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...
| Main Authors: | , , , |
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| Format: | Article |
| Language: | English |
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eLife Sciences Publications Ltd
2021-03-01
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| Series: | eLife |
| Subjects: | |
| Online Access: | https://elifesciences.org/articles/59390 |
| _version_ | 1818019848839495680 |
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| author | Boris P Chagnaud Jonathan T Perelmuter Paul M Forlano Andrew H Bass |
| author_facet | Boris P Chagnaud Jonathan T Perelmuter Paul M Forlano Andrew H Bass |
| author_sort | Boris P Chagnaud |
| collection | DOAJ |
| 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. |
| first_indexed | 2024-04-14T07:57:54Z |
| format | Article |
| id | doaj.art-ccd14a3276254249823ade32180c0e42 |
| institution | Directory Open Access Journal |
| issn | 2050-084X |
| language | English |
| last_indexed | 2024-04-14T07:57:54Z |
| publishDate | 2021-03-01 |
| publisher | eLife Sciences Publications Ltd |
| record_format | Article |
| series | eLife |
| spelling | doaj.art-ccd14a3276254249823ade32180c0e422022-12-22T02:05:00ZengeLife Sciences Publications LtdeLife2050-084X2021-03-011010.7554/eLife.59390Gap junction-mediated glycinergic inhibition ensures precise temporal patterning in vocal behaviorBoris P Chagnaud0https://orcid.org/0000-0001-5939-8541Jonathan T Perelmuter1https://orcid.org/0000-0001-9785-8211Paul M Forlano2https://orcid.org/0000-0003-4258-5708Andrew H Bass3https://orcid.org/0000-0002-0182-6715Institute of Biology, Karl-Franzens-University Graz, Graz, AustriaDepartment of Neurobiology and Behavior, Cornell University, Ithaca, NY, United StatesDepartment of Biology, Brooklyn College, City University of New York, Brooklyn, NY, United States; Subprograms in Behavioral and Cognitive Neuroscience, Neuroscience, and Ecology, Evolutionary Biology and Behavior, The Graduate Center, City University of New York, New York, NY, United StatesDepartment of Neurobiology and Behavior, Cornell University, Ithaca, NY, United StatesPrecise 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.https://elifesciences.org/articles/59390toadfishvocal systemopsanus betafeed-forwardnetworkinhibition |
| spellingShingle | Boris P Chagnaud Jonathan T Perelmuter Paul M Forlano Andrew H Bass Gap junction-mediated glycinergic inhibition ensures precise temporal patterning in vocal behavior eLife toadfish vocal system opsanus beta feed-forward network inhibition |
| 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 | toadfish vocal system opsanus beta feed-forward network inhibition |
| url | https://elifesciences.org/articles/59390 |
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