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.

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.

Metrics

  • 1,497
    views
  • 164
    downloads
  • 17
    citations

Views, downloads and citations are aggregated across all versions of this paper published by eLife.

Download links

A two-part list of links to download the article, or parts of the article, in various formats.

Downloads (link to download the article as PDF)

Open citations (links to open the citations from this article in various online reference manager services)

Cite this article (links to download the citations from this article in formats compatible with various reference manager tools)

  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

Share this article

https://doi.org/10.7554/eLife.63355

Further reading

    1. Neuroscience
    Walter Senn, Dominik Dold ... Mihai A Petrovici
    Research Article

    One of the most fundamental laws of physics is the principle of least action. Motivated by its predictive power, we introduce a neuronal least-action principle for cortical processing of sensory streams to produce appropriate behavioral outputs in real time. The principle postulates that the voltage dynamics of cortical pyramidal neurons prospectively minimizes the local somato-dendritic mismatch error within individual neurons. For output neurons, the principle implies minimizing an instantaneous behavioral error. For deep network neurons, it implies the prospective firing to overcome integration delays and correct for possible output errors right in time. The neuron-specific errors are extracted in the apical dendrites of pyramidal neurons through a cortical microcircuit that tries to explain away the feedback from the periphery, and correct the trajectory on the fly. Any motor output is in a moving equilibrium with the sensory input and the motor feedback during the ongoing sensory-motor transform. Online synaptic plasticity reduces the somatodendritic mismatch error within each cortical neuron and performs gradient descent on the output cost at any moment in time. The neuronal least-action principle offers an axiomatic framework to derive local neuronal and synaptic laws for global real-time computation and learning in the brain.

    1. Cell Biology
    2. Neuroscience
    Josse Poppinga, Nolan J Barrett ... Jan RT van Weering
    Research Article

    Sorting nexin 4 (SNX4) is an evolutionary conserved organizer of membrane recycling. In neurons, SNX4 accumulates in synapses, but how SNX4 affects synapse function remains unknown. We generated a conditional SNX4 knock-out mouse model and report that SNX4 cKO synapses show enhanced neurotransmission during train stimulation, while the first evoked EPSC was normal. SNX4 depletion did not affect vesicle recycling, basic autophagic flux, or the levels and localization of SNARE-protein VAMP2/synaptobrevin-2. However, SNX4 depletion affected synapse ultrastructure: an increase in docked synaptic vesicles at the active zone, while the overall vesicle number was normal, and a decreased active zone length. These effects together lead to a substantially increased density of docked vesicles per release site. In conclusion, SNX4 is a negative regulator of synaptic vesicle docking and release. These findings suggest a role for SNX4 in synaptic vesicle recruitment at the active zone.