Olfactory responses of Drosophila are encoded in the organization of projection neurons

  1. Kiri Choi  Is a corresponding author
  2. Won Kyu Kim  Is a corresponding author
  3. Changbong Hyeon  Is a corresponding author
  1. Korea Institute for Advanced Study, Republic of Korea

Abstract

The projection neurons (PNs), reconstructed from electron microscope (EM) images of the Drosophila olfactory system, offer a detailed view of neuronal anatomy, providing glimpses into information flow in the brain. About 150 uPNs constituting 58 glomeruli in the antennal lobe (AL) are bundled together in the axonal extension, routing the olfactory signal received at AL to mushroom body (MB) calyx and lateral horn (LH). Here we quantify the neuronal organization in terms of the inter-PN distances and examine its relationship with the odor types sensed by Drosophila. The homotypic uPNs that constitute glomeruli are tightly bundled and stereotyped in position throughout the neuropils, even though the glomerular PN organization in AL is no longer sustained in the higher brain center. Instead, odor-type dependent clusters consisting of multiple homotypes innervate the MB calyx and LH. Pheromone-encoding and hygro/thermo-sensing homotypes are spatially segregated in MB calyx, whereas two distinct clusters of food-related homotypes are found in LH in addition to the segregation of pheromone-encoding and hygro/thermo-sensing homotypes. We find that there are statistically significant associations between the spatial organization among a group of homotypic uPNs and certain stereotyped olfactory responses. Additionally, the signals from some of the tightly bundled homotypes converge to a specific group of lateral horn neurons (LHNs), which indicates that homotype (or odor type) specific integration of signals occurs at the synaptic interface between PNs and LHNs. Our findings suggest that before neural computation in the inner brain, some of the olfactory information are already encoded in the spatial organization of uPNs, illuminating that a certain degree of labeled-line strategy is at work in the Drosophila olfactory system.

Data availability

All data generated during this study and Python script are available in DrosophilaOlfaction-main.zip included as the supporting file. They are also available at https://github.com/kirichoi/DrosophilaOlfaction.

The following previously published data sets were used

Article and author information

Author details

  1. Kiri Choi

    School of Computational Sciences, Korea Institute for Advanced Study, Seoul, Republic of Korea
    For correspondence
    ckiri0315@kias.re.kr
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-0156-8410
  2. Won Kyu Kim

    School of Computational Sciences, Korea Institute for Advanced Study, Seoul, Republic of Korea
    For correspondence
    wonkyukim@kias.re.kr
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-6286-0925
  3. Changbong Hyeon

    School of Computational Sciences, Korea Institute for Advanced Study, Seoul, Republic of Korea
    For correspondence
    hyeoncb@kias.re.kr
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-4844-7237

Funding

KIAS individual grant (CG077001)

  • Kiri Choi

KIAS individual grant (CG076002)

  • Won Kyu Kim

KIAS individual grant (CG035003)

  • Changbong Hyeon

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

Reviewing Editor

  1. Sonia Sen, Tata Institute for Genetics and Society, India

Version history

  1. Received: February 9, 2022
  2. Preprint posted: February 25, 2022 (view preprint)
  3. Accepted: September 18, 2022
  4. Accepted Manuscript published: September 29, 2022 (version 1)
  5. Version of Record published: October 28, 2022 (version 2)

Copyright

© 2022, Choi 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. Kiri Choi
  2. Won Kyu Kim
  3. Changbong Hyeon
(2022)
Olfactory responses of Drosophila are encoded in the organization of projection neurons
eLife 11:e77748.
https://doi.org/10.7554/eLife.77748

Share this article

https://doi.org/10.7554/eLife.77748

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