A model of visual–olfactory integration for odour localisation in free-flying fruit flies

Flying fruit flies (Drosophila melanogaster) locate a concealed appetitive odour source most accurately in environments containing vertical visual contrasts. To investigate how visuomotor and olfactory responses may be integrated, we examine the free-flight behaviour of flies in three visual conditions, with and without food odour present. While odour localisation is facilitated by uniformly distributed vertical contrast as compared with purely horizontal contrast, localised vertical contrast also facilitates odour localisation, but only if the odour source is situated close to it. We implement a model of visuomotor control consisting of three parallel subsystems: an optomotor response stabilising the model fly's yaw orientation; a collision avoidance system to saccade away from looming obstacles; and a speed regulation system. This model reproduces many of the behaviours we observe in flies, including visually mediated 'rebound' turns following saccades. Using recordings of real odour plumes, we simulate the presence of an odorant in the arena, and investigate ways in which the olfactory input could modulate visuomotor control. We reproduce the experimental results by using the change in odour intensity to regulate the sensitivity of collision avoidance, resulting in visually mediated chemokinesis. Additionally, it is necessary to amplify the optomotor response whenever odour is present, increasing the model fly's tendency to steer towards features of the visual environment. We conclude that visual and olfactory responses of Drosophila are not independent, but that relatively simple interaction between these modalities can account for the observed visual dependence of odour source localisation.