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Mesencephalic origin of the inferior lobe in zebrafish

BACKGROUND: Although the overall brain organization is shared in vertebrates, there are significant differences within subregions among different groups, notably between Sarcopterygii (lobe-finned fish) and Actinopterygii (ray-finned fish). Recent comparative studies focusing on the ventricular morp...

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Autores principales: Bloch, Solal, Thomas, Manon, Colin, Ingrid, Galant, Sonya, Machado, Elodie, Affaticati, Pierre, Jenett, Arnim, Yamamoto, Kei
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2019
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6407210/
https://www.ncbi.nlm.nih.gov/pubmed/30849972
http://dx.doi.org/10.1186/s12915-019-0631-y
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author Bloch, Solal
Thomas, Manon
Colin, Ingrid
Galant, Sonya
Machado, Elodie
Affaticati, Pierre
Jenett, Arnim
Yamamoto, Kei
author_facet Bloch, Solal
Thomas, Manon
Colin, Ingrid
Galant, Sonya
Machado, Elodie
Affaticati, Pierre
Jenett, Arnim
Yamamoto, Kei
author_sort Bloch, Solal
collection PubMed
description BACKGROUND: Although the overall brain organization is shared in vertebrates, there are significant differences within subregions among different groups, notably between Sarcopterygii (lobe-finned fish) and Actinopterygii (ray-finned fish). Recent comparative studies focusing on the ventricular morphology have revealed a large diversity of the hypothalamus. Here, we study the development of the inferior lobe (IL), a prominent structure forming a bump on the ventral surface of the teleost brain. Based on its position, IL has been thought to be part of the hypothalamus (therefore forebrain). RESULTS: Taking advantage of genetic lineage-tracing techniques in zebrafish, we reveal that cells originating from her5-expressing progenitors in the midbrain-hindbrain boundary (MHB) participate in the formation of a large part of the IL. 3D visualization demonstrated how IL develops in relation to the ventricular system. We found that IL is constituted by two developmental components: the periventricular zone of hypothalamic origin and the external zone of mesencephalic origin. The mesencephalic external zone grows progressively until adulthood by adding new cells throughout development. CONCLUSION: Our results disprove a homology between the IL and the mammalian lateral hypothalamus. We suggest that the IL is likely to be involved in multimodal sensory integration rather than feeding motivation. The teleost brain is not a simpler version of the mammalian brain, and our study highlights the evolutionary plasticity of the brain which gives rise to novel structures. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (10.1186/s12915-019-0631-y) contains supplementary material, which is available to authorized users.
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spelling pubmed-64072102019-03-21 Mesencephalic origin of the inferior lobe in zebrafish Bloch, Solal Thomas, Manon Colin, Ingrid Galant, Sonya Machado, Elodie Affaticati, Pierre Jenett, Arnim Yamamoto, Kei BMC Biol Research Article BACKGROUND: Although the overall brain organization is shared in vertebrates, there are significant differences within subregions among different groups, notably between Sarcopterygii (lobe-finned fish) and Actinopterygii (ray-finned fish). Recent comparative studies focusing on the ventricular morphology have revealed a large diversity of the hypothalamus. Here, we study the development of the inferior lobe (IL), a prominent structure forming a bump on the ventral surface of the teleost brain. Based on its position, IL has been thought to be part of the hypothalamus (therefore forebrain). RESULTS: Taking advantage of genetic lineage-tracing techniques in zebrafish, we reveal that cells originating from her5-expressing progenitors in the midbrain-hindbrain boundary (MHB) participate in the formation of a large part of the IL. 3D visualization demonstrated how IL develops in relation to the ventricular system. We found that IL is constituted by two developmental components: the periventricular zone of hypothalamic origin and the external zone of mesencephalic origin. The mesencephalic external zone grows progressively until adulthood by adding new cells throughout development. CONCLUSION: Our results disprove a homology between the IL and the mammalian lateral hypothalamus. We suggest that the IL is likely to be involved in multimodal sensory integration rather than feeding motivation. The teleost brain is not a simpler version of the mammalian brain, and our study highlights the evolutionary plasticity of the brain which gives rise to novel structures. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (10.1186/s12915-019-0631-y) contains supplementary material, which is available to authorized users. BioMed Central 2019-03-08 /pmc/articles/PMC6407210/ /pubmed/30849972 http://dx.doi.org/10.1186/s12915-019-0631-y 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 Research Article
Bloch, Solal
Thomas, Manon
Colin, Ingrid
Galant, Sonya
Machado, Elodie
Affaticati, Pierre
Jenett, Arnim
Yamamoto, Kei
Mesencephalic origin of the inferior lobe in zebrafish
title Mesencephalic origin of the inferior lobe in zebrafish
title_full Mesencephalic origin of the inferior lobe in zebrafish
title_fullStr Mesencephalic origin of the inferior lobe in zebrafish
title_full_unstemmed Mesencephalic origin of the inferior lobe in zebrafish
title_short Mesencephalic origin of the inferior lobe in zebrafish
title_sort mesencephalic origin of the inferior lobe in zebrafish
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6407210/
https://www.ncbi.nlm.nih.gov/pubmed/30849972
http://dx.doi.org/10.1186/s12915-019-0631-y
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