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Local and Distant Dysregulation of Synchronization Around Interictal Spikes in BECTS.

ABSTRACT: Objective: High Density electroencephalography (HD EEG) is the reference non-invasive technique to investigate the dynamics of neuronal networks in Benign Epilepsy with Centro-Temporal Spikes (BECTS). Analysis of local dynamic changes surrounding Interictal Epileptic Spikes (IES) might improve our knowledge of the mechanisms that propel neurons to the hypersynchronization of IES in BECTS. Transient distant changes in the dynamics of neurons populations may also interact with neuronal networks involved in various functions that are impaired in BECTS patients. Methods: HD EEG (64 electrodes) of eight well-characterized BECTS patients (8 males; mean age: 7.2 years, range: 5-9 years) were analyzed. Unilateral IES were selected in 6 patients. They were bilateral and independent in 2 other patients. This resulted in a total of 10 groups of IES. Time-frequency analysis was performed on HD EEG epochs around the peak of the IES (±1000 ms), including phase-locked and non-phase-locked activities to the IES. The time frequency analyses were calculated for the frequencies between 4 and 200 Hz. Results: Time-frequency analysis revealed two patterns of dysregulation of the synchronization between neuronal networks preceding and following hypersynchronization of interictal spikes (±400 ms) in the epileptogenic zone. Dysregulation consists of either desynchronization (n = 6) or oscillating synchronization (n = 4) (4-50 Hz) surrounding the IES. The 2 patients with bilateral IES exhibited only local desynchronization whatever the IES considered. Distant desynchronization in low frequencies within the same window occurs simultaneously in bilateral frontal, temporal and occipital areas (n = 7). Significance: Using time-frequency analysis of HD EEG data in a well-defined population of BECTS, we demonstrated repeated complex changes in the dynamics of neuronal networks not only during, but also, before and after the IES. In the epileptogenic zone, our results found more complex reorganization of the local network than initially thought. In line with previous results obtained at a microscopic or macroscopic level, these changes suggested the variability strategies of neuronal assemblies to raise IES. Distant changes from the epileptogenic zone in desynchronization observed in the same time window suggested interactions between larger embedded networks and opened new avenues about their possible role in the underlying mechanism leading to cognitive deficits.

SUBMITTER: Bourel-Ponchel E

PROVIDER: S-EPMC5301021 | biostudies-literature | 2017

REPOSITORIES: biostudies-literature

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Local and Distant Dysregulation of Synchronization Around Interictal Spikes in BECTS.

Bourel-Ponchel Emilie E Mahmoudzadeh Mahdi M Berquin Patrick P Wallois Fabrice F

Frontiers in neuroscience 20170210

<b>Objective:</b> High Density electroencephalography (HD EEG) is the reference non-invasive technique to investigate the dynamics of neuronal networks in Benign Epilepsy with Centro-Temporal Spikes (BECTS). Analysis of local dynamic changes surrounding Interictal Epileptic Spikes (IES) might improve our knowledge of the mechanisms that propel neurons to the hypersynchronization of IES in BECTS. Transient distant changes in the dynamics of neurons populations may also interact with neuronal netw ...[more]

PMID: 28239337

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Project description:Objective: To evaluate local and distant blood oxygen level dependent (BOLD) signal changes related to interictal epileptiform discharges (IED) in drug-resistant temporal lobe epilepsy (TLE). Methods: Thirty-three TLE patients undergoing EEG-functional Magnetic Resonance Imaging (fMRI) as part of the presurgical workup were consecutively enrolled. First, a single-subject spike-related analysis was performed: (a) to verify the BOLD concordance with the presumed Epileptogenic Zone (EZ); and (b) to investigate the Intrinsic Connectivity Networks (ICN) involvement. Then, a group analysis was performed to search for common BOLD changes in TLE. Results: Interictal epileptiform discharges were recorded in 25 patients and in 19 (58%), a BOLD response was obtained at the single-subject level. In 42% of the cases, BOLD changes were observed in the temporal lobe, although only one patient had a pure concordant finding, with a single fMRI cluster overlapping (and limited to) the EZ identified by anatomo-electro-clinical correlations. In the remaining 58% of the cases, BOLD responses were localized outside the temporal lobe and the presumed EZ. In every patient, with a spike-related fMRI map, at least one ICN appeared to be involved. Four main ICNs were preferentially involved, namely, motor, visual, auditory/motor speech, and the default mode network. At the single-subject level, EEG-fMRI proved to have high specificity (above 65%) in detecting engagement of an ICN and the corresponding ictal/postictal symptom, and good positive predictive value (above 67%) in all networks except the visual one. Finally, in the group analysis of BOLD changes related to IED revealed common activations at the right precentral gyrus, supplementary motor area, and middle cingulate gyrus. Significance: Interictal temporal spikes affect several distant extra-temporal areas, and specifically the motor/premotor cortex. EEG-fMRI in patients with TLE eligible for surgery is recommended not for strictly localizing purposes rather it might be useful to investigate ICNs alterations at the single-subject level.

Project description:The location of interictal spikes is used to aid surgical planning in patients with medically refractory epilepsy; however, their spatial and temporal dynamics are poorly understood. In this study, we analysed the spatial distribution of interictal spikes over time in 20 adult and paediatric patients (12 females, mean age = 34.5 years, range = 5-58) who underwent intracranial EEG evaluation for epilepsy surgery. Interictal spikes were detected in the 24 h surrounding each seizure and spikes were clustered based on spatial location. The temporal dynamics of spike spatial distribution were calculated for each patient and the effects of sleep and seizures on these dynamics were evaluated. Finally, spike location was assessed in relation to seizure onset location. We found that spike spatial distribution fluctuated significantly over time in 14/20 patients (with a significant aggregate effect across patients, Fisher's method: P < 0.001). A median of 12 sequential hours were required to capture 80% of the variability in spike spatial distribution. Sleep and postictal state affected the spike spatial distribution in 8/20 and 4/20 patients, respectively, with a significant aggregate effect (Fisher's method: P < 0.001 for each). There was no evidence of pre-ictal change in the spike spatial distribution for any patient or in aggregate (Fisher's method: P = 0.99). The electrode with the highest spike frequency and the electrode with the largest area of downstream spike propagation both localized the seizure onset zone better than predicted by chance (Wilcoxon signed-rank test: P = 0.005 and P = 0.002, respectively). In conclusion, spikes localize seizure onset. However, temporal fluctuations in spike spatial distribution, particularly in relation to sleep and post-ictal state, can confound localization. An adequate duration of intracranial recording-ideally at least 12 sequential hours-capturing both sleep and wakefulness should be obtained to sufficiently sample the interictal network.

Project description:In temporal lobe epilepsy (TLE), the epileptogenic focus is focal and unilateral in the majority of patients. A key characteristic of focal TLE is the presence of subclinical epileptiform activity in both the ictal and contralateral "healthy" hemisphere. Such interictal activity is clinically important, as it may reflect the spread of pathology, potentially leading to secondary epileptogenesis. The role played by white matter pathways in this process is unknown.We compared three interhemispheric white matter tracts (anterior commissure, fornix, and tapetum) to determine the pathway most associated with the presence of contralateral interictal spikes. Forty patients with unilateral left or right TLE were categorized based on the presence or absence of contralateral interictal spikes. Analyses of variance (ANOVAs) were run on diffusion properties from each tract.The analyses revealed that patients with left TLE and with bilateral interictal spikes had lower fractional anisotropy (FA) and higher mean diffusivity (MD) in the tapetum. Patients with right TLE did not show this effect. No significant associations with bilateral activity were observed for the other tracts. Blood oxygen level-dependent (BOLD) functional connectivity data revealed that homotopic lateral, not mesial, temporal areas were reliably correlated in bilateral patients, independent of ictal side.Our results indicate that, among the tracts investigated, only the tapetum was associated with contralateral epileptiform activity, implicating this structure in seizures and possible secondary epileptogenesis. We describe two mechanisms that might explain this association (the interruption of inhibitory signals or the toxic effect of carrying epileptiform signals toward the healthy hemisphere), but also acknowledge other rival factors that may be at work. We also report that patients with TLE with bilateral spikes had increased lateral bitemporal lobe connectivity. Our current results can be seen as bringing together important functional and structural data to elucidate the basis of contralateral interictal activity in focal, unilateral epilepsy. A PowerPoint slide summarizing this article is available for download in the Supporting Information section here.

Dataset Information

Local and Distant Dysregulation of Synchronization Around Interictal Spikes in BECTS.

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Local and Distant Dysregulation of Synchronization Around Interictal Spikes in BECTS.

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