First-order visual interneurons distribute distinct contrast and luminance information across ON and OFF pathways to achieve stable behavior

Abstract

The accurate processing of contrast is the basis for all visually guided behaviors. Visual scenes with rapidly changing illumination challenge contrast computation because photoreceptor adaptation is not fast enough to compensate for such changes. Yet, human perception of contrast is stable even when the visual environment is quickly changing, suggesting rapid post receptor luminance gain control. Similarly, in the fruit fly Drosophila, such gain control leads to luminance invariant behavior for moving OFF stimuli. Here we show that behavioral responses to moving ON stimuli also utilize a luminance gain, and that ON-motion guided behavior depends on inputs from three first-order interneurons L1, L2 and L3. Each of these neurons encodes contrast and luminance differently and distributes information asymmetrically across both ON and OFF contrast-selective pathways. Behavioral responses to both ON and OFF stimuli rely on a luminance-based correction provided by L1 and L3, wherein L1 supports contrast computation linearly, and L3 non-linearly amplifies dim stimuli. Therefore, L1, L2 and L3 are not specific inputs to ON and OFF pathways but the lamina serves as a separate processing layer that distributes distinct luminance and contrast information across ON and OFF pathways to support behavior in varying conditions.

Data availability

Analysis code is available at https://github.com/silieslab/Ketkar-Gur-MolinaObando-etal2022, and source data can be found on Zenodo: https://doi.org/10.5281/zenodo.6335347.

The following data sets were generated

Article and author information

Author details

  1. Madhura D Ketkar

    Institute of Developmental Biology and Neurobiology, Johannes Gutenberg University of Mainz, Mainz, Germany
    Competing interests
    The authors declare that no competing interests exist.
  2. Burak Gür

    Institute of Developmental Biology and Neurobiology, Johannes Gutenberg University of Mainz, Mainz, Germany
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-8221-9767
  3. Sebastian Molina-Obando

    Institute of Developmental Biology and Neurobiology, Johannes Gutenberg University of Mainz, Mainz, Germany
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-1222-723X
  4. Maria Ioannidou

    Institute of Developmental Biology and Neurobiology, Johannes Gutenberg University of Mainz, Mainz, Germany
    Competing interests
    The authors declare that no competing interests exist.
  5. Carlotta Martelli

    Institute of Developmental Biology and Neurobiology, Johannes Gutenberg University of Mainz, Mainz, Germany
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-5663-6580
  6. Marion Silies

    Institute of Developmental Biology and Neurobiology, Johannes Gutenberg University of Mainz, Mainz, Germany
    For correspondence
    msilies@uni-mainz.de
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-2810-9828

Funding

European Commission (ERC Starting Grant,No 716512)

  • Marion Silies

Deutsche Forschungsgemeinschaft (CRC1080,project C06)

  • Marion Silies

Deutsche Forschungsgemeinschaft (MA 7804/2-1)

  • Carlotta Martelli

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

Reviewing Editor

  1. Damon A Clark, Yale University, United States

Version history

  1. Received: October 22, 2021
  2. Preprint posted: November 5, 2021 (view preprint)
  3. Accepted: March 3, 2022
  4. Accepted Manuscript published: March 9, 2022 (version 1)
  5. Version of Record published: March 30, 2022 (version 2)

Copyright

© 2022, Ketkar 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. Madhura D Ketkar
  2. Burak Gür
  3. Sebastian Molina-Obando
  4. Maria Ioannidou
  5. Carlotta Martelli
  6. Marion Silies
(2022)
First-order visual interneurons distribute distinct contrast and luminance information across ON and OFF pathways to achieve stable behavior
eLife 11:e74937.
https://doi.org/10.7554/eLife.74937

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https://doi.org/10.7554/eLife.74937

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