Watanabe Hidehiro, Ogata Shoji, Nodomi Nonoka, Tateishi Kosuke, Nishino Hiroshi, Matsubara Ryosuke, Ozaki Mamiko, Yokohari Fumio
Department of Earth System Science, Fukuoka University, Fukuoka, Japan.
Research Institute for Electronic Science, Hokkaido University, Sapporo, Japan.
Front Cell Neurosci. 2023 Feb 6;17:1084803. doi: 10.3389/fncel.2023.1084803. eCollection 2023.
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, , 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.
为维持蚁群的群居特性,蚂蚁能够识别特定蚁群表皮碳氢化合物(CHCs)集合中的细微差异。CHCs由雌性特有的触角锥形感器接收,并在特定脑区进行处理。然而,究竟是外周神经机制还是中枢神经机制主要负责CHC混合物的辨别,这一点存在争议。在日本木工蚁中,约140个感觉神经元(SNs)共同存在于单个锥形感器中,并接收由18种CHCs组成的特定蚁群混合物。这种CHC感觉过程的复杂性使得外周识别同巢蚂蚁的神经基础难以理解。在此,我们通过电生理学方法记录了单个锥形感器对18种合成CHCs中每一种的反应,并确定了共同存在于单个感器中的每个SN的CHC反应。每种CHC激活不同组的SNs,且每个SN对CHCs具有广泛的调谐。给定感器中的多个SNs同步放电,而缝隙连接抑制剂处理会损害峰电位的同步性。这些结果表明单个锥形感器中的SNs存在电耦合。定量分析表明,日本木工蚁有潜力基于激活的SNs的组合模式来辨别CHCs的化学结构。来自不同蚁群的蚂蚁的SNs表现出不同的CHC反应谱。此外,从同一蚁群收集但分开饲养的蚂蚁也表现出不同的CHC反应谱。这些结果支持了外周感觉机制对辨别同巢和非同巢蚂蚁很重要这一假说。