Abstract
Fat represents a calorically potent food source that yields approximately twice the amount of energy as carbohydrates or proteins per unit of mass. The highly palatable taste of free fatty acids (FAs), one of the building blocks of fat, promotes food consumption, activates reward circuitry, and is thought to contribute to hedonic feeding underlying many metabolism-related disorders. Despite a role in the etiology of metabolic diseases, little is known about how dietary fats are detected by the gustatory system to promote feeding. Previously, we showed that a broad population of sugar-sensing taste neurons expressing Gustatory Receptor 64f (Gr64f) is required for reflexive feeding responses to both FAs and sugars. Here, we report a genetic silencing screen to identify specific populations of taste neurons that mediate fatty acid (FA) taste. We find neurons identified by expression of Ionotropic Receptor 56d (IR56d) are necessary and sufficient for reflexive feeding response to FAs. Functional imaging reveals that IR56d-expressing neurons are responsive to short- and medium-chain FAs. Silencing IR56d neurons selectively abolishes FA taste, and their activation is sufficient to drive feeding responses. Analysis of co-expression with Gr64f identifies two subpopulations of IR56d-expressing neurons. While physiological imaging reveals that both populations are responsive to FAs, IR56d/Gr64f neurons are activated by medium-chain FAs and are sufficient for reflexive feeding response to FAs. Moreover, flies can discriminate between sugar and FAs in an aversive taste memory assay, indicating that FA taste is a unique modality in Drosophila. Taken together, these findings localize FA taste within the Drosophila gustatory center and provide an opportunity to investigate discrimination between different categories of appetitive tastants.
Highlights
Fat represents a calorically potent food source that yields approximately twice the amount of energy as carbohydrates or proteins per unit of mass
We previously reported that silencing Gustatory Receptor 64f (Gr64f)-expressing taste neurons abolishes behavioral responses to both sugars and fatty acids (FAs) [10]
Our findings reveal the population of Ionotropic Receptor 56d (IR56d) neurons that innervate the anterior subesophageal zone (SEZ), which emanate from the taste pegs, are dispensable for Proboscis Extension Reflex (PER) in response to FAs
Summary
Fat represents a calorically potent food source that yields approximately twice the amount of energy as carbohydrates or proteins per unit of mass. Tastants are sensed by dedicated gustatory receptors that localize to the taste cells or taste receptor neurons [10,11,12] These cells are sensitive to different taste modalities such as sweet, bitter, salty, sour, or umami, and project to higher order brain structures for processing [10,13,14]. While these taste modalities have been extensively studied, much less is known about how FAs are detected and how this sensory stimulus is processed. Any further characteristics of the physiological response or the specific neuronal identity of the neurons mediating FA response are unknown
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