Systematic morphological and morphometric analysis of identified olfactory receptor neurons in Drosophila melanogaster

  1. Cesar Nava Gonzales
  2. Quintyn McKaughan
  3. Eric A Bushong
  4. Kalyani Cauwenberghs
  5. Renny Ng
  6. Matthew Madany
  7. Mark H Ellisman
  8. Chih-Ying Su  Is a corresponding author
  1. University of California, San Diego, United States
  2. University of California San Diego, United States
  3. National Center for Microscopy and Imaging Research, University of California, San Diego, United States

Abstract

The biophysical properties of sensory neurons are influenced by their morphometric and morphological features, whose precise measurements require high-quality volume electron microscopy (EM). However, systematic surveys of nanoscale characteristics for identified neurons are scarce. Here, we characterize the morphology of Drosophila olfactory receptor neurons (ORNs) across the majority of genetically identified sensory hairs. By analyzing serial block-face electron microscopy (SBEM) images of cryofixed antennal tissues, we compile an extensive morphometric dataset based on 122 reconstructed 3D models for 33 of the 40 identified antennal ORN types. Additionally, we observe multiple novel features - including extracellular vacuoles within sensillum lumen, intricate dendritic branching, mitochondria enrichment in select ORNs, novel sensillum types, and empty sensilla containing no neurons - which raise new questions pertinent to cell biology and sensory neurobiology. Our systematic survey is critical for future investigations into how the size and shape of sensory neurons influence their responses, sensitivity and circuit function.

Data availability

All data generated or analyzed during this study are included in the manuscript and supporting files. Source data files have been provided for Table 1, Table 2 and Individual datasets.The SBEM image volumes are available in the Cell Image Library (http://www.cellimagelibrary.org/home). The accession numbers are CIL:54606 (Or22a/ab3A-labeled volume); CIL:54614 (Or7a/ab4A-labeled volume); CIL:54610 (Or56a/ab4B-labeled volume); CIL:54611 (Ir75c/ac3AII-labeled volume); CIL:54612 (Or47a/ab5B-labeled volume); CIL:54607 and CIL:54608 (Or47b/at4A-labeled volumes); CIL:54609 (Or88a/at4C-labeled volume).

Article and author information

Author details

  1. Cesar Nava Gonzales

    University of California, San Diego, La Jolla, United States
    Competing interests
    The authors declare that no competing interests exist.
  2. Quintyn McKaughan

    University of California, San Diego, La Jolla, United States
    Competing interests
    The authors declare that no competing interests exist.
  3. Eric A Bushong

    University of California San Diego, La Jolla, United States
    Competing interests
    The authors declare that no competing interests exist.
  4. Kalyani Cauwenberghs

    University of California, San Diego, La Jolla, United States
    Competing interests
    The authors declare that no competing interests exist.
  5. Renny Ng

    University of California, San Diego, La Jolla, United States
    Competing interests
    The authors declare that no competing interests exist.
  6. Matthew Madany

    National Center for Microscopy and Imaging Research, University of California, San Diego, La Jolla, United States
    Competing interests
    The authors declare that no competing interests exist.
  7. Mark H Ellisman

    National Center for Microscopy and Imaging Research,, University of California, San Diego, Le Jolla, United States
    Competing interests
    The authors declare that no competing interests exist.
  8. Chih-Ying Su

    University of California, San Diego, La Jolla, United States
    For correspondence
    c8su@ucsd.edu
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-0005-1890

Funding

National Institute on Deafness and Other Communication Disorders (R01DC016466)

  • Chih-Ying Su

National Institute on Deafness and Other Communication Disorders (R01DC015519)

  • Chih-Ying Su

National Institute on Deafness and Other Communication Disorders (R21DC108912)

  • Chih-Ying Su

National Institute of Neurological Disorders and Stroke (U24NS120055)

  • Mark H Ellisman

National Institute of General Medical Sciences (R24GM137200)

  • Mark H Ellisman

National Institute of General Medical Sciences (R01GM082949)

  • Mark H Ellisman

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

Reviewing Editor

  1. Albert Cardona, University of Cambridge, United Kingdom

Version history

  1. Preprint posted: April 29, 2021 (view preprint)
  2. Received: April 29, 2021
  3. Accepted: August 20, 2021
  4. Accepted Manuscript published: August 23, 2021 (version 1)
  5. Version of Record published: September 1, 2021 (version 2)

Copyright

© 2021, Nava Gonzales 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. Cesar Nava Gonzales
  2. Quintyn McKaughan
  3. Eric A Bushong
  4. Kalyani Cauwenberghs
  5. Renny Ng
  6. Matthew Madany
  7. Mark H Ellisman
  8. Chih-Ying Su
(2021)
Systematic morphological and morphometric analysis of identified olfactory receptor neurons in Drosophila melanogaster
eLife 10:e69896.
https://doi.org/10.7554/eLife.69896

Share this article

https://doi.org/10.7554/eLife.69896

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