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 completely 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 moth'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.

Fuelling on the wing: sensory ecology of hawkmoth foraging

“…The visual position control is likely supported by the wide-field motion vision system, since the temporal dynamic of the compensatory movements show similar temporal properties as the wide-field motion-sensitive neurons in the lobula complex and in descending tracts (Wicklein and Varjú 1999 ; Kern 1998 ; Stöckl et al 2017b ). In tethered-flying M. sexta , optic flow in the dorso-lateral region has been found to be critical for flight control (Copley et al 2018 ), and while the spatial resolution and contrast sensitivity decreases in dim light, the preferred temporal frequency remains around 4.5 Hz in all the light intensities (Parthasarathy and Willis 2018 ).…”

Ventral motion parallax enhances fruit fly steering to visual sideslip

“…In contrast with hawkmoths Manduca sexta, that maintain flight control even with the ventral region of their eyes covered [36], steering responses to positional changes in flies may be strongly based on flow fields below the horizon, as demonstrated in blowflies [4]. In fact, flies respond weakly to translational cues present only in the upper visual hemisphere [12].…”

Wind and obstacle motion affect honeybee flight strategies in cluttered environments

“…The observed increase in ground speeds for bees approaching moving obstacles in wind is unexpected because bees, as well as many other insects, are known to regulate their ground speeds based on optic flow from the surrounding visual environment, allowing them to maintain a preferred speed despite any ambient wind (Kennedy, 1951;Willis and Arbas, 1991;Barron and Srinivasan, 2006;Fuller et al, 2014;Copley et al, 2018). In our experiment, bees did display fairly consistent ground speeds when approaching stationary obstacles, regardless of flow condition: the averages [and 95% confidence intervals: (lower, upper limits)] of median ground speeds when bees approached stationary obstacles were 0.36 m s −1 (0.30, 0.43) in still air and 0.39 m s −1 (0.32, 0.47) in tailwinds, and declined slightly to 0.26 m s −1 (0.22, 0.32) in headwinds (slight declines in ground speed were also seen in headwinds by Barron and Srinivasan, 2006).…”