Circuits for integrating learned and innate valences in the insect brain

  1. Claire Eschbach  Is a corresponding author
  2. Akira Fushiki
  3. Michael Winding
  4. Bruno Afonso
  5. Ingrid V Andrade
  6. Benjamin T Cocanougher
  7. Katharina Eichler
  8. Ruben Gepner
  9. Guangwei Si
  10. Javier Valdes-Aleman
  11. Richard D Fetter
  12. Marc Gershow
  13. Gregory SXE Jefferis
  14. Aravinthan DT Samuel
  15. James W Truman
  16. Albert Cardona  Is a corresponding author
  17. Marta Zlatic  Is a corresponding author
  1. University of Cambridge, United Kingdom
  2. Columbia University, Zuckerman Institute, United States
  3. Howard Hughes Medical Institute, United States
  4. University of Puerto Rico Medical Sciences Campus, Puerto Rico
  5. New York University, United States
  6. Harvard University, United States
  7. University of California, United States
  8. MRC Laboratory of Molecular Biology, United Kingdom

Abstract

Animal behavior is shaped both by evolution and by individual experience. Parallel brain pathways encode innate and learned valences of cues, but the way in which they are integrated during action-selection is not well understood. We used electron microscopy to comprehensively map with synaptic resolution all neurons downstream of all Mushroom Body output neurons (encoding learned valences) and characterized their patterns of interaction with Lateral Horn neurons (encoding innate valences) in Drosophila larva. The connectome revealed multiple convergence neuron types that receive convergent Mushroom Body and Lateral Horn inputs. A subset of these receives excitatory input from positive-valence MB and LH pathways and inhibitory input from negative-valence MB pathways. We confirmed functional connectivity from LH and MB pathways and behavioral roles of two of these neurons. These neurons encode integrated odor value and bidirectionally regulate turning. Based on this we speculate that learning could potentially skew the balance of excitation and inhibition onto these neurons and thereby modulate turning. Together, our study provides insights into the circuits that integrate learned and innate to modify behavior.

Data availability

All data generated or analysed during this study are included in the manuscript and supporting files. Source data files are provided for Figures 2 to 6.

Article and author information

Author details

  1. Claire Eschbach

    Zoology, University of Cambridge, Cambridge, United Kingdom
    For correspondence
    ce394@cam.ac.uk
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-8092-3440
  2. Akira Fushiki

    Neuroscience, Columbia University, Zuckerman Institute, New York, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-7987-6405
  3. Michael Winding

    Zoology, University of Cambridge, Cambridge, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
  4. Bruno Afonso

    Janelia Research Campus, Howard Hughes Medical Institute, Ashburn, United States
    Competing interests
    The authors declare that no competing interests exist.
  5. Ingrid V Andrade

    Janelia Research Campus, Howard Hughes Medical Institute, Ashburn, United States
    Competing interests
    The authors declare that no competing interests exist.
  6. Benjamin T Cocanougher

    Janelia Research Campus, Howard Hughes Medical Institute, Ashburn, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-0648-554X
  7. Katharina Eichler

    Institute of Neurobiology, University of Puerto Rico Medical Sciences Campus, San Juan, Puerto Rico
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-7833-8621
  8. Ruben Gepner

    Department of Physics, New York University, New York, United States
    Competing interests
    The authors declare that no competing interests exist.
  9. Guangwei Si

    Department of Physics and Center for Brain Science, Harvard University, Cambridge, United States
    Competing interests
    The authors declare that no competing interests exist.
  10. Javier Valdes-Aleman

    Molecular Cell and Developmental Biology, University of California, Los Angeles, United States
    Competing interests
    The authors declare that no competing interests exist.
  11. Richard D Fetter

    Janelia Research Campus, Howard Hughes Medical Institute, Ashburn, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-1558-100X
  12. Marc Gershow

    Department of Physics, Center for Neural Science, Neuroscience Institute, New York University, New York, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-7528-6101
  13. Gregory SXE Jefferis

    Neurobiology Division, MRC Laboratory of Molecular Biology, Cambridge, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-0587-9355
  14. Aravinthan DT Samuel

    Physics, Harvard University, Cambridge, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-1672-8720
  15. James W Truman

    Janelia Research Campus, Howard Hughes Medical Institute, Ashburn, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-9209-5435
  16. Albert Cardona

    Department of Physiology, Development and Neuroscience, University of Cambridge, Cambridge, United Kingdom
    For correspondence
    ac2040@cam.ac.uk
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-4941-6536
  17. Marta Zlatic

    Neurobiology, MRC Laboratory of Molecular Biology, Cambridge, United Kingdom
    For correspondence
    mzlatic@mrc-lmb.cam.ac.uk
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-3149-2250

Funding

Howard Hughes Medical Institute

  • Claire Eschbach
  • Akira Fushiki
  • Michael Winding
  • Bruno Afonso
  • Ingrid V Andrade
  • Benjamin T Cocanougher
  • Javier Valdes-Aleman
  • James W Truman
  • Albert Cardona
  • Marta Zlatic

European Research Council (RG95162)

  • Claire Eschbach
  • Michael Winding
  • Marta Zlatic

Wellcome Trust (RG86459)

  • Marta Zlatic

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

Reviewing Editor

  1. K VijayRaghavan, National Centre for Biological Sciences, Tata Institute of Fundamental Research, India

Publication history

  1. Preprint posted: April 24, 2020 (view preprint)
  2. Received: September 30, 2020
  3. Accepted: November 3, 2021
  4. Accepted Manuscript published: November 10, 2021 (version 1)
  5. Accepted Manuscript updated: November 11, 2021 (version 2)
  6. Version of Record published: November 25, 2021 (version 3)

Copyright

© 2021, Eschbach 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. Claire Eschbach
  2. Akira Fushiki
  3. Michael Winding
  4. Bruno Afonso
  5. Ingrid V Andrade
  6. Benjamin T Cocanougher
  7. Katharina Eichler
  8. Ruben Gepner
  9. Guangwei Si
  10. Javier Valdes-Aleman
  11. Richard D Fetter
  12. Marc Gershow
  13. Gregory SXE Jefferis
  14. Aravinthan DT Samuel
  15. James W Truman
  16. Albert Cardona
  17. Marta Zlatic
(2021)
Circuits for integrating learned and innate valences in the insect brain
eLife 10:e62567.
https://doi.org/10.7554/eLife.62567

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