A neuronal ensemble encoding adaptive choice during sensory conflict

Abstract

Feeding decisions are fundamental to survival, and decision making is often disrupted in disease, yet the neuronal and molecular mechanisms of adaptive decision making are not well understood. Here we show that neural activity in a small population of neurons projecting to the fan-shaped body higher-order central brain region of Drosophila represents final food choice during sensory conflict. We found that hungry flies made tradeoffs between appetitive and aversive values of food in a decision making task to choose bittersweet food with high sucrose concentration, but adulterated with bitter quinine, over sweet-only food with less sucrose. Using cell-specific optogenetics and receptor RNAi knockdown during the decision task, we identified an upstream neuropeptidergic and dopaminergic network that relays internal state and other decision-relevant information, such as valence and previous experience, to a specific subset of fan-shaped body neurons. Importantly, calcium imaging revealed that these neurons were strongly inhibited by the taste of the rejected food choice, suggesting that they encode final behavioral food choice. Our findings reveal that fan-shaped body taste responses to food choices are determined not only by taste quality, but also by previous experience (including choice outcome) and hunger state, which are integrated in the fan-shaped body to encode the decision before relay to downstream motor circuits for behavioral implementation. Our results uncover a novel role for the fan-shaped body in choice encoding, and reveal a neural substrate for sensory and internal state integration for decision making in a genetically tractable model organism to enable mechanistic dissection at circuit, cellular, and molecular levels.