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

Abstract

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.

Slow wave sleep and accelerated forgetting

“…Another possibility is that the positive effects of reactivation-mediated consolidation are disrupted. The normal temporal synchronisation between hippocampal activity, spindles and/or neocortical slow waves could be disturbed (Clemens et al., 2007, Holler and Trinka, 2015). Neocortical slow waves might also trigger chaotic hippocampal activity (Holler & Trinka, 2015), which could even reflect the pattern of prior epileptiform activity (Bower et al., 2015), rather than faithful memory reactivations.…”

“…The normal temporal synchronisation between hippocampal activity, spindles and/or neocortical slow waves could be disturbed (Clemens et al., 2007, Holler and Trinka, 2015). Neocortical slow waves might also trigger chaotic hippocampal activity (Holler & Trinka, 2015), which could even reflect the pattern of prior epileptiform activity (Bower et al., 2015), rather than faithful memory reactivations. Finally, it may be that the SWS-associated brain activity patterns are entirely normal but that the memory reactivations exert a negative, rather than positive, effect on memory in this patient group.…”

Slow Activity in Focal Epilepsy During Sleep and Wakefulness

“…31 A further cue in favor of this speculation is that the stronger, selective, and asymmetric slow activity increase was observed during the first sleep cycles, when there is the closest link between delta activity and synaptic plasticity. [32][33][34] To be confirmed, this speculation would and for hemisphere (ie, averaging over electrodes and cycles of each hemisphere), data measure unit 10*log(µV 2 /Hz). (Panel B) Scalp distribution of PSD differences between epilepsy and control groups (epileptic -control, showed as percentage difference with respect to control) by Cycle (columns), Frequency band (rows).…”

Changes in cross-frequency coupling following closed-loop auditory stimulation in non-rapid eye movement sleep

“…Our data suggest that closed-loop auditory stimulation might provide a minimally invasive way to modulate the relationships between the main sleep rhythms in a target region while not (Chan et al, 2017;Ferrarelli, 2015) or epilepsy (Höller and Trinka, 2015).…”