Abstract

The sense of taste is an essential chemosensory modality that enables animals to identify appropriate food sources and control feeding behavior. In particular, the recognition of bitter taste prevents animals from feeding on harmful substances. Feeding is a complex behavior comprised of multiple steps, and food quality is continuously assessed. We here examined the role of pharyngeal gustatory organs in ingestion behavior. As a first step, we constructed a gustatory receptor-to-neuron map of the larval pharyngeal sense organs, and examined corresponding gustatory receptor neuron (GRN) projections in the larval brain. Out of 22 candidate bitter compounds, we found 14 bitter compounds that elicit inhibition of ingestion in a dose-dependent manner. We provide evidence that certain pharyngeal GRNs are necessary and sufficient for the ingestion response of larvae to caffeine. Additionally, we show that a specific pair of pharyngeal GRNs, DP1, responds to caffeine by calcium imaging. In this study we show that a specific pair of GRNs in the pharyngeal sense organs coordinates caffeine sensing with regulation of behavioral responses such as ingestion. Our results indicate that in Drosophila larvae, the pharyngeal GRNs have a major role in sensing food palatability to regulate ingestion behavior. The pharyngeal sense organs are prime candidates to influence ingestion due to their position in the pharynx, and they may act as first level sensors of ingested food.

Highlights

  • Food intake, or feeding, is composed of a series of behavioral modules or subprograms (Pool and Scott, 2014) that encompass the search for food, ingestion of food, digestion, and nutrient absorption

  • By combining molecular genetic tools, behavioral assays, and genetically coded calcium sensors to assess neuronal activity, we show that a specific pair of gustatory receptor neuron (GRN) in the pharyngeal sense organs, DP1, has a major role in caffeine-driven ingestion in Drosophila larvae

  • Gr9a-GAL4 expression was observed in the DPS in addition to the C1 neuron in the terminal organ, and Gr93d-GAL4 expression was observed in one pair of neurons in the DPS in addition to the previously reported expression in the PPS

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Summary

Introduction

Feeding, is composed of a series of behavioral modules or subprograms (Pool and Scott, 2014) that encompass the search for food, ingestion of food, digestion, and nutrient absorption. Once the food source is confirmed as palatable, foraging stops and meal consumption/ingestion is initiated. During this process, chemical cues of the food source are continuously assessed to determine if the food source qualifies for ingestion and digestion. Understanding the molecular and cellular basis of the sequential neural circuits involved in each step of feeding is still at an early stage. Foraging and ingesting food are extremely robust behaviors in Drosophila larvae, rendering it an ideal model to study the mechanisms of the initial feeding processes. A Caffeine-Sensing Pharyngeal Neuron in Drosophila Larvae

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