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Putative Neural Network Within an Olfactory Sensory Unit for Nestmate and Non-nestmate Discrimination in the Japanese Carpenter Ant: The Ultra-structures and Mathematical Simulation

Ants are known to use a colony-specific blend of cuticular hydrocarbons (CHCs) as a pheromone to discriminate between nestmates and non-nestmates and the CHCs were sensed in the basiconic type of antennal sensilla (S. basiconica). To investigate the functional design of this type of antennal sensill...

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Autores principales: Takeichi, Yusuke, Uebi, Tatsuya, Miyazaki, Naoyuki, Murata, Kazuyoshi, Yasuyama, Kouji, Inoue, Kanako, Suzaki, Toshinobu, Kubo, Hideo, Kajimura, Naoko, Takano, Jo, Omori, Toshiaki, Yoshimura, Ryoichi, Endo, Yasuhisa, Hojo, Masaru K., Takaya, Eichi, Kurihara, Satoshi, Tatsuta, Kenta, Ozaki, Koichi, Ozaki, Mamiko
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2018
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6157317/
https://www.ncbi.nlm.nih.gov/pubmed/30283303
http://dx.doi.org/10.3389/fncel.2018.00310
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author Takeichi, Yusuke
Uebi, Tatsuya
Miyazaki, Naoyuki
Murata, Kazuyoshi
Yasuyama, Kouji
Inoue, Kanako
Suzaki, Toshinobu
Kubo, Hideo
Kajimura, Naoko
Takano, Jo
Omori, Toshiaki
Yoshimura, Ryoichi
Endo, Yasuhisa
Hojo, Masaru K.
Takaya, Eichi
Kurihara, Satoshi
Tatsuta, Kenta
Ozaki, Koichi
Ozaki, Mamiko
author_facet Takeichi, Yusuke
Uebi, Tatsuya
Miyazaki, Naoyuki
Murata, Kazuyoshi
Yasuyama, Kouji
Inoue, Kanako
Suzaki, Toshinobu
Kubo, Hideo
Kajimura, Naoko
Takano, Jo
Omori, Toshiaki
Yoshimura, Ryoichi
Endo, Yasuhisa
Hojo, Masaru K.
Takaya, Eichi
Kurihara, Satoshi
Tatsuta, Kenta
Ozaki, Koichi
Ozaki, Mamiko
author_sort Takeichi, Yusuke
collection PubMed
description Ants are known to use a colony-specific blend of cuticular hydrocarbons (CHCs) as a pheromone to discriminate between nestmates and non-nestmates and the CHCs were sensed in the basiconic type of antennal sensilla (S. basiconica). To investigate the functional design of this type of antennal sensilla, we observed the ultra-structures at 2D and 3D in the Japanese carpenter ant, Camponotus japonicus, using a serial block-face scanning electron microscope (SBF-SEM), and conventional and high-voltage transmission electron microscopes. Based on the serial images of 352 cross sections of SBF-SEM, we reconstructed a 3D model of the sensillum revealing that each S. basiconica houses > 100 unbranched dendritic processes, which extend from the same number of olfactory receptor neurons (ORNs). The dendritic processes had characteristic beaded-structures and formed a twisted bundle within the sensillum. At the “beads,” the cell membranes of the processes were closely adjacent in the interdigitated profiles, suggesting functional interactions via gap junctions (GJs). Immunohistochemistry with anti-innexin (invertebrate GJ protein) antisera revealed positive labeling in the antennae of C. japonicus. Innexin 3, one of the five antennal innexin subtypes, was detected as a dotted signal within the S. basiconica as a sensory organ for nestmate recognition. These morphological results suggest that ORNs form an electrical network via GJs between dendritic processes. We were unable to functionally certify the electric connections in an olfactory sensory unit comprising such multiple ORNs; however, with the aid of simulation of a mathematical model, we examined the putative function of this novel chemosensory information network, which possibly contributes to the distinct discrimination of colony-specific blends of CHCs or other odor detection.
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spelling pubmed-61573172018-10-03 Putative Neural Network Within an Olfactory Sensory Unit for Nestmate and Non-nestmate Discrimination in the Japanese Carpenter Ant: The Ultra-structures and Mathematical Simulation Takeichi, Yusuke Uebi, Tatsuya Miyazaki, Naoyuki Murata, Kazuyoshi Yasuyama, Kouji Inoue, Kanako Suzaki, Toshinobu Kubo, Hideo Kajimura, Naoko Takano, Jo Omori, Toshiaki Yoshimura, Ryoichi Endo, Yasuhisa Hojo, Masaru K. Takaya, Eichi Kurihara, Satoshi Tatsuta, Kenta Ozaki, Koichi Ozaki, Mamiko Front Cell Neurosci Neuroscience Ants are known to use a colony-specific blend of cuticular hydrocarbons (CHCs) as a pheromone to discriminate between nestmates and non-nestmates and the CHCs were sensed in the basiconic type of antennal sensilla (S. basiconica). To investigate the functional design of this type of antennal sensilla, we observed the ultra-structures at 2D and 3D in the Japanese carpenter ant, Camponotus japonicus, using a serial block-face scanning electron microscope (SBF-SEM), and conventional and high-voltage transmission electron microscopes. Based on the serial images of 352 cross sections of SBF-SEM, we reconstructed a 3D model of the sensillum revealing that each S. basiconica houses > 100 unbranched dendritic processes, which extend from the same number of olfactory receptor neurons (ORNs). The dendritic processes had characteristic beaded-structures and formed a twisted bundle within the sensillum. At the “beads,” the cell membranes of the processes were closely adjacent in the interdigitated profiles, suggesting functional interactions via gap junctions (GJs). Immunohistochemistry with anti-innexin (invertebrate GJ protein) antisera revealed positive labeling in the antennae of C. japonicus. Innexin 3, one of the five antennal innexin subtypes, was detected as a dotted signal within the S. basiconica as a sensory organ for nestmate recognition. These morphological results suggest that ORNs form an electrical network via GJs between dendritic processes. We were unable to functionally certify the electric connections in an olfactory sensory unit comprising such multiple ORNs; however, with the aid of simulation of a mathematical model, we examined the putative function of this novel chemosensory information network, which possibly contributes to the distinct discrimination of colony-specific blends of CHCs or other odor detection. Frontiers Media S.A. 2018-09-19 /pmc/articles/PMC6157317/ /pubmed/30283303 http://dx.doi.org/10.3389/fncel.2018.00310 Text en Copyright © 2018 Takeichi, Uebi, Miyazaki, Murata, Yasuyama, Inoue, Suzaki, Kubo, Kajimura, Takano, Omori, Yoshimura, Endo, Hojo, Takaya, Kurihara, Tatsuta, Ozaki and Ozaki. http://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 Neuroscience
Takeichi, Yusuke
Uebi, Tatsuya
Miyazaki, Naoyuki
Murata, Kazuyoshi
Yasuyama, Kouji
Inoue, Kanako
Suzaki, Toshinobu
Kubo, Hideo
Kajimura, Naoko
Takano, Jo
Omori, Toshiaki
Yoshimura, Ryoichi
Endo, Yasuhisa
Hojo, Masaru K.
Takaya, Eichi
Kurihara, Satoshi
Tatsuta, Kenta
Ozaki, Koichi
Ozaki, Mamiko
Putative Neural Network Within an Olfactory Sensory Unit for Nestmate and Non-nestmate Discrimination in the Japanese Carpenter Ant: The Ultra-structures and Mathematical Simulation
title Putative Neural Network Within an Olfactory Sensory Unit for Nestmate and Non-nestmate Discrimination in the Japanese Carpenter Ant: The Ultra-structures and Mathematical Simulation
title_full Putative Neural Network Within an Olfactory Sensory Unit for Nestmate and Non-nestmate Discrimination in the Japanese Carpenter Ant: The Ultra-structures and Mathematical Simulation
title_fullStr Putative Neural Network Within an Olfactory Sensory Unit for Nestmate and Non-nestmate Discrimination in the Japanese Carpenter Ant: The Ultra-structures and Mathematical Simulation
title_full_unstemmed Putative Neural Network Within an Olfactory Sensory Unit for Nestmate and Non-nestmate Discrimination in the Japanese Carpenter Ant: The Ultra-structures and Mathematical Simulation
title_short Putative Neural Network Within an Olfactory Sensory Unit for Nestmate and Non-nestmate Discrimination in the Japanese Carpenter Ant: The Ultra-structures and Mathematical Simulation
title_sort putative neural network within an olfactory sensory unit for nestmate and non-nestmate discrimination in the japanese carpenter ant: the ultra-structures and mathematical simulation
topic Neuroscience
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6157317/
https://www.ncbi.nlm.nih.gov/pubmed/30283303
http://dx.doi.org/10.3389/fncel.2018.00310
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