Sub-second dynamics of theta-gamma coupling in Hippocampal CA1

  1. Lu Zhang
  2. John Lee
  3. Christopher Rozell
  4. Annabelle C Singer  Is a corresponding author
  1. Georgia Institute of Technology and Emory University, United States
  2. Georgia Institute of Technology, United States

Abstract

Oscillatory brain activity reflects different internal brain states including neurons' excitatory state and synchrony among neurons. However, characterizing these states is complicated by the fact that different oscillations are often coupled, such as gamma oscillations nested in theta in the hippocampus, and changes in coupling are thought to reflect distinct states. Here, we describe a new method to separate single oscillatory cycles into distinct states based on frequency and phase coupling. Using this method, we identified four theta-gamma coupling states in rat hippocampal CA1. These states differed in abundance across behaviors, phase synchrony with other hippocampal subregions, and neural coding properties suggesting that these states are functionally distinct. We captured cycle-to-cycle changes in oscillatory coupling states and found frequent switching between theta-gamma states showing that the hippocampus rapidly shifts between different functional states. This method provides a new approach to investigate oscillatory brain dynamics broadly.

Data availability

All data are available from the CRCNS data repository.

The following previously published data sets were used

Article and author information

Author details

  1. Lu Zhang

    Coulter Department of Biomedical Engineering, Georgia Institute of Technology and Emory University, Atlanta, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-7300-1037
  2. John Lee

    School of Electrical and Computer Engineering, Georgia Institute of Technology, Atlanta, United States
    Competing interests
    The authors declare that no competing interests exist.
  3. Christopher Rozell

    Coulter Department of Biomedical Engineering, Georgia Institute of Technology and Emory University, Atlanta, United States
    Competing interests
    The authors declare that no competing interests exist.
  4. Annabelle C Singer

    Coulter Department of Biomedical Engineering, Georgia Institute of Technology and Emory University, Atlanta, United States
    For correspondence
    asinger@gatech.edu
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-6003-0488

Funding

National Institutes of Health (R01 NS109226)

  • Annabelle C Singer

Packard Foundation

  • Annabelle C Singer

National Science Foundation (CCF-1409422)

  • Christopher Rozell

DSO National Laboratories of Singapore.

  • John Lee

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

Ethics

Animal experimentation: All protocols were approved by the Institutional Animal Care and Use Committee of Rutgers University (hc-3) or New York University (hc-11).

Reviewing Editor

  1. Frances K Skinner, Krembil Research Institute, University Health Network, Canada

Version history

  1. Received: December 11, 2018
  2. Accepted: July 28, 2019
  3. Accepted Manuscript published: July 29, 2019 (version 1)
  4. Version of Record published: August 6, 2019 (version 2)

Copyright

© 2019, Zhang et al.

This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.

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  1. Lu Zhang
  2. John Lee
  3. Christopher Rozell
  4. Annabelle C Singer
(2019)
Sub-second dynamics of theta-gamma coupling in Hippocampal CA1
eLife 8:e44320.
https://doi.org/10.7554/eLife.44320

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