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Sensory cells and the organization of the peripheral nervous system of the siboglinid Oligobrachia haakonmosbiensis Smirnov, 2000

BACKGROUND: The nervous system of siboglinids has been studied mainly in Osedax and some Vestimentifera, while data in Frenulata – one of the four pogonophoran main branches – is still fragmentary. In most of the studies, the focus is almost always on the central nervous system, while the peripheral...

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Autores principales: Zaitseva, Olga V., Smirnov, Roman V., Starunova, Zinaida I., Vedenin, Andrey A., Starunov, Viktor V.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2022
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Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10127031/
https://www.ncbi.nlm.nih.gov/pubmed/37170298
http://dx.doi.org/10.1186/s40850-022-00114-z
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author Zaitseva, Olga V.
Smirnov, Roman V.
Starunova, Zinaida I.
Vedenin, Andrey A.
Starunov, Viktor V.
author_facet Zaitseva, Olga V.
Smirnov, Roman V.
Starunova, Zinaida I.
Vedenin, Andrey A.
Starunov, Viktor V.
author_sort Zaitseva, Olga V.
collection PubMed
description BACKGROUND: The nervous system of siboglinids has been studied mainly in Osedax and some Vestimentifera, while data in Frenulata – one of the four pogonophoran main branches – is still fragmentary. In most of the studies, the focus is almost always on the central nervous system, while the peripheral nervous system has traditionally received little attention. In contrast to other annelids, the structure and diversity of sensory structures in siboglinids are still quite undescribed. Meanwhile, the peripheral nervous system, as well as sensory elements, are extremely evolutionarily labile, and information about their organization is of high importance to understand lifestyles and behavior as well as main trends that lead siboglinids to their peculiar organization. RESULTS: The structure of the peripheric nervous system, sensory elements, and neuromuscular relationships of Oligobrachia haakonmosbiensis were studied using both scanning electron and confocal laser microscopy. A significant number of monociliary sensory cells, as well as sensory complexes located diffusely in the epithelium of the whole body were revealed. The latter include the cephalic tentacles, sensory cells accumulations along the dorsal furrow and ciliary band, areas of the openings of the tubiparous glands, and papillae. The oval ciliary spot located on the cephalic lobe at the base of the tentacles can also be regarded as a sensory organ. Most of the detected sensory cells show immunoreactivity to substance P and/or acetylated α-tubulin. FMRFamide- and serotonin-like immunoreactivity are manifested by neurons that mainly innervate tentacles, muscles, body wall epithelium, skin glands, tubiparous glands, and papillae. In the larva of O. haakonmosbiensis, monociliary sensory elements were revealed in the region of the apical organ, along the body, and on the pygidium. CONCLUSIONS: The diversity of sensory structures in O. haakonmosbiensis comprises epidermal solitary sensory cells, sensory spots around tubiparous glands openings, and putative sensory organs such as cephalic tentacles, an oval ciliary spot on the cephalic lobe, the dorsal furrow, and papillae. Sensory structures associated with papillae and tubiparous glands play presumable mechanosensory functions and are associated with regulation of tube building as well as anchorage of the worm inside the tube. Sensory structures of the dorsal furrow are presumably engaged in the regulation of reproductive behavior. An overall low level of morphological differentiation of O. haakonmosbiensis peripheral nervous system is not typical even for annelids with the intraepithelial nervous system. This can be considered as a plesiomorphic feature of its peripheral plexus’s organization, or as evidence for the neotenic origin of Siboglinidae. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s40850-022-00114-z.
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spelling pubmed-101270312023-04-26 Sensory cells and the organization of the peripheral nervous system of the siboglinid Oligobrachia haakonmosbiensis Smirnov, 2000 Zaitseva, Olga V. Smirnov, Roman V. Starunova, Zinaida I. Vedenin, Andrey A. Starunov, Viktor V. BMC Zool Research BACKGROUND: The nervous system of siboglinids has been studied mainly in Osedax and some Vestimentifera, while data in Frenulata – one of the four pogonophoran main branches – is still fragmentary. In most of the studies, the focus is almost always on the central nervous system, while the peripheral nervous system has traditionally received little attention. In contrast to other annelids, the structure and diversity of sensory structures in siboglinids are still quite undescribed. Meanwhile, the peripheral nervous system, as well as sensory elements, are extremely evolutionarily labile, and information about their organization is of high importance to understand lifestyles and behavior as well as main trends that lead siboglinids to their peculiar organization. RESULTS: The structure of the peripheric nervous system, sensory elements, and neuromuscular relationships of Oligobrachia haakonmosbiensis were studied using both scanning electron and confocal laser microscopy. A significant number of monociliary sensory cells, as well as sensory complexes located diffusely in the epithelium of the whole body were revealed. The latter include the cephalic tentacles, sensory cells accumulations along the dorsal furrow and ciliary band, areas of the openings of the tubiparous glands, and papillae. The oval ciliary spot located on the cephalic lobe at the base of the tentacles can also be regarded as a sensory organ. Most of the detected sensory cells show immunoreactivity to substance P and/or acetylated α-tubulin. FMRFamide- and serotonin-like immunoreactivity are manifested by neurons that mainly innervate tentacles, muscles, body wall epithelium, skin glands, tubiparous glands, and papillae. In the larva of O. haakonmosbiensis, monociliary sensory elements were revealed in the region of the apical organ, along the body, and on the pygidium. CONCLUSIONS: The diversity of sensory structures in O. haakonmosbiensis comprises epidermal solitary sensory cells, sensory spots around tubiparous glands openings, and putative sensory organs such as cephalic tentacles, an oval ciliary spot on the cephalic lobe, the dorsal furrow, and papillae. Sensory structures associated with papillae and tubiparous glands play presumable mechanosensory functions and are associated with regulation of tube building as well as anchorage of the worm inside the tube. Sensory structures of the dorsal furrow are presumably engaged in the regulation of reproductive behavior. An overall low level of morphological differentiation of O. haakonmosbiensis peripheral nervous system is not typical even for annelids with the intraepithelial nervous system. This can be considered as a plesiomorphic feature of its peripheral plexus’s organization, or as evidence for the neotenic origin of Siboglinidae. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s40850-022-00114-z. BioMed Central 2022-03-29 /pmc/articles/PMC10127031/ /pubmed/37170298 http://dx.doi.org/10.1186/s40850-022-00114-z Text en © The Author(s) 2022 https://creativecommons.org/licenses/by/4.0/Open AccessThis article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) . The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/ (https://creativecommons.org/publicdomain/zero/1.0/) ) applies to the data made available in this article, unless otherwise stated in a credit line to the data.
spellingShingle Research
Zaitseva, Olga V.
Smirnov, Roman V.
Starunova, Zinaida I.
Vedenin, Andrey A.
Starunov, Viktor V.
Sensory cells and the organization of the peripheral nervous system of the siboglinid Oligobrachia haakonmosbiensis Smirnov, 2000
title Sensory cells and the organization of the peripheral nervous system of the siboglinid Oligobrachia haakonmosbiensis Smirnov, 2000
title_full Sensory cells and the organization of the peripheral nervous system of the siboglinid Oligobrachia haakonmosbiensis Smirnov, 2000
title_fullStr Sensory cells and the organization of the peripheral nervous system of the siboglinid Oligobrachia haakonmosbiensis Smirnov, 2000
title_full_unstemmed Sensory cells and the organization of the peripheral nervous system of the siboglinid Oligobrachia haakonmosbiensis Smirnov, 2000
title_short Sensory cells and the organization of the peripheral nervous system of the siboglinid Oligobrachia haakonmosbiensis Smirnov, 2000
title_sort sensory cells and the organization of the peripheral nervous system of the siboglinid oligobrachia haakonmosbiensis smirnov, 2000
topic Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10127031/
https://www.ncbi.nlm.nih.gov/pubmed/37170298
http://dx.doi.org/10.1186/s40850-022-00114-z
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