Early life experience with natural odors modifies olfactory behavior through an associative process

Abstract

Past work has shown that chronic exposure of Drosophila to intense monomolecular odors in early life leads to homeostatic adaptation of olfactory neural responses and behavioral habituation to the familiar odor. Here, we found that, in contrast, persistent exposure to natural odors in early life increases behavioral attraction selectively to familiar odors. Odor experience increases the attractiveness of natural odors that are innately attractive and decreases the aversiveness of natural odors that are innately aversive. These changes in olfactory behavior are unlikely to arise from changes in the sensitivity of olfactory neurons at the first stages of olfactory processing: odor-evoked output from antennal lobe projection neurons was unchanged by chronic exposure to natural odors in terms of olfactory sensitivity, relational distances between odors, or response dynamics. We reveal a requirement for additional features of the environment beyond the odor in establishing odor experience-dependent behavioral plasticity. Passive odor exposure in a featureless environment lacking strong reinforcing cues was insufficient to elicit changes in olfactory preference; however, the same odor exposure resulted in behavioral plasticity when food was present in the environment. Together, these results indicate that behavioral plasticity elicited by persistent exposure to natural odors in early life is mediated by an associative process. In addition, they highlight the importance of using naturalistic odor stimuli for investigating olfactory function.

Chronic exposure to odors at naturally occurring concentrations triggers limited plasticity in early stages of Drosophila olfactory processing

“…In one study where flies were chronically exposed to monomolecular odors at lower concentrations (~0.01–1%) that are attractive to flies, odor experience increased behavioral attraction toward the familiar odor ( Chakraborty et al, 2009 ). In agreement, other work from our laboratory shows that chronic exposure of flies in early life to odors from natural sources increases behavioral attraction to these odors ( Dylla et al, 2023 ). These observations argue against habituation being the dominant effect of chronic odor exposure on behavior since, if that were the case, reduced attraction to familiar attractive odors is expected.…”

Experience-dependent plasticity of a highly specific olfactory circuit inDrosophila melanogaster

“…Our findings contradict some earlier results that either showed a general decrease (Das et al, 2011;McCann et al, 2011;Sachse et al, 2007;Sudhakaran et al, 2013) or an increase (Kidd & Lieber, 2016;Kidd et al, 2015) of PN signaling after long-term odor exposure. The consistency of the neuronal signals we observed within the circuit indicates that physiological changes downstream of PNs may be responsible for the behavioral effects, as also suggested by two recent studies (Dylla et al, 2023;Gugel et al, 2023) that obtained similar physiological results. It is conceivable that glomerulus-or odor-specific mechanisms cause the different physiological effects observed across studies.…”

“…Although some previous studies demonstrated that long-term exposure of odorants causes behavioral changes in flies (Chodankar et al, 2020;Devaud et al, 2001;Devaud et al, 2003;McCann et al, 2011;Sachse et al, 2007;Sudhakaran et al, 2013), it was never shown that such changes can also be induced by a highly specific and unambiguous odorant like geosmin. Our T-maze and oviposition experiments demonstrated that female flies previously exposed to geosmin were subsequently less repelled by this odorant, likely due to an associative learning process (Dylla et al, 2023). This challenges the postulated predictability in the behavioral outcome of "labeled line" signaling in the olfactory system (Keesey & Hansson, 2021).…”