NEURAL CIRCUITS THAT REGULATE EXPLORATORY ODOR-DRIVEN BEHAVIOR

Successful exploration requires the flexibility to rapidly override innate drives and adjust strategies when expectations are unmet. During foraging, for example, animals flexibly use known olfactory cues to locate possible food sources. The neural circuits and computations that control flexible odour driven exploration remain poorly understood.
Here we study the adaptive decision process of fruit flies when they disengage from an unrewarded appetitive odour in a free-walking assay. We show that flies re-evaluate their approach of an appetitive cue in the absence of reward, regardless of starvation state and even when the odour has been explicitly associated to a sugar reward. This flexibility is valence-specific and requires active behaviour, as flies persistently avoid innately aversive odours despite the absence of an explicit punishment.
In insects, innate olfactory behaviours are driven by the lateral horn (LH) and modulated through learning by the mushroom body (MB). We hypothesized that the transition from pursuing a cue to exploring the environment required the continuous update of MB output via dopamine signalling to override innate LH-drive. Surprisingly, acute silencing of the MB and MB-associated dopaminergic neurons (PAM and PPL1) didn’t impair behavioural re-evaluation of innately appetitive odours. Instead, blocking the synaptic output of a subset of DANs acting outside of the canonical MB learning pathway prevented flies from abandoning the unrewarded appetitive odour source, leading to a maladaptive accumulation at the odour location. Together, these findings identify a previously unrecognized dopaminergic pathway that overrides innate biases enabling adaptive adjustment of foraging strategies.