Origin of wiring specificity in an olfactory map revealed by neuron type-specific, time-lapse imaging of dendrite targeting

Abstract
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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.

The following previously published data sets were used

1. Xie Q
2. Brbic M
3. Horns F
4. Kolluru SS
5. Jones RC
6. Li J
7. Reddy AR
8. Xie A
9. Kohani S
10. Li Z
11. McLaughlin CN
12. Li T
13. Xu C
14. Vacek D
15. Luginbuhl DJ
16. Leskovec J
17. Quake SR
18. Luo L
19. Li H
(2021) Temporal evolution of single-cell transcriptomes of Drosophila olfactory projection neurons
NCBI Gene Expression Omnibus, GSE161228.

https://www.ncbi.nlm.nih.gov/geo/query/acc.cgi?acc=GSE161228

Article and author information

Author details

Kenneth Kin Lam Wong

1Department of Biology, Howard Hughes Medical Institute, Stanford University, Stanford, United States

Competing interests
The authors declare that no competing interests exist.
Tongchao Li

1Department of Biology, Howard Hughes Medical Institute, Stanford University, Stanford, United States

For correspondence
ltongchao@outlook.com

Competing interests
The authors declare that no competing interests exist.
Tian-Ming Fu

Janelia Research Campus, Ashburn, United States

Competing interests
The authors declare that no competing interests exist.

"This ORCID iD identifies the author of this article:" 0000-0001-6265-0859
Gaoxiang Liu

Department of Molecular and Cell Biology, University of California, Berkeley, Berkeley, United States

Competing interests
The authors declare that no competing interests exist.
Cheng Lyu

Department of Biology, Howard Hughes Medical Institute, Stanford University, Stanford, United States

Competing interests
The authors declare that no competing interests exist.
Sayeh Kohani

Department of Biology, Howard Hughes Medical Institute, Stanford University, Stanford, United States

Competing interests
The authors declare that no competing interests exist.
Qijing Xie

Department of Biology, Howard Hughes Medical Institute, Stanford University, Stanford, United States

Competing interests
The authors declare that no competing interests exist.
David J Luginbuhl

Department of Biology, Howard Hughes Medical Institute, Stanford University, Stanford, United States

Competing interests
The authors declare that no competing interests exist.
Srigokul Upadhyayula

Department of Molecular and Cell Biology, University of California, Berkeley, Berkeley, United States

Competing interests
The authors declare that no competing interests exist.
Eric Betzig

Janelia Research Campus, Ashburn, United States

Competing interests
The authors declare that no competing interests exist.
Liqun Luo

Department of Biology, Howard Hughes Medical Institute, Stanford University, Stanford, United States

For correspondence
lluo@stanford.edu

Competing interests
The authors declare that no competing interests exist.

"This ORCID iD identifies the author of this article:" 0000-0001-5467-9264

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.

Copyright

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.