Spherical arena reveals optokinetic response tuning to stimulus location, size, and frequency across entire visual field of larval zebrafish

  1. Florian Alexander Dehmelt
  2. Rebecca Meier
  3. Julian Hinz
  4. Takeshi Yoshimatsu
  5. Clara A Simacek
  6. Ruoyu Huang
  7. Kun Wang
  8. Tom Baden
  9. Aristides B Arrenberg  Is a corresponding author
  1. University of Tuebingen, Germany
  2. University of Sussex, UK, United Kingdom
  3. University of Sussex, United Kingdom

Abstract

Many animals have large visual fields, and sensory circuits may sample those regions of visual space most relevant to behaviours such as gaze stabilisation and hunting. Despite this, relatively small displays are often used in vision neuroscience. To sample stimulus locations across most of the visual field, we built a spherical stimulus arena with 14,848 independently controllable LEDs. We measured the optokinetic response gain of immobilised zebrafish larvae to stimuli of different steradian size and visual field locations. We find that the two eyes are less yoked than previously thought and that spatial frequency tuning is similar across visual field positions. However, zebrafish react most strongly to lateral, nearly equatorial stimuli, consistent with previously reported spatial densities of red, green and blue photoreceptors. Upside-down experiments suggest further extra-retinal processing. Our results demonstrate that motion vision circuits in zebrafish are anisotropic, and preferentially monitor areas with putative behavioural relevance.

Data availability

Analysis code, pre-processed data and examples of raw data have been deposited in GIN by G-Node and published under Digital Object Identifier 10.12751/g-node.qergnn

The following data sets were generated
The following previously published data sets were used

Article and author information

Author details

  1. Florian Alexander Dehmelt

    Werner Reichardt Centre for Integrative Neuroscience and Institute of Neurobiology, University of Tuebingen, Tuebingen, Germany
    Competing interests
    The authors declare that no competing interests exist.
  2. Rebecca Meier

    Werner Reichardt Centre for Integrative Neuroscience and Institute of Neurobiology, University of Tuebingen, Tuebingen, Germany
    Competing interests
    The authors declare that no competing interests exist.
  3. Julian Hinz

    Werner Reichardt Centre for Integrative Neuroscience and Institute of Neurobiology, University of Tuebingen, Tuebingen, Germany
    Competing interests
    The authors declare that no competing interests exist.
  4. Takeshi Yoshimatsu

    School of Life Sciences, University of Sussex, UK, Brighton, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
  5. Clara A Simacek

    Werner Reichardt Centre for Integrative Neuroscience and Institute of Neurobiology, University of Tuebingen, Tuebingen, Germany
    Competing interests
    The authors declare that no competing interests exist.
  6. Ruoyu Huang

    Werner Reichardt Centre for Integrative Neuroscience and Institute of Neurobiology, University of Tuebingen, Tuebingen, Germany
    Competing interests
    The authors declare that no competing interests exist.
  7. Kun Wang

    Werner Reichardt Centre for Integrative Neuroscience and Institute of Neurobiology, University of Tuebingen, Tuebingen, Germany
    Competing interests
    The authors declare that no competing interests exist.
  8. Tom Baden

    School of Life Sciences, University of Sussex, Brighton, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-2808-4210
  9. Aristides B Arrenberg

    Werner Reichardt Centre for Integrative Neuroscience and Institute of Neurobiology, University of Tuebingen, Tuebingen, Germany
    For correspondence
    aristides.arrenberg@uni-tuebingen.de
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-8262-7381

Funding

Deutsche Forschungsgemeinschaft (EXC307 (Werner-Reichardt-Centrum))

  • Aristides B Arrenberg

Human Frontier Science Program (Young Investigator Grant RGY0079)

  • Aristides B Arrenberg

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

Ethics

Animal experimentation: Animal experiments were performed in accordance with licenses granted by local government authorities (Regierungspräsidium Tübingen) in accordance with German federal law and Baden-Württemberg state law. Approval of this license followed consultation of both in-house animal welfare officers and an external ethics board appointed by the local government.

Reviewing Editor

  1. Kristin Tessmar-Raible, University of Vienna, Austria

Version history

  1. Received: September 22, 2020
  2. Accepted: June 7, 2021
  3. Accepted Manuscript published: June 8, 2021 (version 1)
  4. Version of Record published: June 25, 2021 (version 2)

Copyright

© 2021, Dehmelt 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. Florian Alexander Dehmelt
  2. Rebecca Meier
  3. Julian Hinz
  4. Takeshi Yoshimatsu
  5. Clara A Simacek
  6. Ruoyu Huang
  7. Kun Wang
  8. Tom Baden
  9. Aristides B Arrenberg
(2021)
Spherical arena reveals optokinetic response tuning to stimulus location, size, and frequency across entire visual field of larval zebrafish
eLife 10:e63355.
https://doi.org/10.7554/eLife.63355

Further reading

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    The functional complementarity of the vestibulo-ocular reflex (VOR) and optokinetic reflex (OKR) allows for optimal combined gaze stabilization responses (CGR) in light. While sensory substitution has been reported following complete vestibular loss, the capacity of the central vestibular system to compensate for partial peripheral vestibular loss remains to be determined. Here, we first demonstrate the efficacy of a 6-week subchronic ototoxic protocol in inducing transient and partial vestibular loss which equally affects the canal- and otolith-dependent VORs. Immunostaining of hair cells in the vestibular sensory epithelia revealed that organ-specific alteration of type I, but not type II, hair cells correlates with functional impairments. The decrease in VOR performance is paralleled with an increase in the gain of the OKR occurring in a specific range of frequencies where VOR normally dominates gaze stabilization, compatible with a sensory substitution process. Comparison of unimodal OKR or VOR versus bimodal CGR revealed that visuo-vestibular interactions remain reduced despite a significant recovery in the VOR. Modeling and sweep-based analysis revealed that the differential capacity to optimally combine OKR and VOR correlates with the reproducibility of the VOR responses. Overall, these results shed light on the multisensory reweighting occurring in pathologies with fluctuating peripheral vestibular malfunction.

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