Distinct synaptic transfer functions in same-type photoreceptors

  1. Cornelius Schroeder  Is a corresponding author
  2. Jonathan Oesterle
  3. Philipp Berens
  4. Takeshi Yoshimatsu
  5. Tom Baden  Is a corresponding author
  1. University of Tuebingen, Germany
  2. University of Tübingen, Germany
  3. University of Sussex, United Kingdom

Abstract

Many sensory systems use ribbon-type synapses to transmit their signals to downstream circuits. The properties of this synaptic transfer fundamentally dictate which aspects in the original stimulus will be accentuated or suppressed, thereby partially defining the detection limits of the circuit. Accordingly, sensory neurons have evolved a wide variety of ribbon geometries and vesicle pool properties to best support their diverse functional requirements. However, the need for diverse synaptic functions does not only arise across neuron types, but also within. Here we show that UV-cones, a single type of photoreceptor of the larval zebrafish eye, exhibit striking differences in their synaptic ultrastructure and consequent calcium to glutamate transfer function depending on their location in the eye. We arrive at this conclusion by combining serial section electron microscopy and simultaneous 'dual-colour' 2-photon imaging of calcium and glutamate signals from the same synapse in vivo. We further use the functional dataset to fit a cascade-like model of the ribbon synapse with different vesicle pool sizes, transfer rates and other synaptic properties. Exploiting recent developments in simulation-based inference, we obtain full posterior estimates for the parameters and compare these across different retinal regions. The model enables us to extrapolate to new stimuli and to systematically investigate different response behaviours of various ribbon configurations. We also provide an interactive, easy-to-use version of this model as an online tool. Overall, we show that already on the synaptic level of single neuron types there exist highly specialized mechanisms which are advantageous for the encoding of different visual features.

Data availability

Data is deposited on Data-dryad under Schroder, Cornelius et al. (2021), Distinct Synaptic Transfer Functions in Same-Type Photoreceptors, Dryad, Dataset, https://doi.org/10.5061/dryad.7wm37pvt0.

The following data sets were generated

Article and author information

Author details

  1. Cornelius Schroeder

    Institute for Ophthalmic Research, University of Tuebingen, Tuebingen, Germany
    For correspondence
    c.schroeder@uni-tuebingen.de
    Competing interests
    The authors declare that no competing interests exist.
  2. Jonathan Oesterle

    Institute for Ophthalmic Research, University of Tübingen, Tübingen, Germany
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-8919-1445
  3. Philipp Berens

    Institute for Ophthalmic Research, University of Tübingen, Tübingen, Germany
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-0199-4727
  4. Takeshi Yoshimatsu

    School of Life Sciences, University of Sussex, Brighton, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
  5. Tom Baden

    School of Life Sciences, University of Sussex, Brighton, United Kingdom
    For correspondence
    t.baden@sussex.ac.uk
    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

Funding

Wellcome Trust (220277/Z/20/Z)

  • Tom Baden

European Research Council (677687)

  • Tom Baden

BBSRC (BB/R014817/1)

  • Tom Baden

German Ministry for Education and Research (01GQ1601,01IS18052C,01IS18039A)

  • Philipp Berens

German Research Foundation (BE5601/4-1,EXC 2064 - 390727645)

  • Philipp Berens

Leverhulme Trust (PLP-2017-005)

  • Tom Baden

Lister Institute for Preventive Medicine (Fellowship)

  • Tom Baden

Marie Curie Sklodowska Actions individual fellowship (748716)

  • Takeshi Yoshimatsu

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

Ethics

Animal experimentation: All procedures were performed in accordance with the UK Animals (Scientific Procedures) act 1986 and approved by the animal welfare committee of the University of Sussex. All licensed procedures (in vivo 2-photon imaging of live zebrafish larvae) are covered by the Project License PPL PE08A2AD2 (to TB).

Reviewing Editor

  1. Fred Rieke, University of Washington, United States

Publication history

  1. Preprint posted: February 24, 2021 (view preprint)
  2. Received: February 25, 2021
  3. Accepted: July 13, 2021
  4. Accepted Manuscript published: July 16, 2021 (version 1)
  5. Accepted Manuscript updated: July 21, 2021 (version 2)
  6. Version of Record published: July 28, 2021 (version 3)

Copyright

© 2021, Schroeder 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. Cornelius Schroeder
  2. Jonathan Oesterle
  3. Philipp Berens
  4. Takeshi Yoshimatsu
  5. Tom Baden
(2021)
Distinct synaptic transfer functions in same-type photoreceptors
eLife 10:e67851.
https://doi.org/10.7554/eLife.67851

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