Normative brain mapping of interictal intracranial EEG to localize epileptogenic tissue.
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ABSTRACT:
SUBMITTER: Taylor PN
PROVIDER: S-EPMC9050535 | biostudies-literature |
REPOSITORIES: biostudies-literature
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Project description:Planning surgery for patients with medically refractory epilepsy often requires recording seizures using intracranial EEG. Quantitative measures derived from interictal intracranial EEG yield potentially appealing biomarkers to guide these surgical procedures; however, their utility is limited by the sparsity of electrode implantation as well as the normal confounds of spatiotemporally varying neural activity and connectivity. We propose that comparing intracranial EEG recordings to a normative atlas of intracranial EEG activity and connectivity can reliably map abnormal regions, identify targets for invasive treatment and increase our understanding of human epilepsy. Merging data from the Penn Epilepsy Center and a public database from the Montreal Neurological Institute, we aggregated interictal intracranial EEG retrospectively across 166 subjects comprising >5000 channels. For each channel, we calculated the normalized spectral power and coherence in each canonical frequency band. We constructed an intracranial EEG atlas by mapping the distribution of each feature across the brain and tested the atlas against data from novel patients by generating a z-score for each channel. We demonstrate that for seizure onset zones within the mesial temporal lobe, measures of connectivity abnormality provide greater distinguishing value than univariate measures of abnormal neural activity. We also find that patients with a longer diagnosis of epilepsy have greater abnormalities in connectivity. By integrating measures of both single-channel activity and inter-regional functional connectivity, we find a better accuracy in predicting the seizure onset zones versus normal brain (area under the curve = 0.77) compared with either group of features alone. We propose that aggregating normative intracranial EEG data across epilepsy centres into a normative atlas provides a rigorous, quantitative method to map epileptic networks and guide invasive therapy. We publicly share our data, infrastructure and methods, and propose an international framework for leveraging big data in surgical planning for refractory epilepsy.
| S-EPMC9630716 | biostudies-literature
Project description:Objective:We investigated the performance of automatic spike detection and subsequent electroencephalogram (EEG) source imaging to localize the epileptogenic zone (EZ) from long-term EEG recorded during video-EEG monitoring. Methods:In 32 patients, spikes were automatically detected in the EEG and clustered according to their morphology. The two spike clusters with most single events in each patient were averaged and localized in the brain at the half-rising time and peak of the spike using EEG source imaging. On the basis of the distance from the sources to the resection and the known patient outcome after surgery, the performance of the automated EEG analysis to localize the EZ was quantified. Results:In 28 out of the 32 patients, the automatically detected spike clusters corresponded with the reported interictal findings. The median distance to the resection in patients with Engel class I outcome was 6.5 and 15 mm for spike cluster 1 and 27 and 26 mm for cluster 2, at the peak and the half-rising time of the spike, respectively. Spike occurrence (cluster 1 vs. cluster 2) and spike timing (peak vs. half-rising) significantly influenced the distance to the resection (p < 0.05). For patients with Engel class II, III, and IV outcomes, the median distance increased to 36 and 36 mm for cluster 1. Localizing spike cluster 1 at the peak resulted in a sensitivity of 70% and specificity of 100%, positive prediction value (PPV) of 100%, and negative predictive value (NPV) of 53%. Including the results of spike cluster 2 led to an increased sensitivity of 79% NPV of 55% and diagnostic OR of 11.4, while the specificity dropped to 75% and the PPV to 90%. Significance:We showed that automated analysis of long-term EEG recordings results in a high sensitivity and specificity to localize the epileptogenic focus.
| S-EPMC5862106 | biostudies-literature
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.
| S-EPMC11372416 | biostudies-literature
Project description:A normative electrographic activity map could be a powerful resource to understand normal brain function and identify abnormal activity. Here, we present a normative brain map using scalp EEG in terms of relative band power. In this exploratory study we investigate its temporal stability, its similarity to other imaging modalities, and explore a potential clinical application. We constructed scalp EEG normative maps of brain dynamics from 17 healthy controls using source-localised resting-state scalp recordings. We then correlated these maps with those acquired from MEG and intracranial EEG to investigate their similarity. Lastly, we use the normative maps to lateralise abnormal regions in epilepsy. Spatial patterns of band powers were broadly consistent with previous literature and stable across recordings. Scalp EEG normative maps were most similar to other modalities in the alpha band, and relatively similar across most bands. Towards a clinical application in epilepsy, we found abnormal temporal regions ipsilateral to the epileptogenic hemisphere. Scalp EEG relative band power normative maps are spatially stable across time, in keeping with MEG and intracranial EEG results. Normative mapping is feasible and may be potentially clinically useful in epilepsy. Future studies with larger sample sizes and high-density EEG are now required for validation.
| S-EPMC10439201 | biostudies-literature
Project description:Synchronized cortical activity is implicated in both normative cognitive functioning and many neurologic disorders. For epilepsy patients with intractable seizures, irregular synchronization within the epileptogenic zone (EZ) is believed to provide the network substrate through which seizures initiate and propagate. Mapping the EZ prior to epilepsy surgery is critical for detecting seizure networks in order to achieve postsurgical seizure control. However, automated techniques for characterizing epileptic networks have yet to gain traction in the clinical setting. Recent advances in signal processing and spike detection have made it possible to examine the spatiotemporal propagation of interictal spike discharges across the epileptic cortex. In this study, we present a novel methodology for detecting, extracting, and visualizing spike propagation and demonstrate its potential utility as a biomarker for the EZ. Eighteen presurgical intracranial EEG recordings were obtained from pediatric patients ultimately experiencing favorable (i.e., seizure-free, n?=?9) or unfavorable (i.e., seizure-persistent, n?=?9) surgical outcomes. Novel algorithms were applied to extract multichannel spike discharges and visualize their spatiotemporal propagation. Quantitative analysis of spike propagation was performed using trajectory clustering and spatial autocorrelation techniques. Comparison of interictal propagation patterns revealed an increase in trajectory organization (i.e., spatial autocorrelation) among Sz-Free patients compared with Sz-Persist patients. The pathophysiological basis and clinical implications of these findings are considered.
| S-EPMC5165024 | biostudies-literature
Project description:BackgroundStereotactic electroencephalography (SEEG) is a minimally invasive neurosurgical method to localize epileptogenic brain regions in epilepsy but requires days in the hospital with interventions to trigger several seizures.ObjectiveTo make initial progress in the development of network analysis methods to identify epileptogenic brain regions using brief, resting-state SEEG data segments, without requiring seizure recordings.MethodsIn a cohort of 15 adult focal epilepsy patients undergoing SEEG, we evaluated functional connectivity (alpha-band imaginary coherence) across sampled regions using brief (2 min) resting-state data segments. Bootstrapped logistic regression was used to generate a model to predict epileptogenicity of individual regions.ResultsCompared to nonepileptogenic structures, we found increased functional connectivity within epileptogenic regions (P < .05) and between epileptogenic areas and other structures (P < .01, paired t-tests, corrected). Epileptogenic areas also demonstrated higher clustering coefficient (P < .01) and betweenness centrality (P < .01), and greater decay of functional connectivity with distance (P < .05, paired t-tests, corrected). Our functional connectivity model to predict epileptogenicity of individual regions demonstrated an area under the curve of 0.78 and accuracy of 80.4%.ConclusionOur study represents a preliminary step towards defining resting-state SEEG functional connectivity patterns to help localize epileptogenic brain regions ahead of neurosurgical treatment without requiring seizure recordings.
| S-EPMC7225010 | biostudies-literature
Project description:OBJECTIVE:When considering all patients with focal drug-resistant epilepsy, as high as 40-50% of patients suffer seizure recurrence after surgery. To achieve seizure freedom without side effects, accurate localization of the epileptogenic tissue is crucial before its resection. We investigate an automated, fast, objective mapping process that uses only interictal data. METHODS:We propose a novel approach based on multiple iEEG features, which are used to train a support vector machine (SVM) model for classification of iEEG electrodes as normal or pathologic using 30 min of inter-ictal recording. RESULTS:The tissue under the iEEG electrodes, classified as epileptogenic, was removed in 17/18 excellent outcome patients and was not entirely resected in 8/10 poor outcome patients. The overall best result was achieved in a subset of 9 excellent outcome patients with the area under the receiver operating curve?=?0.95. CONCLUSION:SVM models combining multiple iEEG features show better performance than algorithms using a single iEEG marker. Multiple iEEG and connectivity features in presurgical evaluation could improve epileptogenic tissue localization, which may improve surgical outcome and minimize risk of side effects. SIGNIFICANCE:In this study, promising results were achieved in localization of epileptogenic regions by SVM models that combine multiple features from 30 min of inter-ictal iEEG recordings.
| S-EPMC6759804 | biostudies-literature
Project description:High frequency oscillations (HFOs) are very brief events that are a well-established biomarker of the epileptogenic zone (EZ) but are rare and comprise only a tiny fraction of the total recorded EEG. We hypothesize that the interictal high frequency 'background' data, which has received little attention but represents the majority of the EEG record, also may contain additional, novel information for identifying the EZ. We analysed intracranial EEG (30-500 Hz frequency range) acquired from 24 patients who underwent resective surgery. We computed 38 quantitative features based on all usable, interictal data (63-307 h per subject), excluding all detected HFOs. We assessed association between each feature and the seizure onset zone (SOZ) and resected volume (RV) using logistic regression. A pathology score per channel was also created via principle component analysis and logistic regression, using hold-out-one-patient cross-validation to avoid in-sample training. Association of the pathology score with the SOZ and RV was quantified using an asymmetry measure. Many features were associated with the SOZ: 23/38 features had odds ratios >1.3 or <0.7 and 17/38 had odds ratios different than zero with high significance (P < 0.001/39, logistic regression with Bonferroni Correction). The pathology score, the rate of HFOs, and their channel-wise product were each strongly associated with the SOZ [median asymmetry ≥0.44, good surgery outcome patients; median asymmetry ≥0.40, patients with other outcomes; 95% confidence interval (CI) > 0.27 in both cases]. The pathology score and the channel-wise product also had higher asymmetry with respect to the SOZ than the HFO rate alone (median difference in asymmetry ≥0.18, 95% CI >0.05). These results support that the high frequency background data contains useful information for determining the EZ, distinct and complementary to information from detected HFOs. The concordance between the high frequency activity pathology score and the rate of HFOs appears to be a better biomarker of epileptic tissue than either measure alone.
| S-EPMC8417455 | biostudies-literature
Project description:Aim: In neuroscience research, data are quite often characterized by an imbalanced distribution between the majority and minority classes, an issue that can limit or even worsen the prediction performance of machine learning methods. Different resampling procedures have been developed to face this problem and a lot of work has been done in comparing their effectiveness in different scenarios. Notably, the robustness of such techniques has been tested among a wide variety of different datasets, without considering the performance of each specific dataset. In this study, we compare the performances of different resampling procedures for the imbalanced domain in stereo-electroencephalography (SEEG) recordings of the patients with focal epilepsies who underwent surgery. Methods: We considered data obtained by network analysis of interictal SEEG recorded from 10 patients with drug-resistant focal epilepsies, for a supervised classification problem aimed at distinguishing between the epileptogenic and non-epileptogenic brain regions in interictal conditions. We investigated the effectiveness of five oversampling and five undersampling procedures, using 10 different machine learning classifiers. Moreover, six specific ensemble methods for the imbalanced domain were also tested. To compare the performances, Area under the ROC curve (AUC), F-measure, Geometric Mean, and Balanced Accuracy were considered. Results: Both the resampling procedures showed improved performances with respect to the original dataset. The oversampling procedure was found to be more sensitive to the type of classification method employed, with Adaptive Synthetic Sampling (ADASYN) exhibiting the best performances. All the undersampling approaches were more robust than the oversampling among the different classifiers, with Random Undersampling (RUS) exhibiting the best performance despite being the simplest and most basic classification method. Conclusions: The application of machine learning techniques that take into consideration the balance of features by resampling is beneficial and leads to more accurate localization of the epileptogenic zone from interictal periods. In addition, our results highlight the importance of the type of classification method that must be used together with the resampling to maximize the benefit to the outcome.
| S-EPMC8641296 | biostudies-literature
Project description:While seizure activity may be electrographically widespread, increasing evidence has suggested that ictal discharges may in fact represent travelling waves propagated from a focal seizure source. Interictal epileptiform discharges (IEDs) are an electrographic manifestation of excessive hypersynchronization of cortical activity that occur between seizures and are considered a marker of potentially epileptogenic tissue. The precise relationship between brain regions demonstrating IEDs and those involved in seizure onset, however, remains poorly understood. Here, we hypothesize that IEDs likewise reflect the receipt of travelling waves propagated from the same regions which give rise to seizures. Forty patients from our institution who underwent invasive monitoring for epilepsy, proceeded to surgery and had at least one year of follow-up were included in our study. Interictal epileptiform discharges were detected using custom software, validated by a clinical epileptologist. We show that IEDs reach electrodes in sequences with a consistent temporal ordering, and this ordering matches the timing of receipt of ictal discharges, suggesting that both types of discharges spread as travelling waves. We use a novel approach for localization of ictal discharges, in which time differences of discharge receipt at nearby electrodes are used to compute source location; similar algorithms have been used in acoustics and geophysics. We find that interictal discharges co-localize with ictal discharges. Moreover, interictal discharges tend to localize to the resection territory in patients with good surgical outcome and outside of the resection territory in patients with poor outcome. The seizure source may originate at, and also travel to, spatially distinct IED foci. Our data provide evidence that interictal discharges may represent travelling waves of pathological activity that are similar to their ictal counterparts, and that both ictal and interictal discharges emerge from common epileptogenic brain regions. Our findings have important clinical implications, as they suggest that seizure source localizations may be derived from interictal discharges, which are much more frequent than seizures.
| S-EPMC10411927 | biostudies-literature