Developmental Olfactory Experience Dissociates Hedonic Valence from Exploratory Arousal in Drosophila melanogaster

Abstract

Insects rely on olfactory cues to navigate complex environments, with many innate behaviors governed by evolutionary hardwired neural circuits. However, the extent to which early-life sensory experience can recalibrate these innate responses remains a subject of intense debate. Here, we investigate how chronic exposure to odorants of varying innate valences during development and early adulthood modulates olfactory preference and exploratory drive in Drosophila melanogaster. Using a high-resolution two-choice assay, we demonstrate a fundamental functional dissociation in olfactory plasticity: while the innate hedonic valence of most odorants remains remarkably resilient to developmental environmental manipulation, early-life experience profoundly reprograms exploratory dynamics. Specifically, chronic exposure to propionic acid and benzaldehyde induced sex-specific shifts in locomotor arousal and trap-entry decisions without altering the intrinsic hedonic valuation of the stimuli. Conversely, general exploratory drive toward 1-octanol and isoamyl acetate remained rigidly hardwired, although 1-octanol exhibited subtle, experience-dependent habituation in odor preference. This resilience of innate valence suggests that the olfactory circuit actively prioritizes functional stability to ensure that critical ecological cues remain reliably encoded. Our findings reveal that Drosophila employs a modular adaptive strategy to integrate chronic sensory information: unreinforced early-life experience selectively reconfigures motor reactivity to scale navigational intensity to familiar landscapes, while leaving primary sensory-driven valences largely intact.