Directional selectivity of afferent neurons in zebrafish neuromasts is regulated by Emx2 in presynaptic hair cells

  1. Young Rae Ji
  2. Sunita Warrier
  3. Tao Jiang
  4. Doris K Wu  Is a corresponding author
  5. Katie Kindt  Is a corresponding author
  1. National Institutes of Health, United States

Abstract

The orientation of hair bundles on top of sensory hair cells (HCs) in neuromasts of the lateral line system allows fish to detect direction of water flow. Each neuromast shows hair bundles arranged in two opposing directions and each afferent neuron only innervate HCs of the same orientation. In previous paper, we show that this opposition is established by expression of Emx2 in half of the HCs, where it mediates hair bundle reversal (Jiang et al. 2017). Here, we show that Emx2 also regulates neuronal selection: afferent neurons innervate either Emx2-positive or negative HCs. In emx2 knockout and gain-of-function neuromasts, all HCs are unidirectional and the innervation patterns and physiological responses of the afferent neurons are dependent on the presence or absence of Emx2. Our results indicate that Emx2 mediates the directional selectivity of neuromasts by two distinct processes: regulating hair bundle orientation in HCs and selecting afferent neuronal targets.

Data availability

All data generated or analysed during this study are included in the manuscript. Source data files have been provided for Table1 and figure 2, 4, 5, 6, 7, and 8.

Article and author information

Author details

  1. Young Rae Ji

    Section on Sensory Cell Regeneration and Development, Laboratory of Molecular Biology, National Institutes of Health, Bethesda, United States
    Competing interests
    The authors declare that no competing interests exist.
  2. Sunita Warrier

    Section on Sensory Cell Development and Function, National Institute on Deafness and Other Communication Disorders, National Institutes of Health, Bethesda, United States
    Competing interests
    The authors declare that no competing interests exist.
  3. Tao Jiang

    Section on Sensory Cell Regeneration and Development, Laboratory of Molecular Biology, National Institutes of Health, Bethesda, United States
    Competing interests
    The authors declare that no competing interests exist.
  4. Doris K Wu

    Section on Sensory Cell Regeneration and Development, Laboratory of Molecular Biology, National Institutes of Health, Bethesda, United States
    For correspondence
    wud@nidcd.nih.gov
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-1400-3558
  5. Katie Kindt

    Section on Sensory Cell Development, National Institute on Deafness and Other Communication Disorders, National Institutes of Health, Bethesda, United States
    For correspondence
    katie.kindt@nih.gov
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-1065-8215

Funding

National Institute on Deafness and Other Communication Disorders (Intramural Research Program Grant 1ZIADC000085-01)

  • Katie Kindt

National Institute on Deafness and Other Communication Disorders (Intramural Research Program Grant 1ZIADC000021)

  • Doris K Wu

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

Copyright

This is an open-access article, free of all copyright, and may be freely reproduced, distributed, transmitted, modified, built upon, or otherwise used by anyone for any lawful purpose. The work is made available under the Creative Commons CC0 public domain dedication.

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  1. Young Rae Ji
  2. Sunita Warrier
  3. Tao Jiang
  4. Doris K Wu
  5. Katie Kindt
(2018)
Directional selectivity of afferent neurons in zebrafish neuromasts is regulated by Emx2 in presynaptic hair cells
eLife 7:e35796.
https://doi.org/10.7554/eLife.35796

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https://doi.org/10.7554/eLife.35796