Synaptic targets of photoreceptors specialized to detect color and skylight polarization in Drosophila

Abstract

Color and polarization provide complementary information about the world and are detected by specialized photoreceptors. However, the downstream neural circuits that process these distinct modalities are incompletely understood in any animal. Using electron microscopy, we have systematically reconstructed the synaptic targets of the photoreceptors specialized to detect color and skylight polarization in Drosophila, and we have used light microscopy to confirm many of our findings. We identified known and novel downstream targets that are selective for different wavelengths or polarized light, and followed their projections to other areas in the optic lobes and the central brain. Our results revealed many synapses along the photoreceptor axons between brain regions, new pathways in the optic lobes, and spatially segregated projections to central brain regions. Strikingly, photoreceptors in the polarization-sensitive dorsal rim area target fewer cell types, and lack strong connections to the lobula, a neuropil involved in color processing. Our reconstruction identifies shared wiring and modality-specific specializations for color and polarization vision, and provides a comprehensive view of the first steps of the pathways processing color and polarized light inputs.

Data availability

All data generated or analyzed during this study are included in the manuscript and supporting files. Supplementary File 1 and 3 contain all connectivity data. Supplementary File 2 provides images of all EM skeletons.All code and necessary data to perform the analysis and generate the figures of this manuscript will be available from https://github.com/reiserlab.All reconstructed neurons described in the manuscript will be made available at https://fafb.catmaid.virtualflybrain.org/.

The following previously published data sets were used

Article and author information

Author details

  1. Emil Kind

    Instititut für Biologie, Freie Universität Berlin, Berlin, Germany
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-5228-7638
  2. Kit D Longden

    Janelia Research Campus, Howard Hughes Medical Institute, Ashburn, United States
    Competing interests
    The authors declare that no competing interests exist.
  3. 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
  4. Arthur Zhao

    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:" 0000-0003-2869-4393
  5. Gizem Sancer

    Institut für Biologie, Freie Universität Berlin, Berlin, Germany
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-0367-9421
  6. Miriam A Flynn

    Janelia Research Campus, Howard Hughes Medical Institute, Ashburn, United States
    Competing interests
    The authors declare that no competing interests exist.
  7. Connor W Laughland

    Janelia Research Campus, Howard Hughes Medical Institute, Ashburn, United States
    Competing interests
    The authors declare that no competing interests exist.
  8. Bruck Gezahegn

    Janelia Research Campus, Howard Hughes Medical Institute, Ashburn, United States
    Competing interests
    The authors declare that no competing interests exist.
  9. Henrique DF Ludwig

    Janelia Research Campus, Howard Hughes Medical Institute, Ashburn, United States
    Competing interests
    The authors declare that no competing interests exist.
  10. Alex G Thomson

    Janelia Research Campus, Howard Hughes Medical Institute, Ashburn, United States
    Competing interests
    The authors declare that no competing interests exist.
  11. Tessa Obrusnik

    Institut für Biologie, Freie Universität Berlin, Berlin, Germany
    Competing interests
    The authors declare that no competing interests exist.
  12. Paula G Alarcón

    Institut für Biologie, Freie Universität Berlin, Berlin, Germany
    Competing interests
    The authors declare that no competing interests exist.
  13. Heather Dionne

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

    Janelia Research Campus, Howard Hughes Medical Institute, Ashburn, United States
    Competing interests
    The authors declare that no competing interests exist.
  15. Gerald M Rubin

    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:" 0000-0001-8762-8703
  16. Michael B Reiser

    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:" 0000-0002-4108-4517
  17. Mathias F Wernet

    Institut für Biologie, Freie Universität Berlin, Berlin, Germany
    For correspondence
    mathias.wernet@fu-berlin.de
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-5233-2654

Funding

Howard Hughes Medical Institute

  • Kit D Longden
  • Aljoscha Nern
  • Arthur Zhao
  • Miriam A Flynn
  • Connor W Laughland
  • Bruck Gezahegn
  • Henrique DF Ludwig
  • Alex G Thomson
  • Heather Dionne
  • Davi D Bock
  • Gerald M Rubin
  • Michael B Reiser

Freie Universität Berlin

  • Emil Kind
  • Gizem Sancer
  • Tessa Obrusnik
  • Paula G Alarcón
  • Mathias F Wernet

Deutsche Forschungsgemeinschaft (WE 5761/2-1)

  • Mathias F Wernet

Deutsche Forschungsgemeinschaft (WE 5761/4-1)

  • Mathias F Wernet

Air Force Office of Scientific Research (FA9550-19-1-7005)

  • Mathias F Wernet

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

Reviewing Editor

  1. Ronald L Calabrese, Emory University, United States

Publication history

  1. Preprint posted: May 17, 2021 (view preprint)
  2. Received: July 1, 2021
  3. Accepted: December 15, 2021
  4. Accepted Manuscript published: December 16, 2021 (version 1)
  5. Accepted Manuscript updated: January 4, 2022 (version 2)
  6. Version of Record published: January 25, 2022 (version 3)

Copyright

© 2021, Kind 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. Emil Kind
  2. Kit D Longden
  3. Aljoscha Nern
  4. Arthur Zhao
  5. Gizem Sancer
  6. Miriam A Flynn
  7. Connor W Laughland
  8. Bruck Gezahegn
  9. Henrique DF Ludwig
  10. Alex G Thomson
  11. Tessa Obrusnik
  12. Paula G Alarcón
  13. Heather Dionne
  14. Davi D Bock
  15. Gerald M Rubin
  16. Michael B Reiser
  17. Mathias F Wernet
(2021)
Synaptic targets of photoreceptors specialized to detect color and skylight polarization in Drosophila
eLife 10:e71858.
https://doi.org/10.7554/eLife.71858
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