Most primary olfactory neurons have individually neutral effects on behavior

  1. Tayfun Tumkaya
  2. Safwan Burhanudin
  3. Asghar Khalilnezhad
  4. James Stewart
  5. Hyungwon Choi
  6. Adam Claridge-Chang  Is a corresponding author
  1. A*STAR, Singapore
  2. Duke-NUS Medical School, Singapore
  3. National University of Singapore, Singapore

Abstract

Animals use olfactory receptors to navigate mates, food, and danger. However, for complex olfactory systems, it is unknown what proportion of primary olfactory sensory neurons can individually drive avoidance or attraction. Similarly, the rules that govern behavioral responses to receptor combinations are unclear. We used optogenetic analysis in Drosophila to map the behavior elicited by olfactory-receptor neuron (ORN) classes: just one-fifth of ORN-types drove either avoidance or attraction. Although wind and hunger are closely linked to olfaction, neither had much effect on single-class responses. Several pooling rules have been invoked to explain how ORN types combine their behavioral influences; we activated two-way combinations and compared patterns of single- and double-ORN responses: these comparisons were inconsistent with simple pooling. We infer that the majority of primary olfactory sensory neurons have neutral behavioral effects individually, but participate in broad, odor-elicited ensembles with potent behavioral effects arising from complex interactions.

Data availability

Data and code availability:All of the data generated by this study are available to download from Zenodo (https://doi.org/10.5281/zenodo.3994033). The code is available at https://github.com/ttumkaya/WALiSuite_V2.0.

The following data sets were generated

Article and author information

Author details

  1. Tayfun Tumkaya

    Institute for Molecular and Cell Biology, A*STAR, Singapore, Singapore
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-8425-3360
  2. Safwan Burhanudin

    Institute for Molecular and Cell Biology, A*STAR, Singapore, Singapore
    Competing interests
    The authors declare that no competing interests exist.
  3. Asghar Khalilnezhad

    Institute for Molecular and Cell Biology, A*STAR, Singapore, Singapore
    Competing interests
    The authors declare that no competing interests exist.
  4. James Stewart

    Program in Neuroscience and Behavioral Disorders, Duke-NUS Medical School, Singapore, Singapore
    Competing interests
    The authors declare that no competing interests exist.
  5. Hyungwon Choi

    Department of Medicine, National University of Singapore, Singapore, Singapore
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-6687-3088
  6. Adam Claridge-Chang

    Program in Neuroscience and Behavioral Disorders, Duke-NUS Medical School, Singapore, Singapore
    For correspondence
    claridge-chang.adam@duke-nus.edu.sg
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-4583-3650

Funding

Agency for Science, Technology and Research (AGA-SINGA)

  • Tayfun Tumkaya

Agency for Science, Technology and Research (Block grant)

  • Tayfun Tumkaya
  • James Stewart
  • Hyungwon Choi
  • Adam Claridge-Chang

Ministry of Education - Singapore (MOE2013-T2-2-054)

  • Tayfun Tumkaya
  • James Stewart
  • Adam Claridge-Chang

Ministry of Education - Singapore (MOE2017-T2-1-089)

  • Tayfun Tumkaya
  • James Stewart
  • Adam Claridge-Chang

Ministry of Education - Singapore (MOE-2016-T2-1-001)

  • Hyungwon Choi

National Medical Research Council (NMRC-CG-2017-M009)

  • Hyungwon Choi

Duke-NUS Medical School (Block grant)

  • Adam Claridge-Chang

Agency for Science, Technology and Research (JCO-1231AFG030)

  • James Stewart
  • Adam Claridge-Chang

Agency for Science, Technology and Research (JCO-1431AFG120)

  • James Stewart
  • Adam Claridge-Chang

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. Preprint posted: June 10, 2021 (view preprint)
  2. Received: June 13, 2021
  3. Accepted: January 17, 2022
  4. Accepted Manuscript published: January 19, 2022 (version 1)
  5. Accepted Manuscript updated: January 21, 2022 (version 2)
  6. Version of Record published: February 1, 2022 (version 3)
  7. Version of Record updated: May 16, 2022 (version 4)

Copyright

© 2022, Tumkaya 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. Tayfun Tumkaya
  2. Safwan Burhanudin
  3. Asghar Khalilnezhad
  4. James Stewart
  5. Hyungwon Choi
  6. Adam Claridge-Chang
(2022)
Most primary olfactory neurons have individually neutral effects on behavior
eLife 11:e71238.
https://doi.org/10.7554/eLife.71238
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