Abstract

To optimize fitness, animals must dynamically match food choices to their current needs. For drosophilids, yeast fulfills most dietary protein and micronutrient requirements. While several yeast metabolites activate known gustatory receptor neurons (GRNs) in Drosophila melanogaster, the chemosensory channels mediating yeast feeding remain unknown. Here we identify a class of proboscis GRNs required for yeast intake. Within this class, taste peg GRNs are specifically required to sustain yeast feeding. Sensillar GRNs, however, mediate feeding initiation. Furthermore, the response of yeast GRNs, but not sweet GRNs, is enhanced following deprivation from amino acids, providing a potential basis for protein-specific appetite. Although nutritional and reproductive states synergistically increase yeast appetite, reproductive state acts independently of nutritional state, modulating processing downstream of GRNs. Together, these results suggest that different internal states act at distinct levels of a dedicated gustatory circuit to elicit nutrient-specific appetites towards a complex, ecologically relevant protein source.

Highlights

  • Decision-making is a key function of the brain

  • We further demonstrate that the response of these sensory neurons to yeast is modulated by the internal amino acids (AAs) state of the fly: deprivation from dietary AAs increases both yeast feeding and the gain of sensory neuron responses

  • While sugars provide flies with energy, yeast is the primary source of non-caloric nutrients for the adult fly, and of amino acids (AAs) and proteins

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Summary

Introduction

Decision-making is a key function of the brain. One of the most ancestral and consequential decisions animals need to make is which foods to eat, since balancing the intake of multiple classes of nutrients is critical to optimizing lifespan and reproduction[1]. Several populations of central neurons driving consumption of specific nutrients have been identified in different species[6,7,8,9] How these circuits modulate sensory processing to elicit state-specific behavioral responses, is poorly understood. Protein is essential for sustaining key physiological processes such as reproduction, excessive protein intake has detrimental effects on aging and health[16,17,18,19,20]. This emphasizes the importance of this tight control of protein intake

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