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

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 fi...

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Main Authors: Joshua M Tworig, Chandler J Coate, Marla B Feller
Format: Article
Language:English
Published: eLife Sciences Publications Ltd 2021-12-01
Series:eLife
Subjects:
Online Access:https://elifesciences.org/articles/73202
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author Joshua M Tworig
Chandler J Coate
Marla B Feller
author_facet Joshua M Tworig
Chandler J Coate
Marla B Feller
author_sort Joshua M Tworig
collection DOAJ
description 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 that 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 regions 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.
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spelling doaj.art-e688afd306b94c618d29e5f39cfc96e22022-12-22T04:28:58ZengeLife Sciences Publications LtdeLife2050-084X2021-12-011010.7554/eLife.73202Excitatory neurotransmission activates compartmentalized calcium transients in Müller glia without affecting lateral process motilityJoshua M Tworig0https://orcid.org/0000-0001-7798-4480Chandler J Coate1Marla B Feller2https://orcid.org/0000-0002-9137-5849Department of Molecular and Cell Biology, University of California, Berkeley, Berkeley, United StatesDepartment of Molecular and Cell Biology, University of California, Berkeley, Berkeley, United StatesDepartment of Molecular and Cell Biology, University of California, Berkeley, Berkeley, United StatesNeural 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 that 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 regions 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.https://elifesciences.org/articles/73202retina developmentneuron-glia interactionstwo-photon calcium imagingglial morphologyspontaneous activity
spellingShingle Joshua M Tworig
Chandler J Coate
Marla B Feller
Excitatory neurotransmission activates compartmentalized calcium transients in Müller glia without affecting lateral process motility
eLife
retina development
neuron-glia interactions
two-photon calcium imaging
glial morphology
spontaneous activity
title Excitatory neurotransmission activates compartmentalized calcium transients in Müller glia without affecting lateral process motility
title_full Excitatory neurotransmission activates compartmentalized calcium transients in Müller glia without affecting lateral process motility
title_fullStr Excitatory neurotransmission activates compartmentalized calcium transients in Müller glia without affecting lateral process motility
title_full_unstemmed Excitatory neurotransmission activates compartmentalized calcium transients in Müller glia without affecting lateral process motility
title_short Excitatory neurotransmission activates compartmentalized calcium transients in Müller glia without affecting lateral process motility
title_sort excitatory neurotransmission activates compartmentalized calcium transients in muller glia without affecting lateral process motility
topic retina development
neuron-glia interactions
two-photon calcium imaging
glial morphology
spontaneous activity
url https://elifesciences.org/articles/73202
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AT chandlerjcoate excitatoryneurotransmissionactivatescompartmentalizedcalciumtransientsinmullergliawithoutaffectinglateralprocessmotility
AT marlabfeller excitatoryneurotransmissionactivatescompartmentalizedcalciumtransientsinmullergliawithoutaffectinglateralprocessmotility