Origin of wiring specificity in an olfactory map revealed by neuron type-specific, time-lapse imaging of dendrite targeting
- Howard Hughes Medical Institute, Stanford University, United States
- Janelia Research Campus, United States
- University of California, Berkeley, United States
Abstract
How does wiring specificity of neural maps emerge during development? Formation of the adult Drosophila olfactory glomerular map begins with patterning of projection neuron (PN) dendrites at the early pupal stage. To better understand the origin of wiring specificity of this map, we created genetic tools to systematically characterize dendrite patterning across development at PN type-specific resolution. We find that PNs use lineage and birth order combinatorially to build the initial dendritic map. Specifically, birth order directs dendrite targeting in rotating and binary manners for PNs of the anterodorsal and lateral lineages, respectively. Two-photon- and adaptive optical lattice light-sheet microscope-based time-lapse imaging reveals that PN dendrites initiate active targeting with direction-dependent branch stabilization on the timescale of seconds. Moreover, PNs that are used in both the larval and adult olfactory circuits prune their larval-specific dendrites and re-extend new dendrites simultaneously to facilitate timely olfactory map organization. Our work highlights the power and necessity of type-specific neuronal access and time-lapse imaging in identifying wiring mechanisms that underlie complex patterns of functional neural maps.
Data availability
Figure 3 - Source Data 1, Figure 5 - Source Data 1, Figure 6 - Source Data 1, and Figure 7 - Source Data 1 contain the numerical and statistical data used to generate the figures.
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Temporal evolution of single-cell transcriptomes of Drosophila olfactory projection neuronsNCBI Gene Expression Omnibus, GSE161228.
Article and author information
Author details
Funding
National Institutes of Health (R01 DC005982)
- Liqun Luo
Philomathia Foundation
- Gaoxiang Liu
- Srigokul Upadhyayula
Chan Zuckerberg Initiative
- Srigokul Upadhyayula
National Institutes of Health (1K99DC01883001)
- Tongchao Li
Howard Hughes Medical Institute
- Eric Betzig
- Liqun Luo
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: December 11, 2022
- Preprint posted: December 29, 2022 (view preprint)
- Accepted: March 27, 2023
- Accepted Manuscript published: March 28, 2023 (version 1)
- Version of Record published: May 18, 2023 (version 2)
Copyright
© 2023, Wong 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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Origin of wiring specificity in an olfactory map revealed by neuron type-specific, time-lapse imaging of dendrite targeting
eLife 12:e85521.
https://doi.org/10.7554/eLife.85521
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