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

Yusuke Takeichi, Tatsuya Uebi, Naoyuki Miyazaki, Kazuyoshi Murata, Kouji Yasuyama, Kanako Inoue, Toshinobu Suzaki, Hideo Kubo, Naoko Kajimura, Jo Takano, Toshiaki Omori, Ryoichi Yoshimura, Yasuhisa Endo, Masaru K. Hojo, Eichi Takaya, Satoshi Kurihara, Kenta Tatsuta, Koichi Ozaki, Mamiko Ozaki

Research output: Contribution to journalArticle

Abstract

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.

Original languageEnglish
Article number310
JournalFrontiers in Cellular Neuroscience
Volume12
DOIs
Publication statusPublished - 2018 Sep 19
Externally publishedYes

Fingerprint

Sensilla
Ants
Olfactory Receptor Neurons
Hydrocarbons
Gap Junctions
Electrons
Connexins
Information Services
Pheromones
Invertebrates
Immune Sera
Theoretical Models
Immunohistochemistry
Cell Membrane

Keywords

  • Ant
  • Chemical communication
  • Chemosensillum
  • Innexin
  • Mathematical simulation
  • Olfactory receptor
  • Ultra-structures

ASJC Scopus subject areas

  • Cellular and Molecular Neuroscience

Cite this

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.

In: Frontiers in Cellular Neuroscience, Vol. 12, 310, 19.09.2018.

Research output: Contribution to journalArticle

Takeichi, Y, Uebi, T, Miyazaki, N, Murata, K, Yasuyama, K, Inoue, K, Suzaki, T, Kubo, H, Kajimura, N, Takano, J, Omori, T, Yoshimura, R, Endo, Y, Hojo, MK, Takaya, E, Kurihara, S, Tatsuta, K, Ozaki, K & Ozaki, M 2018, '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', Frontiers in Cellular Neuroscience, vol. 12, 310. https://doi.org/10.3389/fncel.2018.00310
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. In: Frontiers in Cellular Neuroscience. 2018 ; Vol. 12.
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