Properties of multi-vesicular release from mouse rod photoreceptors support transmission of single photon responses

  1. Cassandra L Hays
  2. Asia L Sladek
  3. Greg D Field  Is a corresponding author
  4. Wallace B Thoreson  Is a corresponding author
  1. University of Nebraska Medical Center, United States
  2. Duke University School of Medicine, United States

Abstract

Vision under starlight requires rod photoreceptors transduce and transmit single photon responses to the visual system. Small single photon voltage changes must therefore cause detectable reductions in glutamate release. We found that rods achieve this by employing mechanisms that enhance release regularity and its sensitivity to small voltage changes. At the resting membrane potential in darkness, mouse rods exhibit coordinated and regularly timed multivesicular release events, each consisting of ~17 vesicles and occurring 2-3 times more regularly than predicted by Poisson statistics. Hyperpolarizing rods to mimic the voltage change produced by a single photon abruptly reduced the probability of multivesicular release nearly to zero with a rebound increase at stimulus offset. Simulations of these release dynamics indicate that this regularly timed, multivesicular release promotes transmission of single photon responses to post-synaptic rod bipolar cells. Furthermore, the mechanism is efficient, requiring lower overall release rates than uniquantal release governed by Poisson statistics.

Data availability

All data generated or analyzed during this study are included in the manuscript and supporting file. Source data for Fig. 5B are provided.

Article and author information

Author details

  1. Cassandra L Hays

    Truhlsen Eye Institute, Department of Ophthalmology and Visual Sciences, University of Nebraska Medical Center, Omaha, United States
    Competing interests
    The authors declare that no competing interests exist.
  2. Asia L Sladek

    Truhlsen Eye Institute, Department of Ophthalmology and Visual Sciences, University of Nebraska Medical Center, Omaha, United States
    Competing interests
    The authors declare that no competing interests exist.
  3. Greg D Field

    Department of Neurobiology, Duke University School of Medicine, Durham, United States
    For correspondence
    field@neuro.duke.edu
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-5942-2679
  4. Wallace B Thoreson

    Truhlsen Eye Institute, Department of Ophthalmology and Visual Sciences, University of Nebraska Medical Center, Omaha, United States
    For correspondence
    wbthores@unmc.edu
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-7104-042X

Funding

National Eye Institute (EY10542)

  • Wallace B Thoreson

National Eye Institute (EY32396)

  • Wallace B Thoreson

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 handling protocols were approved by the University of Nebraska Medical Center Institutional Animal Care and Use Committee. Mice of both sexes aged 4-12 weeks were euthanized in accordance with AVMA Guidelines for the Euthanasia of Animals by CO2 asphyxiation followed by cervical dislocation (protocol 18-077-06).

Reviewing Editor

  1. Marla B Feller, University of California, Berkeley, United States

Publication history

  1. Received: February 11, 2021
  2. Accepted: March 20, 2021
  3. Accepted Manuscript published: March 26, 2021 (version 1)
  4. Version of Record published: April 8, 2021 (version 2)

Copyright

© 2021, Hays 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. Cassandra L Hays
  2. Asia L Sladek
  3. Greg D Field
  4. Wallace B Thoreson
(2021)
Properties of multi-vesicular release from mouse rod photoreceptors support transmission of single photon responses
eLife 10:e67446.
https://doi.org/10.7554/eLife.67446
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