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Multisensory interactions regulate feeding behavior in Drosophila

Significance Many studies show how a single sensory cue contributes to behaviors. To better understand external environments, however, animals use multisensory integration, referring to the enhancement of response induced by single sensory cue due to concurrent inputs from other sensory modalities. We show the proboscis extension reflex (PER), a proxy for food preference, is accomplished via multisensory integration in Drosophila. The taste-evoked PER is significantly enhanced by concurrent inputs of food odor and texture. Controlled delivery of three different sensory cues proves the simultaneous activation of three distinct sensory modalities produces a supraadditive PER. Our work shows flies employ an efficient way to find and ingest foods when the taste of the food alone is insufficient to stimulate feeding. The integration of two or more distinct sensory cues can help animals make more informed decisions about potential food sources, but little is known about how feeding-related multimodal sensory integration happens at the cellular and molecular levels. Here, we show that multimodal sensory integration contributes to a stereotyped feeding behavior in the model organism Drosophila melanogaster. Simultaneous olfactory and mechanosensory inputs significantly influence a taste-evoked feeding behavior called the proboscis extension reflex (PER). Olfactory and mechanical information are mediated by antennal Or35a neurons and leg hair plate mechanosensory neurons, respectively. We show that the controlled delivery of three different sensory cues can produce a supra-additive PER via the concurrent stimulation of olfactory, taste, and mechanosensory inputs. We suggest that the fruit fly is a versatile model system to study multisensory integration related to feeding, which also likely exists in vertebrates.