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Electroclinical characteristics of posterior lateral temporal epilepsy
Epilepsy & Behavior 26 (2013) 126–131
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Electroclinical characteristics of posterior lateral temporal epilepsy Fang Wang a, Xingzhou Liu a, b,⁎, Sipei Pan a, Mengyang Wang b, Shuhua Chen b a b
Department of Neurology, Fu Xing Hospital, Capital Medical University, Beijing, PR China Beijing Sanbo Brain Hospital, Beijing, PR China
a r t i c l e
i n f o
Article history: Received 23 August 2012 Revised 22 September 2012 Accepted 24 September 2012 Available online 28 November 2012 Keywords: Temporal lobe epilepsy Posterior temporal lobe epilepsy Electroclinical characteristics Ictal heart rate
a b s t r a c t The current study aimed to investigate the electroclinical differences between mesial temporal lobe epilepsy (MTLE) and posterior lateral temporal lobe epilepsy (PLTLE). All patients had Engel class I outcomes after surgery for at least one year. In MTLE patients, the epileptogenic zone was inside the boundary of a standard temporal lobectomy, whereas in PLTLE, the epileptogenic zone was behind the boundary of a standard temporal lobectomy. Febrile convulsion, history of psychic aura, oroalimentary automatism, and diffuse interictal epileptiform discharges were more frequent in MTLE. Theta wave and increasing heart rate were more evident at the seizure onset in MTLE, whereas an ictal onset fast rhythm was more evident in PLTLE. Tonic head turning was more frequent in PLTLE. Distinguishing between MTLE and PLTLE was easier than distinguishing MTLE from lateral TLE (LTLE), which may be helpful in planning epilepsy surgery. Combinations of these manifestations and signs can provide vital clues to distinguish between MTLE and PLTLE. © 2012 Elsevier Inc. All rights reserved.
1. Introduction
2. Material and methods
Temporal lobe epilepsy (TLE), a form of partial epilepsy, is characterized by seizures originating from one or several anatomic divisions of the temporal lobe and propagating through interconnected neuronal networks within or beyond its boundaries [1]. In 1989, the International League against Epilepsy [2] classified TLE into two subtypes: medial TLE (MTLE) and lateral TLE (LTLE). Since the proposal of the “MTLE syndrome” in 1993 [3], it has been extensively studied and generally accepted. However, studies on the “LTLE syndrome” are still questioned. From a functional anatomy point of view, dense interconnections exist between the limbic and neocortical regions [4]; thus, the epileptogenic zone may be multifarious. Nonetheless, it is widely accepted that the epileptogenic zone should be included in the resected area. Standard temporal lobectomy includes mesio-temporal lobe structures and a temporal pole. Therefore, we defined two subtypes of TLE: the epileptogenic zone within the scope of standard temporal lobectomy called mesial temporal lobe epilepsy (MTLE) and the epileptogenic zone behind the scope of the standard temporal lobectomy called posterior lateral temporal lobe epilepsy (PLTLE). The purpose of the present study was to analyze the characteristics of MTLE and PLTLE and to thereby guide the selection of the appropriate surgical approach.
2.1. Participants
⁎ Corresponding author at: Beijing Sanbo Brain Hospital, Beijing, PR China. Fax: +86 10 62856902. E-mail address: [email protected] (X. Liu). 1525-5050/$ – see front matter © 2012 Elsevier Inc. All rights reserved. http://dx.doi.org/10.1016/j.yebeh.2012.09.036
We retrospectively studied 32 patients with medically intractable epilepsy from a group undergoing evaluation for surgical treatment from 2004 to 2009. All 32 patients had prior comprehensive evaluation, including a detailed history and neurologic examination, routine magnetic resonance imaging study, and video-electroencephalography (EEG) recordings of seizures. Posterior lateral temporal lobe epilepsy patients were selected on the basis of the following criteria: (i) had a discrete lesion in the scope of PLTLE confirmed by imaging, (ii) had lesion resection performed, and (iii) had an outcome consistent with class 1 of Engel's classification after at least 1-year follow-up. Mesial temporal lobe epilepsy patients were selected based on the following criteria: (i) had standard temporal lobectomy performed and (ii) had an outcome consistent with class 1 of Engel's classification for more than 1 year. This method of material selection strongly supports the assumption that the epileptogenic zone was indeed localized within the resected area. The PLTLE group consisted of 11 males and 4 females. The mean age of seizure onset in the 15 PLTLE patients was 10.38 years ± 6.88 years. The mean interval between seizure onset and surgery was 8.83 years ± 5.98 years. Subsequent pathological examination revealed cortical dysplasia (4 pts), encephalomalacia (6 pts), ganglioneuroma (1 pt), and cicatrix gyrus (4 pts). The mean age of seizure onset in the 17 MTLE patients, 12 of whom were males, was 9.35 ± 9.74 years. The mean interval between seizure onset and surgery was 13.4 ± 7.25 years. Subsequent pathological examination showed mesial temporal sclerosis (14 pts), low grade astrocytoma (1 pt), and cysts (2 pts). Demographic data, age at onset, auras, febrile
F. Wang et al. / Epilepsy & Behavior 26 (2013) 126–131
convulsion, and resection side of the patients were extracted from their medical records and are listed in Table 1. History characteristics were recorded (Table 2). Auras were classified as epigastric, auditory, vertigo, visual, olfactory, head, or psychic. The definitions of the various classes of aura are listed in Appendix A. 2.2. EEG test The electrodes were placed according to the international 10-10 system. Sphenoidal (Sp) electrodes were inserted, or temporo-mandibular incisure electrodes (M) were applied. All 129 seizures were reviewed, but in order to avoid biasing our quantitative analysis, we analyzed only one seizure per patient. We decided to analyze the first seizure clearly recognized by the patient or the patient's family as typical of the patient's epilepsy, and in which we could identify the commonest clinical signs reported [5]. Ictal onset was defined by the occurrence of a low-voltage fast activity, by a well-localized flattening, by a rhythmic theta activity, or by the disappearance of interictal EEG abnormalities and periodic lateralized epileptiform discharges. The end of a seizure was defined as the end of the ictal EEG rhythm. The ictal characteristics are listed in Appendix A. The ictal behavior was classified as follows: oroalimentary automatism, hand automatism, dystonia of the upper extremity, staring or behavior arrest, and tonic head turning. Post-ictal coughing and hypersalivation were recorded. The baseline heart rate was defined as the heart rate when the patients were calm and conscious at least 30 min before ictal onset. The heart rates at the onset and at the end of the ictus were recorded. The maximal heart rates during seizures were recorded. Distribution of the interictal discharge (IID) and superiority focus of the IID of the two groups were compared separately. Focal distribution of the IID was calculated using the electrode numbers exhibiting epileptic discharge. Two investigators who were blind to the patients' clinical history reviewed the EEG data separately. The symptoms/signs that appeared only once in the patients' seizures were excluded. 2.3. Statistical analysis The demographic data and history, the ictal and post-ictal behavior, the distribution of IID, and the onset of EEG ictal features were compared using Fisher's exact test or Chi-square test. The heart rates were compared using t-test. Statistical analysis was performed using the SPSS software (version 11.5 for Windows). p b 0.05 was considered to indicate statistical significance. 3. Results 3.1. Clinical characteristics A history of febrile seizures was significantly higher in patients with MTLE (29.4%) than in PLTLE (0%, p b 0.05). The epilepsy duration was significantly longer in MTLE (13.4 ± 7.25) than in PLTLE (8.83 ± 5.98, p b 0.05). Significantly more patients who underwent left-sided operation had MTLE that PLTLE. This result may point to a greater Table 1 Clinical characteristics.
Age (year) Gender (male) Age at epilepsy onset Epilepsy duration (year) Right-handed Febrile convulsion Surgery side (left) a b
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Table 2 Symptoms in history.
Aura Epigastric aura Visual aura Auditory aura Vertigo Olfactory aura Cephalic aura Psychic aura Oroalimentary automatism Head turning Category of aura Category of ictal
PLTLE (15)
MTLE (17)
p-Value
14 1 4 2 1 0 6 0 3 9 1.58 ± 1.73 2.68 ± 1.03
13 6 3 1 0 0 2 6 10 5 0.95 ± 0.69 2.30 ± 1.08
0.338 0.088 0.383 0.212 Noa No 0.423 0.019⁎⁎ 0.036⁎⁎ 0.423 0.112b 0.100b
⁎⁎ p b 0.05, statistical level was reached. a The statistical analysis was not performed because of the small sampling size. b t-test was performed.
risk in performing operations on the left side for treatment of PLTLE. Age and gender had no correlation with MTLE and PLTLE (Table 1). Incidence rates of auras were similar in the two groups (MTLE 76.47% and PLTLE 93.33%). The types of ictal behavior between the two groups showed no difference. In the MTLE group, six out of the 17 patients (35.30%) were recorded with psychic aura, whereas no patient in the PLTLE group was recorded with psychic aura (p b 0.05). The incidence of epigastric aura was higher in the MTLE group (41.18%) than in the PLTLE group (6.67%). The difference in epigastric aura between the two groups approached statistical significance (p = 0.088). The other auras, including visual, auditory, olfactory, head turning, and vertigo, showed no difference between the two groups (Table 2).
3.2. Ictal behavior Tonic head turning was significantly more frequent in the PLTLE group (60%) than in the MTLE group (17.65%, p = 0.027). Staring and arrest were more frequent in the PLTLE group but showed no statistical difference from the MTLE group. Oroalimentary and hand automatisms were significantly more frequent in MTLE than in PLTLE, and a significant difference was found between the two groups. Tonic head turning in the PLTLE group was significantly more frequent than in the MTLE group (p b 0.05). No statistical differences were found in dystonia, hypermotor, post-ictal nose wiping, hypersalivation, and post-ictal coughing, which may be due to the small sampling size. Post-ictal coughing was observed only in MTLE patients; two had undergone a right-sided operation, and one had undergone a left-sided operation. The coughs came after a generalized tonic-clonic seizure (GTCS), urinary incontinence, and hiccough, respectively, in the three patients. Post-ictal hypersalivation occurred in four PLTLE patients, originating from the left side in two patients and the right side in the other two. Only one patient with MTLE had hypersalivation. Data on ictal behavior are listed in Table 3.
3.3. Interictal EEG PLTLE (15)
MTLE (17)
p-Value
19.2 ± 7.00 11 10.38 ± 6.88 8.83 ± 5.98 18 0 6
23.77 ± 7.05 12 9.35 ± 9.74 13.4 ± 7.25 19 5 14
0.086a 1.000 0.709a 0.041a,b 1.000 0.047b 0.026b
t-test was used, and the statistical level was reached. Fisher's exact test was used, and the statistical level was reached.
Temporal electrodes were defined as F7, F8, T3, T4, T5, T6, T7, and T8. All patients demonstrated spike-wave discharges during the interictal period and showed a predominance of discharges at the M or Sp electrodes (PLTLE 53.33% and MTLE 70.59%). The distribution of IID showed a significant difference between the two groups. The IID of PLTLE were more frequently seen in P (73.33%) but but were rarely present in the extratemporal electrodes in MTLE (17.65%, p = 0.002). One IID was involved in Fp, and the other two involved P. A significant difference was detected between the two groups (Table 4).
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Table 3 Ictal behavior.
Tonic head turning Head turning without tonic posturing Staring and arrest Oroalimentary automatism Hand automatism Tonic Dystonia Nystagmus Post-ictal wiping nose Post-ictal hypersalivation Post-ictal coughing
Table 5 Onset of ictal EEG. PLTLE (15)
MTLE (17)
p-Value
9 (60%) 0 (0%) 10 (66.67%) 1 (6.667%) 3 (20.00%) 13 (86.67%) 0 (0%) 1 (5.88%) 0 (0%) 4 (26.67%) 0 (0%)
3 (17.65%) 4 (23.52%) 5 (29.41%) 10 (58.82%) 10 (58.82%) 4 (23.53%) 3 (17.65%) 0 (0%) 3 (17.65%) 1 (5.88%) 3 (17.65%)
0.027⁎⁎ 0.104 0.074 0.003⁎⁎ 0.036⁎⁎ 0.000⁎⁎ Noa Noa Noa Noa Noa
⁎⁎ p b 0.05, statistical level was reached. a Statistical analysis was not performed because of the small sampling size.
3.4. Ictal EEG Patients in the PLTLE group exhibited a rapid rhythm at ictal onset more frequently than those in the MTLE group (p b 0.05). Theta activity of approximately 6 Hz to 7 Hz was observed in the MTLE group at ictal onset, and a statistical difference in ictal-onset theta activity was found between the two groups (p b 0.05). Background attenuation and frequency of periodic lateralized epileptiform discharges showed no statistically significant differences between the two groups (Table 5). 3.5. Cardiac manifestations in seizures The baseline heart rate between the two groups exhibited no statistical difference. Pre-ictal heart rate was defined as the heart rate at the beginning of the ictal EEG. The end of the ictal heart rate was defined as the heart rate at the end of the ictal EEG. Patients in both groups showed increasing heart rates during seizures. Pre-ictal heart rate increased significantly compared with the baseline heart rate in the MTLE group (p b 0.05); however, no significant change was found between pre-ictal heart rate and baseline heart rate in the PLTLE group (Table 6). In both MTLE and PLTLE groups, post-ictal heart rate increased significantly compared with baseline heart rate (Table 7). Post-ictal heart rates in the two groups were not significantly different. A significant difference was found in the pre-ictal heart rate between the PLTLE and MTLE groups. The increase in pre-ictal heart rate was 11.37% and 42.07% in PLTLE and MTLE, respectively (Table 7). Given that the statistical standard for heart rate increase is 20%, then an analogous result can also be achieved. Pre-ictal heart rate increased significantly compared with baseline heart rate in the MTLE group. A statistical difference was found in the pre-ictal heart rate between PLTLE and MTLE (p b 0.05). 4. Discussion
Fast rhythm Background attenuation Periodic lateralized epileptiform discharges θ wave
PLTLE (15)
MTLE (17)
p-Value
6 2 7 3
1 (5.88%) 4 (23.53%) 3 (17.65%) 10 (58.82%)
0.033⁎⁎ 0.659 0.128 0.036⁎⁎
(40.00%) (13.33%) (46.67%) (20.00%)
⁎⁎ p b 0.05, statistical level was reached.
[6,7]. Epigastric aura is one of the typical auras in MTLE patients [6]. Recently, Maillard et al. [8] have used a new method to classify TLE. They divided temporal epilepsy into three subtypes according to stereo-EEG: medial, lateral, and medial-lateral (M-LTLE). Their study showed that MTLE exhibits more frequent psychic and visceral sense auras than M-LTLE and LTLE, which is similar to the results of the present study. Previous studies revealed that viscerosensory symptoms occur with mesial temporal area stimulation [9,10]. These electric stimulation results consist of clinical manifestations. However, conflicting data exist. Viscerosensory symptoms can be elicited by stimulating electrode contacts in the central part of the insula [11]. The symptomatogenic cortex giving rise to epigastric auras was therefore most likely to be the insular cortex. Thus, the fast and facilitated propagation of the epileptic activity from mesial moreso than from neocortical temporal structures to the insular cortex could explain why epigastric auras are more frequently associated with mesial temporal seizure onset [12]. In the present study, epigastric aura probably originated from the mesial temporal lobe rather than propagated to the insular cortex because most of the patients with MTLE were aura-free after having standard temporal lobectomy, and none of the patients had the typical characteristics of insular seizures: early occurrence of laryngeal discomfort or throat tightening associated with unpleasant paresthesias or sensations of warmth affecting the perioral region or large somatic territories [13]. We did not find a significant difference in epigastric aura between MTLE and PLTLE, which may be due to the small sample size. In the present study, psychic aura was found to be significantly more frequent in MTLE than in PLTLE. However, other studies reported that it is more frequent in PLTLE than in MTLE [14]. This discrepancy may be due to the difference in the classification of aura types. In a temporal lobe stimulation study, the amygdala and the hippocampus played dominant roles in provoking dreamy states [15]. In another study, fear was produced by activation of the amygdala, hippocampus, mesial frontal region, or temporal neocortex [9]. Therefore, psychic aura may suggest MTLE. The activity in the anterior hippocampus−perirhinal regions was reported to be functionally
Table 6 Heart rate evaluation during ictus.
4.1. Aura The association found in the present study between epigastric auras and MTLE is consistent with that reported by other studies
PLTLE MTLE
Pre-ictal
Fastest heart rate during ictus
The end of the ictus
0.179⁎ 0⁎
0⁎ 0⁎
0⁎ 0⁎
⁎ The P value of the comparison between the baseline heart rate and the heart rate of the other three conditions.
Table 4 Interictal epileptic discharge (IID).
Ipsilateral IID Bilateral IID Predominant in M or Sp electrodes Contaminate extratemporal
PLTLE (15)
MTLE (17)
p-Value
5 (33.33%) 10 (66.67%) 8 (53.33%) 11 (73.33%)*
8 9 12 3
0.430 0.430 0.314 0.002**
(47.06%) (52.94%) (70.59%) (17.65%)☆
p-Value was obtained from Chi-square. **p b 0.05, statistical level was reached. * P was contaminated in the 11 patients. ☆ Fp was contaminated in 1 of the 3 patients, and the P was contaminated in 2 of the 3 patients.
Table 7 Variation of heart rate between the two groups.
Baseline Pre-ictal Fastest heart rate At the end of the ictus
PLTLE
MTLE
p-Value (t-test)
1.187 ± 0.196 1.327 ± 0.341 2.120 ± 0.455 2.080 ± 0.454
1.218 ± 0.17 1.824 ± 0.499 2.182 ± 0.349 1.924 ± 0.361
0.524 0.016⁎⁎ 0.663 0.274
⁎⁎ p b 0.05, statistical level was reached.
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correlated with the lateral anterior and temporal pole regions [16]. Thus, we regarded the anterior and mesial temporal lobes as one epileptogenic zone to avoid confusion about where the psychic aura really originated. 4.2. Ictal behavior Oroalimentary automatism has been investigated extensively since the MTLE syndrome has been proposed [17]. The results of our research are consistent with those of previous studies [18], which showed that prominent and early oroalimentary automatism is closely linked to ictal involvement not only of the amygdala but also of the anterior temporopolar region [19,20]. The studies were consistent in showing that electrical stimulation of the amygdala produces oroalimentary automatisms only when a widespread limbic and temporal neocortical afterdischarge is observed [9]. Thus, we hypothesize that the anterior and mesial temporal lobes could be combined as one epileptogenic zone. In the current study, hand automatisms were more frequent in MTLE than in PLTLE. A total of 13 patients exhibited hand automatisms, and 3 of the 10 MTLE patients had ipsilateral automatisms in the presence of contralateral dystonic posturing. The other MTLE patients had ipsilateral automatisms in the presence of contralateral immobility. Immobility should be noticeable because of the rare appearance of dystonia. Ipsilateral hand automatisms in the presence of contralateral dystonic posturing were observed in complex partial seizures originating from the temporal lobe [21]. Ictal limb immobility is not a well-defined symptom, but it has a lateralizing value for the contralateral hemisphere [22]. The findings of the present study support this notion. The origin of ictal manual automatism remains controversial. Oral and hand automatisms can be evoked by stimulating the anterior gyrus cinguli and mesiotemporal structures, indicating that automatisms can be caused by spreading ictal activity [23,24]. However, the concept that automatism is caused by inactivation cannot be supported because all patients had become seizure free after surgery in our study. In 1995, ipsilateral hand automatism with contralateral paresis was found in 27 of the 34 cases with complex partial seizures [25], which was highly lateralizing to the epileptic focus. Ictal paresis is not a newly observed phenomenon. Gowers [26] attributed it to the inhibition of motor centers as a result of discharges in related sensory centers and compared it with the inhibition of reflex actions by strong painful cutaneous impressions. An electrical stimulation study [27] supported the view that stimulation of the second somatosensory area, the supplementary motor area, or the perirolandic area inhibits voluntary movements. Thus, paresis occurs when the activity in the cortical region responsible for voluntary movement is disrupted by electrical stimulation. A seizure discharge may similarly interfere with the function of these regions, resulting in ictal paresis. However, in the current study, three patients who had unilateral hand automatism without contralateral dystonic posturing in PLTLE had their seizure focus lateralized to the contralateral hemisphere and their unilateral hand automatisms evolved to unilateral tonic posturing. This result is similar to the previous findings [28,29]. This type of automatism was called “dystonic automatisms.” Dystonic automatisms may result from the spread of seizures to the different subcortical regions, basal ganglia, or thalamic structures [30]. Our results suggest that the ictal discharge may involve the basal ganglia slightly and propagate to the frontal lobe, resulting in a tonic seizure. This emphasizes the close anatomical connectivity of the posterior temporal lobe to the frontal lobe. Tonic head turning was significantly more frequent in PLTLE than in MTLE. The epileptogenic zone of the three PLTLE patients that exhibited tonic head turning without GTCS was located on the opposite side of the direction of head turning. Therefore, tonic head turning both had lateralizing value as well as distinguished MTLE from PLTLE. Theories on the mechanism of ictal contraversion were
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supported by reports on contraversive tonic head turning elicited by electrical stimulation of Brodmann's area 6 [31]. These data indicated that contraversion resulted from the ictal activation of frontal contraversive fields anterior to the precentral area. In a recent SPECT study, versive seizure has been found to be associated with pronounced hyperperfusion in the contralateral frontal eye field [32]. Therefore, version seizure was primarily due to the transcortical propagation of seizure discharge to the frontal contraversive centers in the hemisphere of seizure onset [33]. The findings of our study support this viewpoint. Our results further support a close anatomical connectivity of the posterior temporal lobe to the frontal lobe. In the present study, staring and arrest were found to be more frequent in PLTLE than in MTLE but with no statistically significant difference (p=0.074). Seo-young et al. [18] reported the same finding but with a statistically significant difference (pb 0.05). Staring and arrest are the most common manifestations of neocortical temporal lobe seizures [18,34] but are not distinguishing features of MTLE and LTLE [35]. A recent positron emission tomography study has shown a larger interictal temporal hypometabolism in MTLE when associated with loss of contact, which was suggestive of a medial–lateral propagation pathway [36]. A SPECT study demonstrated that the thalamus and the upper brain stem are involved in consciousness disturbance in different types of focal epileptic seizures. For example, consciousness impairment has a strong association with secondary hyperperfusion in the thalamic/upper brainstem region [37]. Thus, staring and arrest may result from the extensive involvement of the ipsilateral temporal lobe or other subcortical structures. In the present study, the frequency of staring and arrest in PLTLE patients may be due to the rapid propagation of ictal discharges. One patient in the PLTLE group but none in the MTLE group had twitching movements of the face and the upper limb. The frequencies of these face and limb movements in the PLTLE group were both 5.3%; those in the MTLE group were 5.6% and 7.4% and 17.6% and 0% in the anterior LTLE (ALTLE) group, respectively [18]. The results of the current study are in accordance with a previous report [18]. This result suggested that facial twitching was frequent in ALTLE and rare in PLTLE. Thus, dividing the temporal lobe into two epileptogenic zones MTLE and PLTLE - may be more clinically suitable. 4.3. Interictal EEG Previous studies showed that the IID in MTLE is more frequently projected to the bilateral cortex [38,39]. However, in this study, no statistical difference was found between MTLE and neocortical temporal lobe epilepsy(NTLE). In previous work, interictal abnormalities predominantly were limited to anterior temporal and Sp electrodes in the patients with MTLE [38], which is consistent with the current results. An overlap in interictal findings exists in patients suffering from MTLE and in patients suffering from NTLE. Interictal epileptiform activity in MTLE usually shows a predominance of discharges at the anterior temporal or sphenoidal electrodes and less often at the mid-temporal or posterior temporal electrodes [40]. The current study shows that the posterior temporal electrodes were more frequently active in PLTLE than in MTLE (73.33% in PLTLE and 17.65% in MTLE; p b 0.05). This finding is similar to that reported by Duchowny [29]. The predominant electrodes in MTLE and PLTLE were coincident, which may be attributed to the high density of connections between the limbic structures and the temporal neocortex [40]. The posterior temporal electrodes may be used to distinguish MTLE from PLTLE [40]. However, the distribution of IID in anterior temporal lobe epilepsy is very similar to that in MTLE. This overlap was avoided in our research. 4.4. Ictal EEG Luders [41] proposed that an ictal-onset rapid rhythm is a characteristic of neocortical epilepsy, especially in patients with lesions.
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Previous research found that rapid rhythm is more frequent in association with seizures in extratemporal lobe epilepsy [42], PLTLE, and ALTLE than in MTLE [18]. Our findings are consistent with these results. Furthermore, ictal theta waves of 6 Hz to 7 Hz were found to be a characteristic of MTLE and associated with mesial temporal sclerosis [18], which are also consistent with the results of the current study. Rapid rhythms have been proposed to result from the short distance between the electrode and the epileptogenic zone [41]. 4.5. Heart rate The MTLE group exhibited a more rapid pre-ictal heart rate compared with the PLTLE group. This result is in accordance with the previous reports [43,44]. Therefore, heart rate has a significant localization value. Human cortical stimulation studies showed that the insula is important in the generation of cardiac effects [45]. The amygdala was hypothesized to play a key role in the neural regulation of heart rate and rhythm in previous studies [46,47]. The results of the present study are consistent with this theory. Early heart rate changes are likely caused by direct activation of autonomic control centers by epileptic discharges. At the initial stage of a seizure, epileptic discharges may be confined to a brain area too small or too deep to be detected by scalp EEG.
Appendix Appendix AA (continued) (continued) No.
Motor signs 1 Oroalimentary automatism 2 Tonic head turning 3 Staring and arrest 4 Tonic 5 Dystonia
6 7 8
10
Generally, our results showed that the characteristics of MTLE included the following: history of febrile convulsion, psychic aura, localization of interictal epileptic discharge in the temporal area, prominent oroalimentary ictal behavior, and hand automatism without tonic posturing on the same side as the epileptogenic zone. In addition, rapid pre-ictal heart rate and ipsilateral temporal theta waves at the seizure onset were present in MTLE patients. The symptomatogenic zone can be explained by the anatomy of the limbic system. The characteristics of PLTLE included the following: absence of febrile convulsion, rare oroalimentary and psychic aura, and widespread interictal epileptic discharges. The IID of PLTLE usually involved P. In addition, prominent ictal behavior of PLTLE patients included the following movements: tonic, tonic versive, rare oroalimentary, and hand automatism. The direction of tonic head turning and hand automatism with tonic posturing were both contralateral to the epileptogenic zone. Rapid pre-ictal heart rate was not obvious, and the EEG onset was characterized by fast activity. The symptomatogenic zone can be explained by the structural anatomy of the neocortex, specifically the lateral posterior temporal lobe and its connections with the frontal lobe. Taken together, the manifestations and signs provide useful evidence for distinguishing MTLE from PLTLE. Thus, comprehensive information on patients with epilepsy should be considered. Furthermore, we found that MTLE might be more easily distinguished from PLTLE than from LTLE, which may be helpful in clinical settings. Acknowledgements This study was supported by Capital Medical Development Fundation 2007–3106. Appendix A
No. Aura 1 2 3 4
Symptoms and signs
Definition
Somatosensory Visual Auditory Olfactory
Localized sensation of numbness, tingling, pain, or cold Visual illusions or hallucinations Tinnitus, music, and voices Smell
Definition
Aura 5 Gustatory Taste 6 Cephalic sensation Sensation referred to the head 7 Epigastric sensations 8 Psychic Emotional symptoms, memory illusions, and memory hallucinations 9 Vertigo
9
5. Conclusion
Symptoms and signs
Chewing, lip smacking, swallowing Forced, involuntary tonic or clonic movement of the head and eyes in a sustained and unnatural position Immobile, fixed gaze with or without eyelid retraction Stiffness in any part of the body A persistent attitude or posture due to the co-contraction of agonist and antagonist muscles in one region of the body
Nystagmus Post-ictal nose wiping Post-ictal hypersalivation Post-ictal coughing Hand automatism Repetitive, distal fingering, fumbling, grasping, patting as well as proximal moment of the arms
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Epilepsy & Behavior journal homepage: www.elsevier.com/locate/yebeh
Electroclinical characteristics of posterior lateral temporal epilepsy Fang Wang a, Xingzhou Liu a, b,⁎, Sipei Pan a, Mengyang Wang b, Shuhua Chen b a b
Department of Neurology, Fu Xing Hospital, Capital Medical University, Beijing, PR China Beijing Sanbo Brain Hospital, Beijing, PR China
a r t i c l e
i n f o
Article history: Received 23 August 2012 Revised 22 September 2012 Accepted 24 September 2012 Available online 28 November 2012 Keywords: Temporal lobe epilepsy Posterior temporal lobe epilepsy Electroclinical characteristics Ictal heart rate
a b s t r a c t The current study aimed to investigate the electroclinical differences between mesial temporal lobe epilepsy (MTLE) and posterior lateral temporal lobe epilepsy (PLTLE). All patients had Engel class I outcomes after surgery for at least one year. In MTLE patients, the epileptogenic zone was inside the boundary of a standard temporal lobectomy, whereas in PLTLE, the epileptogenic zone was behind the boundary of a standard temporal lobectomy. Febrile convulsion, history of psychic aura, oroalimentary automatism, and diffuse interictal epileptiform discharges were more frequent in MTLE. Theta wave and increasing heart rate were more evident at the seizure onset in MTLE, whereas an ictal onset fast rhythm was more evident in PLTLE. Tonic head turning was more frequent in PLTLE. Distinguishing between MTLE and PLTLE was easier than distinguishing MTLE from lateral TLE (LTLE), which may be helpful in planning epilepsy surgery. Combinations of these manifestations and signs can provide vital clues to distinguish between MTLE and PLTLE. © 2012 Elsevier Inc. All rights reserved.
1. Introduction
2. Material and methods
Temporal lobe epilepsy (TLE), a form of partial epilepsy, is characterized by seizures originating from one or several anatomic divisions of the temporal lobe and propagating through interconnected neuronal networks within or beyond its boundaries [1]. In 1989, the International League against Epilepsy [2] classified TLE into two subtypes: medial TLE (MTLE) and lateral TLE (LTLE). Since the proposal of the “MTLE syndrome” in 1993 [3], it has been extensively studied and generally accepted. However, studies on the “LTLE syndrome” are still questioned. From a functional anatomy point of view, dense interconnections exist between the limbic and neocortical regions [4]; thus, the epileptogenic zone may be multifarious. Nonetheless, it is widely accepted that the epileptogenic zone should be included in the resected area. Standard temporal lobectomy includes mesio-temporal lobe structures and a temporal pole. Therefore, we defined two subtypes of TLE: the epileptogenic zone within the scope of standard temporal lobectomy called mesial temporal lobe epilepsy (MTLE) and the epileptogenic zone behind the scope of the standard temporal lobectomy called posterior lateral temporal lobe epilepsy (PLTLE). The purpose of the present study was to analyze the characteristics of MTLE and PLTLE and to thereby guide the selection of the appropriate surgical approach.
2.1. Participants
⁎ Corresponding author at: Beijing Sanbo Brain Hospital, Beijing, PR China. Fax: +86 10 62856902. E-mail address: [email protected] (X. Liu). 1525-5050/$ – see front matter © 2012 Elsevier Inc. All rights reserved. http://dx.doi.org/10.1016/j.yebeh.2012.09.036
We retrospectively studied 32 patients with medically intractable epilepsy from a group undergoing evaluation for surgical treatment from 2004 to 2009. All 32 patients had prior comprehensive evaluation, including a detailed history and neurologic examination, routine magnetic resonance imaging study, and video-electroencephalography (EEG) recordings of seizures. Posterior lateral temporal lobe epilepsy patients were selected on the basis of the following criteria: (i) had a discrete lesion in the scope of PLTLE confirmed by imaging, (ii) had lesion resection performed, and (iii) had an outcome consistent with class 1 of Engel's classification after at least 1-year follow-up. Mesial temporal lobe epilepsy patients were selected based on the following criteria: (i) had standard temporal lobectomy performed and (ii) had an outcome consistent with class 1 of Engel's classification for more than 1 year. This method of material selection strongly supports the assumption that the epileptogenic zone was indeed localized within the resected area. The PLTLE group consisted of 11 males and 4 females. The mean age of seizure onset in the 15 PLTLE patients was 10.38 years ± 6.88 years. The mean interval between seizure onset and surgery was 8.83 years ± 5.98 years. Subsequent pathological examination revealed cortical dysplasia (4 pts), encephalomalacia (6 pts), ganglioneuroma (1 pt), and cicatrix gyrus (4 pts). The mean age of seizure onset in the 17 MTLE patients, 12 of whom were males, was 9.35 ± 9.74 years. The mean interval between seizure onset and surgery was 13.4 ± 7.25 years. Subsequent pathological examination showed mesial temporal sclerosis (14 pts), low grade astrocytoma (1 pt), and cysts (2 pts). Demographic data, age at onset, auras, febrile
F. Wang et al. / Epilepsy & Behavior 26 (2013) 126–131
convulsion, and resection side of the patients were extracted from their medical records and are listed in Table 1. History characteristics were recorded (Table 2). Auras were classified as epigastric, auditory, vertigo, visual, olfactory, head, or psychic. The definitions of the various classes of aura are listed in Appendix A. 2.2. EEG test The electrodes were placed according to the international 10-10 system. Sphenoidal (Sp) electrodes were inserted, or temporo-mandibular incisure electrodes (M) were applied. All 129 seizures were reviewed, but in order to avoid biasing our quantitative analysis, we analyzed only one seizure per patient. We decided to analyze the first seizure clearly recognized by the patient or the patient's family as typical of the patient's epilepsy, and in which we could identify the commonest clinical signs reported [5]. Ictal onset was defined by the occurrence of a low-voltage fast activity, by a well-localized flattening, by a rhythmic theta activity, or by the disappearance of interictal EEG abnormalities and periodic lateralized epileptiform discharges. The end of a seizure was defined as the end of the ictal EEG rhythm. The ictal characteristics are listed in Appendix A. The ictal behavior was classified as follows: oroalimentary automatism, hand automatism, dystonia of the upper extremity, staring or behavior arrest, and tonic head turning. Post-ictal coughing and hypersalivation were recorded. The baseline heart rate was defined as the heart rate when the patients were calm and conscious at least 30 min before ictal onset. The heart rates at the onset and at the end of the ictus were recorded. The maximal heart rates during seizures were recorded. Distribution of the interictal discharge (IID) and superiority focus of the IID of the two groups were compared separately. Focal distribution of the IID was calculated using the electrode numbers exhibiting epileptic discharge. Two investigators who were blind to the patients' clinical history reviewed the EEG data separately. The symptoms/signs that appeared only once in the patients' seizures were excluded. 2.3. Statistical analysis The demographic data and history, the ictal and post-ictal behavior, the distribution of IID, and the onset of EEG ictal features were compared using Fisher's exact test or Chi-square test. The heart rates were compared using t-test. Statistical analysis was performed using the SPSS software (version 11.5 for Windows). p b 0.05 was considered to indicate statistical significance. 3. Results 3.1. Clinical characteristics A history of febrile seizures was significantly higher in patients with MTLE (29.4%) than in PLTLE (0%, p b 0.05). The epilepsy duration was significantly longer in MTLE (13.4 ± 7.25) than in PLTLE (8.83 ± 5.98, p b 0.05). Significantly more patients who underwent left-sided operation had MTLE that PLTLE. This result may point to a greater Table 1 Clinical characteristics.
Age (year) Gender (male) Age at epilepsy onset Epilepsy duration (year) Right-handed Febrile convulsion Surgery side (left) a b
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Table 2 Symptoms in history.
Aura Epigastric aura Visual aura Auditory aura Vertigo Olfactory aura Cephalic aura Psychic aura Oroalimentary automatism Head turning Category of aura Category of ictal
PLTLE (15)
MTLE (17)
p-Value
14 1 4 2 1 0 6 0 3 9 1.58 ± 1.73 2.68 ± 1.03
13 6 3 1 0 0 2 6 10 5 0.95 ± 0.69 2.30 ± 1.08
0.338 0.088 0.383 0.212 Noa No 0.423 0.019⁎⁎ 0.036⁎⁎ 0.423 0.112b 0.100b
⁎⁎ p b 0.05, statistical level was reached. a The statistical analysis was not performed because of the small sampling size. b t-test was performed.
risk in performing operations on the left side for treatment of PLTLE. Age and gender had no correlation with MTLE and PLTLE (Table 1). Incidence rates of auras were similar in the two groups (MTLE 76.47% and PLTLE 93.33%). The types of ictal behavior between the two groups showed no difference. In the MTLE group, six out of the 17 patients (35.30%) were recorded with psychic aura, whereas no patient in the PLTLE group was recorded with psychic aura (p b 0.05). The incidence of epigastric aura was higher in the MTLE group (41.18%) than in the PLTLE group (6.67%). The difference in epigastric aura between the two groups approached statistical significance (p = 0.088). The other auras, including visual, auditory, olfactory, head turning, and vertigo, showed no difference between the two groups (Table 2).
3.2. Ictal behavior Tonic head turning was significantly more frequent in the PLTLE group (60%) than in the MTLE group (17.65%, p = 0.027). Staring and arrest were more frequent in the PLTLE group but showed no statistical difference from the MTLE group. Oroalimentary and hand automatisms were significantly more frequent in MTLE than in PLTLE, and a significant difference was found between the two groups. Tonic head turning in the PLTLE group was significantly more frequent than in the MTLE group (p b 0.05). No statistical differences were found in dystonia, hypermotor, post-ictal nose wiping, hypersalivation, and post-ictal coughing, which may be due to the small sampling size. Post-ictal coughing was observed only in MTLE patients; two had undergone a right-sided operation, and one had undergone a left-sided operation. The coughs came after a generalized tonic-clonic seizure (GTCS), urinary incontinence, and hiccough, respectively, in the three patients. Post-ictal hypersalivation occurred in four PLTLE patients, originating from the left side in two patients and the right side in the other two. Only one patient with MTLE had hypersalivation. Data on ictal behavior are listed in Table 3.
3.3. Interictal EEG PLTLE (15)
MTLE (17)
p-Value
19.2 ± 7.00 11 10.38 ± 6.88 8.83 ± 5.98 18 0 6
23.77 ± 7.05 12 9.35 ± 9.74 13.4 ± 7.25 19 5 14
0.086a 1.000 0.709a 0.041a,b 1.000 0.047b 0.026b
t-test was used, and the statistical level was reached. Fisher's exact test was used, and the statistical level was reached.
Temporal electrodes were defined as F7, F8, T3, T4, T5, T6, T7, and T8. All patients demonstrated spike-wave discharges during the interictal period and showed a predominance of discharges at the M or Sp electrodes (PLTLE 53.33% and MTLE 70.59%). The distribution of IID showed a significant difference between the two groups. The IID of PLTLE were more frequently seen in P (73.33%) but but were rarely present in the extratemporal electrodes in MTLE (17.65%, p = 0.002). One IID was involved in Fp, and the other two involved P. A significant difference was detected between the two groups (Table 4).
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Table 3 Ictal behavior.
Tonic head turning Head turning without tonic posturing Staring and arrest Oroalimentary automatism Hand automatism Tonic Dystonia Nystagmus Post-ictal wiping nose Post-ictal hypersalivation Post-ictal coughing
Table 5 Onset of ictal EEG. PLTLE (15)
MTLE (17)
p-Value
9 (60%) 0 (0%) 10 (66.67%) 1 (6.667%) 3 (20.00%) 13 (86.67%) 0 (0%) 1 (5.88%) 0 (0%) 4 (26.67%) 0 (0%)
3 (17.65%) 4 (23.52%) 5 (29.41%) 10 (58.82%) 10 (58.82%) 4 (23.53%) 3 (17.65%) 0 (0%) 3 (17.65%) 1 (5.88%) 3 (17.65%)
0.027⁎⁎ 0.104 0.074 0.003⁎⁎ 0.036⁎⁎ 0.000⁎⁎ Noa Noa Noa Noa Noa
⁎⁎ p b 0.05, statistical level was reached. a Statistical analysis was not performed because of the small sampling size.
3.4. Ictal EEG Patients in the PLTLE group exhibited a rapid rhythm at ictal onset more frequently than those in the MTLE group (p b 0.05). Theta activity of approximately 6 Hz to 7 Hz was observed in the MTLE group at ictal onset, and a statistical difference in ictal-onset theta activity was found between the two groups (p b 0.05). Background attenuation and frequency of periodic lateralized epileptiform discharges showed no statistically significant differences between the two groups (Table 5). 3.5. Cardiac manifestations in seizures The baseline heart rate between the two groups exhibited no statistical difference. Pre-ictal heart rate was defined as the heart rate at the beginning of the ictal EEG. The end of the ictal heart rate was defined as the heart rate at the end of the ictal EEG. Patients in both groups showed increasing heart rates during seizures. Pre-ictal heart rate increased significantly compared with the baseline heart rate in the MTLE group (p b 0.05); however, no significant change was found between pre-ictal heart rate and baseline heart rate in the PLTLE group (Table 6). In both MTLE and PLTLE groups, post-ictal heart rate increased significantly compared with baseline heart rate (Table 7). Post-ictal heart rates in the two groups were not significantly different. A significant difference was found in the pre-ictal heart rate between the PLTLE and MTLE groups. The increase in pre-ictal heart rate was 11.37% and 42.07% in PLTLE and MTLE, respectively (Table 7). Given that the statistical standard for heart rate increase is 20%, then an analogous result can also be achieved. Pre-ictal heart rate increased significantly compared with baseline heart rate in the MTLE group. A statistical difference was found in the pre-ictal heart rate between PLTLE and MTLE (p b 0.05). 4. Discussion
Fast rhythm Background attenuation Periodic lateralized epileptiform discharges θ wave
PLTLE (15)
MTLE (17)
p-Value
6 2 7 3
1 (5.88%) 4 (23.53%) 3 (17.65%) 10 (58.82%)
0.033⁎⁎ 0.659 0.128 0.036⁎⁎
(40.00%) (13.33%) (46.67%) (20.00%)
⁎⁎ p b 0.05, statistical level was reached.
[6,7]. Epigastric aura is one of the typical auras in MTLE patients [6]. Recently, Maillard et al. [8] have used a new method to classify TLE. They divided temporal epilepsy into three subtypes according to stereo-EEG: medial, lateral, and medial-lateral (M-LTLE). Their study showed that MTLE exhibits more frequent psychic and visceral sense auras than M-LTLE and LTLE, which is similar to the results of the present study. Previous studies revealed that viscerosensory symptoms occur with mesial temporal area stimulation [9,10]. These electric stimulation results consist of clinical manifestations. However, conflicting data exist. Viscerosensory symptoms can be elicited by stimulating electrode contacts in the central part of the insula [11]. The symptomatogenic cortex giving rise to epigastric auras was therefore most likely to be the insular cortex. Thus, the fast and facilitated propagation of the epileptic activity from mesial moreso than from neocortical temporal structures to the insular cortex could explain why epigastric auras are more frequently associated with mesial temporal seizure onset [12]. In the present study, epigastric aura probably originated from the mesial temporal lobe rather than propagated to the insular cortex because most of the patients with MTLE were aura-free after having standard temporal lobectomy, and none of the patients had the typical characteristics of insular seizures: early occurrence of laryngeal discomfort or throat tightening associated with unpleasant paresthesias or sensations of warmth affecting the perioral region or large somatic territories [13]. We did not find a significant difference in epigastric aura between MTLE and PLTLE, which may be due to the small sample size. In the present study, psychic aura was found to be significantly more frequent in MTLE than in PLTLE. However, other studies reported that it is more frequent in PLTLE than in MTLE [14]. This discrepancy may be due to the difference in the classification of aura types. In a temporal lobe stimulation study, the amygdala and the hippocampus played dominant roles in provoking dreamy states [15]. In another study, fear was produced by activation of the amygdala, hippocampus, mesial frontal region, or temporal neocortex [9]. Therefore, psychic aura may suggest MTLE. The activity in the anterior hippocampus−perirhinal regions was reported to be functionally
Table 6 Heart rate evaluation during ictus.
4.1. Aura The association found in the present study between epigastric auras and MTLE is consistent with that reported by other studies
PLTLE MTLE
Pre-ictal
Fastest heart rate during ictus
The end of the ictus
0.179⁎ 0⁎
0⁎ 0⁎
0⁎ 0⁎
⁎ The P value of the comparison between the baseline heart rate and the heart rate of the other three conditions.
Table 4 Interictal epileptic discharge (IID).
Ipsilateral IID Bilateral IID Predominant in M or Sp electrodes Contaminate extratemporal
PLTLE (15)
MTLE (17)
p-Value
5 (33.33%) 10 (66.67%) 8 (53.33%) 11 (73.33%)*
8 9 12 3
0.430 0.430 0.314 0.002**
(47.06%) (52.94%) (70.59%) (17.65%)☆
p-Value was obtained from Chi-square. **p b 0.05, statistical level was reached. * P was contaminated in the 11 patients. ☆ Fp was contaminated in 1 of the 3 patients, and the P was contaminated in 2 of the 3 patients.
Table 7 Variation of heart rate between the two groups.
Baseline Pre-ictal Fastest heart rate At the end of the ictus
PLTLE
MTLE
p-Value (t-test)
1.187 ± 0.196 1.327 ± 0.341 2.120 ± 0.455 2.080 ± 0.454
1.218 ± 0.17 1.824 ± 0.499 2.182 ± 0.349 1.924 ± 0.361
0.524 0.016⁎⁎ 0.663 0.274
⁎⁎ p b 0.05, statistical level was reached.
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correlated with the lateral anterior and temporal pole regions [16]. Thus, we regarded the anterior and mesial temporal lobes as one epileptogenic zone to avoid confusion about where the psychic aura really originated. 4.2. Ictal behavior Oroalimentary automatism has been investigated extensively since the MTLE syndrome has been proposed [17]. The results of our research are consistent with those of previous studies [18], which showed that prominent and early oroalimentary automatism is closely linked to ictal involvement not only of the amygdala but also of the anterior temporopolar region [19,20]. The studies were consistent in showing that electrical stimulation of the amygdala produces oroalimentary automatisms only when a widespread limbic and temporal neocortical afterdischarge is observed [9]. Thus, we hypothesize that the anterior and mesial temporal lobes could be combined as one epileptogenic zone. In the current study, hand automatisms were more frequent in MTLE than in PLTLE. A total of 13 patients exhibited hand automatisms, and 3 of the 10 MTLE patients had ipsilateral automatisms in the presence of contralateral dystonic posturing. The other MTLE patients had ipsilateral automatisms in the presence of contralateral immobility. Immobility should be noticeable because of the rare appearance of dystonia. Ipsilateral hand automatisms in the presence of contralateral dystonic posturing were observed in complex partial seizures originating from the temporal lobe [21]. Ictal limb immobility is not a well-defined symptom, but it has a lateralizing value for the contralateral hemisphere [22]. The findings of the present study support this notion. The origin of ictal manual automatism remains controversial. Oral and hand automatisms can be evoked by stimulating the anterior gyrus cinguli and mesiotemporal structures, indicating that automatisms can be caused by spreading ictal activity [23,24]. However, the concept that automatism is caused by inactivation cannot be supported because all patients had become seizure free after surgery in our study. In 1995, ipsilateral hand automatism with contralateral paresis was found in 27 of the 34 cases with complex partial seizures [25], which was highly lateralizing to the epileptic focus. Ictal paresis is not a newly observed phenomenon. Gowers [26] attributed it to the inhibition of motor centers as a result of discharges in related sensory centers and compared it with the inhibition of reflex actions by strong painful cutaneous impressions. An electrical stimulation study [27] supported the view that stimulation of the second somatosensory area, the supplementary motor area, or the perirolandic area inhibits voluntary movements. Thus, paresis occurs when the activity in the cortical region responsible for voluntary movement is disrupted by electrical stimulation. A seizure discharge may similarly interfere with the function of these regions, resulting in ictal paresis. However, in the current study, three patients who had unilateral hand automatism without contralateral dystonic posturing in PLTLE had their seizure focus lateralized to the contralateral hemisphere and their unilateral hand automatisms evolved to unilateral tonic posturing. This result is similar to the previous findings [28,29]. This type of automatism was called “dystonic automatisms.” Dystonic automatisms may result from the spread of seizures to the different subcortical regions, basal ganglia, or thalamic structures [30]. Our results suggest that the ictal discharge may involve the basal ganglia slightly and propagate to the frontal lobe, resulting in a tonic seizure. This emphasizes the close anatomical connectivity of the posterior temporal lobe to the frontal lobe. Tonic head turning was significantly more frequent in PLTLE than in MTLE. The epileptogenic zone of the three PLTLE patients that exhibited tonic head turning without GTCS was located on the opposite side of the direction of head turning. Therefore, tonic head turning both had lateralizing value as well as distinguished MTLE from PLTLE. Theories on the mechanism of ictal contraversion were
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supported by reports on contraversive tonic head turning elicited by electrical stimulation of Brodmann's area 6 [31]. These data indicated that contraversion resulted from the ictal activation of frontal contraversive fields anterior to the precentral area. In a recent SPECT study, versive seizure has been found to be associated with pronounced hyperperfusion in the contralateral frontal eye field [32]. Therefore, version seizure was primarily due to the transcortical propagation of seizure discharge to the frontal contraversive centers in the hemisphere of seizure onset [33]. The findings of our study support this viewpoint. Our results further support a close anatomical connectivity of the posterior temporal lobe to the frontal lobe. In the present study, staring and arrest were found to be more frequent in PLTLE than in MTLE but with no statistically significant difference (p=0.074). Seo-young et al. [18] reported the same finding but with a statistically significant difference (pb 0.05). Staring and arrest are the most common manifestations of neocortical temporal lobe seizures [18,34] but are not distinguishing features of MTLE and LTLE [35]. A recent positron emission tomography study has shown a larger interictal temporal hypometabolism in MTLE when associated with loss of contact, which was suggestive of a medial–lateral propagation pathway [36]. A SPECT study demonstrated that the thalamus and the upper brain stem are involved in consciousness disturbance in different types of focal epileptic seizures. For example, consciousness impairment has a strong association with secondary hyperperfusion in the thalamic/upper brainstem region [37]. Thus, staring and arrest may result from the extensive involvement of the ipsilateral temporal lobe or other subcortical structures. In the present study, the frequency of staring and arrest in PLTLE patients may be due to the rapid propagation of ictal discharges. One patient in the PLTLE group but none in the MTLE group had twitching movements of the face and the upper limb. The frequencies of these face and limb movements in the PLTLE group were both 5.3%; those in the MTLE group were 5.6% and 7.4% and 17.6% and 0% in the anterior LTLE (ALTLE) group, respectively [18]. The results of the current study are in accordance with a previous report [18]. This result suggested that facial twitching was frequent in ALTLE and rare in PLTLE. Thus, dividing the temporal lobe into two epileptogenic zones MTLE and PLTLE - may be more clinically suitable. 4.3. Interictal EEG Previous studies showed that the IID in MTLE is more frequently projected to the bilateral cortex [38,39]. However, in this study, no statistical difference was found between MTLE and neocortical temporal lobe epilepsy(NTLE). In previous work, interictal abnormalities predominantly were limited to anterior temporal and Sp electrodes in the patients with MTLE [38], which is consistent with the current results. An overlap in interictal findings exists in patients suffering from MTLE and in patients suffering from NTLE. Interictal epileptiform activity in MTLE usually shows a predominance of discharges at the anterior temporal or sphenoidal electrodes and less often at the mid-temporal or posterior temporal electrodes [40]. The current study shows that the posterior temporal electrodes were more frequently active in PLTLE than in MTLE (73.33% in PLTLE and 17.65% in MTLE; p b 0.05). This finding is similar to that reported by Duchowny [29]. The predominant electrodes in MTLE and PLTLE were coincident, which may be attributed to the high density of connections between the limbic structures and the temporal neocortex [40]. The posterior temporal electrodes may be used to distinguish MTLE from PLTLE [40]. However, the distribution of IID in anterior temporal lobe epilepsy is very similar to that in MTLE. This overlap was avoided in our research. 4.4. Ictal EEG Luders [41] proposed that an ictal-onset rapid rhythm is a characteristic of neocortical epilepsy, especially in patients with lesions.
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Previous research found that rapid rhythm is more frequent in association with seizures in extratemporal lobe epilepsy [42], PLTLE, and ALTLE than in MTLE [18]. Our findings are consistent with these results. Furthermore, ictal theta waves of 6 Hz to 7 Hz were found to be a characteristic of MTLE and associated with mesial temporal sclerosis [18], which are also consistent with the results of the current study. Rapid rhythms have been proposed to result from the short distance between the electrode and the epileptogenic zone [41]. 4.5. Heart rate The MTLE group exhibited a more rapid pre-ictal heart rate compared with the PLTLE group. This result is in accordance with the previous reports [43,44]. Therefore, heart rate has a significant localization value. Human cortical stimulation studies showed that the insula is important in the generation of cardiac effects [45]. The amygdala was hypothesized to play a key role in the neural regulation of heart rate and rhythm in previous studies [46,47]. The results of the present study are consistent with this theory. Early heart rate changes are likely caused by direct activation of autonomic control centers by epileptic discharges. At the initial stage of a seizure, epileptic discharges may be confined to a brain area too small or too deep to be detected by scalp EEG.
Appendix Appendix AA (continued) (continued) No.
Motor signs 1 Oroalimentary automatism 2 Tonic head turning 3 Staring and arrest 4 Tonic 5 Dystonia
6 7 8
10
Generally, our results showed that the characteristics of MTLE included the following: history of febrile convulsion, psychic aura, localization of interictal epileptic discharge in the temporal area, prominent oroalimentary ictal behavior, and hand automatism without tonic posturing on the same side as the epileptogenic zone. In addition, rapid pre-ictal heart rate and ipsilateral temporal theta waves at the seizure onset were present in MTLE patients. The symptomatogenic zone can be explained by the anatomy of the limbic system. The characteristics of PLTLE included the following: absence of febrile convulsion, rare oroalimentary and psychic aura, and widespread interictal epileptic discharges. The IID of PLTLE usually involved P. In addition, prominent ictal behavior of PLTLE patients included the following movements: tonic, tonic versive, rare oroalimentary, and hand automatism. The direction of tonic head turning and hand automatism with tonic posturing were both contralateral to the epileptogenic zone. Rapid pre-ictal heart rate was not obvious, and the EEG onset was characterized by fast activity. The symptomatogenic zone can be explained by the structural anatomy of the neocortex, specifically the lateral posterior temporal lobe and its connections with the frontal lobe. Taken together, the manifestations and signs provide useful evidence for distinguishing MTLE from PLTLE. Thus, comprehensive information on patients with epilepsy should be considered. Furthermore, we found that MTLE might be more easily distinguished from PLTLE than from LTLE, which may be helpful in clinical settings. Acknowledgements This study was supported by Capital Medical Development Fundation 2007–3106. Appendix A
No. Aura 1 2 3 4
Symptoms and signs
Definition
Somatosensory Visual Auditory Olfactory
Localized sensation of numbness, tingling, pain, or cold Visual illusions or hallucinations Tinnitus, music, and voices Smell
Definition
Aura 5 Gustatory Taste 6 Cephalic sensation Sensation referred to the head 7 Epigastric sensations 8 Psychic Emotional symptoms, memory illusions, and memory hallucinations 9 Vertigo
9
5. Conclusion
Symptoms and signs
Chewing, lip smacking, swallowing Forced, involuntary tonic or clonic movement of the head and eyes in a sustained and unnatural position Immobile, fixed gaze with or without eyelid retraction Stiffness in any part of the body A persistent attitude or posture due to the co-contraction of agonist and antagonist muscles in one region of the body
Nystagmus Post-ictal nose wiping Post-ictal hypersalivation Post-ictal coughing Hand automatism Repetitive, distal fingering, fumbling, grasping, patting as well as proximal moment of the arms
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