Sleep-dependent memory consolidation in children with self-limited focal epilepsies

Abstract

ObjectiveChildren with self-limited focal epilepsies of childhood (SLFE) are known to show impaired memory functions, particularly in the verbal domain. Interictal epileptiform discharges (IED) in these epilepsies are more pronounced in nonrapid eye movement (NREM) sleep. Nonrapid eye movement sleep is crucial for consolidation of newly-encoded memories. Therefore, we hypothesize that sleep-dependent memory consolidation is altered in relation to IED in children with SLFE. Methods: We conducted a prospective case-control study. We applied a verbal (word pair) and a visuospatial (two-dimensional [2D] object location) learning task, both previously shown to benefit from sleep in terms of memory consolidation. Learning took place in the evening, and retrieval was tested in the morning after a night of sleep. Electroencephalogram (EEG) was recorded across night. After sleep-stage scoring, the spike-wave index (SWI) was assessed at the beginning and the end of sleep. Fourteen patients with SLFE (age: 5.5 to 11.6 years) were compared with 15 healthy controls (age: 6.8 to 9.1 years) examined in a previous study. Results: In contrast to healthy controls (mean: +12.9% recalled word pairs, p = .003, standard deviation (SD) = 12.4%), patients did not show overnight performance gains in the verbal memory task (mean: +6.4% recalled word pairs, p > .05, SD = 17.3) Neither patients nor controls showed significant overnight changes in visuospatial task performance. Spike-wave index was negatively correlated with recall performance in the verbal but not in the visuospatial task. Significance: We found evidence for impaired overnight improvement of performance in children with SLFE in a verbal learning task, with high SWI rates predicting low recall performance. We speculate that spike-waves hamper long-term memory consolidation by interfering with NREM sleep.

Altered Sleep-Related Consolidation and Neurocognitive Comorbidity in CECTS

“…Hippocampus-dependent memory is traditionally studied using declarative memory tasks including verbal and visuospatial tasks (non-verbal). Initial findings suggest that SRC is altered in CECTS ( Urbain et al, 2011 ; Galer et al, 2015 ; Storz et al, 2020 ) meaning that language and visuospatial deficits could be partially explained on the basis of long-term problematic consolidation of this type of material. Indeed, a measure that involved IES in NREM sleep was associated with poorer performance on a visuospatial task in IFE subjects ( Galer et al, 2015 ).…”

“…It has been suggested that IES may interfere with the neurophysiological consolidation processes subserving learning. This hypothesis is strengthened by associations between behavioral and cognitive deficits and IES severity at the acute epileptic phase ( Storz et al, 2020 ). It is also supported by a pilot study documenting that an IES-free EEG signal tends to revert the cognitive deficits ( Urbain et al, 2011 ).…”

6-year course of sleep homeostasis in a case with epilepsy-aphasia spectrum disorder

“…SLECTS. However there exists some studies reporting a relation between SWI and impaired memory consolidation in these patients [33] , [34] .…”