Abstract

A common CNS architecture is observed in all chordates, from vertebrates to basal chordates like the ascidian Ciona. Ciona stands apart among chordates in having a complete larval connectome. Starting with visuomotor circuits predicted by the Ciona connectome, we used expression maps of neurotransmitter use with behavioral assays to identify two parallel visuomotor circuits that are responsive to different components of visual stimuli. The first circuit is characterized by glutamatergic photoreceptors and responds to the direction of light. These photoreceptors project to cholinergic motor neurons, via two tiers of cholinergic interneurons. The second circuit responds to changes in ambient light and mediates an escape response. This circuit uses GABAergic photoreceptors which project to GABAergic interneurons, and then to cholinergic interneurons. Our observations on the behavior of larvae either treated with a GABA receptor antagonist or carrying a mutation that eliminates photoreceptors indicate the second circuit is disinhibitory.

Data availability

All data generated or analysed during this study are included in the manuscript and supporting files. Source data files have been provided for Figures 1, 2, 5 and 6.

Article and author information

Author details

  1. Matthew J Kourakis

    Neuroscience Research Institute, University of California, Santa Barbara, Santa Barbara, United States
    Competing interests
    The authors declare that no competing interests exist.
  2. Cezar Borba

    Department of Molecular, Cell and Developmental Biology, University of California, Santa Barbara, Santa Barbara, United States
    Competing interests
    The authors declare that no competing interests exist.
  3. Angela Zhang

    Department of Electrical and Computer Engineering, University of California, Santa Barbara, Santa Barbara, United States
    Competing interests
    The authors declare that no competing interests exist.
  4. Erin Newman-Smith

    Department of Molecular, Cell and Developmental Biology, University of California, Santa Barbara, Santa Barbara, United States
    Competing interests
    The authors declare that no competing interests exist.
  5. Priscilla Salas

    Department of Molecular, Cell and Developmental Biology, University of California, Santa Barbara, Santa Barbara, United States
    Competing interests
    The authors declare that no competing interests exist.
  6. B Manjunath

    Department of Electrical and Computer Engineering, University of California, Santa Barbara, Santa Barbara, United States
    Competing interests
    The authors declare that no competing interests exist.
  7. William C Smith

    Neuroscience Research Institute, University of California, Santa Barbara, Santa Barbara, United States
    For correspondence
    w_smith@ucsb.edu
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-6257-7695

Funding

National Institute of Neurological Disorders and Stroke (R01NS103774)

  • William C Smith

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

Reviewing Editor

  1. Oliver Hobert, Howard Hughes Medical Institute, Columbia University, United States

Version history

  1. Received: December 28, 2018
  2. Accepted: April 11, 2019
  3. Accepted Manuscript published: April 18, 2019 (version 1)
  4. Version of Record published: May 3, 2019 (version 2)

Copyright

© 2019, Kourakis 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. Matthew J Kourakis
  2. Cezar Borba
  3. Angela Zhang
  4. Erin Newman-Smith
  5. Priscilla Salas
  6. B Manjunath
  7. William C Smith
(2019)
Parallel visual circuitry in a basal chordate
eLife 8:e44753.
https://doi.org/10.7554/eLife.44753

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