Effects of hippocampal interictal discharge timing, duration, and spatial extent on list learning

Beth Leeman-Markowski, Richard Hardstone, Lynn Lohnas, Benjamin Cowen, Lila Davachi, Werner Doyle, Patricia Dugan, Daniel Friedman, Anli Liu, Lucia Melloni, Ivan Selesnick, Binhuan Wang, Kimford Meador, Orrin Devinsky

Research output: Contribution to journalArticlepeer-review

Abstract

Interictal epileptiform discharges (IEDs) can impair memory. The properties of IEDs most detrimental to memory, however, are undefined. We studied the impact of temporal and spatial characteristics of IEDs on list learning. Subjects completed a memory task during intracranial EEG recordings including hippocampal depth and temporal neocortical subdural electrodes. Subjects viewed a series of objects, and after a distracting task, recalled the objects from the list. The impacts of IED presence, duration, and propagation to neocortex during encoding of individual stimuli were assessed. The effects of IED total number and duration during maintenance and recall periods on delayed recall performance were also determined. The influence of IEDs during recall was further investigated by comparing the likelihood of IEDs preceding correctly recalled items vs. periods of no verbal response. Across 6 subjects, we analyzed 28 hippocampal and 139 lateral temporal contacts. Recall performance was poor, with a median of 17.2% correct responses (range 10.4–21.9%). Interictal epileptiform discharges during encoding, maintenance, and recall did not significantly impact task performance, and there was no significant difference between the likelihood of IEDs during correct recall vs. periods of no response. No significant effects of discharge duration during encoding, maintenance, or recall were observed. Interictal epileptiform discharges with spread to lateral temporal cortex during encoding did not adversely impact recall. A post hoc analysis refining model assumptions indicated a negative impact of IED count during the maintenance period, but otherwise confirmed the above results. Our findings suggest no major effect of hippocampal IEDs on list learning, but study limitations, such as baseline hippocampal dysfunction, should be considered. The impact of IEDs during the maintenance period may be a focus of future research.

Original languageEnglish (US)
Article number108209
JournalEpilepsy and Behavior
Volume123
DOIs
StatePublished - Oct 2021
Externally publishedYes

Keywords

  • EEG
  • Electrocorticography
  • Intracranial EEG
  • Intracranial electroencephalography
  • Learning
  • Memory

ASJC Scopus subject areas

  • Neurology
  • Clinical Neurology
  • Behavioral Neuroscience

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