Abstract

Animals use spatial differences in environmental light levels for visual navigation; however, how light inputs are translated into coordinated motor outputs remains poorly understood. Here we reconstruct the neuronal connectome of a four-eye visual circuit in the larva of the annelid Platynereis using serial-section transmission electron microscopy. In this 71-neuron circuit, photoreceptors connect via three layers of interneurons to motorneurons, which innervate trunk muscles. By combining eye ablations with behavioral experiments, we show that the circuit compares light on either side of the body and stimulates body bending upon left-right light imbalance during visual phototaxis. We also identified an interneuron motif that enhances sensitivity to different light intensity contrasts. The Platynereis eye circuit has the hallmarks of a visual system, including spatial light detection and contrast modulation, illustrating how image-forming eyes may have evolved via intermediate stages contrasting only a light and a dark field during a simple visual task.

Article and author information

Author details

  1. Nadine Randel

    Max Planck Institute for Developmental Biology, Tübingen, Germany
    Competing interests
    The authors declare that no competing interests exist.
  2. Albina Asadulina

    Max Planck Institute for Developmental Biology, Tübingen, Germany
    Competing interests
    The authors declare that no competing interests exist.
  3. Luis A Bezares-Calderón

    Max Planck Institute for Developmental Biology, Tübingen, Germany
    Competing interests
    The authors declare that no competing interests exist.
  4. Csaba Verasztó

    Max Planck Institute for Developmental Biology, Tübingen, Germany
    Competing interests
    The authors declare that no competing interests exist.
  5. Elizabeth A Williams

    Max Planck Institute for Developmental Biology, Tübingen, Germany
    Competing interests
    The authors declare that no competing interests exist.
  6. Markus Conzelmann

    Max Planck Institute for Developmental Biology, Tübingen, Germany
    Competing interests
    The authors declare that no competing interests exist.
  7. Réza Shahidi

    Max Planck Institute for Developmental Biology, Tübingen, Germany
    Competing interests
    The authors declare that no competing interests exist.
  8. Gáspár Jékely

    Max Planck Institute for Developmental Biology, Tübingen, Germany
    For correspondence
    gaspar.jekely@tuebingen.mpg.de
    Competing interests
    The authors declare that no competing interests exist.

Ethics

Animal experimentation: This study only used invertebrate animals.

Copyright

© 2014, Randel 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. Nadine Randel
  2. Albina Asadulina
  3. Luis A Bezares-Calderón
  4. Csaba Verasztó
  5. Elizabeth A Williams
  6. Markus Conzelmann
  7. Réza Shahidi
  8. Gáspár Jékely
(2014)
Neuronal connectome of a sensory-motor circuit for visual navigation
eLife 3:e02730.
https://doi.org/10.7554/eLife.02730

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https://doi.org/10.7554/eLife.02730

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