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Ancient origin of somatic and visceral neurons

BACKGROUND: A key to understanding the evolution of the nervous system on a large phylogenetic scale is the identification of homologous neuronal types. Here, we focus this search on the sensory and motor neurons of bilaterians, exploiting their well-defined molecular signatures in vertebrates. Sens...

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Autores principales: Nomaksteinsky, Marc, Kassabov, Stefan, Chettouh, Zoubida, Stoeklé, Henri-Corto, Bonnaud, Laure, Fortin, Gilles, Kandel, Eric R, Brunet, Jean-François
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2013
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3660236/
https://www.ncbi.nlm.nih.gov/pubmed/23631531
http://dx.doi.org/10.1186/1741-7007-11-53
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author Nomaksteinsky, Marc
Kassabov, Stefan
Chettouh, Zoubida
Stoeklé, Henri-Corto
Bonnaud, Laure
Fortin, Gilles
Kandel, Eric R
Brunet, Jean-François
author_facet Nomaksteinsky, Marc
Kassabov, Stefan
Chettouh, Zoubida
Stoeklé, Henri-Corto
Bonnaud, Laure
Fortin, Gilles
Kandel, Eric R
Brunet, Jean-François
author_sort Nomaksteinsky, Marc
collection PubMed
description BACKGROUND: A key to understanding the evolution of the nervous system on a large phylogenetic scale is the identification of homologous neuronal types. Here, we focus this search on the sensory and motor neurons of bilaterians, exploiting their well-defined molecular signatures in vertebrates. Sensorimotor circuits in vertebrates are of two types: somatic (that sense the environment and respond by shaping bodily motions) and visceral (that sense the interior milieu and respond by regulating vital functions). These circuits differ by a small set of largely dedicated transcriptional determinants: Brn3 is expressed in many somatic sensory neurons, first and second order (among which mechanoreceptors are uniquely marked by the Brn3+/Islet1+/Drgx+ signature), somatic motoneurons uniquely co-express Lhx3/4 and Mnx1, while the vast majority of neurons, sensory and motor, involved in respiration, blood circulation or digestion are molecularly defined by their expression and dependence on the pan-visceral determinant Phox2b. RESULTS: We explore the status of the sensorimotor transcriptional code of vertebrates in mollusks, a lophotrochozoa clade that provides a rich repertoire of physiologically identified neurons. In the gastropods Lymnaea stagnalis and Aplysia californica, we show that homologues of Brn3, Drgx, Islet1, Mnx1, Lhx3/4 and Phox2b differentially mark neurons with mechanoreceptive, locomotory and cardiorespiratory functions. Moreover, in the cephalopod Sepia officinalis, we show that Phox2 marks the stellate ganglion (in line with the respiratory — that is, visceral— ancestral role of the mantle, its target organ), while the anterior pedal ganglion, which controls the prehensile and locomotory arms, expresses Mnx. CONCLUSIONS: Despite considerable divergence in overall neural architecture, a molecular underpinning for the functional allocation of neurons to interactions with the environment or to homeostasis was inherited from the urbilaterian ancestor by contemporary protostomes and deuterostomes.
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spelling pubmed-36602362013-05-22 Ancient origin of somatic and visceral neurons Nomaksteinsky, Marc Kassabov, Stefan Chettouh, Zoubida Stoeklé, Henri-Corto Bonnaud, Laure Fortin, Gilles Kandel, Eric R Brunet, Jean-François BMC Biol Research Article BACKGROUND: A key to understanding the evolution of the nervous system on a large phylogenetic scale is the identification of homologous neuronal types. Here, we focus this search on the sensory and motor neurons of bilaterians, exploiting their well-defined molecular signatures in vertebrates. Sensorimotor circuits in vertebrates are of two types: somatic (that sense the environment and respond by shaping bodily motions) and visceral (that sense the interior milieu and respond by regulating vital functions). These circuits differ by a small set of largely dedicated transcriptional determinants: Brn3 is expressed in many somatic sensory neurons, first and second order (among which mechanoreceptors are uniquely marked by the Brn3+/Islet1+/Drgx+ signature), somatic motoneurons uniquely co-express Lhx3/4 and Mnx1, while the vast majority of neurons, sensory and motor, involved in respiration, blood circulation or digestion are molecularly defined by their expression and dependence on the pan-visceral determinant Phox2b. RESULTS: We explore the status of the sensorimotor transcriptional code of vertebrates in mollusks, a lophotrochozoa clade that provides a rich repertoire of physiologically identified neurons. In the gastropods Lymnaea stagnalis and Aplysia californica, we show that homologues of Brn3, Drgx, Islet1, Mnx1, Lhx3/4 and Phox2b differentially mark neurons with mechanoreceptive, locomotory and cardiorespiratory functions. Moreover, in the cephalopod Sepia officinalis, we show that Phox2 marks the stellate ganglion (in line with the respiratory — that is, visceral— ancestral role of the mantle, its target organ), while the anterior pedal ganglion, which controls the prehensile and locomotory arms, expresses Mnx. CONCLUSIONS: Despite considerable divergence in overall neural architecture, a molecular underpinning for the functional allocation of neurons to interactions with the environment or to homeostasis was inherited from the urbilaterian ancestor by contemporary protostomes and deuterostomes. BioMed Central 2013-04-30 /pmc/articles/PMC3660236/ /pubmed/23631531 http://dx.doi.org/10.1186/1741-7007-11-53 Text en Copyright © 2013 Nomaksteinsky et al.; licensee BioMed Central Ltd. http://creativecommons.org/licenses/by/2.0 This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/2.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.
spellingShingle Research Article
Nomaksteinsky, Marc
Kassabov, Stefan
Chettouh, Zoubida
Stoeklé, Henri-Corto
Bonnaud, Laure
Fortin, Gilles
Kandel, Eric R
Brunet, Jean-François
Ancient origin of somatic and visceral neurons
title Ancient origin of somatic and visceral neurons
title_full Ancient origin of somatic and visceral neurons
title_fullStr Ancient origin of somatic and visceral neurons
title_full_unstemmed Ancient origin of somatic and visceral neurons
title_short Ancient origin of somatic and visceral neurons
title_sort ancient origin of somatic and visceral neurons
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3660236/
https://www.ncbi.nlm.nih.gov/pubmed/23631531
http://dx.doi.org/10.1186/1741-7007-11-53
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