Excitatory neurotransmission activates compartmentalized calcium transients in Müller glia without affecting lateral process motility

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Abstract

Neural activity has been implicated in the motility and outgrowth of glial cell processes throughout the central nervous system. Here we explore this phenomenon in Müller glia, which are specialized radial astroglia that are the predominant glial type of the vertebrate retina. Müller glia extend fine filopodia-like processes into retinal synaptic layers, in similar fashion to brain astrocytes and radial glia which exhibit perisynaptic processes. Using two-photon volumetric imaging, we found that during the second postnatal week, Müller glial processes were highly dynamic, with rapid extensions and retractions that were mediated by cytoskeletal rearrangements. During this same stage of development, retinal waves led to increases in cytosolic calcium within Müller glial lateral processes and stalks. These comprised distinct calcium compartments, distinguished by variable participation in waves, timing, and sensitivity to an M1 muscarinic acetylcholine receptor antagonist. However, we found that motility of lateral processes was unaffected by the presence of pharmacological agents that enhanced or blocked wave-associated calcium transients. Finally, we found that mice lacking normal cholinergic waves in the first postnatal week also exhibited normal Müller glial process morphology. Hence, outgrowth of Müller glial lateral processes into synaptic layers is determined by factors that are independent of neuronal activity.

Data availability

Source data for all figures is available and is uploaded to a linked Dryad repository as well as directly with this submission.

The following data sets were generated

(2021) Data from: Excitatory neurotransmission activates compartmentalized calcium transients in Müller glia without affecting lateral process motility
Dryad Digital Repository, doi:10.6078/d12d9f.

https://dx.doi.org/10.6078/d12d9f

Article and author information

Author details

Joshua M Tworig

Department of Molecular and Cell Biology, University of California, Berkeley, Berkeley, United States

Competing interests
No competing interests declared.
Chandler Coate

Department of Molecular and Cell Biology, University of California, Berkeley, Berkeley, United States

Competing interests
No competing interests declared.
Marla B Feller

Department of Molecular and Cell Biology, University of California, Berkeley, Berkeley, United States

For correspondence
mfeller@berkeley.edu

Competing interests
Marla B Feller, Reviewing editor, eLife.

"This ORCID iD identifies the author of this article:" 0000-0002-9137-5849

Funding

National Science Foundation (DGE 1752814)

Joshua M Tworig

National Institutes of Health (R01EY019498)

Joshua M Tworig
Marla B Feller

National Institutes of Health (R01EY013528)

Joshua M Tworig
Marla B Feller

National Eye Institute (P30EY003176)

Joshua M Tworig
Marla B Feller

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

Ethics

Animal experimentation: This study 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 of the animals were handled according to approved institutional animal care and use committee (IACUC) protocols of the University of California, Berkeley. The protocol was approved by the University of California Animal Care and Use Committee Office for Animal Care and Use (Protocol Number: AUP-2015-10-8080-1).

Copyright

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.