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Feeding, a critical behavior for survival, consists of a complex series of behavioral steps. In Drosophila larvae, the initial steps of feeding are food choice, during which the quality of a potential food source is judged, and ingestion, during which the selected food source is ingested into the digestive tract. It remains unclear whether these steps employ different mechanisms of neural perception. Here, we provide insight into the two initial steps of feeding in Drosophila larva. We find that substrate choice and ingestion are determined by independent circuits at the cellular level. First, we took 22 candidate bitter compounds and examined their influence on choice preference and ingestion behavior. Interestingly, certain bitter tastants caused different responses in choice and ingestion, suggesting distinct mechanisms of perception. We further provide evidence that certain gustatory receptor neurons (GRNs) in the external terminal organ (TO) are involved in determining choice preference, and a pair of larval pharyngeal GRNs is involved in mediating both avoidance and suppression of ingestion. Our results show that feeding behavior is coordinated by a multistep regulatory process employing relatively independent neural elements. These findings are consistent with a model in which distinct sensory pathways act as modulatory circuits controlling distinct subprograms during feeding.

Feeding, a critical behavior for survival, consists of a complex series of behavioral steps. In Drosophila larvae, the initial steps of feeding are food choice, during which the quality of a potential food source is judged, and ingestion, during which the selected food source is ingested into the digestive tract. It remains unclear whether these steps employ different mechanisms of neural perception. Here, we provide insight into the two initial steps of feeding in Drosophila larva. We find that substrate choice and ingestion are determined by independent circuits at the cellular level. First, we took 22 candidate bitter compounds and examined their influence on choice preference and ingestion behavior. Interestingly, certain bitter tastants caused different responses in choice and ingestion, suggesting distinct mechanisms of perception. We further provide evidence that certain gustatory receptor neurons (GRNs) in the external terminal organ are involved in determining choice preference, and a pair of larval pharyngeal GRNs is involved in mediating both avoidance and suppression of ingestion. Our results show that feeding behavior is coordinated by a multi-step regulatory process employing relatively independent neural elements. These findings are consistent with a model in which distinct sensory pathways act as modulatory circuits controlling distinct subprograms during feeding. Significance Statement Here we provide molecular and cellular evidence that feeding can indeed be dissected into two distinct steps, namely the determination of preference and initiation of ingestion. We find that bitter tastants have individual characteristics when negatively affecting feeding, with most chemicals negatively affecting both preference and ingestion, and certain chemicals negatively affecting only preference. These characteristics are due to different sensory neurons being responsible for detecting different bitter compounds. The different sensory neurons appear to act in relatively independent neural circuits to differentially affect the multiple steps that comprise feeding.