Odors drive feeding through gustatory receptor neurons in Drosophila

Abstract

Odors are intimately tied to the taste system to aid food selection and determine the sensory experience of food. However, how smell and taste are integrated in the nervous system to drive feeding remains elusive. We show in Drosophila that odors alone activate gustatory receptor neurons (GRNs), trigger proboscis extension reflex (PER), a canonical taste-evoked feeding behavior, and enhance food intake. Odor-evoked PER requires the function of sugar-sensing GRNs but not olfactory organs. Calcium imaging and electrophysiological recording show that GRNs directly respond to odors. Odor-evoked PER is mediated by the Gr5a receptor, and is bidirectionally modulated by olfactory binding proteins. Finally, odors and sucrose co-applied to GRNs synergistically enhance PER and food consumption. These results reveal a cell-intrinsic mechanism for odor-taste multimodal integration that takes place as early as in GRNs, indicating that unified chemosensory experience is a product of layered integration in peripheral neurons and in the brain.