Electrical Stimulation Modulates High γ Activity and Human Memory Performance

• Type of Material: Article
• Authors: Michal T. Berry, Mayo Clinic; Brent M. Kremen, Mayo Clinic; Vaclav Miller, Mayo Clinic; Laura Miller Khadjevand, Mayo Clinic; Fatemeh Ezzyat, University of Pennsylvania; Youssef Stein, University of Pennsylvania; Joel Wanda, University of Pennsylvania; Paul Sperling, Thomas Jefferson University Hospital; Michael R. Gorniak, Thomas Jefferson University Hospital; Richard Davis, University of Pennsylvania; Kathryn Jobst, Dartmouth-Hitchcock Medical Center; Barbara Gross, Emory University; Michal T. Kucewicz, Mayo Clinic; Bradley Lega, UT Southwestern Medical Center; S. Matt Stead, Mayo Clinic; Daniel S. Rizzuto, University of Pennsylvania; Michael J. Kahana, University of Pennsylvania; Gregory A. Worrell, Mayo Clinic
• Language: English
• Date: 2018-01-01
• Publisher: Emory University Libraries
• Publication Version: Final Published Version
• Copyright Statement: © 2018 Kucewicz et al.
• License: Creative Commons Attribution 4.0 International
• Final Published Version (URL): http://dx.doi.org/10.1523/ENEURO.0369-17.2018
• Title of Journal or Parent Work: eNeuro
• Volume: 5
• Issue: 1
• Grant/Funding Information: This work was supported by the DARPA Restoring Active Memory (RAM) Program (Cooperative Agreement N66001-14-2-4032). V.K. was additionally supported by the Czech Technical University in Prague.
• Keywords: brain stimulation; high-frequency oscillations; ECoG; intracranial EEG; γ-activity; cognitive enhancement
• Research Categories: Engineering, Biomedical; Health Sciences, Medicine and Surgery; Biology, Neuroscience

Abstract

Direct electrical stimulation of the brain has emerged as a powerful treatment for multiple neurological diseases, and as a potential technique to enhance human cognition. Despite its application in a range of brain disorders, it remains unclear how stimulation of discrete brain areas affects memory performance and the underlying electrophysiological activities. Here, we investigated the effect of direct electrical stimulation in four brain regions known to support declarative memory: hippocampus (HP), parahippocampal region (PH) neocortex, prefrontal cortex (PF), and lateral temporal cortex (TC). Intracranial EEG recordings with stimulation were collected from 22 patients during performance of verbal memory tasks. We found that high γ (62-118 Hz) activity induced by word presentation was modulated by electrical stimulation. This modulatory effect was greatest for trials with “poor” memory encoding. The high γ modulation correlated with the behavioral effect of stimulation in a given brain region: it was negative, i.e., the induced high γ activity was decreased, in the regions where stimulation decreased memory performance, and positive in the lateral TC where memory enhancement was observed. Our results suggest that the effect of electrical stimulation on high γ activity induced by word presentation may be a useful biomarker for mapping memory networks and guiding therapeutic brain stimulation.