Segregation of Odor Identity and Intensity during Odor Discrimination in Drosophila Mushroom Body

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Abstract
Molecular and cellular studies have begun to unravel a neurobiological basis of olfactory processing, which appears conserved among vertebrate and invertebrate species. Studies have shown clearly that experience-dependent coding of odor identity occurs in “associative” olfactory centers (the piriform cortex in mammals and the mushroom body [MB] in insects). What remains unclear, however, is whether associative centers also mediate innate (spontaneous) odor discrimination and how ongoing experience modifies odor discrimination. Here we show in naïve flies that Gαq-mediated signaling in MB modulates spontaneous discrimination of odor identity but not odor intensity (concentration). In contrast, experience-dependent modification (conditioning) of both odor identity and intensity occurs in MB exclusively via Gαs-mediated signaling. Our data suggest that spontaneous responses to odor identity and odor intensity discrimination are segregated at the MB level, and neural activity from MB further modulates olfactory processing by experience-independent Gαq-dependent encoding of odor identity and by experience-induced Gαs-dependent encoding of odor intensity and identity. Considerable progress has been made in understanding how olfaction works as the receptor proteins, sensory neurons, and brain circuitry responsible have become increasingly well-characterized. However, olfactory processing in higher brain centers, where neuronal activity is assembled into the perception of odor quality, is poorly understood. Here, we have addressed how the mushroom body (MB)—a secondary olfactory center—is involved in olfactory discrimination. We manipulated the MB by ablation, disruption of synaptic transmission, and interruption of key cellular signaling molecules in naïve flies and in flies trained to discriminate odors. We first show that although both odor identity and intensity are encoded in the MB, only the former requires Gαq-dependent signaling and is necessary for naïve flies to spontaneously discriminate different odors. We then show that training flies to alter their olfactory response requires Gαs-mediated signaling in MB for both odor intensity and odor identity. We have thus identified (i) segregation of odor identity and odor intensity at the MB level in naïve flies and (ii) different G-protein-dependent signaling pathways for spontaneous versus experience-dependent olfactory discrimination.