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Acquisition of innate odor preference depends on spontaneous and experiential activities during critical period

  1. Qiang Qiu
  2. Yunming Wu
  3. Limei Ma
  4. Wenjing Xu
  5. Max Hills Jnr
  6. Vivekanandan Ramalingam
  7. C Ron Yu  Is a corresponding author
  1. Stowers Institute for Medical Research, United States
Research Article
  • Cited 2
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Cite this article as: eLife 2021;10:e60546 doi: 10.7554/eLife.60546

Abstract

Animals possess an inborn ability to recognize certain odors to avoid predators, seek food and find mates. Innate odor preference has been thought to be genetically hardwired. Here we report that acquisition of innate odor recognition requires spontaneous neural activity and is influenced by sensory experience during early postnatal development. Genetic silencing of mouse olfactory sensory neurons during the critical period has little impact on odor sensitivity, discrimination, and recognition later in life. However, it abolishes innate odor preference and alters the patterns of activation in brain centers. Moreover, exposure to an aversive odor during the critical period abolishes aversion in adulthood in an odor-specific manner. The loss of innate aversion is associated with broadened projection of OSNs. Thus, a delicate balance of neural activity is required during the critical period in establishing innate odor preference and ectopic projection is a convergent mechanism to alter innate odor valence.

Data availability

Sequencing data have been deposited in GEO under accession codes GSE166457.All other data generated or analysed during this study will be available at https://www.stowers.org/research/publications/LIBPB-1613_2021.

The following data sets were generated

Article and author information

Author details

  1. Qiang Qiu

    Stowers Institute for Medical Research, Kansas City, United States
    Competing interests
    The authors declare that no competing interests exist.
  2. Yunming Wu

    Stowers Institute for Medical Research, Kansas City, United States
    Competing interests
    The authors declare that no competing interests exist.
  3. Limei Ma

    Stowers Institute for Medical Research, Kansas City, United States
    Competing interests
    The authors declare that no competing interests exist.
  4. Wenjing Xu

    Stowers Institute for Medical Research, Kansas City, United States
    Competing interests
    The authors declare that no competing interests exist.
  5. Max Hills Jnr

    Stowers Institute for Medical Research, Kansas City, United States
    Competing interests
    The authors declare that no competing interests exist.
  6. Vivekanandan Ramalingam

    Stowers Institute for Medical Research, Kansas City, United States
    Competing interests
    The authors declare that no competing interests exist.
  7. C Ron Yu

    Stowers Institute for Medical Research, Kansas City, United States
    For correspondence
    cry@stowers.org
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-1555-8683

Funding

National Institutes of Health (R01DC008003)

  • C Ron Yu

National Institutes of Health (R01DC014701)

  • C Ron Yu

National Institutes of Health (R01DC016696)

  • C Ron Yu

Stowers Institute for Medical Research (1021)

  • C Ron Yu

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

Ethics

Animal experimentation: Experimental protocols were approved by the Institutional Animal Care and Use Committee at Stowers Institute (protocol 2019-102) and in compliance with the NIH Guide for Care and Use of Animals.

Reviewing Editor

  1. Stephen Liberles, Harvard Medical School, United States

Publication history

  1. Received: June 29, 2020
  2. Accepted: March 24, 2021
  3. Accepted Manuscript published: March 26, 2021 (version 1)
  4. Version of Record published: April 8, 2021 (version 2)

Copyright

© 2021, Qiu 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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