Foramen Ovale Recordings Research Articles

P372 Inference of intra and inter hippocampal directed causal relationships based on foramen ovale recordings

Objectives The traditional method for seizure onset zone determination is based on the temporal order in the appearance of pathological waveforms. However, this method assumes, that the well observable pathological waveforms are really the first signs of those processes, which play important role in the seizure generation. Our objective is to develop and apply new mathematical methods to identify the causal relations between brain areas during epileptic activity. Methods The Convergent Cross Mapping method of Sugihara was modified to reveal temporal dynamics of causal connections, and applied to current source density distribution data calculated from multichannel foramen ovale electrode recordings. Results The causality analysis revealed directed connections between the two hippocampi and specific changes in intra and inter-hippocampal connections comparing interictal and ictal periods: intrahippocampal connections get stronger and spread away spatially, while inter-hippocampal connections show more complex temporal development patterns during the seizures: the functional connectivity decreases during initial phase of the seizures in some cases, while increases during the full blown seizures. Onset of the tonic phases accompanied by temporal increase of the causal connections between the two hippocampi as well. Conclusions New mathematical analysis method, such as Convergent Cross Mapping raise the possibility of objective determination the causal relationships at the initiation of the seizure, without specific assumptions about the waveforms. Significance Causality analysis can support more precise identification of seizure onset zones, thus results in better surgical outcome.

Extrahippocampal Desynchronization in Nonlesional Temporal Lobe Epilepsy

Although temporal lobe epilepsy (TLE) is traditionally associated with both hypersynchronous activity in the form of interictal epileptic discharges and hippocampal sclerosis, recent findings suggest that desynchronization also plays a central role in the dynamics of this pathology. The objective of this work is to show the imbalance existing between mesial activities in patients suffering from mesial TLE, with normal mesial structures. Foramen ovale recordings from six patients with mesial TLE and one with lateral TLE were analyzed through a cluster analysis and synchronization matrices. None of the patients present findings in the MRI presurgical evaluation. Numerical analysis was carried out in three different situations: awake and sleep interictal and also during the preictal stage. High levels of desynchronization ipsilateral to the epileptic side were present in mesial TLE patients. Low levels of desynchronization were present in the lateral TLE patient during the interictal stage and almost zero in the preictal stage. Implications of these findings in relation with seizure spreading are discussed.

Foramen ovale electrodes in the evaluation of epilepsy surgery: Conventional and unconventional uses

Foramen ovale (FO) electrodes have been used in the evaluation of epilepsy surgery for more than 25years. Their traditional application was in patients with mesial temporal lobe epilepsy. Due in part to advances in neuroimaging, their use has declined. We describe our cumulative experience with FO electrodes and use examples to illustrate a range of indications for FO recordings that extend beyond their conventional utility for mesial temporal lobe cases. We also summarize the pros and cons of FO electrodes implantation and attempt to reestablish their utility in presurgical evaluation.

Epidural and foramen‐ovale electrodes in the diagnostic evaluation of patients considered for epilepsy surgery

To evaluate the clinical utility of epidural and foramen-ovale recordings and associated morbidity in the pre-surgical evaluation of epilepsy. We retrospectively analysed 59 epilepsy patients, who underwent recordings with epidural (n = 59) and foramen-ovale electrodes (n = 46) as part of their pre-surgical evaluation between 1990-1999. The epidural and foramen-ovale evaluation was based on the results of the non-invasive EEG-video recordings in patients, in whom non-invasive evaluation failed to localise seizure onset (75%, 44 patients) or where EEG, and imaging studies were discrepant (25%, 15 patients) but allowed a testable hypothesis on the seizure onset zone. Most patients (n = 57) were evaluated between 1990-1994. Only two patients were evaluated later. The results of the epidural (n = 559) and foramen-ovale (n = 83) electrode recordings allowed us to proceed to resective epilepsy surgery in 31% (n = 18) and to exclude further invasive evaluation in 15% (n = 9) of the patients. In 49% (n = 29) of the patients the results guided further invasive recordings using subdural and/or depth electrodes. For only three patients no additional information was gained by the electrode recordings. Temporary morbidity included local infection (epidural; n = 1) and facial pain (foramen ovale; n = 1) but no permanent complication occurred. Epidural and foramen-ovale electrodes have almost been abandoned in recent years, most likely because of the improvement of neuroimaging techniques such as MRI, PET and ictal SPECT. However, in selected patients, epidural electrodes and foramen-ovale electrodes are either useful as a measure to avoid invasive evaluation or serve to guide invasive evaluation.

Characteristics of scalp electrical fields associated with deep medial temporal epileptiform discharges

Objective To determine scalp characteristics of epileptiform discharges arising from medial temporal structures (MT). Methods Signal-to-noise ratio was increased by averaging simultaneous recordings from intracranial and scalp electrodes synchronised on discharges recorded by foramen ovale (FO) electrodes. The topography, amplitude and distribution of averaged scalp signals were analysed. Results Four thousand three hundred and twenty-seven discharges from 20 patients were averaged into 77 patterns. Before averaging, only 9% of discharges were detectable on the scalp without the need of simultaneous FO recordings (SED). A further 72.3% of discharges fell into averaged patterns that could be detected on the scalp as small transients before or after averaging (STBA or STAA). In 18.7% of discharges, no scalp signal was seen after averaging. Whereas most SED patterns had largest amplitude on the scalp at anterior temporal electrodes, STBA and STAA patterns showed greater variability and more widespread scalp fields, suggesting a deeper source. Dipole source localisation modelled the majority of SED patterns as radial dipoles located just behind the eye. In contrast, dipoles corresponding to STBA or STAA patterns showed greater variability in location and orientation and tended to be located at MT. Conclusions SED patterns seem to arise from widespread subtemporal and/or superficial neocortical activation, generating EEG fields that are distorted by the high electrical conductivity of anterior cranial foramina. In contrast, STBA and STAA patterns represent electrical fields from neuronal activity more restricted to MT, that reach the scalp highly attenuated by volume-conduction and less distorted by cranial foramina. Significance Low amplitude scalp signals can be related to MT activity and must be taken into consideration for the diagnosis of temporal lobe epilepsy, pre-surgical assessment and for valid modelling of deep sources from the scalp EEG and magnetoencephalogram.

Foramen ovale Recordings: A Presurgical Investigation in Epilepsy

The aim of our study was to determine when foramen ovale recordings add useful information to scalp EEG recordings and magnetic resonance imaging (MRI) with hippocampal measurements. We evaluated the outcome of 79 patients with non-lesional partial epilepsy with presumed temporal seizure onset. Ictal foramen ovale recordings were performed in 16 patients with normal MRI (‘MRI-negative group’) and 41 patients with lateralizing MRI but non-lateralizing scalp EEG (‘discordant group’). 22 patients with concordant MRI and scalp EEG were not investigated with foramen ovale recordings (‘concordant group’). The seizure-free rate was higher in concordant than discordant patients despite additional investigation with foramen ovale electrodes (71 and 55% seizure free, respectively). No useful localizing information was added with foramen ovale recordings in MRI-negative patients.

Voxel based morphometry of grey matter abnormalities in patients with medically intractable temporal lobe epilepsy: effects of side of seizure onset and epilepsy duration

Objectives: To investigate the use of whole brain voxel based morphometry (VBM) and stereological analysis to study brain morphology in patients with medically intractable temporal lobe epilepsy; and to determine...

Sensitivity of recordings at sphenoidal electrode site for detecting seizure onset: evidence from scalp, superficial and deep foramen ovale recordings

Objectives: Some authors have recently stressed that the position of the tip of sphenoidal electrodes plays a crucial role in their efficacy in detecting ictal onset. An opportunity to test this hypothesis is provided by recordings from the most superficial contacts of foramen ovale (FO) electrode bundles because these contacts are located at the FO, in a position equivalent to that of optimally located sphenoidal electrodes. To simplify wording, recordings obtained by superficial FO electrodes will hereafter be called sphenoidal recordings, although they have not been obtained with standard sphenoidal electrodes. The sensitivities of simultaneous scalp and sphenoidal recordings for detecting ictal onset have been compared with each other, and with a ‘gold standard’ provided by simultaneous deep intracranial FO recordings from the mesial aspect of the temporal lobe. Methods: Three hundred and fourteen seizures obtained from 110 patients under telemetric presurgical assessment for temporal lobe epilepsy have been studied. Scalp electrodes included anterior temporal placements. All scalp electrodes were considered when identifying seizure onset but the anterior temporal electrodes were most frequently involved. Results: Ictal onset time at sphenoidal and scalp recordings: initial ictal changes appeared simultaneously in scalp and sphenoidal recordings in 123 seizures (39.2%). Initial changes occurred earlier in sphenoidal recordings in 63 seizures (20.1%), whereas they were seen earlier on the scalp in 76 seizures (24.2%). Artefacts prevented the comparison between sphenoidal and scalp recordings in 16 seizures (5.1%) and no ictal changes were seen on the scalp and/or sphenoidal recordings in 36 seizures (11.5%). In most of the 63 seizures where ictal changes appeared earlier in sphenoidal recordings, a delayed ipsilateral scalp onset was seen as the signal amplitude increased or scalp changes could be identified retrospectively on the scalp with an onset which appeared simultaneous and ipsilateral to the initial sphenoidal changes. Sphenoidal recordings supplied additional information when compared to scalp recordings in only 22 seizures (7%): in 5 seizures with artefacts on the scalp, in 6 seizures with no changes on the scalp and in 11 seizures with discrepant laterality at onset. Congruence in laterality with respect to deep intracraneal FO recordings: of the 61 seizures with unilateral onset on the scalp, onsets at sphenoidal recordings and deep FO electrodes were ipsilateral in most cases. In only 3 of these 61 seizures (4.9%), sphenoidal recordings lateralized ipsilateral to the deep FO electrodes in the presence of a contralateral onset on the scalp. In 14 among the 122 seizures (11.5%) with bilateral asymmetrical onset on the scalp, sphenoidal recordings lateralized seizure onset ipsilateral to the deep FO electrodes in the presence of a contralateral scalp onset. Thus, when compared with scalp EEG, sphenoidal recordings increased laterality congruence with respect to deep FO electrodes in 17 seizures (5.4%). Conclusions: Extracranial electrodes located next to the FO at the sphenoidal electrode site yield an improvement over suitable surface electrodes in the identification of ictal onset in only 5.4–7% of seizures. Such improvement derives from the fact that the low amplitude signals often seen at seizure onset may show higher amplitude on sphenoidal than on scalp recordings.

Quantitative magnetic resonance imaging in consecutive patients evaluated for surgical treatment of temporal lobe epilepsy

We present the results of quantitative Magnetic Resonance Imaging (MRI) in 55 consecutively referred patients with clinical evidence of temporal lobe epilepsy (TLE). The Cavalieri method was used in combination with point counting to provide unbiased estimates of the volume of the left and right hippocampus, amygdala, temporal lobe, lateral ventricles and cerebral hemisphere, and pixel by pixel maps of the T2 relaxation time were computed for both central and anterior sections of the hippocampus. The 99th centiles of hippocampal volume, hippocampal volume asymmetry and T2 relaxation times in 20 control subjects provided limits which identified the presence of MTS. The results of the quantitative MRI were compared with the results of conventional diagnostic MRI, foramen ovale (FO) recording and the WADA test. Thirty-one patients were found to have unilateral MTS (17 left and 14 right) and 7 bilateral MTS. No evidence of MTS was detected in 16 patients. Of the 31 patients diagnosed with unilateral MTS on the basis of hippocampal volume and T2 measurement, 74% and 77% would respectively have received the same diagnosis on the basis of hippocampal volume and T2 measurements alone. In comparison to FO recording, quantitative MRI has a sensitivity of 55% and a specificity of 86%, while conventional diagnostic MRI has a sensitivity of 42% and a specificity of 80% for detection of MTS. Unilateral abnormalities were detected by FO recording in 30% cent of patients who appeared normal on quantitative MRI. WADA test results were available for 40 patients. The findings were consistent with quantitative MRI showing reduced memory function ipsilateral to unilateral MTS in 18 patients, but reduced memory function contralateral to unilateral MTS in two patients, and reduced memory function without MR abnormality in seven patients. WADA testing revealed unilateral memory impairments where MRI found bilateral pathology in 4 patients and in 4 patients in whom quantitative MRI detected unilateral MTS there was no evidence of reduced memory during WADA testing of the corresponding cerebral hemisphere. In the patients with unilateral right MTS a highly significant negative correlation ( p = 0.0003) was observed between age of onset and the volume of the contralateral temporal lobe. Quantitative MR imaging of the hippocampus (i.e. volume and T2 measurement) is preferable to conventional radiological reporting for providing objective evidence of the presence of MTS on which to base the referral of patients for surgery, and since it has associated morbidity FO recording is now only being used in selected patients. Furthermore, stereology provides a convenient method for estimating the volume of other brain structures, which is relevant to obtaining a better understanding of the effects of laterality and age of onset of TLE.

Utility of stereoelectroencephalography in preoperative assessment of temporal lobe epilepsy.

Of 269 consecutive patients entered into a preoperative assessment programme for possible surgical treatment of epilepsy, 33 had intracranial recording (SEEG) with combined subdural and depth electrodes for the purpose of localising a suspected temporal site of seizure onset. The findings in these patients are analysed with particular reference to: 1) the criteria of selection for SEEG and their validity; 2) information on SEEG compared with that obtained by less invasive means, including foramen ovale telemetry; 3) information on the use of intracerebral electrodes compared with subdural placements; 4) possible predictors of failure of localisation by SEEG and of surgical outcome. It was concluded that SEEG had usefully contributed to the management of 69% of the patients in whom it was used, establishing a previously unidentified site of seizure onset in 33%, correcting an erroneous localisation in 15%, and establishing inoperability in 21% of patients. No predictors of failure of SEEG or of surgery emerged; thus there was no evidence of unnecessary use of this procedure. Five patients were found with incorrect lateralisation of seizure onset on foramen ovale recording (of a total of 192 foramen ovale telemetries). Localisation of the ictal onset zone either by the distribution of inter-ictal discharges or by the initial ictal changes at subdural electrodes was unreliable, confirming the need for ictal, depth recordings.

Analysis of Foramen Ovale Electrode‐Recorded Seizures and Correlation with Outcome Following Amygdalohippocampectomy

We report a detailed electroclinical analysis of 320 seizures recorded by foramen ovale electrodes in 77 potential candidates for selective temporal lobe surgery because of antiepileptic drug-resistant seizures. The exact localization of the origin of seizure discharges, the electroencephalographic (EEG) seizure onset patterns, transhemispheric propagation, propagation time, duration of discharge, laterality of discharge termination, postictal focal slowing, correspondence between foramen ovale recordings and the scalp EEG, and the influence of antiepileptic drug modifications were studied and correlated with the clinical seizure semiology and with postoperative outcome following selective amygdalohippocampectomy. In general, the foramen ovale electrode technique provided good neurophysiological information in candidates for selective amygdalohippocampectomy. The following ictal signs predicted a good surgical outcome: (a) unilateral and anterior mediobasal temporal lobe seizure onset, (b) short seizure duration, (c) no or infrequent contralateral seizure discharge propagation, and (d) if propagation to the contralateral mediobasal temporal lobe occurred, the postoperative outcome was better the later the contralateral mediobasal temporal lobe was affected. Postoperative outcome was also better the less frequently contralateral interictal spikes occurred. No direct predictive value could be attributed to the presence of an initial arrest reaction.

Pre-operative assessment for epilepsy surgery: the role of foramen ovale recording : P. Chesterman, C.D. Binnie and C.E. Polkey (The Maudsley Hospital, London, England)

Higher-order thalamic nuclei, like the pulvinar, have extensive connections with cortex, suggesting a role in the coordination of cortical communication. A recent study in Science by Saalmann et al. (2012) implicates the pulvinar in promoting cortical alpha-band synchronization that subserves communication of attended information.

The ‘foramen ovale electrode’: a new recording method for the preoperative evaluation of patients suffering from mesio-basal temporal lobe epilepsy

A technique to record from the mesio-basal aspect of the temperal lobe by a subdural electrode inserted through the foramen ovale (FO) is described. For this purpose a special electrode was developed that, in addition, allowed epicortical DC recording. After having tested its value experimentally in dogs with penicillin-induced hippocampal seizure foci, this ‘FO electrode’ was subsequently applied to 10 patients. Nine of them suffered from drug-resistant complex partial seizures suspected to be of mesio-basal limbic origin. Seven patients had in addition to the FO electode depth electrodes stereotactically implanted within the hippocampus and nucleus amygdalae, thus allowing an evaluation of this new FO recording technique by direct comparison with stereo-EEG. Our results indicate that interictal epileptiform potentials as well as ictal discharges are reliably picked up by the FO electrode whenever nucleus amygdalae, hippocampus and parahippocampal gyrus show synchronous epileptic activity. As a rule, these events are not reflected in conventional scalp EEG records. Epileptiform activity in subcompartments of the mesio-basal limbic structures is not reliably reflected by the FO electrode. Negative epicortical DC shifts recorded by the FO electrode are a sensitive indicator of epileptic activity within the underlying deeper structures. In conclusion, in certain patients with drug-resistant epilepsy of suspected mesio-basal limbic origin the use of FO recording in the presurgical evaluation might provide sufficient information to give an indication for resective surgery, either by anterior temporal lobectomy or by selective amygdalo-hippocampectomy.