Theta Oscillations in the Human Medial Temporal Lobe during Real-World Ambulatory Movement

Zahra M. Aghajan, Peter Schuette, Tony A. Fields, Michelle E. Tran, Sameed M. Siddiqui, Nicholas R. Hasulak, Thomas K. Tcheng, Dawn Eliashiv, Emily A. Mankin, John Stern, Itzhak Fried, Nanthia Suthana*

*Corresponding author for this work

Research output: Contribution to journalArticlepeer-review

112 Scopus citations

Abstract

The theta rhythm—a slow (6–12 Hz) oscillatory component of the local field potential—plays a critical role in spatial navigation and memory by coordinating the activity of neuronal ensembles within the medial temporal lobe (MTL). Although theta has been extensively studied in freely moving rodents, its presence in humans has been elusive and primarily investigated in stationary subjects. Here we used a unique clinical opportunity to examine theta within the human MTL during untethered, real-world ambulatory movement. We recorded intracranial electroencephalographic activity from participants chronically implanted with the wireless NeuroPace responsive neurostimulator (RNS) and tracked their motion with sub-millimeter precision. Our data revealed that movement-related theta oscillations indeed exist in humans, such that theta power is significantly higher during movement than immobility. Unlike in rodents, however, theta occurs in short bouts, with average durations of ∼400 ms, which are more prevalent during fast versus slow movements. In a rare opportunity to study a congenitally blind participant, we found that both the prevalence and duration of theta bouts were increased relative to the sighted participants. These results provide critical support for conserved neurobiological characteristics of theta oscillations during ambulatory spatial navigation, while highlighting some fundamental differences across species in these oscillations between humans and rodents. Aghajan et al. record deep brain activity, during untethered freely moving behavior, from participants chronically implanted with depth electrodes. They demonstrate that 8 Hz theta oscillations, the hallmark of spatial navigation in rodents, also occur in humans, albeit in shorter bouts that are more prevalent during fast versus slow movements.

Original languageEnglish
Pages (from-to)3743-3751.e3
JournalCurrent Biology
Volume27
Issue number24
DOIs
StatePublished - 18 Dec 2017

Funding

FundersFunder number
National Institute of Neurological Disorders and StrokeT32NS058280, NS084017
Defense Advanced Research Projects AgencyN66001-14-2-4029
A.P. Giannini Foundation
University of California at Los Angeles

    Keywords

    • MTL
    • NeuroPace responsive neurostimulator
    • human
    • medial temporal lobe
    • navigation
    • theta oscillations
    • wireless intracranial recordings

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