Hippocampal Interictal Spikes during Sleep Impact Long‐Term Memory Consolidation

Abstract

Objective: Non-rapid eye movement (NREM) sleep is supposed to play a key role in long-term memory consolidation transferring information from hippocampus to neocortex. However, sleep also activates epileptic activities in medial temporal regions. This study investigated whether interictal hippocampal spikes during sleep would impair long-term memory consolidation. Method: We prospectively measured visual and verbal memory performance in 20 patients with epilepsy investigated with stereoelectroencephalography (SEEG) at immediate, 30-minute, and 1-week delays, and studied the correlations between interictal hippocampal spike frequency during waking and the first cycle of NREM sleep and memory performance, taking into account the number of seizures occurring during the consolidation period and other possible confounding factors, such as age and epilepsy duration. Results: Retention of verbal memory over 1 week was negatively correlated with hippocampal spike frequency during sleep, whereas no significant correlation was found with hippocampal interictal spikes during waking. No significant result was found for visual memory. Regression tree analysis showed that the number of seizures was the first factor that impaired the verbal memory retention between 30 minutes and 1 week. When the number of seizures was below 5, spike frequency during sleep higher than 13 minutes was associated with impaired memory retention over 1 week. Interpretation: Our results show that activation of interictal spikes in the hippocampus during sleep and seizures specifically impair long-term memory consolidation. We hypothesize that hippocampal interictal spikes during sleep interrupt hippocampal-neocortical transfer of information.

Cognitive and Emotional Mapping With SEEG

“…The use of memory paradigms combined with properly designed electrophysiological study (e.g., CCEPs, single unit recordings) could powerfully increase our knowledge of this critical brain function. Recent work with human and non-human primates, for example, is exploring the relationship between the electrophysiology of sleep (e.g., occurrence of sleep spindles) to memory consolidation processes (200)(201)(202). Of note, standard clinical neuropsychological batteries only assess patients after time spans under 1 h and never assess patients after periods of sleep (203).…”

Association of Accelerated Long-term Forgetting and Senescence-related Blood-borne Factors in Asymptomatic Individuals From Families With Autosomal Dominant Alzheimer’s Disease

“…Therefore, it is currently believed that impaired memory consolidation caused by Hippocampal dysfunction might produce accelerated long-term forgetting. For example, a recent study has shown that both seizures and interictal spikes in hippocampus during sleep impair long-term memory consolidation, supporting the notion that hippocampal dysfunction causes accelerated long-term forgetting [26] .…”

Altered Sleep-Related Consolidation and Neurocognitive Comorbidity in CECTS

“…IES in CECTS, due to their centrotemporal location and NREM occurrence, may perturb one or more of the oscillations within the hippocampal area as well as their neuronal coupling potentially leading to neurocognitive deficits. This is partially supported by the fact that in adults, hippocampal interictal spikes in NREM sleep negatively correlate with memory consolidation performance (Lambert et al, 2020).…”