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Neural architecture of Galathowenia oculata Zach, 1923 (Oweniidae, Annelida)

BACKGROUND: Oweniids are marine tubeworms burrowing in muddy sediments that in current phylogenies form an early branching lineage within Annelida. Little is known about their general morphology, in particular the nervous system. Here we provide an immunocytochemical investigation of the nervous sys...

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Autores principales: Rimskaya-Korsakova, Nadezhda N., Kristof, Alen, Malakhov, Vladimir V., Wanninger, Andreas
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2016
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4746771/
https://www.ncbi.nlm.nih.gov/pubmed/26862347
http://dx.doi.org/10.1186/s12983-016-0136-2
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author Rimskaya-Korsakova, Nadezhda N.
Kristof, Alen
Malakhov, Vladimir V.
Wanninger, Andreas
author_facet Rimskaya-Korsakova, Nadezhda N.
Kristof, Alen
Malakhov, Vladimir V.
Wanninger, Andreas
author_sort Rimskaya-Korsakova, Nadezhda N.
collection PubMed
description BACKGROUND: Oweniids are marine tubeworms burrowing in muddy sediments that in current phylogenies form an early branching lineage within Annelida. Little is known about their general morphology, in particular the nervous system. Here we provide an immunocytochemical investigation of the nervous system of Galathowenia oculata in order to discuss putative ancestral neuronal features in Oweniidae. RESULTS: Adult Galathowenia oculata have neither a supraesophageal ganglion nor ganglia associated with the ventral nerve cord. Instead, there is a dorsal brain commissure in the head collar that is engulfed by a cellular cortex. Accordingly, we herein term this neural structure “medullary brain commissure”. The anterior margin of the head collar exhibits numerous neurites that emerge from the brain commissure. The dorsolateral folds are innervated by the ventrolateral neurite bundles extending from the circumesophageal connectives. In the anterior uniramous and biramous segments immunoreactive somata are distributed evenly along the ventral nerve cord and arranged metamerically in the posterior-most short segments. One dorsal and two pairs of lateral neurite bundles extend longitudinally along the body. Numerous serially arranged circular neurite bundles were labeled in anteriormost long segments. Metameric arrangement of the circular neurite bundles stained against FMRFamide and acetylated α-tubulin is revealed in posterior short segments. For the first time immunoreactive somata arranged in clusters are reported within the pygidium in oweniids. CONCLUSIONS: Due to the lack of head appendages and a sedentary mode of life, G. oculata exhibits a single dorsal commissure (versus a brain with four commissures in most annelids). A “medullary brain commissure” is known so far only in Oweniidae and Echiura. Lack of ganglia and metamery in the ventral nerve cord of the anteriormost segments might be the result of the elongation of these segments. In the short posterior segments the metamery of immunoreactive somata and circular neurite bundles is conserved. We hypothesize that the unpaired ventral nerve cord in adult oweniids might be a result of an initially paired ventral nerve cord that fuses during development, a condition not uncommon within Annelida.
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spelling pubmed-47467712016-02-10 Neural architecture of Galathowenia oculata Zach, 1923 (Oweniidae, Annelida) Rimskaya-Korsakova, Nadezhda N. Kristof, Alen Malakhov, Vladimir V. Wanninger, Andreas Front Zool Research BACKGROUND: Oweniids are marine tubeworms burrowing in muddy sediments that in current phylogenies form an early branching lineage within Annelida. Little is known about their general morphology, in particular the nervous system. Here we provide an immunocytochemical investigation of the nervous system of Galathowenia oculata in order to discuss putative ancestral neuronal features in Oweniidae. RESULTS: Adult Galathowenia oculata have neither a supraesophageal ganglion nor ganglia associated with the ventral nerve cord. Instead, there is a dorsal brain commissure in the head collar that is engulfed by a cellular cortex. Accordingly, we herein term this neural structure “medullary brain commissure”. The anterior margin of the head collar exhibits numerous neurites that emerge from the brain commissure. The dorsolateral folds are innervated by the ventrolateral neurite bundles extending from the circumesophageal connectives. In the anterior uniramous and biramous segments immunoreactive somata are distributed evenly along the ventral nerve cord and arranged metamerically in the posterior-most short segments. One dorsal and two pairs of lateral neurite bundles extend longitudinally along the body. Numerous serially arranged circular neurite bundles were labeled in anteriormost long segments. Metameric arrangement of the circular neurite bundles stained against FMRFamide and acetylated α-tubulin is revealed in posterior short segments. For the first time immunoreactive somata arranged in clusters are reported within the pygidium in oweniids. CONCLUSIONS: Due to the lack of head appendages and a sedentary mode of life, G. oculata exhibits a single dorsal commissure (versus a brain with four commissures in most annelids). A “medullary brain commissure” is known so far only in Oweniidae and Echiura. Lack of ganglia and metamery in the ventral nerve cord of the anteriormost segments might be the result of the elongation of these segments. In the short posterior segments the metamery of immunoreactive somata and circular neurite bundles is conserved. We hypothesize that the unpaired ventral nerve cord in adult oweniids might be a result of an initially paired ventral nerve cord that fuses during development, a condition not uncommon within Annelida. BioMed Central 2016-02-08 /pmc/articles/PMC4746771/ /pubmed/26862347 http://dx.doi.org/10.1186/s12983-016-0136-2 Text en © Rimskaya-Korsakova et al. 2016 Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.
spellingShingle Research
Rimskaya-Korsakova, Nadezhda N.
Kristof, Alen
Malakhov, Vladimir V.
Wanninger, Andreas
Neural architecture of Galathowenia oculata Zach, 1923 (Oweniidae, Annelida)
title Neural architecture of Galathowenia oculata Zach, 1923 (Oweniidae, Annelida)
title_full Neural architecture of Galathowenia oculata Zach, 1923 (Oweniidae, Annelida)
title_fullStr Neural architecture of Galathowenia oculata Zach, 1923 (Oweniidae, Annelida)
title_full_unstemmed Neural architecture of Galathowenia oculata Zach, 1923 (Oweniidae, Annelida)
title_short Neural architecture of Galathowenia oculata Zach, 1923 (Oweniidae, Annelida)
title_sort neural architecture of galathowenia oculata zach, 1923 (oweniidae, annelida)
topic Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4746771/
https://www.ncbi.nlm.nih.gov/pubmed/26862347
http://dx.doi.org/10.1186/s12983-016-0136-2
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