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Gap junction-mediated glycinergic inhibition ensures precise temporal patterning in vocal behavior

Precise neuronal firing is especially important for behaviors highly dependent on the correct sequencing and timing of muscle activity patterns, such as acoustic signaling. Acoustic signaling is an important communication modality for vertebrates, including many teleost fishes. Toadfishes are well k...

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Autores principales: Chagnaud, Boris P, Perelmuter, Jonathan T, Forlano, Paul M, Bass, Andrew H
Formato: Online Artículo Texto
Lenguaje:English
Publicado: eLife Sciences Publications, Ltd 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7963477/
https://www.ncbi.nlm.nih.gov/pubmed/33721553
http://dx.doi.org/10.7554/eLife.59390
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author Chagnaud, Boris P
Perelmuter, Jonathan T
Forlano, Paul M
Bass, Andrew H
author_facet Chagnaud, Boris P
Perelmuter, Jonathan T
Forlano, Paul M
Bass, Andrew H
author_sort Chagnaud, Boris P
collection PubMed
description Precise neuronal firing is especially important for behaviors highly dependent on the correct sequencing and timing of muscle activity patterns, such as acoustic signaling. Acoustic signaling is an important communication modality for vertebrates, including many teleost fishes. Toadfishes are well known to exhibit high temporal fidelity in synchronous motoneuron firing within a hindbrain network directly determining the temporal structure of natural calls. Here, we investigated how these motoneurons maintain synchronous activation. We show that pronounced temporal precision in population-level motoneuronal firing depends on gap junction-mediated, glycinergic inhibition that generates a period of reduced probability of motoneuron activation. Super-resolution microscopy confirms glycinergic release sites formed by a subset of adjacent premotoneurons contacting motoneuron somata and dendrites. In aggregate, the evidence supports the hypothesis that gap junction-mediated, glycinergic inhibition provides a timing mechanism for achieving synchrony and temporal precision in the millisecond range for rapid modulation of acoustic waveforms.
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spelling pubmed-79634772021-03-17 Gap junction-mediated glycinergic inhibition ensures precise temporal patterning in vocal behavior Chagnaud, Boris P Perelmuter, Jonathan T Forlano, Paul M Bass, Andrew H eLife Neuroscience Precise neuronal firing is especially important for behaviors highly dependent on the correct sequencing and timing of muscle activity patterns, such as acoustic signaling. Acoustic signaling is an important communication modality for vertebrates, including many teleost fishes. Toadfishes are well known to exhibit high temporal fidelity in synchronous motoneuron firing within a hindbrain network directly determining the temporal structure of natural calls. Here, we investigated how these motoneurons maintain synchronous activation. We show that pronounced temporal precision in population-level motoneuronal firing depends on gap junction-mediated, glycinergic inhibition that generates a period of reduced probability of motoneuron activation. Super-resolution microscopy confirms glycinergic release sites formed by a subset of adjacent premotoneurons contacting motoneuron somata and dendrites. In aggregate, the evidence supports the hypothesis that gap junction-mediated, glycinergic inhibition provides a timing mechanism for achieving synchrony and temporal precision in the millisecond range for rapid modulation of acoustic waveforms. eLife Sciences Publications, Ltd 2021-03-15 /pmc/articles/PMC7963477/ /pubmed/33721553 http://dx.doi.org/10.7554/eLife.59390 Text en © 2021, Chagnaud et al http://creativecommons.org/licenses/by/4.0/ http://creativecommons.org/licenses/by/4.0/This article is distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use and redistribution provided that the original author and source are credited.
spellingShingle Neuroscience
Chagnaud, Boris P
Perelmuter, Jonathan T
Forlano, Paul M
Bass, Andrew H
Gap junction-mediated glycinergic inhibition ensures precise temporal patterning in vocal behavior
title Gap junction-mediated glycinergic inhibition ensures precise temporal patterning in vocal behavior
title_full Gap junction-mediated glycinergic inhibition ensures precise temporal patterning in vocal behavior
title_fullStr Gap junction-mediated glycinergic inhibition ensures precise temporal patterning in vocal behavior
title_full_unstemmed Gap junction-mediated glycinergic inhibition ensures precise temporal patterning in vocal behavior
title_short Gap junction-mediated glycinergic inhibition ensures precise temporal patterning in vocal behavior
title_sort gap junction-mediated glycinergic inhibition ensures precise temporal patterning in vocal behavior
topic Neuroscience
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7963477/
https://www.ncbi.nlm.nih.gov/pubmed/33721553
http://dx.doi.org/10.7554/eLife.59390
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