Neuron-glia signaling in developing retina mediated by neurotransmitter spillover

  1. Juliana M Rosa
  2. Rémi Bos
  3. Georgeann S Sack
  4. Cécile Fortuny
  5. Amit Agarwal
  6. Dwight E Bergles
  7. John G Flannery
  8. Marla B Feller  Is a corresponding author
  1. University of California, Berkeley, United States
  2. Johns Hopkins School of Medicine, United States

Abstract

Neuron-glia interactions play a critical role in the maturation of neural circuits; however, little is known about the pathways that mediate their communication in the developing CNS. We investigated neuron-glia signaling in the developing retina, where we demonstrate that retinal waves reliably induce calcium transients in Müller glial cells (MCs). During cholinergic waves, MC calcium transients were blocked by muscarinic acetylcholine receptors antagonists, whereas during glutamatergic waves, MC calcium transients were inhibited by ionotropic glutamate receptor antagonists, indicating that the responsiveness of MCs changes to match the neurotransmitter used to support retinal waves. Using an optical glutamate sensor we show the decline in MC calcium transients is caused by a reduction in the amount of glutamate reaching MCs. Together, these studies indicate that neurons and MCs exhibit correlated activity during a critical period of retinal maturation that is enabled by neurotransmitter spillover from retinal synapses.

Article and author information

Author details

  1. Juliana M Rosa

    Department of Molecular and Cell Biology, University of California, Berkeley, Berkeley, United States
    Competing interests
    The authors declare that no competing interests exist.
  2. Rémi Bos

    Department of Molecular and Cell Biology, University of California, Berkeley, Berkeley, United States
    Competing interests
    The authors declare that no competing interests exist.
  3. Georgeann S Sack

    Department of Molecular and Cell Biology, University of California, Berkeley, Berkeley, United States
    Competing interests
    The authors declare that no competing interests exist.
  4. Cécile Fortuny

    Vision Science Graduate Program
, University of California, Berkeley, Berkeley, United States
    Competing interests
    The authors declare that no competing interests exist.
  5. Amit Agarwal

    Department of Neuroscience, Johns Hopkins School of Medicine, Baltimore, United States
    Competing interests
    The authors declare that no competing interests exist.
  6. Dwight E Bergles

    Department of Neuroscience, Johns Hopkins School of Medicine, Baltimore, United States
    Competing interests
    The authors declare that no competing interests exist.
  7. John G Flannery

    Department of Molecular and Cell Biology, University of California, Berkeley, Berkeley, United States
    Competing interests
    The authors declare that no competing interests exist.
  8. Marla B Feller

    Department of Molecular and Cell Biology, University of California, Berkeley, Berkeley, United States
    For correspondence
    mfeller@berkeley.edu
    Competing interests
    The authors declare that no competing interests exist.

Reviewing Editor

  1. Ben Barres, Stanford School of Medicine, United States

Version history

  1. Received: June 20, 2015
  2. Accepted: August 13, 2015
  3. Accepted Manuscript published: August 14, 2015 (version 1)
  4. Version of Record published: September 11, 2015 (version 2)

Copyright

© 2015, Rosa 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. Juliana M Rosa
  2. Rémi Bos
  3. Georgeann S Sack
  4. Cécile Fortuny
  5. Amit Agarwal
  6. Dwight E Bergles
  7. John G Flannery
  8. Marla B Feller
(2015)
Neuron-glia signaling in developing retina mediated by neurotransmitter spillover
eLife 4:e09590.
https://doi.org/10.7554/eLife.09590

Share this article

https://doi.org/10.7554/eLife.09590

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