Temporal lobe interictal spikes disrupt encoding and retrieval of verbal memory: A subregion analysis

Liliana Camarillo-Rodriguez, Iwin Leenen, Zachary Waldman, Mijail Serruya, Paul A. Wanda, Nora A. Herweg, Michael J. Kahana, Daniel Rubinstein, Iren Orosz, Bradley Lega, Irina Podkorytova, Robert E. Gross, Gregory Worrell, Kathryn A. Davis, Barbara C. Jobst, Sameer A. Sheth, Shennan A. Weiss, Michael R. Sperling

Research output: Contribution to journalArticlepeer-review

Abstract

Objective: The medial temporal lobe (MTL) encodes and recalls memories and can be a predominant site for interictal spikes (IS) in patients with focal epilepsy. It is unclear whether memory deficits are due to IS in the MTL producing a transient decline. Here, we investigated whether IS in the MTL subregions and lateral temporal cortex impact episodic memory encoding and recall. Methods: Seventy-eight participants undergoing presurgical evaluation for medically refractory focal epilepsy with depth electrodes placed in the temporal lobe participated in a verbal free recall task. IS were manually annotated during the pre-encoding, encoding, and recall epochs. We examined the effect of IS on word recall using mixed-effects logistic regression. Results: IS in the left hippocampus (odds ratio [OR] =.73, 95% confidence interval [CI] =.63–.84, p <.001) and left middle temporal gyrus (OR =.46, 95% CI =.27–.78, p <.05) during word encoding decreased subsequent recall performance. Within the left hippocampus, this effect was specific for area CA1 (OR =.76, 95% CI =.66–.88, p <.01) and dentate gyrus (OR =.74, 95% CI =.62–.89, p <.05). IS in other MTL subregions or inferior and superior temporal gyrus and IS occurring during the prestimulus window did not affect word encoding (p >.05). IS during retrieval in right hippocampal (OR =.22, 95% CI =.08–.63, p =.01) and parahippocampal regions (OR =.24, 95% CI =.07–.8, p <.05) reduced the probability of recalling a word. Significance: IS in medial and lateral temporal cortex contribute to transient memory decline during verbal episodic memory.

Original languageEnglish (US)
JournalEpilepsia
DOIs
StateAccepted/In press - 2022

Keywords

  • CA1
  • dentate gyrus
  • episodic memory
  • interictal epileptiform discharges
  • intracranial EEG
  • lateral temporal cortex
  • medial temporal lobe

ASJC Scopus subject areas

  • Neurology
  • Clinical Neurology

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