Functional development and regeneration of hair cells in the zebrafish lateral line
Key points We investigated hair‐cell regeneration in the zebrafish lateral line following the application of the ototoxic compound copper. In early‐larval zebrafish (<10 days post‐fertilisation), regenerated hair cells drive action potentials (APs) in the afferent neurons 24 h post‐copper treatme...
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Published in | The Journal of physiology Vol. 599; no. 16; pp. 3913 - 3936 |
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Main Authors | , , , , , |
Format | Journal Article |
Language | English |
Published |
England
Wiley Subscription Services, Inc
01.08.2021
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Subjects | |
Online Access | Get full text |
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Summary: | Key points
We investigated hair‐cell regeneration in the zebrafish lateral line following the application of the ototoxic compound copper.
In early‐larval zebrafish (<10 days post‐fertilisation), regenerated hair cells drive action potentials (APs) in the afferent neurons 24 h post‐copper treatment (24 hpt).
Full regeneration of the early‐larval neuromasts, the organs containing the hair cells, requires ∼48 h due to the progressive addition of hair cells and synaptic refinement.
In older larval zebrafish, regenerated hair cells are active and drive afferent APs by 48 hpt, which is comparable to larvae, but the functional recovery of their neuromasts requires >120 hpt.
Afferent terminals within the regenerating neuromast appear to initially contact supporting cells, and their complete ablation prevents the timely reappearance of supporting cells and hair cells.
We conclude that the regeneration of zebrafish neuromasts is slower after the initial developmental stages, and that the afferent input plays a key role in driving this process.
Hair cells are mechanosensory receptors responsible for transducing auditory and vestibular information into electrical signals, which are then transmitted with remarkable precision to afferent neurons. Different from mammals, the hair cells of lower vertebrates, including those present in the neuromasts of the zebrafish lateral line, regenerate following environmental or chemical insults. Here we investigate the time course of regeneration of hair cells in vivo using electrophysiology, two‐photon imaging and immunostaining applied to wild‐type and genetically encoded fluorescent indicator zebrafish lines. Functional hair cells drive spontaneous action potentials in the posterior lateral line afferent fibres, the frequency of which progressively increases over the first 10 days post‐fertilisation (dpf). Higher firing‐rate fibres are only observed from ∼6 dpf. Following copper treatment, newly formed hair cells become functional and are able to drive APs in the afferent fibres within 48 h in both early‐larval (≤8 dpf) and late‐larval (12–17 dpf) zebrafish. However, the complete functional regeneration of the entire neuromast is delayed in late‐larval compared to early‐larval zebrafish. We propose that while individual regenerating hair cells can rapidly become active, the acquisition of fully functional neuromasts progresses faster at early‐larval stages, a time when hair cells are still under development. At both ages, the afferent terminals in the regenerating neuromast appear to make initial contact with supporting cells. The ablation of the lateral line afferent neurons prevents the timely regeneration of supporting cells and hair cells. These findings indicate that the afferent system is likely to facilitate or promote the neuromast regeneration process.
Key points
We investigated hair‐cell regeneration in the zebrafish lateral line following the application of the ototoxic compound copper.
In early‐larval zebrafish (<10 days post‐fertilisation), regenerated hair cells drive action potentials (APs) in the afferent neurons 24 h post‐copper treatment (24 hpt).
Full regeneration of the early‐larval neuromasts, the organs containing the hair cells, requires ∼48 h due to the progressive addition of hair cells and synaptic refinement.
In older larval zebrafish, regenerated hair cells are active and drive afferent APs by 48 hpt, which is comparable to larvae, but the functional recovery of their neuromasts requires >120 hpt.
Afferent terminals within the regenerating neuromast appear to initially contact supporting cells, and their complete ablation prevents the timely reappearance of supporting cells and hair cells.
We conclude that the regeneration of zebrafish neuromasts is slower after the initial developmental stages, and that the afferent input plays a key role in driving this process. |
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Bibliography: | This is an Editor's Choice article from the 15 August 2021 issue. https://doi.org/10.1113/JP281522#support‐information‐section Linked articles: This article is highlighted in a Perspectives article by Sheets. To read this article, visit The peer review history is available in the Supporting Information section of this article Edited by: Ian Forsythe & Corne Kros https://doi.org/10.1113/JP282012 Katherine Hardy, Ana E. Amariutei and Francesca De Faveri contributed equally to this work. . ObjectType-Article-1 SourceType-Scholarly Journals-1 ObjectType-Feature-2 content type line 23 Present address: Hopwood Centre for Neurobiology, Lifelong Health Theme, South Australian Health and Medical Research Institute (SAHMRI), Adelaide, South Australia 5000, Australia |
ISSN: | 0022-3751 1469-7793 |
DOI: | 10.1113/JP281522 |