Integration of parallel pathways for flight control in a hawkmoth reflects prevalence and relevance of natural visual cues

Abstract

AbstractAn animal’s behaviour is the result of multiple neural pathways acting in parallel, receiving information across and within sensory modalities at the same time. How these pathways are integrated, particularly when their individual outputs are in conflict, is key to understanding complex natural behaviours. We investigated this question in the visually guided flight control of hummingbird hawkmoths, which were recently shown to partition their visual field into using optic-flow for flight control ventrolaterally, while the same stimuli in dorsal view evoke a novel directional response. Using behavioural experiments in flight tunnels, we demonstrated that the dorsal response does not bear hallmarks of optic flow-based flight control, but aims at reducing contrast cues in the visual field. Combining environmental imaging with behavioural experiments, we dissected the response hierarchy of these two systems. We show that partitioning of the visual field followed the prevalence of visual cues in the hawkmoths’ natural habitats, while the integration hierarchy matched the relevance of these cues for the animals’ flight safety, rather than their magnitude in the experimental setup or in natural habitats.