Impaired sleep-related consolidation of declarative memories in idiopathic focal epilepsies of childhood

Galer, Sophie; Urbain, Charline; Tiège, Xavier De; Emeriau, Mathilde; Leproult, Rachel; Deliens, Gaétane; Nonclerq, Antoine; Peigneux, Philippe; Bogaert, Patrick Van

doi:10.1016/j.yebeh.2014.11.032

Cited by 41 publications

(45 citation statements)

References 38 publications

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“…Improving the sleep EEG by hydrocortisone treatment also normalized overnight memory performance. A similar lack of consolidation during sleep was reported in children with idiopathic focal epilepsies with frequent interictal epileptiform discharges (Gaier et al, 2015). Similarly, Sud et al (2014) reported that children with epilepsy did not benefit more from sleep than from wakefulness for memory consolidation.…”

Section: Slow Waves During Sleep Seizures and Memory Problemssupporting

confidence: 80%

Is There a Relation between EEG-Slow Waves and Memory Dysfunction in Epilepsy? A Critical Appraisal

Höller

Trinka

2015

Front. Hum. Neurosci.

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Is there a relationship between peri-ictal slow waves, loss of consciousness, memory, and slow-wave sleep, in patients with different forms of epilepsy? We hypothesize that mechanisms, which result in peri-ictal slow-wave activity as detected by the electroencephalogram, could negatively affect memory processes. Slow waves (≤4 Hz) can be found in seizures with impairment of consciousness and also occur in focal seizures without impairment of consciousness but with inhibited access to memory functions. Peri-ictal slow waves are regarded as dysfunctional and are probably caused by mechanisms, which are essential to disturb the consolidation of memory entries in these patients. This is in strong contrast to physiological slow-wave activity during deep sleep, which is thought to group memory-consolidating fast oscillatory activity. In patients with epilepsy, slow waves may not only correlate with the peri-ictal clouding of consciousness, but could be the epiphenomenon of mechanisms, which interfere with normal brain function in a wider range. These mechanisms may have transient impacts on memory, such as temporary inhibition of memory systems, altered patterns of hippocampal–neocortical interactions during slow-wave sleep, or disturbed cross-frequency coupling of slow and fast oscillations. In addition, repeated tonic–clonic seizures over the years in uncontrolled chronic epilepsy may cause a progressive cognitive decline. This hypothesis can only be assessed in long-term prospective studies. These studies could disentangle the reversible short-term impacts of seizures, and the impacts of chronic uncontrolled seizures. Chronic uncontrolled seizures lead to irreversible memory impairment. By contrast, short-term impacts do not necessarily lead to a progressive cognitive decline but result in significantly impaired peri-ictal memory performance.

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Section: Slow Waves During Sleep Seizures and Memory Problemssupporting

confidence: 80%

Is There a Relation between EEG-Slow Waves and Memory Dysfunction in Epilepsy? A Critical Appraisal

Höller

Trinka

2015

Front. Hum. Neurosci.

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“…EEG focal spikes temporally and regionally correlate with transient cognitive impairment [21], and are associated in RE probands with attentional impairment [32] and might disrupt overnight memory consolidation [27]. Although this present study was limited to the subset of the sibling dataset that were in the appropriate age range to demonstrate focal sharp waves on their EEG, and were also able to travel to an EEG center (83/159), we found no evidence of association between focal sharp waves and RD among siblings.…”

Section: Discussionmentioning

confidence: 99%

Risk factors for reading disability in families with rolandic epilepsy

Vega

Smith

Cockerill

et al. 2015

Epilepsy & Behavior

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OBJECTIVE The high prevalence and impact of neurodevelopmental comorbidities in childhood epilepsy are now well known, as are the increased risks and familial aggregation of reading disability (RD) and speech sound disorder (SSD) in rolandic epilepsy (RE). The risk factors for RD in the general population include male sex, SSD and ADHD but it is not known if these are the same in RE or whether there is a contributory role of seizure and treatment related variables. METHODS An observational study of 108 RE probands (age range 3.6–22 years) and their 159 siblings (age range 1–29 years; 83 with EEG data) singly ascertained in the US or UK through an affected RE proband. We used a nested case-control design, multiple logistic regression and generalized estimating equations to test the hypothesis of association between RD and seizure variables or antiepileptic drug treatment in RE; we also assessed an association between EEG focal sharp waves and RD in siblings. RESULTS RD was reported in 42% of probands and 22% of siblings. Among probands, RD was strongly associated with a history of SSD (OR 9.64, 95% CI: 2.45–37.21), ADHD symptoms (OR 10.31, 95% CI: 2.15–49.44), and male sex (OR 3.62, 95% CI: 1.11–11.75), but not with seizure or treatment variables. Among siblings, RD was independently associated only with SSD (OR 4.30, 95%CI: 1.42–13.0) and not with the presence of interictal EEG focal sharp waves. SIGNIFICANCE The principal risk factors for RD in RE are SSD, ADHD and male sex, the same risk factors as for RD without epilepsy. Seizure or treatment variables do not appear to be important risk factors for RD in RE probands, and there was no evidence to support interictal EEG focal sharp waves as a risk factor for RD in siblings. Future studies should focus on the precise neuropsychological characterisation of RD in RE families, and on the effectiveness of standard oral-language and reading interventions.

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“…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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Impaired sleep-related consolidation of declarative memories in idiopathic focal epilepsies of childhood

Cited by 41 publications

References 38 publications

Is There a Relation between EEG-Slow Waves and Memory Dysfunction in Epilepsy? A Critical Appraisal

Is There a Relation between EEG-Slow Waves and Memory Dysfunction in Epilepsy? A Critical Appraisal

Risk factors for reading disability in families with rolandic epilepsy

Slow wave sleep and accelerated forgetting

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