Encoding of antennal position and velocity by the Johnston's organ in hawkmoths

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.