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Olfactory modulation of visual object behaviors in Drosophila melanogaster

Abstract

Visual objects in the natural world convey many meanings to vinegar flies, signifying the presence of predators, food sources, or potential mates. How animals rapidly distinguish among these small objects remains unclear at the mechanistic level. It is thought that multimodal integration of sensory cues, likely via actions of neuromodulators, is one mechanism for this behavioral plasticity. In this thesis, we begin by reviewing the current understanding of neuromodulation of insect vision. Next, we describe innate object behaviors in a flight simulator paradigm in both freely rotating, magnetically-tethered and yaw-restricted, rigidly-tethered melanogaster. The experimental paradigm in rigidly-tethered flies is then modified to assess the effects of odor on object responses. In a paradigm in which visual stimuli positions were negatively coupled to the fly’s steering effort, we find that appetitive odor reduces the probability that flies engage in aversive behaviors in response to encountering small visual objects. In a complementary paradigm in which visual stimuli position were restricted to the visual periphery, we show that the presence of appetitive food odors reverses innate object avoidance to attraction, whereby flies begin to approach and track the small object. We term this behavior odor-induced visual valence reversal. Subsequently, we show through optogenetic activation studies that this modulation seems in part to be induced by the neuromodulator octopamine, the insect orthologs of norepinephrine, as well as small-field visual motion detectors, T4/T5 neurons. Efforts to assess whether octopamine and T4/T5 neurons mediate object valence reversal via the same neural circuit were inconclusive, likely due to off-target effects and genetic backgrounds. Separately, in vivo calcium imaging of T4/T5 responses to visual objects with pharmacological application of octopamine or its agonist, chlordimeform, suggest that variation in T4/T5 visual responses were likely due to the quiescent animal’s internal state. Our results identify neural components involved in olfactory modulation of object vision and highlight the importance to further assess the contributions of locomotion in understanding neuromodulatory mechanisms.

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