Chronic exposure to odors at naturally occurring concentrations triggers limited plasticity in early stages of Drosophila olfactory processing
- California Institute of Technology, United States
Abstract
In insects and mammals, olfactory experience in early life alters olfactory behavior and function in later life. In the vinegar fly Drosophila, flies chronically exposed to a high concentration of a monomolecular odor exhibit reduced behavioral aversion to the familiar odor when it is re-encountered. This change in olfactory behavior has been attributed to selective decreases in the sensitivity of second-order olfactory projection neurons (PNs) in the antennal lobe that respond to the overrepresented odor. However, since odorant compounds do not occur at similarly high concentrations in natural sources, the role of odor experience-dependent plasticity in natural environments is unclear. Here, we investigated olfactory plasticity in the antennal lobe of flies chronically exposed to odors at concentrations that are typically encountered in natural odor sources. These stimuli were chosen to each strongly and selectively excite a single class of primary olfactory receptor neuron (ORN), thus facilitating a rigorous assessment of the selectivity of olfactory plasticity for PNs directly excited by overrepresented stimuli. Unexpectedly, we found that chronic exposure to three such odors did not result in decreased PN sensitivity, but rather mildly increased responses to weak stimuli in most PN types. Odor-evoked PN activity in response to stronger stimuli was mostly unaffected by odor experience. When present, plasticity was observed broadly in multiple PN types and thus was not selective for PNs receiving direct input from the chronically active ORNs. We further investigated the DL5 olfactory coding channel and found that chronic odor-mediated excitation of its input ORNs did not affect PN intrinsic properties, local inhibitory innervation, ORN responses, or ORN-PN synaptic strength; however, broad-acting lateral excitation evoked by some odors was increased. These results show that PN odor coding is only mildly affected by strong persistent activation of a single olfactory input, highlighting the stability of early stages of insect olfactory processing to significant perturbations in the sensory environment.
Data availability
The new transgenic fly generated in this study, Or7a-lexA (III), will be deposited in the Bloomington Drosophila Resource Center for public distribution. Source data from electrophysiology, functional imaging, and confocal imaging experiments used to generate Figures 2-7 are publicly available on the Dryad repository (https://doi.org/10.5061/dryad.v15dv420q).
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Gugel, Maurais, Hong (2022). Source data figures 2-7Dryad Digital Repository, doi:10.5061/dryad.v15dv420q.
Article and author information
Author details
Elizabeth G Maurais
Funding
National Science Foundation (Award #1556230)
- Elizabeth J Hong
National Institutes of Health (1RF1MH117825)
- Elizabeth J Hong
Shurl and Kay Curci Foundation
- Elizabeth J Hong
Clare Boothe Luce professorship
- Elizabeth J Hong
Amgen Scholars Program
- Elizabeth G Maurais
The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.
Copyright
© 2023, Gugel et al.
This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.
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Chronic exposure to odors at naturally occurring concentrations triggers limited plasticity in early stages of Drosophila olfactory processing
eLife 12:e85443.
https://doi.org/10.7554/eLife.85443
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