Adaptive Expansion of Taste Neuron Response Profiles by Congruent Aroma in Drosophila

Pairing of food aroma with selected taste can lead to enhanced food flavor and eating euphoria, but how cross-modal sensory combinations are integrated to increase food reward value remains largely unclear. Here we report that combined stimulation by food aroma and taste drastically increased appetite in well-nourished Drosophila larvae, and the appetizing effect involves a previously uncharacterized smell-taste integration process at axon terminals of two Gr43a gustatory neurons. Molecular genetic analyses of the smell-taste integration reveal a G protein-mediated tuning mechanism in two central neuropeptide F (NPF) neurons. This mechanism converts selected odor stimuli to NPF-encoded appetizing signals that potentiate Gr43a neuronal response to otherwise non-stimulating glucose or oleic acid. Further, NPF-potentiated responses to glucose and oleic acid require a Gr43a-independent and Gr43a-dependent pathway, respectively. Our finding of adaptive expansion of taste neuron response profiles by congruent aroma reveals a previously uncharacterized layer of neural complexity in food flavor perception.