Optomotor steering and flight control requires a specific sub-section of the compound eye in the hawkmoth, Manduca sexta

Abstract

While tracking odor plumes, male hawkmoths use optic flow cues to stabilize their flight movements with respect to their environment. We studied the responses of freely flying moths tracking odor plumes in a laboratory wind tunnel and tethered moths in an optomotor flight simulator to determine the locations on the compound eye on which critical optic flow cues are detected. In these behavioral experiments, we occluded specific regions of the compound eye and systematically examined the moths’ behavior for specific deficits in optic flow processing. Freely flying moths with the dorsal half of the compound eye painted were unable to maintain stable flight and track the wind-borne odor plume. However, the plume tracking performance of moths with the ventral half of their compound eyes painted was the same as unpainted controls. In a matched set of experiments, we presented tethered moths with moving vertically-oriented sinusoidal gratings and found that individuals with their eyes unpainted, ventrally-painted, and medially-painted all responded by attempting optomotor-driven turns in the same proportion. In contrast, individuals with their compound eyes, dorsally-painted, laterally-painted, and totally-painted showed no optomotor turning response. We decreased the contrast of the visual stimulus and found that this relationship was consistent down to a contrast level of 2.5%. We conclude that visual input from the dorso-lateral region of the animal's visual world is critical for successful maintenance of flight stability and that this species’ visual environment must meet or exceed a contrast ratio of 2.5% to support visual flight control.