Cargando…
Ontogenesis of the asymmetric parapineal organ in the zebrafish epithalamus
The parapineal organ is a midline-derived epithalamic structure that in zebrafish adopts a left-sided position at embryonic stages to promote the development of left-right asymmetries in the habenular nuclei. Despite extensive knowledge about its embryonic and larval development, it is still unknown...
Autores principales: | , , , , , , , |
---|---|
Formato: | Online Artículo Texto |
Lenguaje: | English |
Publicado: |
Frontiers Media S.A.
2022
|
Materias: | |
Acceso en línea: | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9780773/ https://www.ncbi.nlm.nih.gov/pubmed/36568973 http://dx.doi.org/10.3389/fcell.2022.999265 |
_version_ | 1784856911284273152 |
---|---|
author | Palma, Karina Signore, Iskra A. Meynard, Margarita M. Ibarra, Jazmin Armijo-Weingart, Lorena Cayuleo, Marcos Härtel, Steffen Concha, Miguel L. |
author_facet | Palma, Karina Signore, Iskra A. Meynard, Margarita M. Ibarra, Jazmin Armijo-Weingart, Lorena Cayuleo, Marcos Härtel, Steffen Concha, Miguel L. |
author_sort | Palma, Karina |
collection | PubMed |
description | The parapineal organ is a midline-derived epithalamic structure that in zebrafish adopts a left-sided position at embryonic stages to promote the development of left-right asymmetries in the habenular nuclei. Despite extensive knowledge about its embryonic and larval development, it is still unknown whether the parapineal organ and its profuse larval connectivity with the left habenula are present in the adult brain or whether, as assumed from historical conceptions, this organ degenerates during ontogeny. This paper addresses this question by performing an ontogenetic analysis using an integrative morphological, ultrastructural and neurochemical approach. We find that the parapineal organ is lost as a morphological entity during ontogeny, while parapineal cells are incorporated into the posterior wall of the adult left dorsal habenular nucleus as small clusters or as single cells. Despite this integration, parapineal cells retain their structural, neurochemical and connective features, establishing a reciprocal synaptic connection with the more dorsal habenular neuropil. Furthermore, we describe the ultrastructure of parapineal cells using transmission electron microscopy and report immunoreactivity in parapineal cells with antibodies against substance P, tachykinin, serotonin and the photoreceptor markers arrestin3a and rod opsin. Our findings suggest that parapineal cells form an integral part of a neural circuit associated with the left habenula, possibly acting as local modulators of the circuit. We argue that the incorporation of parapineal cells into the habenula may be part of an evolutionarily relevant developmental mechanism underlying the presence/absence of the parapineal organ in teleosts, and perhaps in a broader sense in vertebrates. |
format | Online Article Text |
id | pubmed-9780773 |
institution | National Center for Biotechnology Information |
language | English |
publishDate | 2022 |
publisher | Frontiers Media S.A. |
record_format | MEDLINE/PubMed |
spelling | pubmed-97807732022-12-24 Ontogenesis of the asymmetric parapineal organ in the zebrafish epithalamus Palma, Karina Signore, Iskra A. Meynard, Margarita M. Ibarra, Jazmin Armijo-Weingart, Lorena Cayuleo, Marcos Härtel, Steffen Concha, Miguel L. Front Cell Dev Biol Cell and Developmental Biology The parapineal organ is a midline-derived epithalamic structure that in zebrafish adopts a left-sided position at embryonic stages to promote the development of left-right asymmetries in the habenular nuclei. Despite extensive knowledge about its embryonic and larval development, it is still unknown whether the parapineal organ and its profuse larval connectivity with the left habenula are present in the adult brain or whether, as assumed from historical conceptions, this organ degenerates during ontogeny. This paper addresses this question by performing an ontogenetic analysis using an integrative morphological, ultrastructural and neurochemical approach. We find that the parapineal organ is lost as a morphological entity during ontogeny, while parapineal cells are incorporated into the posterior wall of the adult left dorsal habenular nucleus as small clusters or as single cells. Despite this integration, parapineal cells retain their structural, neurochemical and connective features, establishing a reciprocal synaptic connection with the more dorsal habenular neuropil. Furthermore, we describe the ultrastructure of parapineal cells using transmission electron microscopy and report immunoreactivity in parapineal cells with antibodies against substance P, tachykinin, serotonin and the photoreceptor markers arrestin3a and rod opsin. Our findings suggest that parapineal cells form an integral part of a neural circuit associated with the left habenula, possibly acting as local modulators of the circuit. We argue that the incorporation of parapineal cells into the habenula may be part of an evolutionarily relevant developmental mechanism underlying the presence/absence of the parapineal organ in teleosts, and perhaps in a broader sense in vertebrates. Frontiers Media S.A. 2022-12-09 /pmc/articles/PMC9780773/ /pubmed/36568973 http://dx.doi.org/10.3389/fcell.2022.999265 Text en Copyright © 2022 Palma, Signore, Meynard, Ibarra, Armijo-Weingart, Cayuleo, Härtel and Concha. https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms. |
spellingShingle | Cell and Developmental Biology Palma, Karina Signore, Iskra A. Meynard, Margarita M. Ibarra, Jazmin Armijo-Weingart, Lorena Cayuleo, Marcos Härtel, Steffen Concha, Miguel L. Ontogenesis of the asymmetric parapineal organ in the zebrafish epithalamus |
title | Ontogenesis of the asymmetric parapineal organ in the zebrafish epithalamus |
title_full | Ontogenesis of the asymmetric parapineal organ in the zebrafish epithalamus |
title_fullStr | Ontogenesis of the asymmetric parapineal organ in the zebrafish epithalamus |
title_full_unstemmed | Ontogenesis of the asymmetric parapineal organ in the zebrafish epithalamus |
title_short | Ontogenesis of the asymmetric parapineal organ in the zebrafish epithalamus |
title_sort | ontogenesis of the asymmetric parapineal organ in the zebrafish epithalamus |
topic | Cell and Developmental Biology |
url | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9780773/ https://www.ncbi.nlm.nih.gov/pubmed/36568973 http://dx.doi.org/10.3389/fcell.2022.999265 |
work_keys_str_mv | AT palmakarina ontogenesisoftheasymmetricparapinealorganinthezebrafishepithalamus AT signoreiskraa ontogenesisoftheasymmetricparapinealorganinthezebrafishepithalamus AT meynardmargaritam ontogenesisoftheasymmetricparapinealorganinthezebrafishepithalamus AT ibarrajazmin ontogenesisoftheasymmetricparapinealorganinthezebrafishepithalamus AT armijoweingartlorena ontogenesisoftheasymmetricparapinealorganinthezebrafishepithalamus AT cayuleomarcos ontogenesisoftheasymmetricparapinealorganinthezebrafishepithalamus AT hartelsteffen ontogenesisoftheasymmetricparapinealorganinthezebrafishepithalamus AT conchamiguell ontogenesisoftheasymmetricparapinealorganinthezebrafishepithalamus |