Ciliomotor circuitry underlying whole-body coordination of ciliary activity in the Platynereis larva
Ciliated surfaces harbouring synchronously beating cilia can generate fluid flow or drive locomotion. In ciliary swimmers, ciliary beating, arrests, and changes in beat frequency are often coordinated across extended or discontinuous surfaces. To understand how such coordination is achieved, we stud...
| Main Authors: | , , , , , , |
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| Format: | Article |
| Language: | English |
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eLife Sciences Publications Ltd
2017-05-01
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| Series: | eLife |
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| Online Access: | https://elifesciences.org/articles/26000 |
| _version_ | 1811236918101278720 |
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| author | Csaba Verasztó Nobuo Ueda Luis A Bezares-Calderón Aurora Panzera Elizabeth A Williams Réza Shahidi Gáspár Jékely |
| author_facet | Csaba Verasztó Nobuo Ueda Luis A Bezares-Calderón Aurora Panzera Elizabeth A Williams Réza Shahidi Gáspár Jékely |
| author_sort | Csaba Verasztó |
| collection | DOAJ |
| description | Ciliated surfaces harbouring synchronously beating cilia can generate fluid flow or drive locomotion. In ciliary swimmers, ciliary beating, arrests, and changes in beat frequency are often coordinated across extended or discontinuous surfaces. To understand how such coordination is achieved, we studied the ciliated larvae of Platynereis dumerilii, a marine annelid. Platynereis larvae have segmental multiciliated cells that regularly display spontaneous coordinated ciliary arrests. We used whole-body connectomics, activity imaging, transgenesis, and neuron ablation to characterize the ciliomotor circuitry. We identified cholinergic, serotonergic, and catecholaminergic ciliomotor neurons. The synchronous rhythmic activation of cholinergic cells drives the coordinated arrests of all cilia. The serotonergic cells are active when cilia are beating. Serotonin inhibits the cholinergic rhythm, and increases ciliary beat frequency. Based on their connectivity and alternating activity, the catecholaminergic cells may generate the rhythm. The ciliomotor circuitry thus constitutes a stop-and-go pacemaker system for the whole-body coordination of ciliary locomotion. |
| first_indexed | 2024-04-12T12:16:23Z |
| format | Article |
| id | doaj.art-11094962dd5f436d98b1b751538b37fb |
| institution | Directory Open Access Journal |
| issn | 2050-084X |
| language | English |
| last_indexed | 2024-04-12T12:16:23Z |
| publishDate | 2017-05-01 |
| publisher | eLife Sciences Publications Ltd |
| record_format | Article |
| series | eLife |
| spelling | doaj.art-11094962dd5f436d98b1b751538b37fb2022-12-22T03:33:24ZengeLife Sciences Publications LtdeLife2050-084X2017-05-01610.7554/eLife.26000Ciliomotor circuitry underlying whole-body coordination of ciliary activity in the Platynereis larvaCsaba Verasztó0https://orcid.org/0000-0001-6295-7148Nobuo Ueda1Luis A Bezares-Calderón2https://orcid.org/0000-0001-6678-6876Aurora Panzera3Elizabeth A Williams4Réza Shahidi5Gáspár Jékely6https://orcid.org/0000-0001-8496-9836Max Planck Institute for Developmental Biology, Tübingen, GermanyMax Planck Institute for Developmental Biology, Tübingen, GermanyMax Planck Institute for Developmental Biology, Tübingen, GermanyMax Planck Institute for Developmental Biology, Tübingen, GermanyMax Planck Institute for Developmental Biology, Tübingen, GermanyMax Planck Institute for Developmental Biology, Tübingen, GermanyMax Planck Institute for Developmental Biology, Tübingen, GermanyCiliated surfaces harbouring synchronously beating cilia can generate fluid flow or drive locomotion. In ciliary swimmers, ciliary beating, arrests, and changes in beat frequency are often coordinated across extended or discontinuous surfaces. To understand how such coordination is achieved, we studied the ciliated larvae of Platynereis dumerilii, a marine annelid. Platynereis larvae have segmental multiciliated cells that regularly display spontaneous coordinated ciliary arrests. We used whole-body connectomics, activity imaging, transgenesis, and neuron ablation to characterize the ciliomotor circuitry. We identified cholinergic, serotonergic, and catecholaminergic ciliomotor neurons. The synchronous rhythmic activation of cholinergic cells drives the coordinated arrests of all cilia. The serotonergic cells are active when cilia are beating. Serotonin inhibits the cholinergic rhythm, and increases ciliary beat frequency. Based on their connectivity and alternating activity, the catecholaminergic cells may generate the rhythm. The ciliomotor circuitry thus constitutes a stop-and-go pacemaker system for the whole-body coordination of ciliary locomotion.https://elifesciences.org/articles/26000ciliary nerveserotoninzooplanktonconnectomicscatecholaminesacetylcholine |
| spellingShingle | Csaba Verasztó Nobuo Ueda Luis A Bezares-Calderón Aurora Panzera Elizabeth A Williams Réza Shahidi Gáspár Jékely Ciliomotor circuitry underlying whole-body coordination of ciliary activity in the Platynereis larva eLife ciliary nerve serotonin zooplankton connectomics catecholamines acetylcholine |
| title | Ciliomotor circuitry underlying whole-body coordination of ciliary activity in the Platynereis larva |
| title_full | Ciliomotor circuitry underlying whole-body coordination of ciliary activity in the Platynereis larva |
| title_fullStr | Ciliomotor circuitry underlying whole-body coordination of ciliary activity in the Platynereis larva |
| title_full_unstemmed | Ciliomotor circuitry underlying whole-body coordination of ciliary activity in the Platynereis larva |
| title_short | Ciliomotor circuitry underlying whole-body coordination of ciliary activity in the Platynereis larva |
| title_sort | ciliomotor circuitry underlying whole body coordination of ciliary activity in the platynereis larva |
| topic | ciliary nerve serotonin zooplankton connectomics catecholamines acetylcholine |
| url | https://elifesciences.org/articles/26000 |
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