1. Developmental Biology
  2. Neuroscience

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

  1. Kenneth Kin Lam Wong
  2. Tongchao Li  Is a corresponding author
  3. Tian-Ming Fu
  4. Gaoxiang Liu
  5. Cheng Lyu
  6. Sayeh Kohani
  7. Qijing Xie
  8. David J Luginbuhl
  9. Srigokul Upadhyayula
  10. Eric Betzig
  11. Liqun Luo  Is a corresponding author
  1. Howard Hughes Medical Institute, Stanford University, United States
  2. Janelia Research Campus, United States
  3. University of California, Berkeley, United States
https://doi.org/10.7554/eLife.85521
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Cite this article
  1. Kenneth Kin Lam Wong
  2. Tongchao Li
  3. Tian-Ming Fu
  4. Gaoxiang Liu
  5. Cheng Lyu
  6. Sayeh Kohani
  7. Qijing Xie
  8. David J Luginbuhl
  9. Srigokul Upadhyayula
  10. Eric Betzig
  11. Liqun Luo
(2023)
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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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

Article and author information

Author details

  1. 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.

  2. 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.

  3. Tian-Ming Fu

    Janelia Research Campus, Ashburn, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-6265-0859

  4. 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.

  5. Cheng Lyu

    Department of Biology, Howard Hughes Medical Institute, Stanford University, Stanford, United States
    Competing interests
    The authors declare that no competing interests exist.

  6. Sayeh Kohani

    Department of Biology, Howard Hughes Medical Institute, Stanford University, Stanford, United States
    Competing interests
    The authors declare that no competing interests exist.

  7. Qijing Xie

    Department of Biology, Howard Hughes Medical Institute, Stanford University, Stanford, United States
    Competing interests
    The authors declare that no competing interests exist.

  8. 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.

  9. 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.

  10. Eric Betzig

    Janelia Research Campus, Ashburn, United States
    Competing interests
    The authors declare that no competing interests exist.

  11. 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.
    ORCID icon "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.

Reviewing Editor

  1. Sonia Sen, Tata Institute for Genetics and Society, India

Version history

  1. Received: December 11, 2022
  2. Preprint posted: December 29, 2022 (view preprint)
  3. Accepted: March 27, 2023
  4. Accepted Manuscript published: March 28, 2023 (version 1)
  5. 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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  1. Kenneth Kin Lam Wong
  2. Tongchao Li
  3. Tian-Ming Fu
  4. Gaoxiang Liu
  5. Cheng Lyu
  6. Sayeh Kohani
  7. Qijing Xie
  8. David J Luginbuhl
  9. Srigokul Upadhyayula
  10. Eric Betzig
  11. Liqun Luo
(2023)
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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