Modulation of taste sensitivity by the olfactory system inDrosophila

Abstract

An animal's 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 another. Typically, dysfunction of one sense has been associated with elevated function of others, creating a type of sensory homeostasis. 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 communication. 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 taste. However, human studies specifically examining taste are mixed and generally do not support this widely-held belief, and data from animal models is largely lacking. 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.

Olfactory Senses Modulate Food Consumption and Physiology in Drosophila melanogaster

“…The rating of hunger is increased following exposure to food-related odors (Rogers and Hill, 1989). Recent studies found that loss of olfactory input dramatically increases taste sensitivity, which is starvation-independent (Junca et al, 2021). Thus, blocking olfactory signaling inhibits food intake, which may be due to inhibiting appetite behavior.…”

Cross-modal sensory compensation increases mosquito attraction to humans

“…These changes depended on long-distance serotonin signaling originating from the raphe nuclei (10,11). More recently, a study conducted in Drosophila melanogaster flies showed that loss of olfaction led to an enhanced sensitivity to detect sugar that was mediated through an elevated sugar response by the protocerebrum anterior medial dopaminergic neurons in the mushroom body (12). These anatomical and functional studies highlight the diverse mechanisms that each sensory system and organism employs while also emphasizing the shared necessity of the process of sensory compensation.…”

Drosophila olfaction: past, present and future

“…There is also growing appreciation that, as in humans, odours induce many other responses in D. melanogaster that do not directly involve locomotor circuitry, but rather impinge upon other neural or endocrine pathways. For example, olfactory perception (or lack of) can affect taste sensation (preprint [ 239 ]), modulate food ingestion and metabolism [ 240 ], contribute to maintenance and development of blood progenitors [ 241 , 242 ], as well as influence general stress responses and lifespan [ 243 ]. When flies do not visibly react to an odour, the olfactory system might still be meaningfully processing the sensory information.…”