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Synaptic circuitry of identified neurons in the antennal lobe of Drosophila melanogaster

In Drosophila melanogaster olfactory sensory neurons (OSNs) establish synapses with projection neurons (PNs) and local interneurons within antennal lobe (AL) glomeruli. Substantial knowledge regarding this circuitry has been obtained by functional studies, whereas ultrastructural evidence of synapti...

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Autores principales: Rybak, Jürgen, Talarico, Giovanni, Ruiz, Santiago, Arnold, Christopher, Cantera, Rafael, Hansson, Bill S.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: John Wiley and Sons Inc. 2016
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6680330/
https://www.ncbi.nlm.nih.gov/pubmed/26780543
http://dx.doi.org/10.1002/cne.23966
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author Rybak, Jürgen
Talarico, Giovanni
Ruiz, Santiago
Arnold, Christopher
Cantera, Rafael
Hansson, Bill S.
author_facet Rybak, Jürgen
Talarico, Giovanni
Ruiz, Santiago
Arnold, Christopher
Cantera, Rafael
Hansson, Bill S.
author_sort Rybak, Jürgen
collection PubMed
description In Drosophila melanogaster olfactory sensory neurons (OSNs) establish synapses with projection neurons (PNs) and local interneurons within antennal lobe (AL) glomeruli. Substantial knowledge regarding this circuitry has been obtained by functional studies, whereas ultrastructural evidence of synaptic contacts is scarce. To fill this gap, we studied serial sections of three glomeruli using electron microscopy. Ectopic expression of a membrane‐bound peroxidase allowed us to map synaptic sites along PN dendrites. Our data prove for the first time that each of the three major types of AL neurons is both pre‐ and postsynaptic to the other two types, as previously indicated by functional studies. PN dendrites carry a large proportion of output synapses, with approximately one output per every three input synapses. Detailed reconstructions of PN dendrites showed that these synapses are distributed unevenly, with input and output sites partially segregated along a proximal–distal gradient and the thinnest branches carrying solely input synapses. Moreover, our data indicate synapse clustering, as we found evidence of dendritic tiling of PN dendrites. PN output synapses exhibited T‐shaped presynaptic densities, mostly arranged as tetrads. In contrast, output synapses from putative OSNs showed elongated presynaptic densities in which the T‐bar platform was supported by several pedestals and contacted as many as 20 postsynaptic profiles. We also discovered synaptic contacts between the putative OSNs. The average synaptic density in the glomerular neuropil was about two synapses/µm(3). These results are discussed with regard to current models of olfactory glomerular microcircuits across species. J. Comp. Neurol. 524:1920–1956, 2016. © 2016 The Authors The Journal of Comparative Neurology Published by Wiley Periodicals, Inc.
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spelling pubmed-66803302019-08-09 Synaptic circuitry of identified neurons in the antennal lobe of Drosophila melanogaster Rybak, Jürgen Talarico, Giovanni Ruiz, Santiago Arnold, Christopher Cantera, Rafael Hansson, Bill S. J Comp Neurol Research Articles In Drosophila melanogaster olfactory sensory neurons (OSNs) establish synapses with projection neurons (PNs) and local interneurons within antennal lobe (AL) glomeruli. Substantial knowledge regarding this circuitry has been obtained by functional studies, whereas ultrastructural evidence of synaptic contacts is scarce. To fill this gap, we studied serial sections of three glomeruli using electron microscopy. Ectopic expression of a membrane‐bound peroxidase allowed us to map synaptic sites along PN dendrites. Our data prove for the first time that each of the three major types of AL neurons is both pre‐ and postsynaptic to the other two types, as previously indicated by functional studies. PN dendrites carry a large proportion of output synapses, with approximately one output per every three input synapses. Detailed reconstructions of PN dendrites showed that these synapses are distributed unevenly, with input and output sites partially segregated along a proximal–distal gradient and the thinnest branches carrying solely input synapses. Moreover, our data indicate synapse clustering, as we found evidence of dendritic tiling of PN dendrites. PN output synapses exhibited T‐shaped presynaptic densities, mostly arranged as tetrads. In contrast, output synapses from putative OSNs showed elongated presynaptic densities in which the T‐bar platform was supported by several pedestals and contacted as many as 20 postsynaptic profiles. We also discovered synaptic contacts between the putative OSNs. The average synaptic density in the glomerular neuropil was about two synapses/µm(3). These results are discussed with regard to current models of olfactory glomerular microcircuits across species. J. Comp. Neurol. 524:1920–1956, 2016. © 2016 The Authors The Journal of Comparative Neurology Published by Wiley Periodicals, Inc. John Wiley and Sons Inc. 2016-03-09 2016-06-15 /pmc/articles/PMC6680330/ /pubmed/26780543 http://dx.doi.org/10.1002/cne.23966 Text en © 2016 The Authors The Journal of Comparative Neurology Published by Wiley Periodicals, Inc. This is an open access article under the terms of the http://creativecommons.org/licenses/by/4.0/ License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited.
spellingShingle Research Articles
Rybak, Jürgen
Talarico, Giovanni
Ruiz, Santiago
Arnold, Christopher
Cantera, Rafael
Hansson, Bill S.
Synaptic circuitry of identified neurons in the antennal lobe of Drosophila melanogaster
title Synaptic circuitry of identified neurons in the antennal lobe of Drosophila melanogaster
title_full Synaptic circuitry of identified neurons in the antennal lobe of Drosophila melanogaster
title_fullStr Synaptic circuitry of identified neurons in the antennal lobe of Drosophila melanogaster
title_full_unstemmed Synaptic circuitry of identified neurons in the antennal lobe of Drosophila melanogaster
title_short Synaptic circuitry of identified neurons in the antennal lobe of Drosophila melanogaster
title_sort synaptic circuitry of identified neurons in the antennal lobe of drosophila melanogaster
topic Research Articles
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6680330/
https://www.ncbi.nlm.nih.gov/pubmed/26780543
http://dx.doi.org/10.1002/cne.23966
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