Interictal Epileptiform Discharges Impair Word Recall in Multiple Brain Areas

• Type of Material: Article
• Authors: Peter C. Horak, Geisel School of Medicine at Dartmouth; Stephen Meisenhelter, Geisel School of Medicine at Dartmouth; Yinchen Song, Geisel School of Medicine at Dartmouth; Markus E. Testorf, Geisel School of Medicine at Dartmouth; Michael J Kahana, University of Pennsylvania; Weston D. Viles, Geisel School of Medicine at Dartmouth; Drzysztof Bujarski, Geisel School of Medicine at Dartmouth; Andrew C. Connolly, Geisel School of Medicine at Dartmouth; Ashlee A. Robbins, Geisel School of Medicine at Dartmouth; Michael R. Sperling, Thomas Jefferson University Hospital; Ashwini D. Sharan, Thomas Jefferson University Hospital; Gregory A. Worrell, Mayo Clinic; Laura R Miller, Mayo Clinic; Robert Gross, Emory University; Kathryn A. Davis, Hospital of the University of Pennsylvania; David W. Roberts, Geisel School of Medicine at Dartmouth; Bradley Lega, University of Texas Southwestern Medical Center; Sameer A. Sheth, Columbia University; Kareem A. Zaghloul, National Institute of Neurological Disorders and Stroke; Joel M. Stein, Hospital of the University of Pennsylvania; Sandhitsu Das, Hospital of the University of Pennsylvania; Daniel S. Rizzuto, University of Pennsylvania; Barbara C. Jobst, Geisel School of Medicine at Dartmouth
• Language: English
• Date: 2017-03-01
• Publisher: Wiley: 12 months
• Publication Version: Author Accepted Manuscript (After Peer Review)
• Copyright Statement: Wiley Periodicals, Inc. © 2016 International League Against Epilepsy
• Final Published Version (URL): http://dx.doi.org/10.1111/epi.13633
• Title of Journal or Parent Work: Epilepsia
• ISSN: 0013-9580
• Volume: 58
• Issue: 3
• Start Page: 373
• End Page: 380
• Grant/Funding Information: This work was supported by the National Institute of Health (Grant R01-NS074450) and by the Defense Advanced Research Projects Agency (DARPA) Restoring Active Memory (RAM) program (Cooperative Agreement N66001-14-2-4032).
• Keywords: SPIKES; TEMPORAL-LOBE EPILEPSY; Memory; LANGUAGE; HIPPOCAMPUS; Neurosciences & Neurology; Brain mapping; STIMULATION; Science & Technology; EEG; Life Sciences & Biomedicine; Interictal spikes; SUBSEQUENT MEMORY; Epilepsy; COGNITIVE IMPAIRMENT; REGISTRATION; Clinical Neurology; Electrocorticography; HUMAN CEREBRAL-CORTEX
• Research Categories: Health Sciences, Medicine and Surgery

Abstract

Interictal epileptiform discharges (IEDs) have been linked to memory impairment, but the spatial and temporal dynamics of this relationship remain elusive. In the present study, we aim to systematically characterize the brain areas and times at which IEDs affect memory. Methods: Eighty epilepsy patients participated in a delayed free recall task while undergoing intracranial electroencephalography (EEG) monitoring. We analyzed the locations and timing of IEDs relative to the behavioral data in order to measure their effects on memory. Results: Overall IED rates did not correlate with task performance across subjects (r = 0.03, p = 0.8). However, at a finer temporal scale, within-subject memory was negatively affected by IEDs during the encoding and recall periods of the task but not during the rest and distractor periods (p < 0.01, p < 0.001, p = 0.3, and p = 0.8, respectively). The effects of IEDs during encoding and recall were stronger in the left hemisphere than in the right (p < 0.05). Of six brain areas analyzed, IEDs in the inferior-temporal, medial-temporal, and parietal areas significantly affected memory (false discovery rate < 0.05). Significance: These findings reveal a network of brain areas sensitive to IEDs with key nodes in temporal as well as parietal lobes. They also demonstrate the time-dependent effects of IEDs in this network on memory.