Rheotaxis in Larval Zebrafish Is Mediated by Lateral Line Mechanosensory Hair Cells

Larval fishes have a remarkable ability to sense and evade the feeding strike of a predator fish with a rapid escape manoeuvre. Although the neuromuscular control of this behaviour is well studied, it is not clear what stimulus allows a larva to sense a predator. Here we show that this escape response is triggered by the water flow created during a predator's strike. Using a novel device, the impulse chamber, zebrafish ( Danio rerio ) larvae were exposed to this accelerating flow with high repeatability. Larvae responded to this stimulus with an escape response having a latency (mode=13–15 ms) that was fast enough to respond to predators. This flow was detected by the lateral line system, which includes mechanosensory hair cells within the skin. Pharmacologically ablating these cells caused the escape response to diminish, but then recover as the hair cells regenerated. These findings demonstrate that the lateral line system plays a role in predator evasion at this vulnerable stage of growth in fishes.

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Macrophages Respond Rapidly to Ototoxic Injury of Lateral Line Hair Cells but Are Not Required for Hair Cell Regeneration

Frontiers in Cellular Neuroscience ◽

10.3389/fncel.2020.613246 ◽

2021 ◽

Vol 14 ◽

Author(s):

Mark E. Warchol ◽

Angela Schrader ◽

Lavinia Sheets

Keyword(s):

Hair Cell ◽

Inner Ear ◽

Lateral Line ◽

Hair Cells ◽

Control Fish ◽

Cell Regeneration ◽

Cellular Interactions ◽

Hair Cell Regeneration ◽

Genetic Ablation ◽

Larval Zebrafish

The sensory organs of the inner ear contain resident populations of macrophages, which are recruited to sites of cellular injury. Such macrophages are known to phagocytose the debris of dying cells but the full role of macrophages in otic pathology is not understood. Lateral line neuromasts of zebrafish contain hair cells that are nearly identical to those in the inner ear, and the optical clarity of larval zebrafish permits direct imaging of cellular interactions. In this study, we used larval zebrafish to characterize the response of macrophages to ototoxic injury of lateral line hair cells. Macrophages migrated into neuromasts within 20 min of exposure to the ototoxic antibiotic neomycin. The number of macrophages in the near vicinity of injured neuromasts was similar to that observed near uninjured neuromasts, suggesting that this early inflammatory response was mediated by “local” macrophages. Upon entering injured neuromasts, macrophages actively phagocytosed hair cell debris. The injury-evoked migration of macrophages was significantly reduced by inhibition of Src-family kinases. Using chemical-genetic ablation of macrophages before the ototoxic injury, we also examined whether macrophages were essential for the initiation of hair cell regeneration. Results revealed only minor differences in hair cell recovery in macrophage-depleted vs. control fish, suggesting that macrophages are not essential for the regeneration of lateral line hair cells.

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Response of mechanosensory hair cells of the zebrafish lateral line to aminoglycosides reveals distinct cell death pathways

Hearing Research ◽

10.1016/j.heares.2009.03.001 ◽

2009 ◽

Vol 253 (1-2) ◽

pp. 32-41 ◽

Cited By ~ 65

Author(s):

Kelly N. Owens ◽

Allison B. Coffin ◽

Lisa S. Hong ◽

Keri O’Connell Bennett ◽

Edwin W Rubel ◽

...

Keyword(s):

Cell Death ◽

Lateral Line ◽

Hair Cells ◽

Cell Death Pathways ◽

Distinct Cell ◽

Mechanosensory Hair Cells

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Macrophages respond rapidly to ototoxic injury of lateral line hair cells but are not required for hair cell regeneration

10.1101/2020.09.28.314922 ◽

2020 ◽

Cited By ~ 1

Author(s):

Mark E. Warchol ◽

Angela Schrader ◽

Lavinia Sheets

Keyword(s):

Hair Cell ◽

Inner Ear ◽

Lateral Line ◽

Hair Cells ◽

Control Fish ◽

Cell Regeneration ◽

Cellular Interactions ◽

Hair Cell Regeneration ◽

Genetic Ablation ◽

Larval Zebrafish

AbstractThe sensory organs of the inner ear contain resident populations of macrophages, which are recruited to sites of cellular injury. Such macrophages are known to phagocytose the debris of dying cells but the full role of macrophages in otic pathology is not understood. Lateral line neuromasts of zebrafish contain hair cells similar to those in the inner ear, and the optical clarity of larval zebrafish permits direct imaging of cellular interactions. In this study, we used larval zebrafish to characterize the response of macrophages to ototoxic injury of lateral line hair cells. Macrophages migrated into neuromasts within 20 min of exposure to the ototoxic antibiotic neomycin. The number of macrophages in close proximity of injured neuromasts was similar to that observed near uninjured neuromasts, suggesting that this early inflammatory response was mediated by ‘local’ macrophages. Upon entering injured neuromasts, macrophages actively phagocytosed hair cell debris. Such phagocytosis was significantly reduced by inhibiting Src-family kinases. Using chemical-genetic ablation of macrophages prior to ototoxic injury, we also examined whether macrophages were essential for the initiation of hair cell regeneration after neomycin exposure. Results revealed only minor differences in hair cell recovery in macrophage-depleted vs. control fish, suggesting that macrophages are not essential for the regeneration of lateral line hair cells.

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Mechanical overstimulation causes acute injury followed by fast recovery in lateral-line neuromasts of larval zebrafish

10.1101/2020.07.15.205492 ◽

2020 ◽

Cited By ~ 1

Author(s):

Melanie Holmgren ◽

Michael E. Ravicz ◽

Kenneth E. Hancock ◽

Olga Strelkova ◽

Artur A. Indzhykulian ◽

...

Keyword(s):

Hair Cell ◽

Lateral Line ◽

Hair Cells ◽

Cell Damage ◽

Acute Injury ◽

Water Current ◽

Functional Changes ◽

Larval Zebrafish ◽

Auditory Nerves ◽

Hair Cell Damage

AbstractNoise exposure damages sensory hair cells, resulting in loss of synaptic connections with auditory nerves and hair-cell death. The cellular mechanisms underlying noise-induced hair-cell damage and subsequent repair are not completely understood. Hair cells in neuromasts (NMs) of larval zebrafish are structurally and functionally comparable to mammalian hair cells but undergo robust regeneration following damage. We therefore developed a model for noise-induced hair-cell damage in this highly tractable system. Free swimming larvae exposed to strong water current for 2 hours displayed damage to NMs, including synapse loss, afferent neurite retraction, damaged hair bundles, and reduced mechanotransduction. Overstimulation also elicited an inflammatory response and macrophage recruitment. Remarkably, NM morphology and function appeared to fully recover within 2 days following exposure. Our results reveal morphological and functional changes in mechanically overstimulated lateral-line NMs that are analogous to changes observed in noise-exposed mammalian ear yet are rapidly and completely repaired.

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Sensing External and Self-Motion with Hair Cells: A Comparison of the Lateral Line and Vestibular Systems from a Developmental and Evolutionary Perspective

Brain Behavior and Evolution ◽

10.1159/000456646 ◽

2017 ◽

Vol 90 (2) ◽

pp. 98-116 ◽

Cited By ~ 32

Author(s):

Boris P. Chagnaud ◽

Jacob Engelmann ◽

Bernd Fritzsch ◽

Joel C. Glover ◽

Hans Straka

Keyword(s):

Lateral Line ◽

Hair Cells ◽

Functional Organization ◽

Body Motion ◽

Efferent Projections ◽

Physical Attributes ◽

Organizational Pattern ◽

External Water ◽

Mechanosensory Hair Cells ◽

Self Motion

Detection of motion is a feature essential to any living animal. In vertebrates, mechanosensory hair cells organized into the lateral line and vestibular systems are used to detect external water or head/body motion, respectively. While the neuronal components to detect these physical attributes are similar between the two sensory systems, the organizational pattern of the receptors in the periphery and the distribution of hindbrain afferent and efferent projections are adapted to the specific functions of the respective system. Here we provide a concise review comparing the functional organization of the vestibular and lateral line systems from the development of the organs to the wiring from the periphery and the first processing stages. The goal of this review is to highlight the similarities and differences to demonstrate how evolution caused a common neuronal substrate to adapt to different functions, one for the detection of external water stimuli and the generation of sensory maps and the other for the detection of self-motion and the generation of motor commands for immediate behavioral reactions.

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Macrophage Recruitment Contributes to Regeneration of Mechanosensory Hair Cells in the Zebrafish Lateral Line

Journal of Cellular Biochemistry ◽

10.1002/jcb.25487 ◽

2016 ◽

Vol 117 (8) ◽

pp. 1880-1889 ◽

Cited By ~ 33

Author(s):

Simón A. Carrillo ◽

Consuelo Anguita-Salinas ◽

Oscar A. Peña ◽

Rodrigo A. Morales ◽

Salomé Muñoz-Sánchez ◽

...

Keyword(s):

Lateral Line ◽

Hair Cells ◽

Macrophage Recruitment ◽

Mechanosensory Hair Cells

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Distinct progenitor populations mediate regeneration in the zebrafish lateral line

eLife ◽

10.7554/elife.43736 ◽

2019 ◽

Vol 8 ◽

Cited By ~ 6

Author(s):

Eric D Thomas ◽

David W Raible

Keyword(s):

Hair Cell ◽

Lateral Line ◽

Hair Cells ◽

Cell Damage ◽

Cell Populations ◽

Support Cell ◽

Cell Ablation ◽

Hair Cell Damage ◽

Transgenic Lines ◽

Mechanosensory Hair Cells

Mechanosensory hair cells of the zebrafish lateral line regenerate rapidly following damage. These renewed hair cells arise from the proliferation of surrounding support cells, which undergo symmetric division to produce two hair cell daughters. Given the continued regenerative capacity of the lateral line, support cells presumably have the ability to replenish themselves. Utilizing novel transgenic lines, we identified support cell populations with distinct progenitor identities. These populations show differences in their ability to generate new hair cells during homeostasis and regeneration. Targeted ablation of support cells reduced the number of regenerated hair cells. Furthermore, progenitors regenerated after targeted support cell ablation in the absence of hair cell damage. We also determined that distinct support cell populations are independently regulated by Notch signaling. The existence of independent progenitor populations could provide flexibility for the continued generation of new hair cells under a variety of conditions throughout the life of the animal.

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Distinct progenitor populations mediate regeneration in the zebrafish lateral line

10.1101/482737 ◽

2018 ◽

Author(s):

Eric D. Thomas ◽

David W. Raible

Keyword(s):

Hair Cell ◽

Lateral Line ◽

Hair Cells ◽

Cell Damage ◽

Cell Populations ◽

Support Cell ◽

Cell Ablation ◽

Hair Cell Damage ◽

Transgenic Lines ◽

Mechanosensory Hair Cells

ABSTRACTMechanosensory hair cells of the zebrafish lateral line regenerate rapidly following damage. These renewed hair cells arise from the proliferation of surrounding support cells, which undergo symmetric division to produce two hair cell daughters. Given the continued regenerative capacity of the lateral line, support cells presumably have the ability to replenish themselves. Utilizing novel transgenic lines, we identified support cell populations with distinct progenitor identities. These populations show differences in their ability to generate new hair cells during homeostasis and regeneration. Targeted ablation of support cells reduced the number of regenerated hair cells. Furthermore, progenitors regenerated after targeted support cell ablation in the absence of hair cell damage. We also determined that distinct support cell populations are independently regulated by Notch signaling. The existence of independent progenitor populations could provide flexibility for the continued generation of new hair cells under a variety of conditions throughout the life of the animal.

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