Natural image statistics in the dorsal and ventral visual field match a switch in flight behaviour of a hawkmoth

Abstract

Many animals use visual cues to navigate their environment. To encode the large input ranges of natural signals optimally, their sensory systems have adapted to the stimulus statistics experienced in their natural habitats¹. A striking example, shared across animal phyla, is the retinal tuning to the relative abundance of blue light from the sky, and green light from the ground, evident in the frequency of each photoreceptor type in the two retinal hemispheres². By adhering only to specific regions of the visual field that contain the relevant information, as for the high-acuity dorsal regions in the eyes of male flies chasing females³, the neural investment can be further reduced. Regionalisation can even lead to activation of the appropriate visual pathway by target location, rather than by stimulus features. This has been shown in fruit flies, which increase their landing attempts when an expanding disc is presented in their frontal visual field, while lateral presentation increases obstacle avoidance responses⁴. We here report a similar switch in behavioural responses for extended visual scenes. Using a free-flight paradigm, we show that the hummingbird hawkmoth (Macroglossum stellatarum) responds with flight-control adjustments to translational optic-flow cues exclusively in their ventral and lateral visual fields, while identical stimuli presented dorsally elicit a novel directional flight response. This response split is predicted by our quantitative imaging data from natural visual scenes in a variety of habitats, which demonstrate higher magnitudes of translational optic flow in the ventral hemisphere, and the opposite distribution for contrast edges containing directional information.