Mechanisms of visual integration and competition in innate behaviours in Drosophila melanogaster

Locomotion is ubiquitous in the animal kingdom because an animal's survival depends on its ability to navigate its environment to find food, avoid predators and locate potential mates. These behaviours require control mechanisms that can extract information from the environment, particularly visual cues. Selective evolutionary pressures have thus refined such visuomotor transformations in a species-specific manner to meet the specific ecological and ethological challenges of each organism. However, a common challenge across organisms as visual information processing becomes increasingly detailed is the mechanisms required to synthesise disparate pieces of information into a coherent percept or unified picture of the world. In this thesis, I investigate how disparate visual information is combined in the brain of Drosophila melanogaster to effectively guide locomotion. For this, I first designed and built a behavioural setup to record locomotion and present visual stimuli to freely-walking fruit flies in a closed-loop manner. This setup allowed the investigation of innate visually-guided behaviours, including the optomotor reflex and courtship. Second, taking advantage of my system I investigated the optomotor response, a reflexive visual stabilisation behaviour in which flies turn in the direction of global motion to minimise retinal slip. This behaviour is thought to be mediated by Lobula plate tangential cells (LPTCs); a complex network of optic-flow-sensitive neurons essential for self-motion estimation. Using a novel genetic mutant, I demonstrate that electrical coupling between two LPTC subtypes, contralateral HS and H2 neurons, regulates the balance between smooth optomotor turning and saccadic anti-optomotor responses. These findings underscore the critical role of binocular motion cue integration in guiding course control. Finally, I developed a novel behavioural paradigm in which a sexually aroused male fruit fly is presented with an optomotor distractor. This setup creates competition between two visual behaviours, courtship tracking and the optomotor response, enabling me to explore how the visual system resolves this conflict. In this setting, males engaged in courtship selectively suppress their optomotor response based on the female's location. Furthermore, when this experiment is replicated with an “artificial female”, optogenetically aroused males alternate between tracking and optomotor responses. The probability and dynamics of this switching are determined by the relative strengths of the two competing stimuli. In summary, the results presented in this thesis explore two mechanisms – integration and competition - through which visual information is combined in the brain of the fruit fly to drive locomotion.