A visual pathway for skylight polarization processing in Drosophila

Abstract

Many insects use patterns of polarized light in the sky to orient and navigate. Here we functionally characterize neural circuitry in the fruit fly, Drosophila melanogaster, that conveys polarized light signals from the eye to the central complex, a brain region essential for the fly's sense of direction. Neurons tuned to the angle of polarization of ultraviolet light are found throughout the anterior visual pathway, connecting the optic lobes with the central complex via the anterior optic tubercle and bulb, in a homologous organization to the 'sky compass' pathways described in other insects. We detail how a consistent, map-like organization of neural tunings in the peripheral visual system is transformed into a reduced representation suited to flexible processing in the central brain. This study identifies computational motifs of the transformation, enabling mechanistic comparisons of multisensory integration and central processing for navigation in the brains of insects.

Data availability

The datasets and analysis code generated during this study are available at the Open Science Framework. doi.org/10.17605/osf.io/3tsd6

The following data sets were generated

Article and author information

Author details

  1. Ben J Hardcastle

    Department of Integrative Biology and Physiology, University of California, Los Angeles, Los Angeles, United States
    For correspondence
    hardcastle@ucla.edu
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-4819-5631
  2. Jaison J Omoto

    Department of Molecular, Cell, and Developmental Biology, University of California, Los Angeles, Los Angeles, United States
    Competing interests
    The authors declare that no competing interests exist.
  3. Pratyush Kandimalla

    Department of Molecular, Cell, and Developmental Biology, University of California, Los Angeles, Los Angeles, United States
    Competing interests
    The authors declare that no competing interests exist.
  4. Bao-Chau M Nguyen

    Department of Molecular, Cell, and Developmental Biology, University of California, Los Angeles, Los Angeles, United States
    Competing interests
    The authors declare that no competing interests exist.
  5. Mehmet F Keleş

    Department of Integrative Biology and Physiology, University of California, Los Angeles, Los Angeles, United States
    Competing interests
    The authors declare that no competing interests exist.
  6. Natalie K Boyd

    Department of Molecular, Cell, and Developmental Biology, University of California, Los Angeles, Los Angeles, United States
    Competing interests
    The authors declare that no competing interests exist.
  7. Volker Hartenstein

    Department of Molecular Cell and Developmental Biology, University of California, Los Angeles, Los Angeles, United States
    Competing interests
    The authors declare that no competing interests exist.
  8. Mark A Frye

    Department of Integrative Biology and Physiology, University of California, Los Angeles, Los Angeles, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-3277-3094

Funding

National Institutes of Health (R01-NS096290)

  • Volker Hartenstein

National Institutes of Health (R01-EY026031)

  • Mark A Frye

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

Reviewing Editor

  1. Claude Desplan, New York University, United States

Publication history

  1. Received: September 18, 2020
  2. Accepted: March 8, 2021
  3. Accepted Manuscript published: March 23, 2021 (version 1)
  4. Version of Record published: April 16, 2021 (version 2)
  5. Version of Record updated: April 30, 2021 (version 3)

Copyright

© 2021, Hardcastle 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. Ben J Hardcastle
  2. Jaison J Omoto
  3. Pratyush Kandimalla
  4. Bao-Chau M Nguyen
  5. Mehmet F Keleş
  6. Natalie K Boyd
  7. Volker Hartenstein
  8. Mark A Frye
(2021)
A visual pathway for skylight polarization processing in Drosophila
eLife 10:e63225.
https://doi.org/10.7554/eLife.63225
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