Prolongation of cortical sleep spindles during hippocampal interictal epileptiform discharges in epilepsy patients
Epilepsia, 2022;
https://doi.org/10.1111/epi.17337
Anna Sákovics1, 2, Gábor Csukly3, Csaba Borbély1, Márta Virág1, Anna Kelemen1, Róbert Bódizs1, 4, Loránd Erőss5, Dániel Fabó1
1 Dept of Neurology, National Institute of Mental Health, Neurology and Neurosurgery, Budapest 1145, Hungary
2 School of PhD, Semmelweis University, Budapest 1089, Hungary
3 Dept of Psychiatry and Psychotherapy, Semmelweis University, Budapest 1089, Hungary
4 Institute of Behavioral Sciences, Semmelweis University, Budapest 1089, Hungary
5 Dept of Functional Neurosurgery, National Institute of Mental Health, Neurology and Neurosurgery, Budapest 1145, Hungary
Abstract
Objective
Memory deficits are frequent among patients with epilepsies affecting the temporal lobe. Hippocampal interictal epileptic discharges (hIED), the presumed epileptic exaggeration of sharp wave-ripples (SWR) are known to contribute to memory dysfunctions, but the potential underlying mechanism is unknown. The precise temporal coordination between hippocampal SWRs and corticothalamic spindles during sleep is critical for memory consolidation. Moreover, previous investigation indicated that hIEDs induce neocortical spindle like oscillation. In the present study we aimed to assess the influence of hIEDs on neocortical spindles.
Methods
We analyzed the spindle characteristics (duration, amplitude, frequency) of 21 epilepsy patients implanted with foramen ovale (FO) electrodes during a whole night sleep. Scalp sleep spindles were categorized based on their temporal relationship to hIEDs detected on the FO electrodes. Three groups were created: (i) spindles coinciding with hIEDs, (ii) spindles “induced” by hIEDs, and (iii) spindles without hIEDs co-occurrence.
Results
We found that spindles co-occurring with hIEDs had altered characteristics in all measured properties, they lasted longer by 126 ± 48 ms (mean±std), had higher amplitude by 3.4 ± 3.2 μV and their frequency range shifted towards the higher frequencies within the 13–15 Hz range. Also hIED-induced spindles had identical oscillatory properties with spindles without any temporal relationships with hIEDs. In more than half of our subjects clear temporal coherence was revealed between hIEDs and spindles, but the direction of the coupling was patient-specific.
Significance
We investigated the effect of hippocampal IEDs on neocortical spindle activity and found spindle alterations in cases of spindle-hIED co-occurrence, but not in cases of hIED-initiated spindles. We propose that this is a marker of a pathologic process, where IEDs may have direct effect on spindle generation. It could mark a potential mechanism where IEDs disrupt memory processes, and also provide a potential therapeutic target to treat memory disturbances in epilepsy.
Keywords: interictal epileptiform discharges, sleep spindle, epilepsy, hippocampus