Olfactory responses of Drosophila are encoded in the organization of projection neurons
Abstract
The projection neurons (PNs), reconstructed from electron microscope (EM) images of the Drosophila olfactory system, offer a detailed view of neuronal anatomy, providing glimpses into information flow in the brain. About 150 uPNs constituting 58 glomeruli in the antennal lobe (AL) are bundled together in the axonal extension, routing the olfactory signal received at AL to mushroom body (MB) calyx and lateral horn (LH). Here we quantify the neuronal organization in terms of the inter-PN distances and examine its relationship with the odor types sensed by Drosophila. The homotypic uPNs that constitute glomeruli are tightly bundled and stereotyped in position throughout the neuropils, even though the glomerular PN organization in AL is no longer sustained in the higher brain center. Instead, odor-type dependent clusters consisting of multiple homotypes innervate the MB calyx and LH. Pheromone-encoding and hygro/thermo-sensing homotypes are spatially segregated in MB calyx, whereas two distinct clusters of food-related homotypes are found in LH in addition to the segregation of pheromone-encoding and hygro/thermo-sensing homotypes. We find that there are statistically significant associations between the spatial organization among a group of homotypic uPNs and certain stereotyped olfactory responses. Additionally, the signals from some of the tightly bundled homotypes converge to a specific group of lateral horn neurons (LHNs), which indicates that homotype (or odor type) specific integration of signals occurs at the synaptic interface between PNs and LHNs. Our findings suggest that before neural computation in the inner brain, some of the olfactory information are already encoded in the spatial organization of uPNs, illuminating that a certain degree of labeled-line strategy is at work in the Drosophila olfactory system.
Data availability
All data generated during this study and Python script are available in DrosophilaOlfaction-main.zip included as the supporting file. They are also available at https://github.com/kirichoi/DrosophilaOlfaction.
Article and author information
Author details
Funding
KIAS individual grant (CG077001)
- Kiri Choi
KIAS individual grant (CG076002)
- Won Kyu Kim
KIAS individual grant (CG035003)
- Changbong Hyeon
The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.
Reviewing Editor
- Sonia Sen, Tata Institute for Genetics and Society, India
Version history
- Received: February 9, 2022
- Preprint posted: February 25, 2022 (view preprint)
- Accepted: September 18, 2022
- Accepted Manuscript published: September 29, 2022 (version 1)
- Version of Record published: October 28, 2022 (version 2)
Copyright
© 2022, Choi 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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