Mukunda Chinmayee L, Sane Sanjay P
National Centre for Biological Sciences, Tata Institute of Fundamental Research, GKVK Campus, Bellary Road, Bangalore 560065, India.
J Exp Biol. 2025 May 1;228(9). doi: 10.1242/jeb.249342. Epub 2025 May 2.
Insect antennae function as versatile, multimodal sensory probes in diverse behavioural contexts. In addition to their primary role as olfactory organs, they serve essential mechanosensory functions across insects, including auditory perception, vestibular feedback, airflow detection, gravity sensing and tactile sensation. These diverse functions are facilitated by the mechanosensory Johnston's organ (JO), located at the joint between the flagellum and the pedicel (second antennal segment). This joint lacks muscles, which means that JOs can perceive only passive deflections of the flagellum. Earlier work that characterized the sensitivity and short response time of the JO sensory units in hawkmoths showed that their sensitivity to a broad frequency range is range-fractionated. This vastly expands the functional repertoire of the JO. However, it is not clear what components of antennal kinematics are encoded by the JO. Here, we conducted experiments to test the hypothesis that JO neurons encode the position and velocity of angular movements of the flagellum. We recorded intracellularly from the axons of primary sensory neurons of the JO while stimulating it with ramp-and-hold stimuli in which either the antennal position or antennal angular velocity was maintained at various constant values. Our study shows that JO neurons encode angular velocity and position of the antenna in their response. We also characterized the neural adaptation of the responses to angular velocities and positions. The majority of neurons were sensitive to a movement in the ventrad direction, in the direction of gravity. The adaptation and directional response properties give rise to a nonlinear hysteresis-like response. Together, these findings highlight the neurophysiological basis underlying the functional versatility of the JO.
昆虫触角在多种行为情境中发挥着多功能、多模态的感觉探测作用。除了作为嗅觉器官的主要作用外，它们在昆虫中还发挥着重要的机械感觉功能，包括听觉感知、前庭反馈、气流检测、重力感应和触觉。位于鞭节和梗节（触角第二节）之间关节处的机械感觉器官约翰斯顿氏器（JO）促进了这些多样的功能。这个关节没有肌肉，这意味着JO只能感知鞭节的被动偏转。早期对天蛾JO感觉单元的敏感性和短响应时间进行表征的研究表明，它们对宽频率范围的敏感性是按频率范围划分的。这极大地扩展了JO的功能范围。然而，尚不清楚JO编码了触角运动学的哪些组成部分。在这里，我们进行了实验，以检验JO神经元编码鞭节角运动的位置和速度这一假设。我们在用斜坡保持刺激刺激JO时，对其初级感觉神经元的轴突进行细胞内记录，在这些刺激中，触角位置或触角角速度保持在各种恒定值。我们的研究表明，JO神经元在其反应中编码触角的角速度和位置。我们还表征了对角速度和位置反应的神经适应性。大多数神经元对腹侧方向（重力方向）的运动敏感。适应性和方向反应特性产生了类似非线性滞后的反应。这些发现共同突出了JO功能多样性背后的神经生理学基础。
