Search

Objective: In the era of stereoelectroencephalography (SEEG), many studies have been devoted to understanding the role of interictal high‐frequency oscillations. High‐frequency activity (HFA) at seizure onset has been identified as a marker of epileptogenic zone. We address the physiological significance of ictal HFAs and their relation to clinical semiology. Methods: We retrospectively identified patients with pure focal primary motor epilepsy. We selected only patients in whom SEEG electrodes were optimally placed in the motor cortex as confirmed by electrical stimulation. Based on these narrow inclusion criteria, we extensively studied 5 patients (3 males and 2 females, mean age = 22.4 years) using time–frequency analysis and time correlation with motor signs onset. Results: A total of 157 analyzable seizures were recorded in 5 subjects. The first 2 subjects had tonic or clonic semiology with rare secondary generalization. Subject 3 had atonic onset followed by clonic hand/arm flexion. Subject 4 had clusters of tonic and atonic facial movements. Subject 5 had upper extremity tonic movements. The median frequency of the fast activity extracted from the Epileptogenic Zone Fingerprint pipeline in the first 4 subjects was 76 Hz (interquartile range = 21.9Hz). Positive motor signs did not occur concomitantly with high gamma activity developing in the motor cortex. Motor signs began at the end of HFAs. Interpretation: This study supports the hypothesis of an inhibitory effect of ictal HFAs. The frequency range in the gamma band was associated with the direction of the clinical output effect. Changes from inhibitory to excitatory effect occurred when discharge frequency dropped to low gamma or beta. ANN NEUROL 2024;95:1127–1137 [ABSTRACT FROM AUTHOR]

Objective: To determine whether brain connectivity differs between focal cortical dysplasia (FCD) types I and II. Methods: We compared cortico‐cortical evoked potentials (CCEPs) as measures of effective brain connectivity in 25 FCD patients with drug‐resistant focal epilepsy who underwent intracranial evaluation with stereo‐electroencephalography (SEEG). We analyzed the amplitude and latency of CCEP responses following ictal‐onset single‐pulse electrical stimulation (iSPES). Results: In comparison to FCD type II, patients with type I demonstrated significantly larger responses in the electrodes near the ictal‐onset zone (<50 mm). These findings persisted when controlling for the location of the epileptogenic zone, as noted in patients with temporal lobe epilepsies, as well as controlling for seizure type, as noted in patients with focal to bilateral tonic‐clonic seizures (FBTCS). In type II, the root mean square (RMS) of CCEP responses dropped substantially from the early segment (10–60 ms) to the middle and late segments (60–600 ms). The middle and late CCEP latency segments showed the largest differences between FCD types I and II. Significance: Focal cortical dysplasia type I may have a greater degree of cortical hyperexcitability as compared with FCD type II. In addition, FCD type II displays a more restrictive area of hyperexcitability in both temporal and spatial domains. In patients with FBTCS and type I FCD, the increased amplitudes of RMS in the middle and late CCEP periods appear consistent with the cortico‐thalamo‐cortical network involvement of FBTCS. The notable differences in degree and extent of hyperexcitability may contribute to the different postsurgical seizure outcomes noted between these two pathological substrates. [ABSTRACT FROM AUTHOR]

Multimodal image integration (MMII) is a promising tool to help delineate the epileptogenic zone (EZ) in patients with medically intractable focal epilepsies undergoing presurgical evaluation. We report here the detailed methodology of MMII and an overview of the utility of MMII at the Cleveland Clinic Epilepsy Center from 2014 to 2018, exemplified by illustrative cases. The image integration was performed using the Curry platform (Compumedics Neuroscan™, Charlotte, NC, USA), including all available diagnostic modalities such as Magnetic resonance imaging (MRI), Positron Emission Tomography (PET), single-photon emission computed tomography (SPECT) and Magnetoencephalography (MEG), with additional capability of trajectory planning for intracranial EEG (ICEEG), particularly stereo-EEG (SEEG), as well as surgical resection planning. In the 5-year time span, 467 patients underwent MMII; of them, 98 patients (21%) had a history of prior neurosurgery and recurring seizures. Of the 467 patients, 425 patients underwent ICEEG implantation with further CT co-registration to identify the electrode locations. A total of 351 patients eventually underwent surgery after MMII, including 197 patients (56%) with non-lesional MRI and 223 patients (64%) with extra-temporal lobe epilepsy. Among 269 patients with 1-year post-operative follow up, 134 patients (50%) had remained completely seizure-free. The most common histopathological finding is focal cortical dysplasia. Our study illustrates the usefulness of MMII to enhance SEEG electrode trajectory planning, assist non-invasive/invasive data interpretation, plan resection strategy, and re-evaluate surgical failures. Information presented by MMII is essential to the understanding of the anatomo-functional-electro-clinical correlations in individual cases, which leads to the ultimate success of presurgical evaluation of patients with medically intractable focal epilepsies. [ABSTRACT FROM AUTHOR]

Objective: To characterize seizure and cognitive outcomes of sparing vs removing an magnetic resonance imaging (MRI)–normal hippocampus in patients with temporal lobe epilepsy. Methods: In this retrospective cohort study, we reviewed clinical, imaging, surgical, and histopathological data on 152 individuals with temporal lobe epilepsy and nonlesional hippocampi categorized into hippocampus‐spared (n = 74) or hippocampus‐resected (n = 78). Extra‐hippocampal lesions were allowed. Pre‐ and postoperative cognitive data were available on 86 patients. Predictors of seizure and cognitive outcomes were identified using Cox‐proportional hazard modeling followed by treatment‐specific model reduction according to Akaike information criterion, and built into an online risk calculator. Results: Seizures recurred in 40% within one postoperative year, and in 63% within six postoperative years. Male gender (P =.03), longer epilepsy duration (P <.01), normal MRI (P =.04), invasive evaluation (P =.02), and acute postoperative seizures (P <.01) were associated with a higher risk of recurrence. We found no significant difference in postoperative seizure freedom rates at 5 years between those whose hippocampus was spared and those whose hippocampus was resected (P =.17). Seizure outcome models built with pre‐ and postoperative data had bootstrap validated concordance indices of 0.65 and 0.72. The dominant hippocampus‐spared group had lower rates of decline in verbal memory (39% vs 70%; P =.03) and naming (41% vs 79%; P =.01) compared to the hippocampus‐resected group. Partial hippocampus sparing had the same risk of verbal memory decline as for complete removal. Significance: Sparing or removing an MRI‐normal hippocampus yielded similar long‐term seizure outcome. A more conservative approach, sparing the hippocampus, only partially shields patients from postoperative cognitive deficits. Risk calculators are provided to facilitate clinical counseling. [ABSTRACT FROM AUTHOR]

Although a number of experimental and clinical studies have pointed out participation or an even more prominent role of basal ganglia in focal seizures, the mode of interaction between cortical and striatal signals remains unclear. In the present study, we took stereoelectroencephalographic (SEEG) recordings in drug-resistant epilepsy patients, to qualitatively and quantitatively analyse the ictal striatum activity as well as its synchronization with cerebral cortex. Eleven patients who underwent SEEG evaluation were prospectively included if they fulfilled two inclusion criteria: (i) at least one orthogonal intracerebral electrode contact explored the basal ganglia, in either their putaminal or caudate part; and (ii) at least two SEEG seizures were recorded. Cortical and subcortical regions of interest were defined and different periods of interest were analysed. SEEG was visually inspected and h2 non-linear correlation analysis performed to study functional connectivity between cortical region of interest and striatum. Six correlation indices were calculated. Two main patterns of striatal activation were recorded: the most frequent was characterized by an early alpha/beta activity that started within the first 5 s after seizure onset, sometimes concomitant with it. The second one was characterized by late, slower, theta/delta activity. A significant difference in h2 correlation indices was observed during the preictal and seizure onset period compared to background for global striatal index, mesio-temporal/striatal index, latero-temporal/striatal index, insular/striatal index, prefrontal/striatal index. In addition, a significant difference in h2 correlation indices was observed during the seizure termination period compared to all the other periods of interest for the six indices calculated. These results indicate that cortico-striatal synchronization can arise from the start of focal seizures. Depending on the ictal frequency pattern, desynchronization can occur later, but a late and terminal hypersynchronization progressively takes over. These changes in synchronization level between cortical and striatal activity might be part of an endogenous mechanism controlling the duration of abnormal oscillations within the striato-thalamo-cortical loop and thereby their termination. Pathophysiology of basal ganglia in focal seizures appears to be much more interlinked with the cortex than expected. Beyond the stereotypical features they could imprint to seizure semiology, their role in strengthening mechanisms underlying cessation of ictal propagation should inspire new rationales for deep brain stimulation in patients with intractable focal epilepsies. [ABSTRACT FROM AUTHOR]

Summary: Objective: To examine the true incidence of hemorrhage related to stereo‐electroencephalography (SEEG) procedures. To analyze risk factors associated with the presence of different types of hemorrhage in SEEG procedures. Methods: This was a retrospective, single‐center observational study examining every SEEG implantation performed at our center from 2009 to 2017. This consisted of 549 consecutive SEEG implantations using a variety of stereotactic and imaging techniques. A hemorrhage grading system was applied by a blinded neuroradiologist to every postimplant and postexplant computed tomography (CT) scan. Hemorrhages were classified as asymptomatic or symptomatic based on neurologic deficit seen on examination. Statistical analysis included multivariate regression using relevant preoperative variables to predict the presence of hemorrhage. Results: One hundred five implantations (19.1%) had any type of hemorrhage seen on postimplant CT. Of these, 93 (16.9%) were asymptomatic and 12 (2.2%) were symptomatic, with 3 implantations (0.6%) resulting in either a permanent deficit (2, 0.4%) or death (1, 0.2%). Male sex, increased number of electrodes, and increasing age were associated with increased risk of postimplant hemorrhage on multivariate analysis. Increasing score in the grading system was related to a statistically significant increase in the likelihood of a symptomatic hemorrhage. Significance: Detailed examination of every postimplant CT reveals that the total hemorrhage rate appears higher than previously reported. Most of these hemorrhages are small and asymptomatic. Our grading system may be useful to risk stratify these hemorrhages and awaits prospective validation. [ABSTRACT FROM AUTHOR]

Summary: Objective: We aimed to determine the rates and predictors of resection and seizure freedom after bilateral stereo‐electroencephalography (SEEG) implantation. Methods: We reviewed 184 patients who underwent bilateral SEEG implantation (2009‐2015). Noninvasive and invasive evaluation findings were collected. Outcomes of interest included subsequent resection and seizure freedom. Statistical analyses employed multivariable logistic regression and proportional hazard modeling. Preoperative and postoperative seizure frequency, severity, and quality of life scales were also compared. Results: Following bilateral SEEG implantation, 106 of 184 patients (58%) underwent resection. Single seizure type (P = 0.007), a family history of epilepsy (P = 0.003), 10 or more seizures per month (P = 0.004), lower number of electrodes (P = 0.02), or sentinel electrode placement (P = 0.04) was predictive of undergoing a resection, as were lack of nonlocalized (P < 0.0001) or bilateral (P < 0.0001) ictal‐onset zones on SEEG. Twenty‐six of 81 patients (32% with follow‐up greater than 1 year) remained seizure‐free. Predictors of seizure freedom were single seizure type (P = 0.01), short epilepsy duration (P = 0.008), use of 2 or fewer antiepileptic drugs (AEDs) at the time of surgery (P = 0.0006), primary localization hypothesis involving the frontal lobe (P = 0.002), sentinel electrode placement only (P = 0.02), and lack of overlap between ictal‐onset zone and eloquent cortex (P = 0.04), along with epilepsy substrate histopathology (P = 0.007). Complete resection of a suspected focal cortical dysplasia showed a trend to increased likelihood of seizure freedom (P = 0.09). The 44 of 55 patients (80%) who underwent resection and experienced seizure recurrence had >50% seizure reduction, as opposed to 26 of 45 patients (58%) who continued medical therapy alone (P = 0.003). Seventy‐two percent of patients had a clinically meaningful quality of life improvement (>10% decrease in the Quality of Life in Epilepsy [QOLIE‐10] score) at 1 year. Significance: A strong preimplantation hypothesis of a suspected unifocal epilepsy increases the odds of resection and seizure freedom. We discuss a tailored approach, taking into account localization hypothesis and suspected epilepsy etiology in guiding implantation and subsequent surgical strategy. [ABSTRACT FROM AUTHOR]

Defining a bio-electrical marker for the brain area responsible for initiating a seizure remains an unsolved problem. Fast gamma activity has been identified as the most specific marker for seizure onset, but conflicting results have been reported. In this study, we describe an alternative marker, based on an objective description of interictal to ictal transition, with the aim of identifying a time-frequency pattern or 'fingerprint' that can differentiate the epileptogenic zone from areas of propagation. Seventeen patients who underwent stereoelectroencephalography were included in the study. Each had seizure onset characterized by sustained gamma activity and were seizure-free after tailored resection or laser ablation. We postulated that the epileptogenic zone was always located inside the resection region based on seizure freedom following surgery. To characterize the ictal frequency pattern, we applied the Morlet wavelet transform to data from each pair of adjacent intracerebral electrode contacts. Based on a visual assessment of the time-frequency plots, we hypothesized that a specific time-frequency pattern in the epileptogenic zone should include a combination of (i) sharp transients or spikes; preceding (ii) multiband fast activity concurrent; with (iii) suppression of lower frequencies. To test this hypothesis, we developed software that automatically extracted each of these features from the time-frequency data. We then used a support vector machine to classify each contact-pair as being within epileptogenic zone or not, based on these features. Our machine learning system identified this pattern in 15 of 17 patients. The total number of identified contacts across all patients was 64, with 58 localized inside the resected area. Subsequent quantitative analysis showed strong correlation between maximum frequency of fast activity and suppression inside the resection but not outside. We did not observe significant discrimination power using only the maximum frequency or the timing of fast activity to differentiate contacts either between resected and non-resected regions or between contacts identified as epileptogenic versus non-epileptogenic. Instead of identifying a single frequency or a single timing trait, we observed the more complex pattern described above that distinguishes the epileptogenic zone. This pattern encompasses interictal to ictal transition and may extend until seizure end. Its time-frequency characteristics can be explained in light of recent models emphasizing the role of fast inhibitory interneurons acting on pyramidal cells as a prominent mechanism in seizure triggering. The pattern clearly differentiates the epileptogenic zone from areas of propagation and, as such, represents an epileptogenic zone 'fingerprint'.awx306media15687076823001. [ABSTRACT FROM AUTHOR]

The authors report a case of 18-year-old woman with partial complex seizures compatible with temporal epilepsy by semiology. Due to medical refractoriness, she was referred to pre-surgical evaluation. Initially, MRI showed no significant structural abnormality and superficial scalp EEG demonstrated epileptiform activity in the frontotemporal areas. Due to the lack of clear MRI abnormalities and the potential involvement of dominant mesial temporal structures by seizure semiology and non-invasive data, extra-operative invasive evaluation using stereo-electroencephalography (SEEG) methodology was indicated. Invasive monitoring demonstrated seizure onset in the left temporal pole with early spread to ipsilateral amygdala. Surgical treatment resulted in resection of the temporal pole and amygdala, with preservation of the remaining mesial temporal lobe structures. Intraoperatively, it was observed that multiple dural defects in the anterior middle temporal fossa with invagination of adjacent temporal pole parenchyma are compatible with temporal encephalocele. Patient remains seizure-free since surgery (12 months follow-up period) with preservation of neuropsychological functions. Although temporal pole resection plus amygdalohippocampectomy has been described as an adequate surgical approach in temporal encephalocele cases, we demonstrated the usefulness of the SEEG methodology in minimizing the volume of temporal lobe resection without compromising seizure and neuropsychological outcomes. The optimal results in this case and the review of the literature may suggest that in medically refractory epilepsies caused by temporal pole encephaloceles, preservation of the temporal lobe mesial structures should be attempted. [ABSTRACT FROM AUTHOR]

Subtraction ictal and interictal single photon emission computed tomography can demonstrate complex ictal perfusion patterns. Regions with ictal hyperperfusion are suggested to reflect seizure onset and propagation pathways. The significance of ictal hypoperfusion is not well understood. The aim of this study was to verify whether ictal perfusion changes, both hyper- and hypoperfusion, correspond to electrically connected brain networks. A total of 36 subtraction ictal and interictal perfusion studies were analysed in 31 consecutive medically refractory focal epilepsy patients, evaluated by stereo-electroencephalography that demonstrated a single focal onset. Cortico-cortical evoked potential studies were performed after repetitive electrical stimulation of the ictal onset zone. Evoked responses at electrode contacts outside the stimulation site were used as a measure of connectivity. The evoked responses at these electrodes were compared to ictal perfusion values noted at these locations. In 67% of studies, evoked responses were significantly larger in hyperperfused compared to baseline-perfused areas. The majority of hyperperfused contacts also had significantly increased evoked responses relative to pre-stimulus electroencephalogram. In contrast, baseline-perfused and hypoperfused contacts mainly demonstrated non-significant evoked responses. Finally, positive significant correlations (P < 0.05) were found between perfusion scores and evoked responses in 61% of studies. When the stimulated ictal onset area was hyperperfused, 82% of studies demonstrated positive significant correlations. Following stimulation of hyperperfused areas outside seizure onset, positive significant correlations between perfusion changes and evoked responses could be seen, suggesting bidirectional connectivity. We conclude that strong connectivity was demonstrated between the ictal onset zone and hyperperfused regions, while connectivity was weaker in the direction of baseline-perfused or hypoperfused areas. In trying to understand a patient's epilepsy, one should consider the contribution of all hyperperfused regions, as these are likely not random, but represent an electrically connected epileptic network. [ABSTRACT FROM AUTHOR]

Although motor control has been extensively studied, most research involving neural recordings has focused on primary motor cortex, pre-motor cortex, supplementary motor area, and cerebellum. These regions are involved during normal movements, however, associative cortices and hippocampus are also likely involved during perturbed movements as one must detect the unexpected disturbance, inhibit the previous motor plan, and create a new plan to compensate. Minimal data is available on these brain regions during such "robust" movements. Here, epileptic patients implanted with intracerebral electrodes performed reaching movements while experiencing occasional unexpected force perturbations allowing study of the fronto-parietal, limbic and hippocampal network at unprecedented high spatial, and temporal scales. Areas including orbitofrontal cortex (OFC) and hippocampus showed increased activation during perturbed trials. These results, coupled with a visual novelty control task, suggest the hippocampal MTL-P300 novelty response is modality independent, and that the OFC is involved in modifying motor plans during robust movement. [ABSTRACT FROM AUTHOR]

Magnetoencephalography and stereo-electroencephalography are often necessary in the course of the non-invasive and invasive presurgical evaluation of challenging patients with medically intractable focal epilepsies. In this study, we aim to examine the significance of magnetoencephalography dipole clusters and their relationship to stereo-electroencephalography findings, area of surgical resection, and seizure outcome. We also aim to define the positive and negative predictors based on magnetoencephalography dipole cluster characteristics pertaining to seizure-freedom. Included in this retrospective study were a consecutive series of 50 patients who underwent magnetoencephalography and stereo-electroencephalography at the Cleveland Clinic Epilepsy Center. Interictal magnetoencephalography localization was performed using a single equivalent current dipole model. Magnetoencephalography dipole clusters were classified based on tightness and orientation criteria. Magnetoencephalography dipole clusters, stereo-electroencephalography findings and area of resection were reconstructed and examined in the same space using the patient's own magnetic resonance imaging scan. Seizure outcomes at 1 year postoperative were dichotomized into seizurefree or not seizure-free. We found that patients in whom the magnetoencephalography clusters were completely resected had a much higher chance of seizure-freedom compared to the partial and no resection groups (P = 0.007). Furthermore, patients had a significantly higher chance of being seizure-free when stereo-electroencephalography completely sampled the area identified by magnetoencephalography as compared to those with incomplete or no sampling of magnetoencephalography results (P = 0.012). Partial concordance between magnetoencephalography and interictal or ictal stereo-electroencephalography was associated with a much lower chance of seizure freedom as compared to the concordant group (P = 0.0075). Patients with one single tight cluster on magnetoencephalography were more likely to become seizure-free compared to patients with a tight cluster plus scatter (P = 0.0049) or patients with loose clusters (P = 0.018). Patients whose magnetoencephalography clusters had a stable orientation perpendicular to the nearest major sulcus had a better chance of seizure-freedom as compared to other orientations (P = 0.042). Our data demonstrate that stereo-electroencephalography exploration and subsequent resection are more likely to succeed, when guided by positive magnetoencephalography findings. As a corollary, magnetoencephalography clusters should not be ignored when planning the stereo-electroencephalography strategy. Magnetoencephalography tight cluster and stable orientation are positive predictors for a good seizure outcome after resective surgery, whereas the presence of scattered sources diminishes the probability of favourable outcomes. The concordance pattern between magnetoencephalography and stereo-electroencephalography is a strong argument in favour of incorporating localization with non-invasive tools into the process of presurgical evaluation before actual placement of electrodes. [ABSTRACT FROM AUTHOR]

Background: Stereotactic electroencephalography (SEEG) is an invasive diagnostic tool for localizing the epileptic zone in patients with medically refractory focal epilepsy. Despite technical and imaging advances in guiding the electrode placement, vascular injury is still one of its most serious complications. Object: To investigate the usefulness of intraoperative cerebral C-arm CT angiogram (CCTA) in avoiding intracranial hemorrhagic complications during SEEG electrode implantation. Methods: Trajectory data from 12 patients who underwent SEEG electrode implantation were studied in detail. This included an analysis of the implantation of 146 SEEG electrodes, which were guided by intraoperative CCTA, as well as the standard planning based on preoperative contrast- enhanced MRI. In addition, a prospective analysis of SEEG hemorrhagic complications using the studied methodology was performed in a total of 87 patients receiving 1,310 electrodes. Results: There was no complication related to the CCTA itself. Intraoperative CCTA entailed modification of the original trajectory based on the preoperative MRI in 27 of 146 electrode implantations (18.5%). In 10 of them, a severe vascular complication was adverted by intraoperative CCTA. The safety of this new approach was also confirmed by the analysis of postinterventional CT, which revealed a symptomatic hematoma caused by 1 single electrode out of the 1,310 implanted. Conclusions: This study showed that intraoperative CCTA in addition to preoperative MRI is useful in guiding a safer SEEG electrode implantation. The combination of both imaging modalities essentially minimizes the risk of serious hemorrhagic complications. [ABSTRACT FROM AUTHOR]