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

doi:10.1016/j.cub.2017.10.062

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

Curr Biol. 2017 Dec 18;27(24):3743-3751.e3. doi: 10.1016/j.cub.2017.10.062. Epub 2017 Nov 30.

Authors

Affiliations

¹ Department of Psychiatry and Biobehavioral Sciences, Semel Institute for Neuroscience and Human Behavior, University of California, Los Angeles, Los Angeles, CA 90095, USA.
² Department of Neurology, University of California, Los Angeles, Los Angeles, CA 90095, USA.
³ Department of Neurosurgery, David Geffen School of Medicine, University of California, Los Angeles, Los Angeles, CA 90095, USA.
⁴ NeuroPace, Inc., Mountain View, CA 94043, USA.
⁵ Department of Psychiatry and Biobehavioral Sciences, Semel Institute for Neuroscience and Human Behavior, University of California, Los Angeles, Los Angeles, CA 90095, USA; Department of Neurosurgery, David Geffen School of Medicine, University of California, Los Angeles, Los Angeles, CA 90095, USA; Functional Neurosurgery Unit, Tel Aviv Medical Center, Tel Aviv 64361, Israel; Sackler Faculty of Medicine, Tel Aviv University, Tel Aviv 69978, Israel.
⁶ Department of Psychiatry and Biobehavioral Sciences, Semel Institute for Neuroscience and Human Behavior, University of California, Los Angeles, Los Angeles, CA 90095, USA; Department of Neurosurgery, David Geffen School of Medicine, University of California, Los Angeles, Los Angeles, CA 90095, USA; Department of Psychology, University of California, Los Angeles, Los Angeles, CA 90095, USA. Electronic address: nsuthana@mednet.ucla.edu.

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.

Keywords: MTL; NeuroPace responsive neurostimulator; human; medial temporal lobe; navigation; theta oscillations; wireless intracranial recordings.

Published by Elsevier Ltd.

MeSH terms

Adult
Electrocorticography
Female
Humans
Implantable Neurostimulators
Male
Middle Aged
Temporal Lobe / physiology*
Theta Rhythm / physiology*
Walking / physiology*

Abstract

MeSH terms

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