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Curr Biol. 2018 Oct 22;28(20):3310-3315.e4. doi: 10.1016/j.cub.2018.08.029. Epub 2018 Oct 11.

Hexadirectional Modulation of Theta Power in Human Entorhinal Cortex during Spatial Navigation.

Author information

1
School of Systems Science, Beijing Normal University, Xinjiekouwai Str. 19, 100875 Beijing, China.
2
Epilepsy Center, Medical Center-University of Freiburg, Faculty of Medicine, University of Freiburg, Breisacher Str. 64, 79106 Freiburg im Breisgau, Germany.
3
Department of Neuropsychology, Institute of Cognitive Neuroscience, Faculty of Psychology, Ruhr University Bochum, Universitätsstraße 150, 44801 Bochum, Germany.
4
School of Systems Science, Beijing Normal University, Xinjiekouwai Str. 19, 100875 Beijing, China; State Key Laboratory of Cognitive Neuroscience and Learning & IDG/McGovern Institute for Brain Research, Beijing Normal University, Xinjiekouwai Str. 19, 100875 Beijing, China.
5
University Medical Center, Stereotactic and Functional Neurosurgery, Breisacher Str. 64, 79106 Freiburg im Breisgau, Germany.
6
Department of Epilepsy Center, Tsinghua University Yuquan Hospital, 5 Shijingshan Road, 100049 Beijing, China.
7
Department of Neurosurgery, First Affiliated Hospital of General Hospital of PLA, 51 Fucheng Road, 100048 Beijing, China.
8
Department of Neuropsychology, Institute of Cognitive Neuroscience, Faculty of Psychology, Ruhr University Bochum, Universitätsstraße 150, 44801 Bochum, Germany. Electronic address: nikolai.axmacher@rub.de.
9
CAS Key Laboratory of Mental Health, Institute of Psychology, 16 Lincui Road, 100101 Beijing, China; CAS Center for Excellence in Brain Science and Intelligence Technology, 320 Yue Yang Road, 200031 Shanghai, China. Electronic address: lwang@psych.ac.cn.

Abstract

Grid cells and theta oscillations are fundamental components of the brain's navigation system. Grid cells provide animals [1, 2] and humans [3, 4] with a spatial map of the environment by exhibiting multiple firing fields arranged in a regular grid of equilateral triangles. This unique firing pattern presumably constitutes the neural basis for path integration [5-8] and may also enable navigation in visual and conceptual spaces [9-12]. Theta frequency oscillations are a prominent mesoscopic network phenomenon during navigation in both rodents and humans [13, 14] and encode movement speed [15-17], distance traveled [18], and proximity to spatial boundaries [19]. Whether theta oscillations may also carry a grid-like signal remains elusive, however. Capitalizing on previous fMRI studies revealing a macroscopic proxy of sum grid cell activity in human entorhinal cortex (EC) [20-22], we examined intracranial EEG recordings from the EC of epilepsy patients (n = 9) performing a virtual navigation task. We found that the power of theta oscillations (4-8 Hz) exhibits 6-fold rotational modulation by movement direction, reminiscent of grid cell-like representations detected using fMRI. Modulation of theta power was specific to 6-fold rotational symmetry and to the EC. Hexadirectional modulation of theta power by movement direction only emerged during fast movements, stabilized over the course of the experiment, and showed sensitivity to the environmental boundary. Our results suggest that oscillatory power in the theta frequency range carries an imprint of sum grid cell activity potentially enabled by a common grid orientation of neighboring grid cells [23].

KEYWORDS:

entorhinal cortex; grid cell; intracranial EEG; navigation; oscillation; theta

PMID:
30318350
DOI:
10.1016/j.cub.2018.08.029

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