Cargando…
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...
Autores principales: | , , , |
---|---|
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 |
_version_ | 1783665611753127936 |
---|---|
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. |
format | Online Article Text |
id | pubmed-7963477 |
institution | National Center for Biotechnology Information |
language | English |
publishDate | 2021 |
publisher | eLife Sciences Publications, Ltd |
record_format | MEDLINE/PubMed |
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 |
work_keys_str_mv | AT chagnaudborisp gapjunctionmediatedglycinergicinhibitionensuresprecisetemporalpatterninginvocalbehavior AT perelmuterjonathant gapjunctionmediatedglycinergicinhibitionensuresprecisetemporalpatterninginvocalbehavior AT forlanopaulm gapjunctionmediatedglycinergicinhibitionensuresprecisetemporalpatterninginvocalbehavior AT bassandrewh gapjunctionmediatedglycinergicinhibitionensuresprecisetemporalpatterninginvocalbehavior |