Disruption of learning and long-term retention of prose passages in patients with focal epilepsy

Ricci, Monica; Mohamed, Armin; Savage, Greg; Miller, Laurie A.

doi:10.1016/j.yebeh.2015.06.016

Cited by 20 publications

(20 citation statements)

References 33 publications

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“…Overnight retention of a story was significantly worse for patients with TLE compared with patients with ETE, which is consistent with previous findings [32,39]. However, dividing patients by site of epileptic focus did not reveal significant differences on any of the other three memory variables, nor did it have an influence on %SWS or REM latency.…”

Section: Discussionsupporting

confidence: 90%

“…Overnight retention of visuospatial information was similar between patients with or without hippocampal lesions whereas retention of verbal and autobiographical memory was worse for patients with hippocampal lesions. These findings suggest that overnight consolidation of visuospatial information is less reliant on the hippocampus compared with the retention of verbal information [39,59]. Indeed, it has been suggested that performance on the RCFT is a poor marker for temporal lobe functioning [60].…”

Section: Discussionmentioning

confidence: 94%

“…The Story Memory Task (SMT) has been described by Ricci and colleagues [39] and was one of the 17 tasks involved in the neuropsychological testing session used to measure AE. A story with 24 elements was read to the patient by the examiner, after which, immediate recall was tested.…”

Section: Verbal Memoryovernight Retentionmentioning

confidence: 99%

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The impact of sleep characteristics and epilepsy variables on memory performance in patients with focal seizures

Schalkwijk

Ricci

Nikpour

et al. 2018

Epilepsy & Behavior

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Disturbed sleep can negatively affect overnight memory retention as well as new learning the subsequent day. In healthy participants, positive associations between memory performance and sleep characteristics (e.g., time spent in slow-wave sleep [SWS]) have been detected. In a previous study, we found that SWS was much reduced in patients with focal seizures, but when correlations between memory complaints and various sleep characteristics were considered, the only significant relationship was with the time to onset of rapid eye movement (REM) sleep (i.e., REM latency). In this study, we investigated the relationships between sleep, epilepsy, and objective memory performance variables. Twenty-five patients with focal seizures had their memory tested while undergoing a two-day ambulatory electroencephalography (EEG). The sleep variables of interest were the percentage of time spent in SWS (%SWS) and REM latency. Epilepsy variables included the presence of (1) seizures, (2) interictal epileptiform discharges, and/or (3) hippocampal lesions as well as site of seizure origin (temporal vs extratemporal). Overnight retention (of autobiographical events, a story, and a complex geometric figure) and the ability to learn a word list on day 2 were the measures of memory. A significant positive correlation was found between word-list learning and %SWS during the previous night. A significant negative correlation was observed between REM latency and overnight retention of autobiographical events. Overnight retention scores for the story and geometric figure were not related to sleep characteristics but were negatively affected by the presence of epileptiform activity. Story retention was also worse for temporal lobe epilepsy (TLE) than for patients with extratemporal epilepsy (ETE). Those with hippocampal lesions were more impaired than those without lesions on word-list learning, autobiographical events' retention, and story retention. When multiple contributing factors were entered into regression analyses, %SWS was found to be the best predictor of subsequent word-list learning, whereas the presence of a hippocampal lesion was the best predictor of overnight retention of autobiographical events and a story. These findings provide further evidence of the ways in which particular sleep characteristics are associated with memory and suggest that treatment of sleep disturbances in patients with epilepsy might be helpful for improving their performance.

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Section: Discussionsupporting

confidence: 90%

Section: Discussionmentioning

confidence: 94%

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The impact of sleep characteristics and epilepsy variables on memory performance in patients with focal seizures

Schalkwijk

Ricci

Nikpour

et al. 2018

Epilepsy & Behavior

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“…Beyond early consolidation, there is increasing interest in the late consolidation of memory or, alternatively, the accelerated forgetting of the information (Baker and Zeman 2017). Accelerated long-term forgetting or ALF is defined as excessive loss of information with longer time intervals, which may be hours or weeks, given unimpaired memory acquisition and early consolidation during the first hour (Elliott et al 2014;Helmstaedter et al 2018;Ricci et al 2015). Some authors have also used the term to indicate loss of information over time in subjects who already showed deficits in the acquisition and early consolidation and defined ALF as loss of the acquired information, greater than seen in control subjects (Helmstaedter et al 2018).…”

Section: Introductionmentioning

confidence: 99%

Story Learning Test: Decelerated Learning and Accelerated Forgetting in Children with Epilepsy

Iterson

2019

J Pediatr Neuropsychol

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Introduction Increasing interest is seen for early and late memory consolidation and accelerated forgetting, but little is known about these phenomena in children with epilepsy. The present study analysed the trajectory of learning and retention in typically developing children and children with epilepsy on a story learning test. Methods 285 children, 126 typically developing children and 159 children with epilepsy, in ages between 4 and 10 years and Full-Scale IQs ≥ 75, were given a specifically designed story learning test (iter-SEIN). The learning phase included Initial reading and a Free Recall trial with 10 Questions, and up to three repetition trials with Questions. Trials of Delayed Free Recall and Questions followed after half an hour, the next day and 1 week later. With several repeated measures analyses of variance, level of performance and gains or losses over time were analysed. Results Age-dependent learning was seen after repetitions. On the Questions, typically developing children outperformed children with epilepsy increasingly, due to smaller gains after the second trial. Learned information was similarly preserved. Free Recall showed similar performance for both groups up to day 2. A week later, a conspicuous loss of information was observed in the children with epilepsy, whilst typically developing children retained the information. On index scores, reliable cognitive loss of information was seen in epilepsy in 24.5% of the children. Semantic neuropsychological tasks and severity measures of epilepsy were associated with level of performance. Discussion The results provided evidence for early decelerated learning and late accelerated forgetting in children with epilepsy.

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“…There is some evidence to suggest that epileptic activity following learning is associated with poor memory retention in people with epilepsy (Fitzgerald et al., 2013, Jokeit et al., 2001, Mameniskiene et al., 2006, Ricci et al., 2015b, Ricci et al., 2015a, Wilkinson et al., 2012). Interictal and ictal epileptiform discharges are enhanced during SWS, compared to wakefulness and REM sleep (Bazil, 2000, Bazil and Walczak, 1997, Goncharova et al., 2009, Kotagal, 2001, Mayanagi, 1977, Nazer and Dickson, 2009, Romcy-Pereira et al., 2009, Rossi et al., 1984, Sammaritano et al., 1991), and could potentially interfere with the SWS-associated brain activity patterns that facilitate memory retention in healthy people (Galer et al., 2015, Shatskikh et al., 2006, Tassinari et al., 2009, Urbain et al., 2011, Verrotti et al., 2014).…”

Section: Introductionmentioning

confidence: 99%

Slow wave sleep and accelerated forgetting

Atherton

Nobre

Lázár

et al. 2016

Cortex

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We investigated whether the benefit of slow wave sleep (SWS) for memory consolidation typically observed in healthy individuals is disrupted in people with accelerated long-term forgetting (ALF) due to epilepsy. SWS is thought to play an active role in declarative memory in healthy individuals and, furthermore, electrographic epileptiform activity is often more prevalent during SWS than during wakefulness or other sleep stages. We studied the relationship between SWS and the benefit of sleep for memory retention using a word-pair associates task. In both the ALF and the healthy control groups, sleep conferred a memory benefit. However, the relationship between the amount of SWS and sleep-related memory benefits differed significantly between the groups. In healthy participants, the amount of SWS correlated positively with sleep-related memory benefits. In stark contrast, the more SWS, the smaller the sleep-related memory benefit in the ALF group. Therefore, contrary to its role in healthy people, SWS-associated brain activity appears to be deleterious for memory in patients with ALF.

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Disruption of learning and long-term retention of prose passages in patients with focal epilepsy

Cited by 20 publications

References 33 publications

The impact of sleep characteristics and epilepsy variables on memory performance in patients with focal seizures

The impact of sleep characteristics and epilepsy variables on memory performance in patients with focal seizures

Story Learning Test: Decelerated Learning and Accelerated Forgetting in Children with Epilepsy

Slow wave sleep and accelerated forgetting

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