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Interictal Epileptiform Discharges and the Quality of Human Intracranial Neurophysiology Data.

ABSTRACT: Intracranial electroencephalography (IEEG) involves recording from electrodes placed directly onto the cortical surface or deep brain locations. It is performed on patients with medically refractory epilepsy, undergoing pre-surgical seizure localization. IEEG recordings, combined with advancements in computational capacity and analysis tools, have accelerated cognitive neuroscience. This Perspective describes a potential pitfall latent in many of these recordings by virtue of the subject population-namely interictal epileptiform discharges (IEDs), which can cause spurious results due to the contamination of normal neurophysiological signals by pathological waveforms related to epilepsy. We first discuss the nature of IED hazards, and why they deserve the attention of neurophysiology researchers. We then describe four general strategies used when handling IEDs (manual identification, automated identification, manual-automated hybrids, and ignoring by leaving them in the data), and discuss their pros, cons, and contextual factors. Finally, we describe current practices of human neurophysiology researchers worldwide based on a cross-sectional literature review and a voluntary survey. We put these results in the context of the listed strategies and make suggestions on improving awareness and clarity of reporting to enrich both data quality and communication in the field.

SUBMITTER: Ammanuel SG

PROVIDER: S-EPMC7062638 | biostudies-literature | 2020

REPOSITORIES: biostudies-literature

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Interictal Epileptiform Discharges and the Quality of Human Intracranial Neurophysiology Data.

Ammanuel Simon G SG Kleen Jonathan K JK Leonard Matthew K MK Chang Edward F EF

Frontiers in human neuroscience 20200303

Intracranial electroencephalography (IEEG) involves recording from electrodes placed directly onto the cortical surface or deep brain locations. It is performed on patients with medically refractory epilepsy, undergoing pre-surgical seizure localization. IEEG recordings, combined with advancements in computational capacity and analysis tools, have accelerated cognitive neuroscience. This Perspective describes a potential pitfall latent in many of these recordings by virtue of the subject populat ...[more]

PMID: 32194384

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Project description:ObjectiveThis study was undertaken to evaluate the influence that subject-specific factors have on intracranial interictal epileptiform discharge (IED) rates in persons with refractory epilepsy.MethodsOne hundred fifty subjects with intracranial electrodes performed multiple sessions of a free recall memory task; this standardized task controlled for subject attention levels. We utilized a dominance analysis to rank the importance of subject-specific factors based on their relative influence on IED rates. Linear mixed-effects models were employed to comprehensively examine factors with highly ranked importance.ResultsAntiseizure medication (ASM) status, time of testing, and seizure onset zone (SOZ) location were the highest-ranking factors in terms of their impact on IED rates. The average IED rate of electrodes in SOZs was 34% higher than the average IED rate of electrodes outside of SOZs (non-SOZ; p < .001). However, non-SOZ electrodes had similar IED rates regardless of the subject's SOZ location (p = .99). Subjects on older generation (p < .001) and combined generation (p < .001) ASM regimens had significantly lower IED rates relative to the group taking no ASMs; newer generation ASM regimens demonstrated a nonsignificant association with IED rates (p = .13). Of the ASMs included in this study, the following ASMs were associated with significant reductions in IED rates: levetiracetam (p < .001), carbamazepine (p < .001), lacosamide (p = .03), zonisamide (p = .01), lamotrigine (p = .03), phenytoin (p = .03), and topiramate (p = .01). We observed a nonsignificant association between time of testing and IED rates (morning-afternoon p = .15, morning-evening p = .85, afternoon-evening p = .26).SignificanceThe current study ranks the relative influence that subject-specific factors have on IED rates and highlights the importance of considering certain factors, such as SOZ location and ASM status, when analyzing IEDs for clinical or research purposes.

Project description:Epileptic cortex is characterized by paroxysmal electrical discharges. Analysis of these interictal discharges typically manifests as spike-wave complexes on electroencephalography, and plays a critical role in diagnosing and treating epilepsy. Despite their fundamental importance, little is known about the neurophysiological mechanisms generating these events in human focal epilepsy. Using three different systems of microelectrodes, we recorded local field potentials and single-unit action potentials during interictal discharges in patients with medically intractable focal epilepsy undergoing diagnostic workup for localization of seizure foci. We studied 336 single units in 20 patients. Ten different cortical areas and the hippocampus, including regions both inside and outside the seizure focus, were sampled. In three of these patients, high density microelectrode arrays simultaneously recorded between 43 and 166 single units from a small (4 mm x 4 mm) patch of cortex. We examined how the firing rates of individual neurons changed during interictal discharges by determining whether the firing rate during the event was the same, above or below a median baseline firing rate estimated from interictal discharge-free periods (Kruskal-Wallis one-way analysis, P<0.05). Only 48% of the recorded units showed such a modulation in firing rate within 500 ms of the discharge. Units modulated during the discharge exhibited significantly higher baseline firing and bursting rates than unmodulated units. As expected, many units (27% of the modulated population) showed an increase in firing rate during the fast segment of the discharge (+ or - 35 ms from the peak of the discharge), while 50% showed a decrease during the slow wave. Notably, in direct contrast to predictions based on models of a pure paroxysmal depolarizing shift, 7.7% of modulated units recorded in or near the seizure focus showed a decrease in activity well ahead (0-300 ms) of the discharge onset, while 12.2% of units increased in activity in this period. No such pre-discharge changes were seen in regions well outside the seizure focus. In many recordings there was also a decrease in broadband field potential activity during this same pre-discharge period. The different patterns of interictal discharge-modulated firing were classified into more than 15 different categories. This heterogeneity in single unit activity was present within small cortical regions as well as inside and outside the seizure onset zone, suggesting that interictal epileptiform activity in patients with epilepsy is not a simple paroxysm of hypersynchronous excitatory activity, but rather represents an interplay of multiple distinct neuronal types within complex neuronal networks.

Project description:Importance:The validity of using electroencephalograms (EEGs) to diagnose epilepsy requires reliable detection of interictal epileptiform discharges (IEDs). Prior interrater reliability (IRR) studies are limited by small samples and selection bias. Objective:To assess the reliability of experts in detecting IEDs in routine EEGs. Design, Setting, and Participants:This prospective analysis conducted in 2 phases included as participants physicians with at least 1 year of subspecialty training in clinical neurophysiology. In phase 1, 9 experts independently identified candidate IEDs in 991 EEGs (1 expert per EEG) reported in the medical record to contain at least 1 IED, yielding 87?636 candidate IEDs. In phase 2, the candidate IEDs were clustered into groups with distinct morphological features, yielding 12?602 clusters, and a representative candidate IED was selected from each cluster. We added 660 waveforms (11 random samples each from 60 randomly selected EEGs reported as being free of IEDs) as negative controls. Eight experts independently scored all 13?262 candidates as IEDs or non-IEDs. The 1051 EEGs in the study were recorded at the Massachusetts General Hospital between 2012 and 2016. Main Outcomes and Measures:Primary outcome measures were percentage of agreement (PA) and beyond-chance agreement (Gwet ?) for individual IEDs (IED-wise IRR) and for whether an EEG contained any IEDs (EEG-wise IRR). Secondary outcomes were the correlations between numbers of IEDs marked by experts across cases, calibration of expert scoring to group consensus, and receiver operating characteristic analysis of how well multivariate logistic regression models may account for differences in the IED scoring behavior between experts. Results:Among the 1051 EEGs assessed in the study, 540 (51.4%) were those of females and 511 (48.6%) were those of males. In phase 1, 9 experts each marked potential IEDs in a median of 65 (interquartile range [IQR], 28-332) EEGs. The total number of IED candidates marked was 87?636. Expert IRR for the 13?262 individually annotated IED candidates was fair, with the mean PA being 72.4% (95% CI, 67.0%-77.8%) and mean ? being 48.7% (95% CI, 37.3%-60.1%). The EEG-wise IRR was substantial, with the mean PA being 80.9% (95% CI, 76.2%-85.7%) and mean ? being 69.4% (95% CI, 60.3%-78.5%). A statistical model based on waveform morphological features, when provided with individualized thresholds, explained the median binary scores of all experts with a high degree of accuracy of 80% (range, 73%-88%). Conclusions and Relevance:This study's findings suggest that experts can identify whether EEGs contain IEDs with substantial reliability. Lower reliability regarding individual IEDs may be largely explained by various experts applying different thresholds to a common underlying statistical model.

Dataset Information

Interictal Epileptiform Discharges and the Quality of Human Intracranial Neurophysiology Data.

Publications

Interictal Epileptiform Discharges and the Quality of Human Intracranial Neurophysiology Data.

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