A peripheral feedforward circuit amplifies taste signals, ensuring behavioral reliability

Mechanisms ensuring reliable behavioral control amid complex, noisy sensory environments are often attributed to the central brain, yet computations occurring at the extreme sensory periphery remain poorly understood. Recent evidence hints at complex computations at the earliest stages of taste detection, but whether peripheral circuits of gustatory receptor neurons (GRNs) exist to perform them remains unknown. Here, using transsynaptic mapping and paired electrophysiological recordings in Drosophila, we reveal a feedforward circuit of monosynaptically connected GRNs. When driven by tastants, these GRNs significantly increase the spiking of follower GRNs, thus integrating, amplifying, and stabilizing taste signals before they reach the central nervous system. Connectivity among these GRNs is selective and directional rather than all-to-all and is mediated by the nicotinic acetylcholine alpha 5 receptor subunit. Genetic ablation of this subunit significantly impairs functional interactions between GRNs and significantly decreases the reliability of taste-driven behaviors, with the phenotypes being reversed by cell-specific rescue of receptor expression. These results demonstrate that GRNs are organized into functional circuits that stabilize taste signals and gustatory behaviors.