4- to 5-Hz pattern over the right temporal region (maximum F8 T8 and SP2), evolving into rhythmic 7-Hz pattern spreading to the left temporal region after 30 seconds. The activity ended abruptly approximately 90 seconds from the onset and was followed by postictal slowing over the right hemisphere (Fig. 2). During the fourth seizure, an ictal single photon emission computed tomography was performed with interictal subtraction and coregistration to magnetic resonance imaging demonstrating subtle increased Tc-99m uptake in the right anterior temporal region. An FDG positron emission tomography was obtained, which also demonstrated subtle asymmetry in the uptake of the right anterior temporal lobe. Additional testing for language lateralization was deferred in view of her typical handedness and preserved ictal speech Copyright Ó 2012 by the American Clinical Neurophysiology Society 369

5 J. D. Kennedy and S. U. Schuele Journal of Clinical Neurophysiology Volume 29, Number 5, October 2012 during automatisms consistent with a nondominant, right temporal lobe epilepsy. A magnetoencephalogram was performed, which localized IEA to the right midtemporal basal region with some anterior propagation (Fig. 3). The patient underwent a right frontotemporal craniotomy with intraoperative electrocorticograpy with a 4 8 grid over the lateral and a 2 6 grid over the anterior basal temporal lobe and two 1 8 stereotactic depth electrodes in the head and body of the hippocampus. Spikes were recorded over the mesial anterior basal temporal lobe (Fig. 4). A resection was performed including the anterior-mesial structures and a more extensive mesial basal resection. Pathologic examination revealed type IIa cortical dysplasia. Postoperatively, the patient had 3 seizures while noncompliant with her medication but has since remained seizure free for.1.5 years. REFERENCES Andermann F. 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