Multi-glomerular projection of single olfactory receptor neurons is conserved among amphibians

Autores
Weiss, Lukas; Jungblut, Lucas David; Pozzi, Andrea Gabriela; Zielinski, Barbara S.; O'Connell, Lauren A.; Hassenklöver, Thomas; Manzini, Ivan
Año de publicación
2020
Idioma
inglés
Tipo de recurso
artículo
Estado
versión publicada
Descripción
Individual receptor neurons in the peripheral olfactory organ extend long axons into the olfactory bulb forming synapses with projection neurons in spherical neuropil regions, called glomeruli. Generally, odor map formation and odor processing in all vertebrates is based on the assumption that receptor neuron axons exclusively connect to a single glomerulus without any axonal branching. We comparatively tested this hypothesis in multiple fish and amphibian species (both sexes) by applying sparse cell electroporation to trace single olfactory receptor neuron axons. Sea lamprey (jawless fish) and zebrafish (bony fish) support the unbranched axon concept, with 94% of axons terminating in single glomeruli. Contrastingly, axonal projections of the axolotl (salamander) branch extensively before entering up to six distinct glomeruli. Receptor neuron axons labeled in frog species (Pipidae, Bufonidae, Hylidae, and Dendrobatidae) predominantly bifurcate before entering a glomerulus and 59 and 50% connect to multiple glomeruli in larval and postmetamorphotic animals, respectively. Independent of developmental stage, lifestyle, and adaptations to specific habitats, it seems to be a common feature of amphibian olfactory receptor neuron axons to frequently bifurcate and connect to multiple glomeruli. Our study challenges the unbranched axon concept as a universal vertebrate feature and it is conceivable that also later diverging vertebrates deviate from it. We propose that this unusual wiring logic evolved around the divergence of the terrestrial tetrapod lineage from its aquatic ancestors and could be the basis of an alternative way of odor processing.
Fil: Weiss, Lukas. Justus Liebig Universitat Giessen.; Alemania
Fil: Jungblut, Lucas David. Consejo Nacional de Investigaciones Científicas y Técnicas. Oficina de Coordinación Administrativa Ciudad Universitaria. Instituto de Biodiversidad y Biología Experimental y Aplicada. Universidad de Buenos Aires. Facultad de Ciencias Exactas y Naturales. Instituto de Biodiversidad y Biología Experimental y Aplicada; Argentina
Fil: Pozzi, Andrea Gabriela. Consejo Nacional de Investigaciones Científicas y Técnicas. Oficina de Coordinación Administrativa Ciudad Universitaria. Instituto de Biodiversidad y Biología Experimental y Aplicada. Universidad de Buenos Aires. Facultad de Ciencias Exactas y Naturales. Instituto de Biodiversidad y Biología Experimental y Aplicada; Argentina
Fil: Zielinski, Barbara S.. University Of Windsor; Canadá
Fil: O'Connell, Lauren A.. University of Stanford; Estados Unidos
Fil: Hassenklöver, Thomas. Justus Liebig Universitat Giessen.; Alemania
Fil: Manzini, Ivan. Justus Liebig Universitat Giessen.; Alemania
Materia
ANURA
AXONAL WIRING
EVOLUTION
FISHES
GLOMERULI
OLFACTION
SENSORY SYSTEM
Nivel de accesibilidad
acceso abierto
Condiciones de uso
https://creativecommons.org/licenses/by/2.5/ar/
Repositorio
CONICET Digital (CONICET)
Institución
Consejo Nacional de Investigaciones Científicas y Técnicas
OAI Identificador
oai:ri.conicet.gov.ar:11336/163613
Acceder
id CONICETDig_01d9ea8641709a78363d056db7b4b4b8
oai_identifier_str oai:ri.conicet.gov.ar:11336/163613
network_acronym_str CONICETDig
repository_id_str 3498
network_name_str CONICET Digital (CONICET)
spelling Multi-glomerular projection of single olfactory receptor neurons is conserved among amphibiansWeiss, LukasJungblut, Lucas DavidPozzi, Andrea GabrielaZielinski, Barbara S.O'Connell, Lauren A.Hassenklöver, ThomasManzini, IvanANURAAXONAL WIRINGEVOLUTIONFISHESGLOMERULIOLFACTIONSENSORY SYSTEMhttps://purl.org/becyt/ford/1.6https://purl.org/becyt/ford/1Individual receptor neurons in the peripheral olfactory organ extend long axons into the olfactory bulb forming synapses with projection neurons in spherical neuropil regions, called glomeruli. Generally, odor map formation and odor processing in all vertebrates is based on the assumption that receptor neuron axons exclusively connect to a single glomerulus without any axonal branching. We comparatively tested this hypothesis in multiple fish and amphibian species (both sexes) by applying sparse cell electroporation to trace single olfactory receptor neuron axons. Sea lamprey (jawless fish) and zebrafish (bony fish) support the unbranched axon concept, with 94% of axons terminating in single glomeruli. Contrastingly, axonal projections of the axolotl (salamander) branch extensively before entering up to six distinct glomeruli. Receptor neuron axons labeled in frog species (Pipidae, Bufonidae, Hylidae, and Dendrobatidae) predominantly bifurcate before entering a glomerulus and 59 and 50% connect to multiple glomeruli in larval and postmetamorphotic animals, respectively. Independent of developmental stage, lifestyle, and adaptations to specific habitats, it seems to be a common feature of amphibian olfactory receptor neuron axons to frequently bifurcate and connect to multiple glomeruli. Our study challenges the unbranched axon concept as a universal vertebrate feature and it is conceivable that also later diverging vertebrates deviate from it. We propose that this unusual wiring logic evolved around the divergence of the terrestrial tetrapod lineage from its aquatic ancestors and could be the basis of an alternative way of odor processing.Fil: Weiss, Lukas. Justus Liebig Universitat Giessen.; AlemaniaFil: Jungblut, Lucas David. Consejo Nacional de Investigaciones Científicas y Técnicas. Oficina de Coordinación Administrativa Ciudad Universitaria. Instituto de Biodiversidad y Biología Experimental y Aplicada. Universidad de Buenos Aires. Facultad de Ciencias Exactas y Naturales. Instituto de Biodiversidad y Biología Experimental y Aplicada; ArgentinaFil: Pozzi, Andrea Gabriela. Consejo Nacional de Investigaciones Científicas y Técnicas. Oficina de Coordinación Administrativa Ciudad Universitaria. Instituto de Biodiversidad y Biología Experimental y Aplicada. Universidad de Buenos Aires. Facultad de Ciencias Exactas y Naturales. Instituto de Biodiversidad y Biología Experimental y Aplicada; ArgentinaFil: Zielinski, Barbara S.. University Of Windsor; CanadáFil: O'Connell, Lauren A.. University of Stanford; Estados UnidosFil: Hassenklöver, Thomas. Justus Liebig Universitat Giessen.; AlemaniaFil: Manzini, Ivan. Justus Liebig Universitat Giessen.; AlemaniaWiley-liss, div John Wiley & Sons Inc.2020-02info:eu-repo/semantics/articleinfo:eu-repo/semantics/publishedVersionhttp://purl.org/coar/resource_type/c_6501info:ar-repo/semantics/articuloapplication/pdfapplication/pdfhttp://hdl.handle.net/11336/163613Weiss, Lukas; Jungblut, Lucas David; Pozzi, Andrea Gabriela; Zielinski, Barbara S.; O'Connell, Lauren A.; et al.; Multi-glomerular projection of single olfactory receptor neurons is conserved among amphibians; Wiley-liss, div John Wiley & Sons Inc.; Journal Of Comparative Neurology; 528; 13; 2-2020; 2239-22530021-9967CONICET DigitalCONICETenginfo:eu-repo/semantics/altIdentifier/doi/10.1002/cne.24887info:eu-repo/semantics/openAccesshttps://creativecommons.org/licenses/by/2.5/ar/reponame:CONICET Digital (CONICET)instname:Consejo Nacional de Investigaciones Científicas y Técnicas2025-09-10T13:16:37Zoai:ri.conicet.gov.ar:11336/163613instacron:CONICETInstitucionalhttp://ri.conicet.gov.ar/Organismo científico-tecnológicoNo correspondehttp://ri.conicet.gov.ar/oai/requestdasensio@conicet.gov.ar; lcarlino@conicet.gov.arArgentinaNo correspondeNo correspondeNo correspondeopendoar:34982025-09-10 13:16:38.141CONICET Digital (CONICET) - Consejo Nacional de Investigaciones Científicas y Técnicasfalse
dc.title.none.fl_str_mv Multi-glomerular projection of single olfactory receptor neurons is conserved among amphibians
title Multi-glomerular projection of single olfactory receptor neurons is conserved among amphibians
spellingShingle Multi-glomerular projection of single olfactory receptor neurons is conserved among amphibians
Weiss, Lukas
ANURA
AXONAL WIRING
EVOLUTION
FISHES
GLOMERULI
OLFACTION
SENSORY SYSTEM
title_short Multi-glomerular projection of single olfactory receptor neurons is conserved among amphibians
title_full Multi-glomerular projection of single olfactory receptor neurons is conserved among amphibians
title_fullStr Multi-glomerular projection of single olfactory receptor neurons is conserved among amphibians
title_full_unstemmed Multi-glomerular projection of single olfactory receptor neurons is conserved among amphibians
title_sort Multi-glomerular projection of single olfactory receptor neurons is conserved among amphibians
dc.creator.none.fl_str_mv Weiss, Lukas
Jungblut, Lucas David
Pozzi, Andrea Gabriela
Zielinski, Barbara S.
O'Connell, Lauren A.
Hassenklöver, Thomas
Manzini, Ivan
author Weiss, Lukas
author_facet Weiss, Lukas
Jungblut, Lucas David
Pozzi, Andrea Gabriela
Zielinski, Barbara S.
O'Connell, Lauren A.
Hassenklöver, Thomas
Manzini, Ivan
author_role author
author2 Jungblut, Lucas David
Pozzi, Andrea Gabriela
Zielinski, Barbara S.
O'Connell, Lauren A.
Hassenklöver, Thomas
Manzini, Ivan
author2_role author
author
author
author
author
author
dc.subject.none.fl_str_mv ANURA
AXONAL WIRING
EVOLUTION
FISHES
GLOMERULI
OLFACTION
SENSORY SYSTEM
topic ANURA
AXONAL WIRING
EVOLUTION
FISHES
GLOMERULI
OLFACTION
SENSORY SYSTEM
purl_subject.fl_str_mv https://purl.org/becyt/ford/1.6
https://purl.org/becyt/ford/1
dc.description.none.fl_txt_mv Individual receptor neurons in the peripheral olfactory organ extend long axons into the olfactory bulb forming synapses with projection neurons in spherical neuropil regions, called glomeruli. Generally, odor map formation and odor processing in all vertebrates is based on the assumption that receptor neuron axons exclusively connect to a single glomerulus without any axonal branching. We comparatively tested this hypothesis in multiple fish and amphibian species (both sexes) by applying sparse cell electroporation to trace single olfactory receptor neuron axons. Sea lamprey (jawless fish) and zebrafish (bony fish) support the unbranched axon concept, with 94% of axons terminating in single glomeruli. Contrastingly, axonal projections of the axolotl (salamander) branch extensively before entering up to six distinct glomeruli. Receptor neuron axons labeled in frog species (Pipidae, Bufonidae, Hylidae, and Dendrobatidae) predominantly bifurcate before entering a glomerulus and 59 and 50% connect to multiple glomeruli in larval and postmetamorphotic animals, respectively. Independent of developmental stage, lifestyle, and adaptations to specific habitats, it seems to be a common feature of amphibian olfactory receptor neuron axons to frequently bifurcate and connect to multiple glomeruli. Our study challenges the unbranched axon concept as a universal vertebrate feature and it is conceivable that also later diverging vertebrates deviate from it. We propose that this unusual wiring logic evolved around the divergence of the terrestrial tetrapod lineage from its aquatic ancestors and could be the basis of an alternative way of odor processing.
Fil: Weiss, Lukas. Justus Liebig Universitat Giessen.; Alemania
Fil: Jungblut, Lucas David. Consejo Nacional de Investigaciones Científicas y Técnicas. Oficina de Coordinación Administrativa Ciudad Universitaria. Instituto de Biodiversidad y Biología Experimental y Aplicada. Universidad de Buenos Aires. Facultad de Ciencias Exactas y Naturales. Instituto de Biodiversidad y Biología Experimental y Aplicada; Argentina
Fil: Pozzi, Andrea Gabriela. Consejo Nacional de Investigaciones Científicas y Técnicas. Oficina de Coordinación Administrativa Ciudad Universitaria. Instituto de Biodiversidad y Biología Experimental y Aplicada. Universidad de Buenos Aires. Facultad de Ciencias Exactas y Naturales. Instituto de Biodiversidad y Biología Experimental y Aplicada; Argentina
Fil: Zielinski, Barbara S.. University Of Windsor; Canadá
Fil: O'Connell, Lauren A.. University of Stanford; Estados Unidos
Fil: Hassenklöver, Thomas. Justus Liebig Universitat Giessen.; Alemania
Fil: Manzini, Ivan. Justus Liebig Universitat Giessen.; Alemania
description Individual receptor neurons in the peripheral olfactory organ extend long axons into the olfactory bulb forming synapses with projection neurons in spherical neuropil regions, called glomeruli. Generally, odor map formation and odor processing in all vertebrates is based on the assumption that receptor neuron axons exclusively connect to a single glomerulus without any axonal branching. We comparatively tested this hypothesis in multiple fish and amphibian species (both sexes) by applying sparse cell electroporation to trace single olfactory receptor neuron axons. Sea lamprey (jawless fish) and zebrafish (bony fish) support the unbranched axon concept, with 94% of axons terminating in single glomeruli. Contrastingly, axonal projections of the axolotl (salamander) branch extensively before entering up to six distinct glomeruli. Receptor neuron axons labeled in frog species (Pipidae, Bufonidae, Hylidae, and Dendrobatidae) predominantly bifurcate before entering a glomerulus and 59 and 50% connect to multiple glomeruli in larval and postmetamorphotic animals, respectively. Independent of developmental stage, lifestyle, and adaptations to specific habitats, it seems to be a common feature of amphibian olfactory receptor neuron axons to frequently bifurcate and connect to multiple glomeruli. Our study challenges the unbranched axon concept as a universal vertebrate feature and it is conceivable that also later diverging vertebrates deviate from it. We propose that this unusual wiring logic evolved around the divergence of the terrestrial tetrapod lineage from its aquatic ancestors and could be the basis of an alternative way of odor processing.
publishDate 2020
dc.date.none.fl_str_mv 2020-02
dc.type.none.fl_str_mv info:eu-repo/semantics/article
info:eu-repo/semantics/publishedVersion
http://purl.org/coar/resource_type/c_6501
info:ar-repo/semantics/articulo
format article
status_str publishedVersion
dc.identifier.none.fl_str_mv http://hdl.handle.net/11336/163613
Weiss, Lukas; Jungblut, Lucas David; Pozzi, Andrea Gabriela; Zielinski, Barbara S.; O'Connell, Lauren A.; et al.; Multi-glomerular projection of single olfactory receptor neurons is conserved among amphibians; Wiley-liss, div John Wiley & Sons Inc.; Journal Of Comparative Neurology; 528; 13; 2-2020; 2239-2253
0021-9967
CONICET Digital
CONICET
url http://hdl.handle.net/11336/163613
identifier_str_mv Weiss, Lukas; Jungblut, Lucas David; Pozzi, Andrea Gabriela; Zielinski, Barbara S.; O'Connell, Lauren A.; et al.; Multi-glomerular projection of single olfactory receptor neurons is conserved among amphibians; Wiley-liss, div John Wiley & Sons Inc.; Journal Of Comparative Neurology; 528; 13; 2-2020; 2239-2253
0021-9967
CONICET Digital
CONICET
dc.language.none.fl_str_mv eng
language eng
dc.relation.none.fl_str_mv info:eu-repo/semantics/altIdentifier/doi/10.1002/cne.24887
dc.rights.none.fl_str_mv info:eu-repo/semantics/openAccess
https://creativecommons.org/licenses/by/2.5/ar/
eu_rights_str_mv openAccess
rights_invalid_str_mv https://creativecommons.org/licenses/by/2.5/ar/
dc.format.none.fl_str_mv application/pdf
application/pdf
dc.publisher.none.fl_str_mv Wiley-liss, div John Wiley & Sons Inc.
publisher.none.fl_str_mv Wiley-liss, div John Wiley & Sons Inc.
dc.source.none.fl_str_mv reponame:CONICET Digital (CONICET)
instname:Consejo Nacional de Investigaciones Científicas y Técnicas
reponame_str CONICET Digital (CONICET)
collection CONICET Digital (CONICET)
instname_str Consejo Nacional de Investigaciones Científicas y Técnicas
repository.name.fl_str_mv CONICET Digital (CONICET) - Consejo Nacional de Investigaciones Científicas y Técnicas
repository.mail.fl_str_mv dasensio@conicet.gov.ar; lcarlino@conicet.gov.ar
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score 12.993085

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