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

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 recep...

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Veröffentlicht in:Journal of comparative neurology (1911) Jg. 528; H. 13; S. 2239 - 2253
Hauptverfasser: Weiss, Lukas, Jungblut, Lucas D., Pozzi, Andrea G., Zielinski, Barbara S., O'Connell, Lauren A., Hassenklöver, Thomas, Manzini, Ivan
Format: Journal Article
Sprache:Englisch
Veröffentlicht: Hoboken, USA John Wiley & Sons, Inc 01.09.2020
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ISSN:0021-9967, 1096-9861, 1096-9861
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Abstract 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. The formation of an odor map in the olfactory bulb of vertebrates is based on the general assumption that axons of individual olfactory receptor neurons do not branch and connect to single glomeruli. Here, we show that this general principle does not apply to the olfactory system of amphibians, which exhibits a multi‐glomerular wiring scheme and a putatively different odor coding strategy. Our data underline the need to acknowledge biological diversity to fully understand odor coding in vertebrates.
AbstractList 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.
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. The formation of an odor map in the olfactory bulb of vertebrates is based on the general assumption that axons of individual olfactory receptor neurons do not branch and connect to single glomeruli. Here, we show that this general principle does not apply to the olfactory system of amphibians, which exhibits a multi‐glomerular wiring scheme and a putatively different odor coding strategy. Our data underline the need to acknowledge biological diversity to fully understand odor coding in vertebrates.
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.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.
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 post-metamorphotic 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. The formation of an odor map in the olfactory bulb of vertebrates is based on the general assumption that axons of individual olfactory receptor neurons do not branch and connect to single glomeruli. Here we show that this general principle does not apply to the olfactory system of amphibians, which exhibits a multi-glomerular wiring scheme and a putatively different odor coding strategy. Our data underline the need to acknowledge biological diversity to fully understand odor coding in vertebrates.
Author Zielinski, Barbara S.
O'Connell, Lauren A.
Jungblut, Lucas D.
Hassenklöver, Thomas
Weiss, Lukas
Pozzi, Andrea G.
Manzini, Ivan
AuthorAffiliation 5 Lead Contact
3 Department of Integrative Biology, University of Windsor, N9B 3P4 Windsor, Ontario, Canada
1 Department of Animal Physiology and Molecular Biomedicine, University of Giessen, 35392 Giessen, Germany
2 Departamento de Biodiversidad y Biología Experimental, IBBEA-CONICET, Universidad de Buenos Aires, C1428EGA Buenos Aires, Argentina
4 Department of Biology, Stanford University, 94305 Stanford, California, USA
AuthorAffiliation_xml – name: 3 Department of Integrative Biology, University of Windsor, N9B 3P4 Windsor, Ontario, Canada
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  surname: Manzini
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Issue 13
Keywords glomeruli
RRID:SCR_002285
RRID:SCR_002609
axonal wiring
sensory system
olfaction
RRID:SCR_007164
evolution
anura
fishes
Language English
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2020 The Authors. The Journal of Comparative Neurology published by Wiley Periodicals, Inc.
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Conceptualization, L.W., T.H. and I.M.; Investigation, Formal Analysis, Visualization and Writing – Original Draft, L.W.; Writing – Review & Editing, L.W., L.D.J., A.G.P., B.S.Z., L.A.O., T.H. and I.M.; Funding Acquisition and Resources, L.D.J., A.G.P., B.S.Z., L.A.O., T.H. and I.M.; Supervision, T.H. and I.M.
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PublicationCentury 2000
PublicationDate September 1, 2020
PublicationDateYYYYMMDD 2020-09-01
PublicationDate_xml – month: 09
  year: 2020
  text: September 1, 2020
  day: 01
PublicationDecade 2020
PublicationPlace Hoboken, USA
PublicationPlace_xml – name: Hoboken, USA
– name: United States
– name: New York
PublicationTitle Journal of comparative neurology (1911)
PublicationTitleAlternate J Comp Neurol
PublicationYear 2020
Publisher John Wiley & Sons, Inc
Wiley Subscription Services, Inc
Publisher_xml – name: John Wiley & Sons, Inc
– name: Wiley Subscription Services, Inc
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Snippet Individual receptor neurons in the peripheral olfactory organ extend long axons into the olfactory bulb forming synapses with projection neurons in spherical...
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StartPage 2239
SubjectTerms Adaptation
anura
axonal wiring
Axons
Dendritic branching
Divergence
Electroporation
evolution
fishes
glomeruli
Neurons
Neuropil
Odor
Odorant receptors
Odors
olfaction
Olfactory bulb
Olfactory glomeruli
Olfactory organs
Olfactory receptor neurons
Reptiles & amphibians
RRID:SCR_002285
RRID:SCR_002609
RRID:SCR_007164
sensory system
Synapses
Vertebrates
Title Multi‐glomerular projection of single olfactory receptor neurons is conserved among amphibians
URI https://onlinelibrary.wiley.com/doi/abs/10.1002%2Fcne.24887
https://www.ncbi.nlm.nih.gov/pubmed/32080843
https://www.proquest.com/docview/2424636224
https://www.proquest.com/docview/2366636208
https://pubmed.ncbi.nlm.nih.gov/PMC7418368
Volume 528
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