Cross-synaptic synchrony and transmission of signal and noise across the mouse retina

  1. William N Grimes
  2. Mrinalini Hoon
  3. Kevin L Briggman
  4. Rachel O Wong
  5. Fred Rieke  Is a corresponding author
  1. Howard Hughes Medical Institute, University of Washington, United States
  2. University of Washington, United States
  3. National Institute of Neurological Disorders and Stroke, United States

Abstract

Cross-synaptic synchrony-correlations in transmitter release across output synapses of a single neuron-is a key determinant of how signal and noise traverse neural circuits. The anatomical connectivity between rod bipolar and A17 amacrine cells in the mammalian retina-specifically that neighboring A17s often receive input from many of the same rod bipolar cells-provides a rare technical opportunity to measure cross-synaptic synchrony under physiological conditions. This approach reveals that synchronization of rod bipolar cell synapses is near perfect in the dark and decreases with increasing light level. Strong synaptic synchronization in the dark minimizes intrinsic synaptic noise and allows rod bipolar cells to faithfully transmit upstream signal and noise to downstream neurons. Desynchronization in steady light lowers the sensitivity of the rod bipolar output to upstream voltage fluctuations. This work reveals how cross-synaptic synchrony shapes retinal responses to physiological light inputs and, more generally, signaling in complex neural networks.

Article and author information

Author details

  1. William N Grimes

    Howard Hughes Medical Institute, University of Washington, Seattle, United States
    Competing interests
    The authors declare that no competing interests exist.
  2. Mrinalini Hoon

    University of Washington, Seattle, United States
    Competing interests
    The authors declare that no competing interests exist.
  3. Kevin L Briggman

    National Institute of Neurological Disorders and Stroke, Bethesda, United States
    Competing interests
    The authors declare that no competing interests exist.
  4. Rachel O Wong

    University of Washington, Seattle, United States
    Competing interests
    The authors declare that no competing interests exist.
  5. Fred Rieke

    Howard Hughes Medical Institute, University of Washington, Seattle, United States
    For correspondence
    rieke@u.washington.edu
    Competing interests
    The authors declare that no competing interests exist.

Ethics

Animal experimentation: This work was performed in strict accordance with the recommendations in the Guide for the Care and Use of Laboratory Animals of the National Institutes of Health. All procedures followed protocols approved by the Institutional Animal Care and Use Committee (protocol 3030-01) of the University of Washington.

Copyright

This is an open-access article, free of all copyright, and may be freely reproduced, distributed, transmitted, modified, built upon, or otherwise used by anyone for any lawful purpose. The work is made available under the Creative Commons CC0 public domain dedication.

Metrics

  • 2,177
    views
  • 235
    downloads
  • 32
    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. William N Grimes
  2. Mrinalini Hoon
  3. Kevin L Briggman
  4. Rachel O Wong
  5. Fred Rieke
(2014)
Cross-synaptic synchrony and transmission of signal and noise across the mouse retina
eLife 3:e03892.
https://doi.org/10.7554/eLife.03892

Share this article

https://doi.org/10.7554/eLife.03892

Further reading

    1. Neuroscience
    Franziska Auer, Katherine Nardone ... David Schoppik
    Research Article

    Cerebellar dysfunction leads to postural instability. Recent work in freely moving rodents has transformed investigations of cerebellar contributions to posture. However, the combined complexity of terrestrial locomotion and the rodent cerebellum motivate new approaches to perturb cerebellar function in simpler vertebrates. Here, we adapted a validated chemogenetic tool (TRPV1/capsaicin) to describe the role of Purkinje cells — the output neurons of the cerebellar cortex — as larval zebrafish swam freely in depth. We achieved both bidirectional control (activation and ablation) of Purkinje cells while performing quantitative high-throughput assessment of posture and locomotion. Activation modified postural control in the pitch (nose-up/nose-down) axis. Similarly, ablations disrupted pitch-axis posture and fin-body coordination responsible for climbs. Postural disruption was more widespread in older larvae, offering a window into emergent roles for the developing cerebellum in the control of posture. Finally, we found that activity in Purkinje cells could individually and collectively encode tilt direction, a key feature of postural control neurons. Our findings delineate an expected role for the cerebellum in postural control and vestibular sensation in larval zebrafish, establishing the validity of TRPV1/capsaicin-mediated perturbations in a simple, genetically tractable vertebrate. Moreover, by comparing the contributions of Purkinje cell ablations to posture in time, we uncover signatures of emerging cerebellar control of posture across early development. This work takes a major step towards understanding an ancestral role of the cerebellum in regulating postural maturation.

    1. Neuroscience
    Jacob A Miller
    Insight

    When navigating environments with changing rules, human brain circuits flexibly adapt how and where we retain information to help us achieve our immediate goals.