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Hippocampal theta oscillations are travelling waves

Nature volume 459, pages 534–539 (2009)Cite this article

Abstract

Theta oscillations clock hippocampal activity during awake behaviour and rapid eye movement (REM) sleep. These oscillations are prominent in the local field potential, and they also reflect the subthreshold membrane potential and strongly modulate the spiking of hippocampal neurons. The prevailing view is that theta oscillations are synchronized throughout the hippocampus, despite the lack of conclusive experimental evidence. In contrast, here we show that in freely behaving rats, theta oscillations in area CA1 are travelling waves that propagate roughly along the septotemporal axis of the hippocampus. Furthermore, we find that spiking in the CA1 pyramidal cell layer is modulated in a consistent travelling wave pattern. Our results demonstrate that theta oscillations pattern hippocampal activity not only in time, but also across anatomical space. The presence of travelling waves indicates that the instantaneous output of the hippocampus is topographically organized and represents a segment, rather than a point, of physical space.

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Figure 1: Interlaminar depth profile of theta oscillations and ripples.
Figure 2: Example of theta phase deviations.
Figure 3: Topographic intralaminar theta phase profiles.
Figure 4: Travelling wave example and wave parameter distributions.
Figure 5: Topographic profile of spiking theta phase preference.
Figure 6: Hippocampal representation of physical space.

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Acknowledgements

We thank C. Wierzynski, M. Gu, G. Laurent, E. Schuman and A. Tolias for critical discussions and comments on the manuscript. We also thank the Caltech Brain Imaging Center and D. Procissi for the MRI brain scans. This work was supported by the Caltech Information Science and Technology Center for Biological Circuit Design, a 21st Century McDonnell Foundation Award, the Bren Foundation, and the McKnight Foundation.

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Authors and Affiliations

  1. Division of Biology, Division of Engineering and Applied Science, California Institute of Technology, Pasadena, California 91125, USA,

    Evgueniy V. Lubenov & Athanassios G. Siapas

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  1. Evgueniy V. Lubenov
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  2. Athanassios G. Siapas
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Correspondence to Evgueniy V. Lubenov or Athanassios G. Siapas.

Supplementary information

Supplementary Information

This file contains Supplementary Methods and Data, Supplementary Notes for Supplementary Movies 1-3, Supplementary References and Supplementary Figures S1-S27 with Legends. (PDF 13325 kb)

Supplementary Movie 1

This movie shows travelling theta wave in rat 1 implanted with 6x5 grid (see file S1 for full Notes). (MOV 748 kb)

Supplementary Movie 2

This movie shows travelling theta wave in rat 2 implanted with 4x8 grid (see file S1 for full Notes). (MOV 730 kb)

Supplementary Movie 3

This movie shows travelling theta wave in rat 3 implanted with 5x6 grid (see file S1 for full Notes). (MOV 787 kb)

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Lubenov, E., Siapas, A. Hippocampal theta oscillations are travelling waves. Nature 459, 534–539 (2009). https://doi.org/10.1038/nature08010

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