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CA2 neuronal activity controls hippocampal low gamma and ripple oscillations

  1. Georgia M Alexander
  2. Logan Y Brown
  3. Shannon Farris
  4. Daniel Lustberg
  5. Caroline Pantazis
  6. Bernd Gloss
  7. Nicholas W Plummer
  8. Patricia Jensen
  9. Serena M Dudek  Is a corresponding author
  1. National Institute of Environmental Health Science, National Institutes of Health, United States
Research Article
  • Cited 3
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Cite this article as: eLife 2018;7:e38052 doi: 10.7554/eLife.38052

Abstract

Hippocampal oscillations arise from coordinated activity among distinct populations of neurons and are associated with cognitive functions. Much progress has been made toward identifying the contribution of specific neuronal populations in hippocampal oscillations, but less is known about the role of hippocampal area CA2, which is thought to support social memory. Furthermore, the little evidence on the role of CA2 in oscillations has yielded conflicting conclusions. Therefore, we sought to identify the contribution of CA2 to oscillations using a controlled experimental system. We used excitatory and inhibitory DREADDs to manipulate CA2 neuronal activity and studied resulting hippocampal-prefrontal cortical network oscillations. We found that modification of CA2 activity bidirectionally regulated hippocampal and prefrontal cortical low gamma oscillations and inversely modulated hippocampal ripple oscillations in mice. These findings support a role for CA2 in low gamma generation and ripple modulation within the hippocampus and underscore the importance of CA2 in extrahippocampal oscillations.

Article and author information

Author details

  1. Georgia M Alexander

    Neurobiology Laboratory, National Institute of Environmental Health Science, National Institutes of Health, Research Triangle Park, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-4245-4417
  2. Logan Y Brown

    Neurobiology Laboratory, National Institute of Environmental Health Science, National Institutes of Health, Research Triangle Park, United States
    Competing interests
    The authors declare that no competing interests exist.
  3. Shannon Farris

    Neurobiology Laboratory, National Institute of Environmental Health Science, National Institutes of Health, Research Triangle Park, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-4473-1684
  4. Daniel Lustberg

    Neurobiology Laboratory, National Institute of Environmental Health Science, National Institutes of Health, Research Triangle Park, United States
    Competing interests
    The authors declare that no competing interests exist.
  5. Caroline Pantazis

    Neurobiology Laboratory, National Institute of Environmental Health Science, National Institutes of Health, Research Triangle Park, United States
    Competing interests
    The authors declare that no competing interests exist.
  6. Bernd Gloss

    Neurobiology Laboratory, National Institute of Environmental Health Science, National Institutes of Health, Research Triangle Park, United States
    Competing interests
    The authors declare that no competing interests exist.
  7. Nicholas W Plummer

    Neurobiology Laboratory, National Institute of Environmental Health Science, National Institutes of Health, Research Triangle Park, United States
    Competing interests
    The authors declare that no competing interests exist.
  8. Patricia Jensen

    Neurobiology Laboratory, National Institute of Environmental Health Science, National Institutes of Health, Research Triangle Park, United States
    Competing interests
    The authors declare that no competing interests exist.
  9. Serena M Dudek

    Neurobiology Laboratory, National Institute of Environmental Health Science, National Institutes of Health, Research Triangle Park, United States
    For correspondence
    dudek@niehs.nih.gov
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-4094-8368

Funding

National Institute of Environmental Health Sciences (ES100221)

  • Serena M Dudek

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

Ethics

Animal experimentation: This study was performed in strict accordance with the recommendations in the Guide for the Care and Use of Laboratory Animals of the National Institutes of Health. All of the animals were handled according to approved institutional animal care and use committee (ACUC) protocol (#2009-0023) of the NIEHS (A4149-1). All surgery was performed under ketamine and xylazine anesthesia, and every effort was made to minimize suffering.

Reviewing Editor

  1. Laura Colgin, The University of Texas at Austin, Center for Learning and Memory, United States

Publication history

  1. Received: May 2, 2018
  2. Accepted: November 2, 2018
  3. Accepted Manuscript published: November 2, 2018 (version 1)
  4. Version of Record published: November 23, 2018 (version 2)

Copyright

This is an open-access article, free of all copyright, and may be freely reproduced, distributed, transmitted, modified, built upon, or otherwise used by anyone for any lawful purpose. The work is made available under the Creative Commons CC0 public domain dedication.

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