Sensing and flying in hawkmoths

Abstract

Flying insects must balance the demands of speed and agility with the precision of their movements to swiftly and accurately respond to environmental stimuli. Achieving this balance requires them to integrate sensory information from various modalities. Of particular importance are visual inputs from their compound eyes and mechanosensory inputs from their antennae, which are crucial for maintaining flight stability. This challenge is particularly pronounced in insects like hawkmoths, which navigate under low light conditions. Prior studies on diverse hawkmoths and other insects have highlighted the critical role of antennal mechanosensory feedback in flight control, akin to the function of halteres in flies. How is such multisensory integration achieved? We addressed this question by conducting recordings from descending neurons in the cervical connective nerve in the Oleander hawkmoths, Daphnis nerii. The moths were provided with visual stimuli comprised of moving spots of light and mechanical stimuli to their antennae. While these stimuli were presented singly or concurrently, we recorded intracellularly from axons of descending interneurons to determine if they respond to one or both stimuli. In addition to a number of exclusively visual or mechanosensory descending neurons, we also identified several neurons that multiplex the visual and mechanosensory signals such that a single neuron encodes both visual stimuli from the compound eyes, and mechanosensory stimuli from the antennal Johnston's organs. Additional experiments at the level of behavior in intact moths reveals that integration of visual and antennal mechanosensory feedback plays a key role in gaze stabilization in flying hawkmoths. Together, these experiments underscore the importance of multisensory integration during flight in hawkmoths.