Dataset Information

Functional connectivity estimated from intracranial EEG predicts surgical outcome in intractable temporal lobe epilepsy.

ABSTRACT: This project aimed to determine if a correlation-based measure of functional connectivity can identify epileptogenic zones from intracranial EEG signals, as well as to investigate the prognostic significance of such a measure on seizure outcome following temporal lobe lobectomy. To this end, we retrospectively analyzed 23 adult patients with intractable temporal lobe epilepsy (TLE) who underwent an invasive stereo-EEG (SEEG) evaluation between January 2009 year and January 2012. A follow-up of at least one year was required. The primary outcome measure was complete seizure-freedom at last follow-up. Functional connectivity between two areas in the temporal lobe that were sampled by two SEEG electrode contacts was defined as Pearson's correlation coefficient of interictal activity between those areas. SEEG signals were filtered between 5 and 50 Hz prior to computing this correlation. The mean and standard deviation of the off diagonal elements in the connectivity matrix were also calculated. Analysis of the mean and standard deviation of the functional connections for each patient reveals that 90% of the patients who had weak and homogenous connections were seizure free one year after temporal lobectomy, whereas 85% of the patients who had stronger and more heterogeneous connections within the temporal lobe had recurrence of seizures. This suggests that temporal lobectomy is ineffective in preventing seizure recurrence for patients in whom the temporal lobe is characterized by weakly connected, homogenous networks. This pilot study shows promising potential of a simple measure of functional brain connectivity to identify epileptogenicity and predict the outcome of epilepsy surgery.

SUBMITTER: Antony AR

PROVIDER: S-EPMC3813548 | biostudies-literature | 2013

REPOSITORIES: biostudies-literature

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Functional connectivity estimated from intracranial EEG predicts surgical outcome in intractable temporal lobe epilepsy.

Antony Arun R AR Alexopoulos Andreas V AV González-Martínez Jorge A JA Mosher John C JC Jehi Lara L Burgess Richard C RC So Norman K NK Galán Roberto F RF

PloS one 20131030 10

This project aimed to determine if a correlation-based measure of functional connectivity can identify epileptogenic zones from intracranial EEG signals, as well as to investigate the prognostic significance of such a measure on seizure outcome following temporal lobe lobectomy. To this end, we retrospectively analyzed 23 adult patients with intractable temporal lobe epilepsy (TLE) who underwent an invasive stereo-EEG (SEEG) evaluation between January 2009 year and January 2012. A follow-up of a ...[more]

PMID: 24205027

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Project description:Patients with drug-resistant temporal lobe epilepsy often undergo intracranial EEG recording to capture multiple seizures in order to lateralize the seizure onset zone. This process is associated with morbidity and often ends in postoperative seizure recurrence. Abundant interictal (between-seizure) data are captured during this process, but these data currently play a small role in surgical planning. Our objective was to predict the laterality of the seizure onset zone using interictal intracranial EEG data in patients with temporal lobe epilepsy. We performed a retrospective cohort study (single-centre study for model development; two-centre study for model validation). We studied patients with temporal lobe epilepsy undergoing intracranial EEG at the University of Pennsylvania (internal cohort) and the Medical University of South Carolina (external cohort) between 2015 and 2022. We developed a logistic regression model to predict seizure onset zone laterality using several interictal EEG features derived from recent publications. We compared the concordance between the model-predicted seizure onset zone laterality and the side of surgery between patients with good and poor surgical outcomes. Forty-seven patients (30 female; ages 20-69; 20 left-sided, 10 right-sided and 17 bilateral seizure onsets) were analysed for model development and internal validation. Nineteen patients (10 female; ages 23-73; 5 left-sided, 10 right-sided, 4 bilateral) were analysed for external validation. The internal cohort cross-validated area under the curve for a model trained using spike rates was 0.83 for a model predicting left-sided seizure onset and 0.68 for a model predicting right-sided seizure onset. Balanced accuracies in the external cohort were 79.3% and 78.9% for the left- and right-sided predictions, respectively. The predicted concordance between the laterality of the seizure onset zone and the side of surgery was higher in patients with good surgical outcome. We replicated the finding that right temporal lobe epilepsy was harder to distinguish in a separate modality of resting-state functional MRI. In conclusion, interictal EEG signatures are distinct across seizure onset zone lateralities. Left-sided seizure onsets are easier to distinguish than right-sided onsets. A model trained on spike rates accurately identifies patients with left-sided seizure onset zones and predicts surgical outcome. A potential clinical application of these findings could be to either support or oppose a hypothesis of unilateral temporal lobe epilepsy when deciding to pursue surgical resection or ablation as opposed to device implantation.

Project description:Over the last decade, several methods for analysis of epileptiform signals in electroencephalography (EEG) have been proposed. These methods mainly use EEG signal features in either the time or the frequency domain to separate regular, interictal, and ictal brain activity. The aim of this work was to evaluate the feasibility of using functional connectivity (FC) based feature extraction methods for the analysis of epileptiform discharges in EEG signals. These signals were obtained from EEG-fMRI sessions of 10 patients with mesial temporal lobe epilepsy (MTLE) with unilateral hippocampal atrophy. The connectivity functions investigated were motif synchronization, imaginary coherence, and magnitude squared coherence in the alpha, beta, and gamma bands of the EEG. EEG signals were sectioned into 1-s epochs and classified according to (using neurologist markers): activity far from interictal epileptiform discharges (IED), activity immediately before an IED and, finally, mid-IED activity. Connectivity matrices for each epoch for each FC function were built, and graph theory was used to obtain the following metrics: strength, cluster coefficient, betweenness centrality, eigenvector centrality (both local and global), and global efficiency. The statistical distributions of these metrics were compared among the three classes, using ANOVA, for each FC function. We found significant differences in all global (p < 0.001) and local (p < 0.00002) graph metrics of the far class compared with before and mid for motif synchronization on the beta band; local betweenness centrality also pointed to a degree of lateralization on the frontotemporal structures. This analysis demonstrates the potential of FC measures, computed using motif synchronization, for the characterization of epileptiform activity of MTLE patients. This methodology may be helpful in the analysis of EEG-fMRI data applied to epileptic foci localization. Nonetheless, the methods must be tested with a larger sample and with other epileptic phenotypes.

Project description:BackgroundCurrently, more than one-third of patients with drug-resistant temporal lobe epilepsy (TLE) continue to develop seizures after resection surgery. Dynamic functional network connectivity (DFNC) analyses, capturing temporal properties of functional connectivity during MRI acquisition, may help us identify unfavorable surgical outcomes. The purpose of this work was to explore the association of DFNC variations of preoperative resting-state MRI and surgical outcomes in patients with drug-resistant TLE.MethodsWe evaluated 61 patients with TLE matched for age and gender with 51 healthy controls (HC). Patients with TLE were classified as seizure-free (n = 39) and not seizure-free (n = 16) based on the Engel surgical outcome scale. Six patients were unable to confirm the postoperative status and were not included in the subgroup analysis. The DFNC was calculated using group spatial independent component analysis and the sliding window approach.ResultsDynamic functional network connectivity analyses suggested two distinct connectivity "States." The dynamic connectivity state of patients with TLE was different from HC. TLE subgroup analyses showed not seizure-free (NSF) patients spent significantly more time in State II compared to seizure-free (SF) patients and HC. Further, the number of transitions from State II to State I was significantly lower in NSF patients. SF patients had compensatory enhancement of DFNC strengths between default and dorsal attention network, as well as within the default network. While reduced DFNC strengths of within-network and inter-network were both observed in NSF patients, patients with abnormally temporal properties and more extension DFNC strength alterations were less likely to receive seizure freedom.ConclusionsOur study indicates that DFNC could offer a better understanding of dynamic neural impairment mechanisms of drug-resistant TLE functional network, epileptic brain network reorganization, and provide an additional preoperative evaluation support for surgical treatment of drug-resistant TLE.

Project description:Executive control function (ECF) deficit is a common complication of temporal lobe epilepsy (TLE). Characteristics of brain network connectivity in TLE with ECF dysfunction are still unknown. The aim of this study was to investigate resting-state functional connectivity (FC) changes in patients with unilateral intractable TLE with impaired ECF. Forty right-handed patients with left TLE confirmed by comprehensive preoperative evaluation and postoperative pathological findings were enrolled. The patients were divided into normal ECF (G1) and decreased ECF (G2) groups according to whether they showed ECF impairment on the Wisconsin Card Sorting Test (WCST). Twenty-three healthy volunteers were recruited as the healthy control (HC) group. All subjects underwent resting-state functional magnetic resonance imaging (rs-fMRI). Group-information-guided independent component analysis (GIG-ICA) was performed to estimate resting-state networks (RSNs) for all subjects. General linear model (GLM) was employed to analyze intra-network FC (p < 0.05, false discovery rate, FDR correction) and inter-network FC (p < 0.05, Bonferroni correction) of RSN among three groups. Pearson correlations between FC and neuropsychological tests were also determined through partial correlation analysis (p < 0.05). Eleven meaningful RSNs were identified from 40 left TLE and 23 HC subjects. Comparison of intra-network FC of all 11 meaningful RSNs did not reveal significant difference among the three groups (p > 0.05, FDR correction). For inter-network analysis, G2 exhibited decreased FC between the executive control network (ECN) and default-mode network (DMN) when compared with G1 (p = 0.000, Bonferroni correction) and HC (p = 0.000, Bonferroni correction). G1 showed no significant difference of FC between ECN and DMN when compared with HC. Furthermore, FC between ECN and DMN had significant negative correlation with perseverative responses (RP), response errors (RE) and perseverative errors (RPE) and had significant positive correlation categories completed (CC) in both G1 and G2 (p < 0.05). No significant difference of Montreal Cognitive Assessment (MoCA) was found between G1 and G2, while intelligence quotient (IQ) testing showed significant difference between G1and G2.There was no correlation between FC and either MoCA or IQ performance. Our findings suggest that ECF impairment in unilateral TLE is not confined to the diseased temporal lobe. Decreased FC between DMN and ECN may be an important characteristic of RSN in intractable unilateral TLE.

Project description:OBJECTIVE:The current practice under which patients with refractory epilepsy are surgically treated is based mainly on the identification of specific cortical areas, mainly the epileptogenic zone, which is believed to be responsible for generation of seizures. A better understanding of the whole epileptic network and its components and properties is required before more effective and less invasive therapies can be developed. The aim of the present study was to partially characterize the evolution of the functional network during the preictal-ictal transition in partial seizures in patients with temporal lobe epilepsy (TLE). METHODS:Scalp and foramen ovale (FOE) recordings from twenty-two TLE patients were analyzed under the complex network perspective. The density of links, average path length, average clustering coefficient, and modularity were calculated during the preictal and the ictal stages. Both linear-Pearson correlation-and non-linear-phase synchronization-measures were used as proxies of functional connectivity between the electrode locations areas. The transition from one stage to the other was evaluated in the whole network and in the mesial sub-networks. The results were compared with a voltage-dependent measure, namely, the spectral entropy. RESULTS:Changes in the global functional network during the transition from the preictal to the ictal stage show, in the linear case, that in sixteen cases (72.7%) the density of the links increased during the seizure, with a decrease in the average path length in fifteen cases (68.1%). There was also a preictal and ictal imbalance in functional connectivity during both stages (77.2% to 86.3%). The SE dropped during the seizure in 95.4% of the cases, but did not show any tendency towards lateralization. When using the nonlinear measure of functional connectivity, the phase synchronization, similar results were obtained. CONCLUSIONS:In TLE patients, the transition to the ictal stage is accompanied by increasing global synchronization and a more ordered spectral content of the signals, indicated by lower spectral entropy. The interictal connectivity imbalance (lower ipsilateral connectivity) is sustained during the seizure, irrespective of any appreciable imbalance in the spectral entropy of the mesial recordings.

Dataset Information

Functional connectivity estimated from intracranial EEG predicts surgical outcome in intractable temporal lobe epilepsy.

Publications

Functional connectivity estimated from intracranial EEG predicts surgical outcome in intractable temporal lobe epilepsy.

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