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Interictal epileptiform discharges impair word recall in multiple brain areas.

ABSTRACT: Interictal epileptiform discharges (IEDs) have been linked to memory impairment, but the spatial and temporal dynamics of this relationship remain elusive. In the present study, we aim to systematically characterize the brain areas and times at which IEDs affect memory.Eighty epilepsy patients participated in a delayed free recall task while undergoing intracranial electroencephalography (EEG) monitoring. We analyzed the locations and timing of IEDs relative to the behavioral data in order to measure their effects on memory.Overall IED rates did not correlate with task performance across subjects (r = 0.03, p = 0.8). However, at a finer temporal scale, within-subject memory was negatively affected by IEDs during the encoding and recall periods of the task but not during the rest and distractor periods (p < 0.01, p < 0.001, p = 0.3, and p = 0.8, respectively). The effects of IEDs during encoding and recall were stronger in the left hemisphere than in the right (p < 0.05). Of six brain areas analyzed, IEDs in the inferior-temporal, medial-temporal, and parietal areas significantly affected memory (false discovery rate < 0.05).These findings reveal a network of brain areas sensitive to IEDs with key nodes in temporal as well as parietal lobes. They also demonstrate the time-dependent effects of IEDs in this network on memory.

SUBMITTER: Horak PC

PROVIDER: S-EPMC5339047 | biostudies-literature | 2017 Mar

REPOSITORIES: biostudies-literature

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Interictal epileptiform discharges impair word recall in multiple brain areas.

Horak Peter C PC Meisenhelter Stephen S Song Yinchen Y Testorf Markus E ME Kahana Michael J MJ Viles Weston D WD Bujarski Krzysztof A KA Connolly Andrew C AC Robbins Ashlee A AA Sperling Michael R MR Sharan Ashwini D AD Worrell Gregory A GA Miller Laura R LR Gross Robert E RE Davis Kathryn A KA Roberts David W DW Lega Bradley B Sheth Sameer A SA Zaghloul Kareem A KA Stein Joel M JM Das Sandhitsu R SR Rizzuto Daniel S DS Jobst Barbara C BC

Epilepsia 20161209 3

<h4>Objectives</h4>Interictal epileptiform discharges (IEDs) have been linked to memory impairment, but the spatial and temporal dynamics of this relationship remain elusive. In the present study, we aim to systematically characterize the brain areas and times at which IEDs affect memory.<h4>Methods</h4>Eighty epilepsy patients participated in a delayed free recall task while undergoing intracranial electroencephalography (EEG) monitoring. We analyzed the locations and timing of IEDs relative to ...[more]

PMID: 27935031

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Project description:The effects of interictal epileptiform discharges on neurocognitive development in children with medically-intractable epilepsy are poorly understood. Such discharges may have a deleterious effect on the brain's intrinsic connectivity networks, which reflect the organization of functional networks at rest, and in turn on neurocognitive development. Using a combined functional magnetic resonance imaging-magnetoencephalography approach, we examine the effects of interictal epileptiform discharges on intrinsic connectivity networks and neurocognitive outcome. Functional magnetic resonance imaging was used to determine the location of regions comprising various intrinsic connectivity networks in 26 children (7-17 years), and magnetoencephalography data were reconstructed from these locations. Inter-regional phase synchronization was then calculated across interictal epileptiform discharges and graph theoretical analysis was applied to measure event-related changes in network topology in the peri-discharge period. The magnitude of change in network topology (network resilience/vulnerability) to interictal epileptiform discharges was associated with neurocognitive outcomes and functional magnetic resonance imaging networks using dual regression. Three main findings are reported: (i) large-scale network changes precede and follow interictal epileptiform discharges; (ii) the resilience of network topologies to interictal discharges is associated with stronger resting-state network connectivity; and (iii) vulnerability to interictal discharges is associated with worse neurocognitive outcomes. By combining the spatial resolution of functional magnetic resonance imaging with the temporal resolution of magnetoencephalography, we describe the effects of interictal epileptiform discharges on neurophysiological synchrony in intrinsic connectivity networks and establish the impact of interictal disruption of functional networks on cognitive outcome in children with epilepsy. The association between interictal discharges, network changes and neurocognitive outcomes suggests that it is of clinical importance to suppress discharges to foster more typical brain network development in children with focal epilepsy.

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: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 impair word recall in multiple brain areas.

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Interictal epileptiform discharges impair word recall in multiple brain areas.

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