Adult-born neurons facilitate olfactory bulb pattern separation during task engagement

  1. Wankun L Li
  2. Monica W Chu
  3. An Wu
  4. Yusuke Suzuki
  5. Itaru Imayoshi  Is a corresponding author
  6. Takaki Komiyama  Is a corresponding author
  1. University of California, San Diego, United States
  2. Kyoto University, Japan

Abstract

The rodent olfactory bulb incorporates thousands of newly generated inhibitory neurons daily throughout adulthood, but the role of adult neurogenesis in olfactory processing is not fully understood. Here we adopted a genetic method to inducibly suppress adult neurogenesis and investigated its effect on behavior and bulbar activity. Mice without young adult-born neurons (ABNs) showed normal ability in discriminating very different odorants but were impaired in fine discrimination. Furthermore, two-photon calcium imaging of mitral cells (MCs) revealed that the ensemble odor representations of similar odorants were more ambiguous in the ablation animals. This increased ambiguity was primarily due to a decrease in MC suppressive responses. Intriguingly, these deficits in MC encoding were only observed during task engagement but not passive exposure. Our results indicate that young olfactory ABNs are essential for the enhancement of MC pattern separation in a task engagement-dependent manner, potentially functioning as a gateway for top-down modulation.

Article and author information

Author details

  1. Wankun L Li

    Neurobiology Section, Center for Neural Circuits and Behavior, University of California, San Diego, La Jolla, United States
    Competing interests
    The authors declare that no competing interests exist.
  2. Monica W Chu

    Neurobiology Section, Center for Neural Circuits and Behavior, University of California, San Diego, La Jolla, United States
    Competing interests
    The authors declare that no competing interests exist.
  3. An Wu

    Neurobiology Section, Center for Neural Circuits and Behavior, University of California, San Diego, La Jolla, United States
    Competing interests
    The authors declare that no competing interests exist.
  4. Yusuke Suzuki

    Graduate School of Medicine, Kyoto University, Kyoto, Japan
    Competing interests
    The authors declare that no competing interests exist.
  5. Itaru Imayoshi

    Graduate School of Biostudies, Kyoto University, Kyoto, Japan
    For correspondence
    iimayosh@virus.kyoto-u.ac.jp
    Competing interests
    The authors declare that no competing interests exist.
  6. Takaki Komiyama

    Neurobiology Section, Center for Neural Circuits and Behavior, University of California, San Diego, La Jolla, United States
    For correspondence
    tkomiyama@ucsd.edu
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-9609-4600

Funding

National Institute on Deafness and Other Communication Disorders (R01 DC014690-01)

  • Takaki Komiyama

Human Frontier Science Program

  • Itaru Imayoshi
  • Takaki Komiyama

Ministry of Education, Culture, Sports, Science, and Technology

  • Itaru Imayoshi

Japan Science and Technology Agency

  • Itaru Imayoshi
  • Takaki Komiyama

National Institute on Deafness and Other Communication Disorders (R21 DC012641)

  • Takaki Komiyama

National Institute on Deafness and Other Communication Disorders (U01 NS094342)

  • Takaki Komiyama

National Eye Institute (P30EY022589)

  • Takaki Komiyama

National Institute of Neurological Disorders and Stroke (R01 NS091010A)

  • Takaki Komiyama

National Eye Institute (R01 EY025349)

  • Takaki Komiyama

New York Stem Cell Foundation

  • Takaki Komiyama

David and Lucile Packard Foundation

  • Takaki Komiyama

Pew Charitable Trusts

  • Takaki Komiyama

McKnight Foundation

  • Takaki Komiyama

Kavli Foundation

  • Takaki Komiyama

National Science Foundation (1734940)

  • Takaki Komiyama

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

Reviewing Editor

  1. Naoshige Uchida, Harvard University, United States

Ethics

Animal experimentation: All procedures were in accordance with protocols approved by the Institutional Animal Care and Use Committee at UCSD (protocol number s10221) or Kyoto University (permit number Med Kyo 16216) and guidelines of the National Institute of Health.

Version history

  1. Received: October 21, 2017
  2. Accepted: March 12, 2018
  3. Accepted Manuscript published: March 13, 2018 (version 1)
  4. Version of Record published: April 23, 2018 (version 2)

Copyright

© 2018, Li 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. Wankun L Li
  2. Monica W Chu
  3. An Wu
  4. Yusuke Suzuki
  5. Itaru Imayoshi
  6. Takaki Komiyama
(2018)
Adult-born neurons facilitate olfactory bulb pattern separation during task engagement
eLife 7:e33006.
https://doi.org/10.7554/eLife.33006

Share this article

https://doi.org/10.7554/eLife.33006

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