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Distinct interhemispheric connectivity at the level of the olfactory bulb emerges during Xenopus laevis metamorphosis

During metamorphosis, the olfactory system of anuran tadpoles undergoes substantial restructuring. The main olfactory epithelium in the principal nasal cavity of Xenopus laevis tadpoles is associated with aquatic olfaction and transformed into the adult air-nose, while a new adult water-nose emerges...

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Autores principales: Weiss, Lukas, Segoviano Arias, Paola, Offner, Thomas, Hawkins, Sara Joy, Hassenklöver, Thomas, Manzini, Ivan
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Springer Berlin Heidelberg 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8595194/
https://www.ncbi.nlm.nih.gov/pubmed/34580751
http://dx.doi.org/10.1007/s00441-021-03527-3
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author Weiss, Lukas
Segoviano Arias, Paola
Offner, Thomas
Hawkins, Sara Joy
Hassenklöver, Thomas
Manzini, Ivan
author_facet Weiss, Lukas
Segoviano Arias, Paola
Offner, Thomas
Hawkins, Sara Joy
Hassenklöver, Thomas
Manzini, Ivan
author_sort Weiss, Lukas
collection PubMed
description During metamorphosis, the olfactory system of anuran tadpoles undergoes substantial restructuring. The main olfactory epithelium in the principal nasal cavity of Xenopus laevis tadpoles is associated with aquatic olfaction and transformed into the adult air-nose, while a new adult water-nose emerges in the middle cavity. Impacts of this metamorphic remodeling on odor processing, behavior, and network structure are still unexplored. Here, we used neuronal tracings, calcium imaging, and behavioral experiments to examine the functional connectivity between the epithelium and the main olfactory bulb during metamorphosis. In tadpoles, olfactory receptor neurons in the principal cavity project axons to glomeruli in the ventral main olfactory bulb. These projections are gradually replaced by receptor neuron axons from the newly forming middle cavity epithelium. Despite this reorganization in the ventral bulb, two spatially segregated odor processing streams remain undisrupted and behavioral responses to waterborne odorants are unchanged. Contemporaneously, new receptor neurons in the remodeling principal cavity innervate the emerging dorsal part of the bulb, which displays distinct wiring features. Glomeruli around its midline are innervated from the left and right nasal epithelia. Additionally, postsynaptic projection neurons in the dorsal bulb predominantly connect to multiple glomeruli, while half of projection neurons in the ventral bulb are uni-glomerular. Our results show that the “water system” remains functional despite metamorphic reconstruction. The network differences between the dorsal and ventral olfactory bulb imply a higher degree of odor integration in the dorsal main olfactory bulb. This is possibly connected with the processing of different odorants, airborne vs. waterborne. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1007/s00441-021-03527-3.
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spelling pubmed-85951942021-11-24 Distinct interhemispheric connectivity at the level of the olfactory bulb emerges during Xenopus laevis metamorphosis Weiss, Lukas Segoviano Arias, Paola Offner, Thomas Hawkins, Sara Joy Hassenklöver, Thomas Manzini, Ivan Cell Tissue Res Regular Article During metamorphosis, the olfactory system of anuran tadpoles undergoes substantial restructuring. The main olfactory epithelium in the principal nasal cavity of Xenopus laevis tadpoles is associated with aquatic olfaction and transformed into the adult air-nose, while a new adult water-nose emerges in the middle cavity. Impacts of this metamorphic remodeling on odor processing, behavior, and network structure are still unexplored. Here, we used neuronal tracings, calcium imaging, and behavioral experiments to examine the functional connectivity between the epithelium and the main olfactory bulb during metamorphosis. In tadpoles, olfactory receptor neurons in the principal cavity project axons to glomeruli in the ventral main olfactory bulb. These projections are gradually replaced by receptor neuron axons from the newly forming middle cavity epithelium. Despite this reorganization in the ventral bulb, two spatially segregated odor processing streams remain undisrupted and behavioral responses to waterborne odorants are unchanged. Contemporaneously, new receptor neurons in the remodeling principal cavity innervate the emerging dorsal part of the bulb, which displays distinct wiring features. Glomeruli around its midline are innervated from the left and right nasal epithelia. Additionally, postsynaptic projection neurons in the dorsal bulb predominantly connect to multiple glomeruli, while half of projection neurons in the ventral bulb are uni-glomerular. Our results show that the “water system” remains functional despite metamorphic reconstruction. The network differences between the dorsal and ventral olfactory bulb imply a higher degree of odor integration in the dorsal main olfactory bulb. This is possibly connected with the processing of different odorants, airborne vs. waterborne. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1007/s00441-021-03527-3. Springer Berlin Heidelberg 2021-09-28 2021 /pmc/articles/PMC8595194/ /pubmed/34580751 http://dx.doi.org/10.1007/s00441-021-03527-3 Text en © The Author(s) 2021 https://creativecommons.org/licenses/by/4.0/Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) .
spellingShingle Regular Article
Weiss, Lukas
Segoviano Arias, Paola
Offner, Thomas
Hawkins, Sara Joy
Hassenklöver, Thomas
Manzini, Ivan
Distinct interhemispheric connectivity at the level of the olfactory bulb emerges during Xenopus laevis metamorphosis
title Distinct interhemispheric connectivity at the level of the olfactory bulb emerges during Xenopus laevis metamorphosis
title_full Distinct interhemispheric connectivity at the level of the olfactory bulb emerges during Xenopus laevis metamorphosis
title_fullStr Distinct interhemispheric connectivity at the level of the olfactory bulb emerges during Xenopus laevis metamorphosis
title_full_unstemmed Distinct interhemispheric connectivity at the level of the olfactory bulb emerges during Xenopus laevis metamorphosis
title_short Distinct interhemispheric connectivity at the level of the olfactory bulb emerges during Xenopus laevis metamorphosis
title_sort distinct interhemispheric connectivity at the level of the olfactory bulb emerges during xenopus laevis metamorphosis
topic Regular Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8595194/
https://www.ncbi.nlm.nih.gov/pubmed/34580751
http://dx.doi.org/10.1007/s00441-021-03527-3
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