The temporopolar cortex plays a pivotal role in temporal lobe seizures

doi:10.1093/brain/awh512 Brain (2005), 128, 1818–1831 The temporopolar cortex plays a pivotal role in temporal lobe seizures Stéphan Chabardès,1 Philippe Kahane,2 Lorella Minotti,2 Laura Tassi,4 Sylvie Grand,3 Dominique Hoffmann1 and Alim Louis Benabid1 1 Department of Neurosurgery, 2Department of Neurology and 3Department of Neuroradiology, CHU Michallon, Grenoble, France and 4Epilepsy Surgery Center ‘C. Munari’, Niguardia Hospital, Milan, Italy Correspondence to: Dr Chabardès E-mail: We investigated the role of the temporal pole (TP) in 48 consecutive patients with drug-refractory temporal lobe epilepsy (TLE). Chronic depth recordings of TP cortex activity were used in association with video recording of ictal symptoms during 48 spontaneous seizures. In 23 cases (48%, group 1) the TP was involved at the onset of the seizure, before or concurrently with the hippocampus. In the remaining 25 patients (52%, group 2) the TP was involved 16.4 6 13.8 s after the hippocampus. A past history of febrile seizures was found in both groups, with no statistical difference. Ictal symptoms did not differentiate TP seizures from seizures originating in the hippocampus but the first clinical sign occurred sooner in group 1 compared with group 2 (respectively 10.56 6 9 and 25.7 6 19 s, respectively, P = 0.005). Loss of awareness also occurred sooner in the case of TP seizures compared with mesiotemporal lobe (MTL) seizures (22.9 6 22.6 versus 42.2 6 18.6 s, P = 0.0002). MRI data analysis showed that hippocampal sclerosis was present in both groups of patients, although it was more frequent in patients with MTL onset. Anterior temporal white matter changes were found ipsilateral to the epileptogenic area and tended to be more frequent in patients with TP seizures. All the patients underwent tailored anterior temporal lobectomy that included the TP, the hippocampus, the parahippocampal gyrus and the anterior part of the lateral temporal cortex. A better postoperative outcome was achieved in group 1 compared with group 2 (Engel class 1, 95 and 72% respectively, P = 0.04). We conclude that the frequent TP involvement at the onset of seizures could be a supplementary explanation for some failures of selective amygdalohippocampectomy, which should be addressed preferentially to well-selected patients. Moreover, the involvement of the TP cortex at the onset of the seizures is a good predicting factor for postoperative seizure outcome. Keywords: temporal lobe epilepsy; SEEG; anterior temporal lobectomy; temporal pole; mesial temporal sclerosis Abbreviations: LVFA = low-voltage fast activity; MTL = mesiotemporal lobe; MTLE = mesiotemporal lobe epilepsy; MTPLE = mesiotemporopolar lobe epilepsy; MTS = mesiotemporal sclerosis; TL = temporal lobe; TLE = temporal lobe epilepsy; TP = temporal pole; SEEG = stereo electroencephalography Received July 30, 2004. Revised January 30, 2005; Second revision March 7, 2005. Accepted March 9, 2005. Advance Access publication April 27, 2005 Introduction Temporal lobe epilepsy (TLE) is the most common form of medically intractable partial epilepsy in adults, and surgery has proved to be effective in the majority of patients. Mesial temporal sclerosis (MTS) is found in about 70% of these cases (Babb et al., 1987; Wolf et al., 1993; Pasquier et al., 1996) and its presence, highly associated with a past history of febrile seizures and with EEG lateralization of the epileptogenic region, is predictive of an excellent postoperative outcome. These findings have led to the definition of the mesial-temporal lobe epilepsy (MTLE) syndrome (Wieser et al., 1993; Cendes et al., 1997; Engel et al., 1997a). This term should be restricted to patients with the typical clinical presentation, MRI evidence of MTS, anterior and mid-inferomedial temporal ictal and interictal discharges on scalp EEG, and additional evidence of temporal lobe dysfunction from functional imaging and neuropsychology consistent with pathology on the same side. In such wellselected cases, one can expect 70–80% of patients to become # The Author (2005). Published by Oxford University Press on behalf of the Guarantors of Brain. All rights reserved. For Permissions, please email: Temporal pole in temporal lobe seizures seizure-free after surgery (Garcia et al., 1994; Arruda et al., 1996). The choice of whether to perform an anterior temporal lobectomy or a selective amygdalohippocampectomy varies among surgical teams. However, this concept of MTLE does not imply that the onset of seizures is always and exclusively confined to the sole sclerotic hippocampus. This point is illustrated by several studies using intracerebral electrodes (Munari et al., 1994; Spanedda et al., 1997; Isnard et al., 2000; Kahane et al., 2001), as well as by increasing evidence of extrahippocampal histological (Pitkanen et al., 1998) and morphological (Kuzniecky et al., 1987) abnormalities. These can involve other limbic structures, as well as paralimbic and temporal neocortical areas. Thus, the epileptogenic zone may extend beyond the atrophic mesial temporal structures, which may explain some failures or long-term relapses of selective mesialtemporal lobe (MTL) resections (Berkovic et al., 1995). Among extrahippocampal areas possibly involved in the genesis of MTL seizures, several studies have focused on the temporal pole (TP), a paralimbic area strongly connected with the amygdala, the hippocampus, the parahippocampal gyrus, the cingulate gyrus, the orbitofrontal cortex and the insula. These studies have clearly highlighted the common occurrence of histological (Choi et al., 1999; Meiners et al., 1999; Mitchell et al., 1999), morphological (Jutila et al., 2001; Moran et al., 2001) and metabolic (Semah et al., 1995; Rubin et al., 1995; Ryvlin et al., 1998; Dupont et al., 2000) changes in the TP. However, data obtained from depth recordings are serendipitous (Munari et al., 1994), and whether this structure can be responsible for seizure onset remains debatable. In a small group of patients implanted with intracerebral electrodes we found that early TP involvement was quite common during temporal lobe (TL) seizures, even when clinical feature associated with MRI evidence of MTS indicated an MTL onset (Chabardès et al., 1999). Therefore, we conducted a retrospective study in a larger population of 48 consecutive patients suffering from TLE. Preoperative stereotactic intracerebral EEG recordings (SEEG) were performed to provide information on the EEG activity of the TP of these patients. The main aim of this work was to assess the involvement of TP cortex during TL seizures and to further delineate the spectrum of TLE with temporopolar onset. Patients were selected using the following inclusion criteria: (i) a final diagnosis of TL seizures; (ii) SEEG investigation including the TP, MTL structures (hippocampus or hippocampus plus amygdala) and the temporal neocortex; (iii) at least one representative spontaneous seizure r (...truncated)