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Peripheral sensory neurons govern development of the nervous system in bivalve larvae

Recent findings regarding early lophotrochozoan development have altered the conventional model of neurogenesis and revealed that peripheral sensory elements play a key role in the initial organization of the larval nervous system. Here, we describe the main neurogenetic events in bivalve mollusks i...

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Autores principales: Yurchenko, Olga V., Savelieva, Anna V., Kolotuchina, Natalia K., Voronezhskaya, Elena E., Dyachuk, Vyacheslav A.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2019
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6743156/
https://www.ncbi.nlm.nih.gov/pubmed/31528326
http://dx.doi.org/10.1186/s13227-019-0133-6
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author Yurchenko, Olga V.
Savelieva, Anna V.
Kolotuchina, Natalia K.
Voronezhskaya, Elena E.
Dyachuk, Vyacheslav A.
author_facet Yurchenko, Olga V.
Savelieva, Anna V.
Kolotuchina, Natalia K.
Voronezhskaya, Elena E.
Dyachuk, Vyacheslav A.
author_sort Yurchenko, Olga V.
collection PubMed
description Recent findings regarding early lophotrochozoan development have altered the conventional model of neurogenesis and revealed that peripheral sensory elements play a key role in the initial organization of the larval nervous system. Here, we describe the main neurogenetic events in bivalve mollusks in comparison with other Lophotrochozoa, emphasizing a novel role for early neurons in establishing larval nervous systems and speculating about the morphogenetic function of the apical organ. We demonstrate that during bivalve development, peripheral sensory neurons utilizing various transmitters differentiate before the apical organ emerges. The first neurons and their neurites serve as a scaffold for the development of the nervous system. During veliger stage, cerebral, pleural, and visceral ganglia form along the lateral (visceral) nerve cords in anterior-to-posterior axis. The pedal ganglia and corresponding ventral (pedal) nerve cords develop much later, after larval settlement and metamorphosis. Pharmacological abolishment of the serotonin gradient within the larval body disrupts the navigation of “pioneer” axons resulting in malformation of the whole nervous system architecture. Comparative morphological data on neurogenetic events in bivalve mollusks shed new light on the origin of the nervous system, mechanisms of early axon navigation, and sequence of the tetraneurous nervous system formation. Furthermore, this information improves our understanding of the basic nervous system architecture in larval Bivalvia and Mollusca.
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spelling pubmed-67431562019-09-16 Peripheral sensory neurons govern development of the nervous system in bivalve larvae Yurchenko, Olga V. Savelieva, Anna V. Kolotuchina, Natalia K. Voronezhskaya, Elena E. Dyachuk, Vyacheslav A. EvoDevo Review Recent findings regarding early lophotrochozoan development have altered the conventional model of neurogenesis and revealed that peripheral sensory elements play a key role in the initial organization of the larval nervous system. Here, we describe the main neurogenetic events in bivalve mollusks in comparison with other Lophotrochozoa, emphasizing a novel role for early neurons in establishing larval nervous systems and speculating about the morphogenetic function of the apical organ. We demonstrate that during bivalve development, peripheral sensory neurons utilizing various transmitters differentiate before the apical organ emerges. The first neurons and their neurites serve as a scaffold for the development of the nervous system. During veliger stage, cerebral, pleural, and visceral ganglia form along the lateral (visceral) nerve cords in anterior-to-posterior axis. The pedal ganglia and corresponding ventral (pedal) nerve cords develop much later, after larval settlement and metamorphosis. Pharmacological abolishment of the serotonin gradient within the larval body disrupts the navigation of “pioneer” axons resulting in malformation of the whole nervous system architecture. Comparative morphological data on neurogenetic events in bivalve mollusks shed new light on the origin of the nervous system, mechanisms of early axon navigation, and sequence of the tetraneurous nervous system formation. Furthermore, this information improves our understanding of the basic nervous system architecture in larval Bivalvia and Mollusca. BioMed Central 2019-09-12 /pmc/articles/PMC6743156/ /pubmed/31528326 http://dx.doi.org/10.1186/s13227-019-0133-6 Text en © The Author(s) 2019 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 Review
Yurchenko, Olga V.
Savelieva, Anna V.
Kolotuchina, Natalia K.
Voronezhskaya, Elena E.
Dyachuk, Vyacheslav A.
Peripheral sensory neurons govern development of the nervous system in bivalve larvae
title Peripheral sensory neurons govern development of the nervous system in bivalve larvae
title_full Peripheral sensory neurons govern development of the nervous system in bivalve larvae
title_fullStr Peripheral sensory neurons govern development of the nervous system in bivalve larvae
title_full_unstemmed Peripheral sensory neurons govern development of the nervous system in bivalve larvae
title_short Peripheral sensory neurons govern development of the nervous system in bivalve larvae
title_sort peripheral sensory neurons govern development of the nervous system in bivalve larvae
topic Review
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6743156/
https://www.ncbi.nlm.nih.gov/pubmed/31528326
http://dx.doi.org/10.1186/s13227-019-0133-6
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