Semiochemical responsive olfactory sensory neurons are sexually dimorphic and plastic

  1. Aashutosh Vihani  Is a corresponding author
  2. Xiaoyang Serene Hu
  3. Sivaji Gundala
  4. Sachiko Koyama
  5. Eric Block
  6. Hiroaki Matsunami  Is a corresponding author
  1. Duke University, United States
  2. University at Albany, State University of New York, United States
  3. Indiana University Bloomington, United States

Abstract

Understanding how genes and experiences work in concert to generate phenotypic variability will provide a better understanding of individuality. Here, we considered this in the main olfactory epithelium, a chemosensory structure with over a thousand distinct cell types in mice. We identified a subpopulation of olfactory sensory neurons, defined by receptor expression, whose abundances were sexually dimorphic. This subpopulation of olfactory sensory neurons was over-represented in sex-separated mice and robustly responsive to sex-specific semiochemicals. Sex-combined housing led to an attenuation of the dimorphic representations. Single-cell sequencing analysis revealed an axis of activity-dependent gene expression amongst a subset of the dimorphic OSN populations. Finally, the pro-apoptotic gene Bax is necessary to generate the dimorphic representations. Altogether, our results suggest a role of experience and activity in influencing homeostatic mechanisms to generate a robust sexually dimorphic phenotype in the main olfactory epithelium.

Data availability

Sequencing data have been deposited in GEO under accession codes GSE160272.

The following data sets were generated
The following previously published data sets were used

Article and author information

Author details

  1. Aashutosh Vihani

    Department of Neurobiology, Duke University, Durham, United States
    For correspondence
    aashutosh.vihani@duke.edu
    Competing interests
    No competing interests declared.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-5979-101X
  2. Xiaoyang Serene Hu

    Department of Molecular Genetics and Microbiology, Duke University, Durham, United States
    Competing interests
    No competing interests declared.
  3. Sivaji Gundala

    Department of Chemistry, University at Albany, State University of New York, Albany, United States
    Competing interests
    No competing interests declared.
  4. Sachiko Koyama

    Biology, Indiana University Bloomington, Bloomington, United States
    Competing interests
    No competing interests declared.
  5. Eric Block

    Department of Chemistry, University at Albany, State University of New York, Albany, United States
    Competing interests
    No competing interests declared.
  6. Hiroaki Matsunami

    Department of Neurobiology, Duke University, Durham, United States
    For correspondence
    hiroaki.matsunami@duke.edu
    Competing interests
    Hiroaki Matsunami, HM receives royalties from Chemcom..

Funding

National Institute on Deafness and Other Communication Disorders (DC014423)

  • Eric Block
  • Hiroaki Matsunami

National Institute on Deafness and Other Communication Disorders (DC016224)

  • Hiroaki Matsunami

National Science Foundation (1556207)

  • Hiroaki Matsunami

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 (IACUC) protocol A128-19-06 at Duke University.

Copyright

© 2020, Vihani 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

  • 2,586
    views
  • 307
    downloads
  • 25
    citations

Views, downloads and citations are aggregated across all versions of this paper published by eLife.

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. Aashutosh Vihani
  2. Xiaoyang Serene Hu
  3. Sivaji Gundala
  4. Sachiko Koyama
  5. Eric Block
  6. Hiroaki Matsunami
(2020)
Semiochemical responsive olfactory sensory neurons are sexually dimorphic and plastic
eLife 9:e54501.
https://doi.org/10.7554/eLife.54501

Share this article

https://doi.org/10.7554/eLife.54501

Further reading

    1. Neuroscience
    Sven Ohl, Martin Rolfs
    Research Article

    Detecting causal relations structures our perception of events in the world. Here, we determined for visual interactions whether generalized (i.e. feature-invariant) or specialized (i.e. feature-selective) visual routines underlie the perception of causality. To this end, we applied a visual adaptation protocol to assess the adaptability of specific features in classical launching events of simple geometric shapes. We asked observers to report whether they observed a launch or a pass in ambiguous test events (i.e. the overlap between two discs varied from trial to trial). After prolonged exposure to causal launch events (the adaptor) defined by a particular set of features (i.e. a particular motion direction, motion speed, or feature conjunction), observers were less likely to see causal launches in subsequent ambiguous test events than before adaptation. Crucially, adaptation was contingent on the causal impression in launches as demonstrated by a lack of adaptation in non-causal control events. We assessed whether this negative aftereffect transfers to test events with a new set of feature values that were not presented during adaptation. Processing in specialized (as opposed to generalized) visual routines predicts that the transfer of visual adaptation depends on the feature similarity of the adaptor and the test event. We show that the negative aftereffects do not transfer to unadapted launch directions but do transfer to launch events of different speeds. Finally, we used colored discs to assign distinct feature-based identities to the launching and the launched stimulus. We found that the adaptation transferred across colors if the test event had the same motion direction as the adaptor. In summary, visual adaptation allowed us to carve out a visual feature space underlying the perception of causality and revealed specialized visual routines that are tuned to a launch’s motion direction.

    1. Neuroscience
    Ulrike Pech, Jasper Janssens ... Patrik Verstreken
    Research Article

    The classical diagnosis of Parkinsonism is based on motor symptoms that are the consequence of nigrostriatal pathway dysfunction and reduced dopaminergic output. However, a decade prior to the emergence of motor issues, patients frequently experience non-motor symptoms, such as a reduced sense of smell (hyposmia). The cellular and molecular bases for these early defects remain enigmatic. To explore this, we developed a new collection of five fruit fly models of familial Parkinsonism and conducted single-cell RNA sequencing on young brains of these models. Interestingly, cholinergic projection neurons are the most vulnerable cells, and genes associated with presynaptic function are the most deregulated. Additional single nucleus sequencing of three specific brain regions of Parkinson’s disease patients confirms these findings. Indeed, the disturbances lead to early synaptic dysfunction, notably affecting cholinergic olfactory projection neurons crucial for olfactory function in flies. Correcting these defects specifically in olfactory cholinergic interneurons in flies or inducing cholinergic signaling in Parkinson mutant human induced dopaminergic neurons in vitro using nicotine, both rescue age-dependent dopaminergic neuron decline. Hence, our research uncovers that one of the earliest indicators of disease in five different models of familial Parkinsonism is synaptic dysfunction in higher-order cholinergic projection neurons and this contributes to the development of hyposmia. Furthermore, the shared pathways of synaptic failure in these cholinergic neurons ultimately contribute to dopaminergic dysfunction later in life.