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.
Additional Information
The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under a CC-BY-NC-ND 4.0 International license. We thank M. Dickinson for sharing Canton-S flies and members of the Dickinson lab for advice on fly tracking. We thank D. J. Anderson for sharing unpublished flies. We are grateful to D. A. Wagenaar and the Caltech Neurotechnology Core for collaborating on the design and construction of the odor trap cores and the custom fly rearing device. We thank V. Hauser and A. Ruiz Sandoval for assisting with fly food preparation, and D. Kim, B. G. Fang, J. Eden-Sung, and J. Saltzman for assistance with processing video data. We thank members of the Hong lab for their careful reading and comments on this manuscript. This work was funded by grants to E.J.H. from the NSF/CIHR/DFG/FRQ/UKRI-MRC Next Generation Networks for Neuroscience Program (NeuroNex Award #2014217) and the Shurl and Kay Curci Foundation. K.V.D. was supported by grants from the Della Martin Foundation and the German Research Foundation (DY 135/1-1). E. J. H. is a Chen Scholar of the Tianqiao and Chrissy Chen Institute for Neuroscience and a Clare Boothe Luce Professor of the Henry Luce Foundation. AUTHOR CONTRIBUTIONS. Kristina V. Dylla: Conceptualization, Methodology, Investigation, Validation, Formal analysis, Writing – Original Draft, Writing – Review & Editing, Visualization. Thomas F. O' Connell: Methodology. Elizabeth J. Hong: Conceptualization, Methodology, Formal analysis, Writing – Original Draft, Writing – Review & Editing, Visualization, Supervision, Funding acquisition. The authors have declared no competing interest.Attached Files
Submitted - 2023.01.08.523155v1.full.pdf
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Additional details
- Eprint ID
- 120157
- Resolver ID
- CaltechAUTHORS:20230316-182588000.44
- DBI-2014217
- NSF
- Shurl and Kay Curci Foundation
- Della Martin Foundation
- DY 135/1-1
- Deutsche Forschungsgemeinschaft (DFG)
- Tianqiao and Chrissy Chen Institute for Neuroscience
- Clare Boothe Luce Professorship
- Created
-
2023-03-18Created from EPrint's datestamp field
- Updated
-
2023-03-18Created from EPrint's last_modified field
- Caltech groups
- Tianqiao and Chrissy Chen Institute for Neuroscience, Division of Biology and Biological Engineering