Ripple oscillations in the left temporal neocortex are associated with impaired verbal episodic memory encoding

Zachary J. Waldman, Liliana Camarillo-Rodriguez, Inna Chervenova, Brent Berry, Shoichi Shimamoto, Bahareh Elahian, Michal Kucewicz, Chaitanya Ganne, Xiao Song He, Leon A. Davis, Joel Stein, Sandhitsu Das, Richard Gorniak, Ashwini D. Sharan, Robert Gross, Cory S. Inman, Bradley C. Lega, Kareem Zaghloul, Barbara C. Jobst, Katheryn A. DavisPaul Wanda, Mehraneh Khadjevand, Joseph Tracy, Daniel S. Rizzuto, Gregory Worrell, Michael Sperling, Shennan A. Weiss

Research output: Contribution to journalArticlepeer-review

4 Scopus citations

Abstract

Background: We sought to determine if ripple oscillations (80–120 Hz), detected in intracranial electroencephalogram (iEEG) recordings of patients with epilepsy, correlate with an enhancement or disruption of verbal episodic memory encoding. Methods: We defined ripple and spike events in depth iEEG recordings during list learning in 107 patients with focal epilepsy. We used logistic regression models (LRMs) to investigate the relationship between the occurrence of ripple and spike events during word presentation and the odds of successful word recall following a distractor epoch and included the seizure onset zone (SOZ) as a covariate in the LRMs. Results: We detected events during 58,312 word presentation trials from 7630 unique electrode sites. The probability of ripple on spike (RonS) events was increased in the SOZ (p < 0.04). In the left temporal neocortex, RonS events during word presentation corresponded with a decrease in the odds ratio (OR) of successful recall, however, this effect only met significance in the SOZ (OR of word recall: 0.71, 95% confidence interval (CI): 0.59–0.85, n = 158 events, adaptive Hochberg, p < 0.01). Ripple on oscillation (RonO) events that occurred in the left temporal neocortex non-SOZ also correlated with decreased odds of successful recall (OR: 0.52, 95% CI: 0.34–0.80, n = 140, adaptive Hochberg, p < 0.01). Spikes and RonS that occurred during word presentation in the left middle temporal gyrus (MTG) correlated with the most significant decrease in the odds of successful recall, irrespective of the location of the SOZ (adaptive Hochberg, p < 0.01). Conclusion: Ripples and spikes generated in the left temporal neocortex are associated with impaired verbal episodic memory encoding. Although physiological and pathological ripple oscillations were not distinguished during cognitive tasks, our results show an association of undifferentiated ripples with impaired encoding. The effect was sometimes specific to regions outside the SOZ, suggesting that widespread effects of epilepsy outside the SOZ may contribute to cognitive impairment.

Original languageEnglish (US)
Pages (from-to)33-40
Number of pages8
JournalEpilepsy and Behavior
Volume88
DOIs
StatePublished - Nov 2018

Bibliographical note

Funding Information:
We thank Blackrock Microsystems for providing neural recording and stimulation equipment. This work was supported by the DARPA Restoring Active Memory (RAM) program (Cooperative Agreement N66001-14-2-4032 ). The views, opinions, and/or findings contained in this material are those of the authors and should not be interpreted as representing the official views or policies of the Department of Defense or the U.S. Government. Dr. Weiss is supported by 1K23NS094633-01A1.

Publisher Copyright:
© 2018 Elsevier Inc.

Keywords

  • Epilepsy
  • Epileptiform discharge
  • High-frequency oscillation
  • Verbal memory

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