Most primary olfactory neurons have individually neutral effects on behavior
Abstract
Animals use olfactory receptors to navigate mates, food, and danger. However, for complex olfactory systems, it is unknown what proportion of primary olfactory sensory neurons can individually drive avoidance or attraction. Similarly, the rules that govern behavioral responses to receptor combinations are unclear. We used optogenetic analysis in Drosophila to map the behavior elicited by olfactory-receptor neuron (ORN) classes: just one-fifth of ORN-types drove either avoidance or attraction. Although wind and hunger are closely linked to olfaction, neither had much effect on single-class responses. Several pooling rules have been invoked to explain how ORN types combine their behavioral influences; we activated two-way combinations and compared patterns of single- and double-ORN responses: these comparisons were inconsistent with simple pooling. We infer that the majority of primary olfactory sensory neurons have neutral behavioral effects individually, but participate in broad, odor-elicited ensembles with potent behavioral effects arising from complex interactions.
Data availability
Data and code availability:All of the data generated by this study are available to download from Zenodo (https://doi.org/10.5281/zenodo.3994033). The code is available at https://github.com/ttumkaya/WALiSuite_V2.0.
-
Dataset for: Majority of olfactory-receptor neurons have individually neutral effects on behaviorZenodo, 10.5281/zenodo.3994033.
Article and author information
Author details
Funding
Agency for Science, Technology and Research (AGA-SINGA)
- Tayfun Tumkaya
Agency for Science, Technology and Research (Block grant)
- Tayfun Tumkaya
- James Stewart
- Hyungwon Choi
- Adam Claridge-Chang
Ministry of Education - Singapore (MOE2013-T2-2-054)
- Tayfun Tumkaya
- James Stewart
- Adam Claridge-Chang
Ministry of Education - Singapore (MOE2017-T2-1-089)
- Tayfun Tumkaya
- James Stewart
- Adam Claridge-Chang
Ministry of Education - Singapore (MOE-2016-T2-1-001)
- Hyungwon Choi
National Medical Research Council (NMRC-CG-2017-M009)
- Hyungwon Choi
Duke-NUS Medical School (Block grant)
- Adam Claridge-Chang
Agency for Science, Technology and Research (JCO-1231AFG030)
- James Stewart
- Adam Claridge-Chang
Agency for Science, Technology and Research (JCO-1431AFG120)
- James Stewart
- Adam Claridge-Chang
The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.
Copyright
© 2022, Tumkaya 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.
Metrics
-
- 1,954
- views
-
- 281
- downloads
-
- 12
- citations
Views, downloads and citations are aggregated across all versions of this paper published by eLife.
Download links
Downloads (link to download the article as PDF)
Open citations (links to open the citations from this article in various online reference manager services)
Cite this article (links to download the citations from this article in formats compatible with various reference manager tools)
Further reading
-
- Neuroscience
γ-Secretase plays a pivotal role in the central nervous system. Our recent development of genetically encoded Förster resonance energy transfer (FRET)-based biosensors has enabled the spatiotemporal recording of γ-secretase activity on a cell-by-cell basis in live neurons in culture. Nevertheless, how γ-secretase activity is regulated in vivo remains unclear. Here, we employ the near-infrared (NIR) C99 720–670 biosensor and NIR confocal microscopy to quantitatively record γ-secretase activity in individual neurons in living mouse brains. Intriguingly, we uncovered that γ-secretase activity may influence the activity of γ-secretase in neighboring neurons, suggesting a potential ‘cell non-autonomous’ regulation of γ-secretase in mouse brains. Given that γ-secretase plays critical roles in important biological events and various diseases, our new assay in vivo would become a new platform that enables dissecting the essential roles of γ-secretase in normal health and diseases.
-
- Neuroscience
The neurotransmitter dopamine helps form long-term memories by increasing the production of proteins through a unique signaling pathway.