Flying insects have evolved sophisticated sensory capabilities to achieve rapid course control during aerial maneuvers. Among two-winged insects such as houseflies and their relatives, the hind wings are modified into club-shaped, mechanosensory halteres, which detect Coriolis forces and thereby mediate flight stability during maneuvers. Here, we show that mechanosensory input from the antennae serves a similar role during flight in hawk moths, which are four-winged insects. The antennae of flying moths vibrate and experience Coriolis forces during aerial maneuvers. The antennal vibrations are transduced by individual units of Johnston's organs at the base of their antennae in a frequency range characteristic of the Coriolis input. Reduction of the mechanical input to Johnston's organs by removing the antennal flagellum of these moths severely disrupted their flight stability, but reattachment of the flagellum restored their flight control. The antennae thus play a crucial role in maintaining flight stability of moths.

Antennal mechanosensors play a key role in control and stability of insect flight. In addition to the well-established role of antennae as airflow detectors, recent studies have indicated that the sensing of antennal vibrations by Johnston's organs also provides a mechanosensory feedback relevant for flight stabilization. However, few studies have addressed how the individual units, or scolopidia, of the Johnston's organs encode these antennal vibrations and communicate it to the brain. Here, we characterize the encoding properties of individual scolopidia from the Johnston's organs in the hawk moth, Manduca sexta, through intracellular neurophysiological recordings from axons of the scolopidial neurons. We stimulated the flagellum-pedicel joint using a custom setup that delivered mechanical stimuli of various (step, sinusoidal, frequency and amplitude sweeps) waveforms. Single units of the Johnston's organs typically displayed phaso-tonic responses to step stimuli with short (3-5 ms) latencies. Their phase-locked response to sinusoidal stimuli in the 0.1-100 Hz frequency range showed high fidelity (vector strengths>0.9). The neurons were able to encode different phases of the stimulus motion and were also extremely sensitive to small amplitude (<0.05 deg) deflections with some indication of directional tuning. In many cases, the firing frequency of the neurons varied linearly as a function of the stimulus frequency at wingbeat and double wingbeat frequencies, which may be relevant to their role in flight stabilization. Iontophoretic fills of these neurons with fluorescent dyes showed that they all projected in the antennal mechanosensory and motor center (AMMC) area of the brain. Taken together, these results showcase the speed and high sensitivity of scolopidia of the Johnston's organs, and hence their ability to encode fine antennal vibrations.

Flying insects employ a vast array of sensory modalities to coordinate complex aerial maneuvers with incredible speed and acuity. One central feature underlying this is their ability to rapidly acquire and process information about rotational motion. In Diptera (flies), gyroscopic sensing is accomplished with halteres, organs that are derived from hindwings. In Lepidoptera (moths and butterflies), a recent study has suggested that antennae serve this critical function. Here, we review the biomechanical and sensory aspects of these biological gyroscopes. We focus on past and ongoing research to understand how the physical and physiological aspects of these inertial guidance units interact to determine their functional performance.

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