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

• Type of Material: Article
• Authors: Zachary J. Waldman, Thomas Jefferson University; Liliana Camarillo-Rodriguez, Thomas Jefferson University; Inna Chervenova, Thomas Jefferson University; Brent Berry, Mayo Clinic; Shoichi Shimamoto, Thomas Jefferson University; Bahareh Elahian, Thomas Jefferson University; Michal Kucewicz, Mayo Clinic; Chaitanya Ganne, Thomas Jefferson University; Xiao-Song He, Thomas Jefferson University; Leon A. Davis, University of Pennsylvania; Joel Stein, University of Pennsylvania; Sandhitsu Das, University of Pennsylvania; Richard Gorniak, Thomas Jefferson University; Ashwini D. Sharan, Thomas Jefferson University; Robert Gross, Emory University; Cory S. Inman, Emory University; Bradley C. Lega, University of Texas Southwestern Medical Center; Kareem Zaghloul, National Institute of Neurological Disorders and Stroke; Barbara C. Jobst, Dartmouth Hitchcock Medical Center; Katheryn A. Davis, University of Pennsylvania; Paul Wanda, University of Pennsylvania; Mehraneh Khadjevand, Mayo Clinic; Joseph Tracy, Thomas Jefferson University; Daniel S. Rizzuto, University of Pennsylvania; Gregory Worrell, Mayo Clinic; Michael Sperling, Thomas Jefferson University; Shennan A. Weiss, Thomas Jefferson University
• Language: English
• Date: 2018-11-01
• Publisher: Elsevier
• Publication Version: Author Accepted Manuscript (After Peer Review)
• Copyright Statement: © 2018 Elsevier Inc.
• License: Creative Commons Attribution-NonCommercial-NoDerivs 4.0 International
• Final Published Version (URL): http://dx.doi.org/10.1016/j.yebeh.2018.08.018
• Title of Journal or Parent Work: Epilepsy and Behavior
• ISSN: 1525-5050
• Volume: 88
• Start Page: 33
• End Page: 40
• Grant/Funding Information: Dr. Weiss is supported by 1K23NS094633–01A1.; This work was supported by the DARPA Restoring Active Memory (RAM) program (Cooperative Agreement N66001–14-2–4032).
• Keywords: Clinical Neurology; REACTIVATION; HIGH-FREQUENCY OSCILLATIONS; LOBE EPILEPSY; CONSOLIDATION; ELECTRICAL-STIMULATION; Science & Technology; HUMANS; Epilepsy; Verbal memory; Neurosciences & Neurology; NEURONAL FIRING PATTERNS; Life Sciences & Biomedicine; High-frequency oscillation; INTERICTAL EPILEPTIFORM DISCHARGES; Behavioral Sciences; SHARP-WAVE RIPPLES; SPIKES; Epileptiforrn discharge; Psychiatry
• Research Categories: Health Sciences, Medicine and Surgery; Biology, Neuroscience; Health Sciences, Radiology

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.