Neural circuit mechanisms for transforming learned olfactory valences into wind-oriented movement

  1. Yoshinori Aso  Is a corresponding author
  2. Daichi Yamada
  3. Daniel Bushey
  4. Karen L Hibbard
  5. Megan Sammons
  6. Hideo Otsuna
  7. Yichun Shuai
  8. Toshihide Hige  Is a corresponding author
  1. Janelia Research Campus, United States
  2. University of North Carolina at Chapel Hill, United States

Abstract

How memories are used by the brain to guide future action is poorly understood. In olfactory associative learning in Drosophila, multiple compartments of the mushroom body act in parallel to assign a valence to a stimulus. Here, we show that appetitive memories stored in different compartments induce different levels of upwind locomotion. Using a photoactivation screen of a new collection of split-GAL4 drivers and EM connectomics, we identified a cluster of neurons postsynaptic to the mushroom body output neurons (MBONs) that can trigger robust upwind steering. These UpWind Neurons (UpWiNs) integrate inhibitory and excitatory synaptic inputs from MBONs of appetitive and aversive memory compartments, respectively. After formation of appetitive memory, UpWiNs acquire enhanced response to reward-predicting odors as the response of the inhibitory presynaptic MBON undergoes depression. Blocking UpWiNs impaired appetitive memory and reduced upwind locomotion during retrieval. Photoactivation of UpWiNs also increased the chance of returning to a location where activation was terminated, suggesting an additional role in olfactory navigation. Thus, our results provide insight into how learned abstract valences are gradually transformed into concrete memory-driven actions through divergent and convergent networks, a neuronal architecture that is commonly found in the vertebrate and invertebrate brains.

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Author details

  1. Yoshinori Aso

    Janelia Research Campus, Ashburn, United States
    For correspondence
    asoy@janelia.hhmi.org
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-2939-1688
  2. Daichi Yamada

    Department of Biology, University of North Carolina at Chapel Hill, Chapel Hill, United States
    Competing interests
    The authors declare that no competing interests exist.
  3. Daniel Bushey

    Janelia Research Campus, Ashburn, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-9258-6579
  4. Karen L Hibbard

    Janelia Research Campus, Ashburn, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-2001-6099
  5. Megan Sammons

    Janelia Research Campus, Ashburn, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-4516-5928
  6. Hideo Otsuna

    Janelia Research Campus, Ashburn, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-2107-8881
  7. Yichun Shuai

    Janelia Research Campus, Ashburn, United States
    Competing interests
    The authors declare that no competing interests exist.
  8. Toshihide Hige

    Department of Biology, University of North Carolina at Chapel Hill, Chapel Hill, United States
    For correspondence
    hige@email.unc.edu
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-0007-3192

Funding

Howard Hughes Medical Institute

  • Yoshinori Aso

National Institutes of Health (R01DC018874)

  • Toshihide Hige

National Science Foundation (2034783)

  • Toshihide Hige

U.S-Israel Binational Science Foundation (2019026)

  • Toshihide Hige

UNC Junior Faculty Development Award

  • Toshihide Hige

Japan Society for the Promotion of Science (Overseas Research Fellowship)

  • Daichi Yamada

Toyobo Biotechnology Foundation (Postdoctoral Fellowship)

  • Daichi Yamada

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

Reviewing Editor

  1. Ilona C Grunwald Kadow, University of Bonn, Germany

Version history

  1. Received: December 22, 2022
  2. Accepted: September 7, 2023
  3. Accepted Manuscript published: September 18, 2023 (version 1)

Copyright

© 2023, Aso 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. Yoshinori Aso
  2. Daichi Yamada
  3. Daniel Bushey
  4. Karen L Hibbard
  5. Megan Sammons
  6. Hideo Otsuna
  7. Yichun Shuai
  8. Toshihide Hige
(2023)
Neural circuit mechanisms for transforming learned olfactory valences into wind-oriented movement
eLife 12:e85756.
https://doi.org/10.7554/eLife.85756

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