Cuticular hydrocarbon reception by sensory neurons in basiconic sensilla of the Japanese carpenter ant
To maintain the eusociality of a colony, ants recognize subtle differences in colony-specific sets of cuticular hydrocarbons (CHCs). The CHCs are received by female-specific antennal basiconic sensilla and processed in specific brain regions. However, it is controversial whether a peripheral or cent...
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| Format: | Article |
| Language: | English |
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Frontiers Media S.A.
2023-02-01
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| Series: | Frontiers in Cellular Neuroscience |
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| Online Access: | https://www.frontiersin.org/articles/10.3389/fncel.2023.1084803/full |
| _version_ | 1811170650129170432 |
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| author | Hidehiro Watanabe Shoji Ogata Nonoka Nodomi Kosuke Tateishi Hiroshi Nishino Ryosuke Matsubara Mamiko Ozaki Mamiko Ozaki Fumio Yokohari |
| author_facet | Hidehiro Watanabe Shoji Ogata Nonoka Nodomi Kosuke Tateishi Hiroshi Nishino Ryosuke Matsubara Mamiko Ozaki Mamiko Ozaki Fumio Yokohari |
| author_sort | Hidehiro Watanabe |
| collection | DOAJ |
| description | To maintain the eusociality of a colony, ants recognize subtle differences in colony-specific sets of cuticular hydrocarbons (CHCs). The CHCs are received by female-specific antennal basiconic sensilla and processed in specific brain regions. However, it is controversial whether a peripheral or central neural mechanism is mainly responsible for discrimination of CHC blends. In the Japanese carpenter ant, Camponotus japonicus, about 140 sensory neurons (SNs) are co-housed in a single basiconic sensillum and receive colony-specific blends of 18 CHCs. The complexity of this CHC sensory process makes the neural basis of peripheral nestmate recognition difficult to understand. Here, we electrophysiologically recorded responses of single basiconic sensilla to each of 18 synthesized CHCs, and identified CHC responses of each SN co-housed in a single sensillum. Each CHC activated different sets of SNs and each SN was broadly tuned to CHCs. Multiple SNs in a given sensillum fired in synchrony, and the synchronicity of spikes was impaired by treatment with a gap junction inhibitor. These results indicated that SNs in single basiconic sensilla were electrically coupled. Quantitative analysis indicated that the Japanese carpenter ants have the potential to discriminate chemical structures of CHCs based on the combinational patterns of activated SNs. SNs of ants from different colonies exhibited different CHC response spectra. In addition, ants collected from the same colony but bred in separate groups also exhibited different CHC response spectra. These results support the hypothesis that the peripheral sensory mechanism is important for discrimination between nestmate and non-nestmate ants. |
| first_indexed | 2024-04-10T17:01:19Z |
| format | Article |
| id | doaj.art-eef466ca0ff34c968882eab35c59e705 |
| institution | Directory Open Access Journal |
| issn | 1662-5102 |
| language | English |
| last_indexed | 2024-04-10T17:01:19Z |
| publishDate | 2023-02-01 |
| publisher | Frontiers Media S.A. |
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| series | Frontiers in Cellular Neuroscience |
| spelling | doaj.art-eef466ca0ff34c968882eab35c59e7052023-02-06T14:37:45ZengFrontiers Media S.A.Frontiers in Cellular Neuroscience1662-51022023-02-011710.3389/fncel.2023.10848031084803Cuticular hydrocarbon reception by sensory neurons in basiconic sensilla of the Japanese carpenter antHidehiro Watanabe0Shoji Ogata1Nonoka Nodomi2Kosuke Tateishi3Hiroshi Nishino4Ryosuke Matsubara5Mamiko Ozaki6Mamiko Ozaki7Fumio Yokohari8Department of Earth System Science, Fukuoka University, Fukuoka, JapanDepartment of Earth System Science, Fukuoka University, Fukuoka, JapanDepartment of Earth System Science, Fukuoka University, Fukuoka, JapanDepartment of Earth System Science, Fukuoka University, Fukuoka, JapanResearch Institute for Electronic Science, Hokkaido University, Sapporo, JapanDepartment of Chemistry, Graduate School of Science, Kobe University, Kobe, JapanDepartment of Biology, Graduate School of Science, Kobe University, Kobe, JapanKYOUSEI Science Center for Life and Nature, Nara Women’s University, Nara, JapanDepartment of Earth System Science, Fukuoka University, Fukuoka, JapanTo maintain the eusociality of a colony, ants recognize subtle differences in colony-specific sets of cuticular hydrocarbons (CHCs). The CHCs are received by female-specific antennal basiconic sensilla and processed in specific brain regions. However, it is controversial whether a peripheral or central neural mechanism is mainly responsible for discrimination of CHC blends. In the Japanese carpenter ant, Camponotus japonicus, about 140 sensory neurons (SNs) are co-housed in a single basiconic sensillum and receive colony-specific blends of 18 CHCs. The complexity of this CHC sensory process makes the neural basis of peripheral nestmate recognition difficult to understand. Here, we electrophysiologically recorded responses of single basiconic sensilla to each of 18 synthesized CHCs, and identified CHC responses of each SN co-housed in a single sensillum. Each CHC activated different sets of SNs and each SN was broadly tuned to CHCs. Multiple SNs in a given sensillum fired in synchrony, and the synchronicity of spikes was impaired by treatment with a gap junction inhibitor. These results indicated that SNs in single basiconic sensilla were electrically coupled. Quantitative analysis indicated that the Japanese carpenter ants have the potential to discriminate chemical structures of CHCs based on the combinational patterns of activated SNs. SNs of ants from different colonies exhibited different CHC response spectra. In addition, ants collected from the same colony but bred in separate groups also exhibited different CHC response spectra. These results support the hypothesis that the peripheral sensory mechanism is important for discrimination between nestmate and non-nestmate ants.https://www.frontiersin.org/articles/10.3389/fncel.2023.1084803/fullantcuticular hydrocarbonsbasiconic sensillasensory neuronsnestmate recognitionsocial insect |
| spellingShingle | Hidehiro Watanabe Shoji Ogata Nonoka Nodomi Kosuke Tateishi Hiroshi Nishino Ryosuke Matsubara Mamiko Ozaki Mamiko Ozaki Fumio Yokohari Cuticular hydrocarbon reception by sensory neurons in basiconic sensilla of the Japanese carpenter ant Frontiers in Cellular Neuroscience ant cuticular hydrocarbons basiconic sensilla sensory neurons nestmate recognition social insect |
| title | Cuticular hydrocarbon reception by sensory neurons in basiconic sensilla of the Japanese carpenter ant |
| title_full | Cuticular hydrocarbon reception by sensory neurons in basiconic sensilla of the Japanese carpenter ant |
| title_fullStr | Cuticular hydrocarbon reception by sensory neurons in basiconic sensilla of the Japanese carpenter ant |
| title_full_unstemmed | Cuticular hydrocarbon reception by sensory neurons in basiconic sensilla of the Japanese carpenter ant |
| title_short | Cuticular hydrocarbon reception by sensory neurons in basiconic sensilla of the Japanese carpenter ant |
| title_sort | cuticular hydrocarbon reception by sensory neurons in basiconic sensilla of the japanese carpenter ant |
| topic | ant cuticular hydrocarbons basiconic sensilla sensory neurons nestmate recognition social insect |
| url | https://www.frontiersin.org/articles/10.3389/fncel.2023.1084803/full |
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