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

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.

Reviewing Editor

  1. Stephen Liberles, Harvard Medical School, United States

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.

Version 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.

Metrics

  • 3,379
    Page views
  • 381
    Downloads
  • 11
    Citations

Article citation count generated by polling the highest count across the following sources: Crossref, PubMed Central, Scopus.

Download links

A two-part list of links to download the article, or parts of the article, in various formats.

Downloads (link to download the article as PDF)

Open citations (links to open the citations from this article in various online reference manager services)

Cite this article (links to download the citations from this article in formats compatible with various reference manager tools)

  1. Qiang Qiu
  2. Yunming Wu
  3. Limei Ma
  4. Wenjing Xu
  5. Max Hills Jnr
  6. Vivekanandan Ramalingam
  7. C Ron Yu
(2021)
Acquisition of innate odor preference depends on spontaneous and experiential activities during critical period
eLife 10:e60546.
https://doi.org/10.7554/eLife.60546

Share this article

https://doi.org/10.7554/eLife.60546

Further reading

    1. Neuroscience
    Songyao Zhang, Tuo Zhang ... Tianming Liu
    Research Article

    Cortical folding is an important feature of primate brains that plays a crucial role in various cognitive and behavioral processes. Extensive research has revealed both similarities and differences in folding morphology and brain function among primates including macaque and human. The folding morphology is the basis of brain function, making cross-species studies on folding morphology important for understanding brain function and species evolution. However, prior studies on cross-species folding morphology mainly focused on partial regions of the cortex instead of the entire brain. Previously, our research defined a whole-brain landmark based on folding morphology: the gyral peak. It was found to exist stably across individuals and ages in both human and macaque brains. Shared and unique gyral peaks in human and macaque are identified in this study, and their similarities and differences in spatial distribution, anatomical morphology, and functional connectivity were also dicussed.

    1. Neuroscience
    Avani Koparkar, Timothy L Warren ... Lena Veit
    Research Article

    Complex skills like speech and dance are composed of ordered sequences of simpler elements, but the neuronal basis for the syntactic ordering of actions is poorly understood. Birdsong is a learned vocal behavior composed of syntactically ordered syllables, controlled in part by the songbird premotor nucleus HVC (proper name). Here, we test whether one of HVC’s recurrent inputs, mMAN (medial magnocellular nucleus of the anterior nidopallium), contributes to sequencing in adult male Bengalese finches (Lonchura striata domestica). Bengalese finch song includes several patterns: (1) chunks, comprising stereotyped syllable sequences; (2) branch points, where a given syllable can be followed probabilistically by multiple syllables; and (3) repeat phrases, where individual syllables are repeated variable numbers of times. We found that following bilateral lesions of mMAN, acoustic structure of syllables remained largely intact, but sequencing became more variable, as evidenced by ‘breaks’ in previously stereotyped chunks, increased uncertainty at branch points, and increased variability in repeat numbers. Our results show that mMAN contributes to the variable sequencing of vocal elements in Bengalese finch song and demonstrate the influence of recurrent projections to HVC. Furthermore, they highlight the utility of species with complex syntax in investigating neuronal control of ordered sequences.