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

Publication 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.

Metrics

  • 879
    Page views
  • 272
    Downloads
  • 0
    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. 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

Further reading

    1. Cancer Biology
    2. Computational and Systems Biology
    Xiangkun Wu, Hong Yan ... Li Liang
    Research Article

    Colorectal cancer (CRC) remains a challenging and deadly disease with high tumor microenvironment (TME) heterogeneity. Using an integrative multi-omics analysis and artificial intelligence-enabled spatial analysis of whole-slide images, we performed a comprehensive characterization of TME in colorectal cancer (CCCRC). CRC samples were classified into four CCCRC subtypes with distinct TME features, namely, C1 as the proliferative subtype with low immunogenicity; C2 as the immunosuppressed subtype with the terminally exhausted immune characteristics; C3 as the immune-excluded subtype with the distinct upregulation of stromal components and a lack of T cell infiltration in the tumor core; and C4 as the immunomodulatory subtype with the remarkable upregulation of anti-tumor immune components. The four CCCRC subtypes had distinct histopathologic and molecular characteristics, therapeutic efficacy, and prognosis. We found that the C1 subtype may be suitable for chemotherapy and cetuximab, the C2 subtype may benefit from a combination of chemotherapy and bevacizumab, the C3 subtype has increased sensitivity to the WNT pathway inhibitor WIKI4, and the C4 subtype is a potential candidate for immune checkpoint blockade treatment. Importantly, we established a simple gene classifier for accurate identification of each CCCRC subtype. Collectively our integrative analysis ultimately established a holistic framework to thoroughly dissect the TME of CRC, and the CCCRC classification system with high biological interpretability may contribute to biomarker discovery and future clinical trial design.

    1. Computational and Systems Biology
    2. Neuroscience
    Bo Shen, Kenway Louie, Paul W Glimcher
    Research Article

    Inhibition is crucial for brain function, regulating network activity by balancing excitation and implementing gain control. Recent evidence suggests that beyond simply inhibiting excitatory activity, inhibitory neurons can also shape circuit function through disinhibition. While disinhibitory circuit motifs have been implicated in cognitive processes including learning, attentional selection, and input gating, the role of disinhibition is largely unexplored in the study of decision-making. Here, we show that disinhibition provides a simple circuit motif for fast, dynamic control of network state and function. This dynamic control allows a disinhibition-based decision model to reproduce both value normalization and winner-take-all dynamics, the two central features of neurobiological decision-making captured in separate existing models with distinct circuit motifs. In addition, the disinhibition model exhibits flexible attractor dynamics consistent with different forms of persistent activity seen in working memory. Fitting the model to empirical data shows it captures well both the neurophysiological dynamics of value coding and psychometric choice behavior. Furthermore, the biological basis of disinhibition provides a simple mechanism for flexible top-down control of the network states, enabling the circuit to capture diverse task-dependent neural dynamics. These results suggest a biologically plausible unifying mechanism for decision-making and emphasize the importance of local disinhibition in neural processing.