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Sleep slow-wave homeostasis and cognitive functioning in children with electrical status epilepticus in sleep


van den Munckhof, Bart; Gefferie, Silvano R; van Noort, Suus A M; van Teeseling, Heleen C; Schijvens, Mischa P; Smit, William; Teunissen, Nico W; Plate, Joost D J; Huiskamp, Geert Jan M; Leijten, Frans S S; Braun, Kees P J; Jansen, Floor E; Bölsterli, Bigna K (2020). Sleep slow-wave homeostasis and cognitive functioning in children with electrical status epilepticus in sleep. Sleep, 43(11):zsaa088.

Abstract

Study objectives: Encephalopathy with electrical status epilepticus in sleep (ESES) is characterized by non-rapid eye movement (non-REM)-sleep-induced epileptiform activity and acquired cognitive deficits. The synaptic homeostasis hypothesis describes the process of daytime synaptic potentiation balanced by synaptic downscaling in non-REM-sleep and is considered crucial to retain an efficient cortical network. We aimed to study the overnight decline of slow waves, an indirect marker of synaptic downscaling, in patients with ESES and explore whether altered downscaling relates to neurodevelopmental and behavioral problems.
Methods: Retrospective study of patients with ESES with at least one whole-night electroencephalogram (EEG) and neuropsychological assessment (NPA) within 4 months. Slow waves in the first and last hour of non-REM-sleep were analyzed. Differences in slow-wave slope (SWS) and overnight slope course between the epileptic focus and non-focus electrodes and relations to neurodevelopment and behavior were analyzed.
Results: A total of 29 patients with 44 EEG ~ NPA combinations were included. Mean SWS decreased from 357 to 327 µV/s (-8%, p < 0.001) across the night and the overnight decrease was less pronounced in epileptic focus than in non-focus electrodes (-5.6% vs. -8.7%, p = 0.003). We found no relation between SWS and neurodevelopmental test results in cross-sectional and longitudinal analyses. Patients with behavioral problems showed less SWS decline than patients without and the difference was most striking in the epileptic focus (-0.9% vs. -8.8%, p = 0.006).
Conclusions: Slow-wave homeostasis-a marker of synaptic homeostasis-is disturbed by epileptiform activity in ESES. Behavioral problems, but not neurodevelopmental test results, were related to severity of this disturbance.

Abstract

Study objectives: Encephalopathy with electrical status epilepticus in sleep (ESES) is characterized by non-rapid eye movement (non-REM)-sleep-induced epileptiform activity and acquired cognitive deficits. The synaptic homeostasis hypothesis describes the process of daytime synaptic potentiation balanced by synaptic downscaling in non-REM-sleep and is considered crucial to retain an efficient cortical network. We aimed to study the overnight decline of slow waves, an indirect marker of synaptic downscaling, in patients with ESES and explore whether altered downscaling relates to neurodevelopmental and behavioral problems.
Methods: Retrospective study of patients with ESES with at least one whole-night electroencephalogram (EEG) and neuropsychological assessment (NPA) within 4 months. Slow waves in the first and last hour of non-REM-sleep were analyzed. Differences in slow-wave slope (SWS) and overnight slope course between the epileptic focus and non-focus electrodes and relations to neurodevelopment and behavior were analyzed.
Results: A total of 29 patients with 44 EEG ~ NPA combinations were included. Mean SWS decreased from 357 to 327 µV/s (-8%, p < 0.001) across the night and the overnight decrease was less pronounced in epileptic focus than in non-focus electrodes (-5.6% vs. -8.7%, p = 0.003). We found no relation between SWS and neurodevelopmental test results in cross-sectional and longitudinal analyses. Patients with behavioral problems showed less SWS decline than patients without and the difference was most striking in the epileptic focus (-0.9% vs. -8.8%, p = 0.006).
Conclusions: Slow-wave homeostasis-a marker of synaptic homeostasis-is disturbed by epileptiform activity in ESES. Behavioral problems, but not neurodevelopmental test results, were related to severity of this disturbance.

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Additional indexing

Item Type:Journal Article, refereed, original work
Communities & Collections:04 Faculty of Medicine > University Children's Hospital Zurich > Medical Clinic
Dewey Decimal Classification:610 Medicine & health
Scopus Subject Areas:Health Sciences > Neurology (clinical)
Health Sciences > Physiology (medical)
Uncontrolled Keywords:Physiology (medical), Clinical Neurology, CSWS; ESES; cognition; sleep; slow waves; synaptic downscaling.
Language:English
Date:12 November 2020
Deposited On:18 Dec 2020 15:23
Last Modified:19 Dec 2020 21:02
Publisher:American Academy of Sleep Medicine
ISSN:0161-8105
OA Status:Hybrid
Free access at:Publisher DOI. An embargo period may apply.
Publisher DOI:https://doi.org/10.1093/sleep/zsaa088
PubMed ID:32374855

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