Modulation of taste sensitivity by the olfactory system in Drosophila

An animals sensory percepts are not raw representations of the outside world. Rather, they are constructs influenced by many factors including the species, past experiences, and internal states. One source of perceptual variability that has fascinated researchers for decades is the effect of losing one sensory modality on the performance of another1. Typically, dysfunction of one sense has been associated with elevated function of others, creating a type of sensory homeostasis2. For example, people with vision loss have been reported to demonstrate enhanced tactile and auditory functions, and deafness has been associated with heightened attention to visual inputs for communication3,4. By contrast, smell and taste--the two chemosensory modalities--are so intrinsically linked in their contributions to flavor that loss of smell is often anecdotally reported as leading to deficiencies in taste5-8. However, human studies specifically examining taste are mixed and generally do not support this widely-held belief, and data from animal models is largely lacking9. Here, we examine the impact of olfactory dysfunction on taste sensitivity in Drosophila melanogaster. We find that partial loss of olfactory input (hyposmia) dramatically enhances flies sensitivity to both appetitive (sugar, low salt) and aversive (bitter, high salt) tastes. This taste enhancement is starvation-independent and occurs following suppression of either first- or second-order olfactory neurons. Moreover, optogenetically increasing olfactory inputs reduces taste sensitivity. Finally, we observed that taste enhancement is not encoded in the activity of peripheral gustatory sensory neurons, but is associated with elevated sugar responses in protocerebrum anterior medial (PAM) dopaminergic neurons of the mushroom bodies. These results suggest a level of homeostatic control over chemosensation, where flies compensate for lack of olfactory input by increasing the salience of taste information.