The connectome of the adult Drosophila mushroom body provides insights into function

  1. Feng Li  Is a corresponding author
  2. Jack W Lindsey
  3. Elizabeth C Marin
  4. Nils Otto
  5. Marisa Dreher
  6. Georgia Dempsey
  7. Ildiko Stark
  8. Alexander S Bates
  9. Markus William Pleijzier
  10. Philipp Schlegel
  11. Aljoscha Nern
  12. Shin-ya Takemura
  13. Nils Eckstein
  14. Tansy Yang
  15. Audrey Francis
  16. Amalia Braun
  17. Ruchi Parekh
  18. Marta Costa
  19. Louis K Scheffer
  20. Yoshi Aso
  21. Gregory SXE Jefferis
  22. Larry F Abbott
  23. Ashok Litwin-Kumar
  24. Scott Waddell
  25. Gerald M Rubin  Is a corresponding author
  1. Howard Hughes Medical Institute, United States
  2. Columbia University, United States
  3. University of Cambridge, United Kingdom
  4. University of Oxford, United Kingdom
  5. MRC Laboratory of Molecular Biology, United Kingdom
  6. Cambridge University, United Kingdom

Abstract

Making inferences about the computations performed by neuronal circuits from synapse-level connectivity maps is an emerging opportunity in neuroscience. The mushroom body (MB) is well positioned for developing and testing such an approach due to its conserved neuronal architecture, recently completed dense connectome, and extensive prior experimental studies of its roles in learning, memory and activity regulation. Here we identify new components of the MB circuit in Drosophila, including extensive visual input and MB output neurons (MBONs) with direct connections to descending neurons. We find unexpected structure in sensory inputs, in the transfer of information about different sensory modalities to MBONs, and in the modulation of that transfer by dopaminergic neurons (DANs). We provide insights into the circuitry used to integrate MB outputs, connectivity between the MB and the central complex and inputs to DANs, including feedback from MBONs. Our results provide a foundation for further theoretical and experimental work.

Data availability

All the primary data used in this study is freely available through a public server (neuprint.janelia.org). All the underlying data behind that server is open source (CC-BY). There is no institutional resource for hosting connectome data. We commit to keeping this available for at least 10 years, and provide procedures where users can copy any or all of it to their own computer. Login is via any Google account; users who wish to remain anonymous can create a separate account for access purposes only.

Article and author information

Author details

  1. Feng Li

    Janelia Research Campus, Howard Hughes Medical Institute, Ashburn, United States
    For correspondence
    lif@janelia.hhmi.org
    Competing interests
    The authors declare that no competing interests exist.
  2. Jack W Lindsey

    Department of Neuroscience, Columbia 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:" 0000-0003-0930-7327
  3. Elizabeth C Marin

    Drosophila Connectomics Group, Department of Zoology, University of Cambridge, Cambridge, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-6333-0072
  4. Nils Otto

    Centre for Neural Circuits & Behaviour, University of Oxford, Oxford, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
  5. Marisa Dreher

    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:" 0000-0002-0041-9229
  6. Georgia Dempsey

    Drosophila Connectomics Group, Department of Zoology, University of Cambridge, Cambridge, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-1854-8336
  7. Ildiko Stark

    Drosophila Connectomics Group, Department of Zoology, University of Cambridge, Cambridge, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
  8. Alexander S Bates

    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:" 0000-0002-1195-0445
  9. Markus William Pleijzier

    Neurobiology Division, University of Cambridge, Cambridge, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-7297-4547
  10. Philipp Schlegel

    Division of Neurobiology, 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:" 0000-0002-5633-1314
  11. Aljoscha Nern

    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:" 0000-0002-3822-489X
  12. Shin-ya Takemura

    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:" 0000-0003-2400-6426
  13. Nils Eckstein

    Janelia Research Campus, Howard Hughes Medical Institute, Ashburn, United States
    Competing interests
    The authors declare that no competing interests exist.
  14. Tansy Yang

    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:" 0000-0003-1131-0410
  15. Audrey Francis

    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:" 0000-0003-1974-7174
  16. Amalia Braun

    Drosophila Connectomics Group, Department of Zoology, Cambridge University, Cambridge, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
  17. Ruchi Parekh

    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:" 0000-0002-8060-2807
  18. Marta Costa

    Department of Zoology, University of Cambridge, Cambridge, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-5948-3092
  19. Louis K Scheffer

    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:" 0000-0002-3289-6564
  20. Yoshi Aso

    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:" 0000-0002-2939-1688
  21. 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
  22. Larry F Abbott

    Department of Neuroscience, Columbia University, New York, United States
    Competing interests
    The authors declare that no competing interests exist.
  23. Ashok Litwin-Kumar

    Department of Neuroscience, Columbia 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:" 0000-0003-2422-6576
  24. Scott Waddell

    Centre for Neural Circuits & Behaviour, University of Oxford, Oxford, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-4503-6229
  25. Gerald M Rubin

    Janelia Research Campus, Howard Hughes Medical Institute, Ashburn, United States
    For correspondence
    rubing@janelia.hhmi.org
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-8762-8703

Funding

Howard Hughes Medical Institute (internal funding)

  • Marisa Dreher
  • Aljoscha Nern
  • Shin-ya Takemura
  • Nils Eckstein
  • Audrey Francis
  • Ruchi Parekh
  • Louis K Scheffer
  • Yoshi Aso
  • Gerald M Rubin

Wellcome Trust (203261/Z/16/Z)

  • Feng Li
  • Elizabeth C Marin
  • Nils Otto
  • Georgia Dempsey
  • Ildiko Stark
  • Philipp Schlegel
  • Tansy Yang
  • Amalia Braun
  • Marta Costa
  • Gregory SXE Jefferis
  • Scott Waddell
  • Gerald M Rubin

Wellcome Trust (200846/Z/16/Z)

  • Scott Waddell

National Science Foundation (NeuroNex DBI-1707398)

  • Jack W Lindsey
  • Larry F Abbott
  • Ashok Litwin-Kumar

Department of Energy (DE-SC0020347)

  • Jack W Lindsey

Medical Research Council (MC-U105188491)

  • Alexander S Bates
  • Markus William Pleijzier
  • Philipp Schlegel
  • Gregory SXE Jefferis

Simons Foundation (SCGB)

  • Jack W Lindsey
  • Yoshi Aso
  • Larry F Abbott
  • Ashok Litwin-Kumar
  • Gerald M Rubin

Burroughs Wellcome Fund (1017109)

  • Ashok Litwin-Kumar

National Institutes of Health (R01EB029858)

  • Ashok Litwin-Kumar

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

Reviewing Editor

  1. Leslie C Griffith, Brandeis University, United States

Version history

  1. Received: August 28, 2020
  2. Accepted: December 11, 2020
  3. Accepted Manuscript published: December 14, 2020 (version 1)
  4. Version of Record published: February 26, 2021 (version 2)

Copyright

© 2020, Li 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. Feng Li
  2. Jack W Lindsey
  3. Elizabeth C Marin
  4. Nils Otto
  5. Marisa Dreher
  6. Georgia Dempsey
  7. Ildiko Stark
  8. Alexander S Bates
  9. Markus William Pleijzier
  10. Philipp Schlegel
  11. Aljoscha Nern
  12. Shin-ya Takemura
  13. Nils Eckstein
  14. Tansy Yang
  15. Audrey Francis
  16. Amalia Braun
  17. Ruchi Parekh
  18. Marta Costa
  19. Louis K Scheffer
  20. Yoshi Aso
  21. Gregory SXE Jefferis
  22. Larry F Abbott
  23. Ashok Litwin-Kumar
  24. Scott Waddell
  25. Gerald M Rubin
(2020)
The connectome of the adult Drosophila mushroom body provides insights into function
eLife 9:e62576.
https://doi.org/10.7554/eLife.62576

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