Olfactory and Neuromodulatory Signals Reverse Visual Object Avoidance to Approach in Drosophila

Behavioral reactions of animals to environmental sensory stimuli are sometimes reflexive and stereotyped but can also vary depending on contextual conditions. Engaging in active foraging or flight provokes a reversal in the valence of carbon dioxide responses from aversion to approach in Drosophila [1, 2], whereas mosquitoes encountering this same chemical cue show enhanced approach toward a small visual object [3]. Sensory plasticity in insects has been broadly attributed to the action of biogenic amines, which modulate behaviors such as olfactory learning, aggression, feeding, and egg laying [4–14]. Octopamine acts rapidly upon the onset of flight to modulate the response gain of directionally selective motion-detecting neurons in Drosophila [15]. How the action of biogenic amines might couple sensory modalities to each other or to locomotive states remains poorly understood. Here, we use a visual flight simulator [16] equipped for odor delivery [17] to confirm that flies avoid a small contrasting visual object in odorless air [18] but that the same animals reverse their preference to approach in the presence of attractive food odor. An aversive odor does not reverse object aversion. Optogenetic activation of either octopaminergic neurons or directionally selective motion-detecting neurons that express octopamine receptors elicits visual valence reversal in the absence of odor. Our results suggest a parsimonious model in which odor-activated octopamine release excites the motion detection pathway to increase the saliency of either a small object or a bar, eliciting tracking responses by both visual features. •A fly’s innate aversion to a small visual object is reversed by odor•Object valence is reversed by attractive odors but not an aversive one•Activating octopaminergic neurons is sufficient to reverse object valence•Motion-detecting neurons are necessary and sufficient to reverse object valence Cheng et al. report on a novel multisensory behavior in Drosophila. The innate aversion to a small visual object in flight is reversed to approach in an attractive food odor. Object valence reversal can be elicited by optogenetic stimulation of octopaminergic neurons and requires the activity of columnar directional motion-detecting neurons.