Evolution and Development of Lateral Line and Electroreception: An Integrated Perception of Neurons, Hair Cells and Brainstem Nuclei

Four sensory systems (vestibular, lateral line, electroreception, auditory) are unique and project exclusively to the brainstem of vertebrates. All sensory neurons depend on a common set of genes (Eya1, Sox2, Neurog1, Neurod1) that project to a dorsal nucleus and an intermediate nucleus, which differentiate into the vestibular ear, lateral line and electroreception in vertebrates. In tetrapods, a loss of two sensory systems (lateral line, electroreception) leads to the development of a unique ear and auditory system in amniotes. Lmx1a/b, Gdf7, Wnt1/3a, BMP4/7 and Atoh1 define the lateral line, electroreception and auditory nuclei. In contrast, vestibular nuclei depend on Neurog1/2, Ascl1, Ptf1a and Olig3, among others, to develop an independent origin of the vestibular nuclei. A common origin of hair cells depends on Eya1, Sox2 and Atoh1, which generate the mechanosensory cells. Several proteins define the polarity of hair cells in the ear and lateral line. A unique connection of stereocilia requires CDH23 and PCDH15 for connections and TMC1/2 proteins to perceive mechanosensory input. Electroreception has no polarity, and a different system is used to drive electroreceptors. All hair cells function by excitation via ribbons to activate neurons that innervate the distinct target areas. An integrated perspective is presented to understand the gain and loss of different sensory systems.

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Inhibition by efferent nerve fibres: action on hair cells and afferent synaptic transmission in the lateral line canal organ of the burbot Lota lota.

The Journal of Physiology ◽

10.1113/jphysiol.1976.sp011355 ◽

1976 ◽

Vol 257 (1) ◽

pp. 45-62 ◽

Cited By ~ 118

Author(s):

A Flock ◽

I Russell

Keyword(s):

Synaptic Transmission ◽

Lateral Line ◽

Hair Cells ◽

Nerve Fibres ◽

Efferent Nerve ◽

Lota Lota ◽

Lateral Line Canal

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Anion Exchanger 1b in Stereocilia Is Required for the Functioning of Mechanotransducer Channels in Lateral-Line Hair Cells of Zebrafish

PLoS ONE ◽

10.1371/journal.pone.0117041 ◽

2015 ◽

Vol 10 (2) ◽

pp. e0117041 ◽

Cited By ~ 1

Author(s):

Yuan-Hsiang Lin ◽

Giun-Yi Hung ◽

Liang-Chun Wu ◽

Sheng-Wen Chen ◽

Li-Yih Lin ◽

...

Keyword(s):

Lateral Line ◽

Hair Cells ◽

Anion Exchanger

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S-100 protein is a selective marker for sensory hair cells of the lateral line system in teleosts

Neuroscience Letters ◽

10.1016/s0304-3940(02)00597-9 ◽

2002 ◽

Vol 329 (2) ◽

pp. 133-136 ◽

Cited By ~ 17

Author(s):

F Abbate ◽

S Catania ◽

A Germanà ◽

T González ◽

B Diaz-Esnal ◽

...

Keyword(s):

Lateral Line ◽

Hair Cells ◽

Lateral Line System ◽

Selective Marker ◽

Line System ◽

Sensory Hair ◽

Sensory Hair Cells ◽

S 100

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Extracellular Receptor Potentials from the Lateral-Line Organ of Xenopus Laevis

Journal of Experimental Biology ◽

10.1242/jeb.86.1.63 ◽

1980 ◽

Vol 86 (1) ◽

pp. 63-77

Author(s):

ALFONS B. A. KROESE ◽

JOHAN M. VAN DER ZALM ◽

JOEP VAN DEN BERCKEN

Keyword(s):

Xenopus Laevis ◽

Lateral Line ◽

Hair Cells ◽

Water Displacement ◽

Stimulus Amplitude ◽

Nerve Fibres ◽

Large Stimulus ◽

Sensory Hair ◽

Lateral Line Organ ◽

Line Organ

1. The response of the epidermal lateral-line organ of Xenopus laevis to stimulation was studied by recording extracellular receptor potentials from the hair cells in single neuromasts in isolated preparations. One neuromast was stimulated by local, sinusoidal water movements induced by a glass sphere positioned at a short distance from the neuromast. 2. The amplitudes of the extracellular receptor potentials were proportional to the stimulus amplitude over a range of 20 dB. The phase of the extracellular receptor potentials with respect to water displacement was independent of the stimulus amplitude. 3. With large stimulus amplitude, and stimulus frequencies between 0.5 Hz and 2 Hz, the extracellular receptor potentials, and responses of single afferent nerve fibres, showed a phase lead of 1.2 π radians with respect to water displacement, i.e. they were almost in phase with water acceleration. 4. It is concluded that under conditions of stimulation with small-amplitude water movements, the hair cells respond to sensory hair displacement, whereas under conditions of stimulation with large-amplitude water movements they respond to sensory hair velocity.

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In Vivo Calcium Imaging of Lateral-line Hair Cells in Larval Zebrafish

Journal of Visualized Experiments ◽

10.3791/58794 ◽

2018 ◽

Cited By ~ 5

Author(s):

Daria Lukasz ◽

Katie S. Kindt

Keyword(s):

Lateral Line ◽

Hair Cells ◽

Calcium Imaging ◽

Larval Zebrafish ◽

In Vivo Calcium Imaging

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Using the Zebrafish Lateral Line to Understand the Roles of Mitochondria in Sensorineural Hearing Loss

Frontiers in Cell and Developmental Biology ◽

10.3389/fcell.2020.628712 ◽

2021 ◽

Vol 8 ◽

Cited By ~ 1

Author(s):

Melanie Holmgren ◽

Lavinia Sheets

Keyword(s):

Cell Death ◽

Hearing Loss ◽

Hair Cell ◽

Sensorineural Hearing Loss ◽

Lateral Line ◽

Hair Cells ◽

High Energy ◽

Sensorineural Hearing ◽

Mitochondrial Activity ◽

Ototoxic Drugs

Hair cells are the mechanosensory receptors of the inner ear and can be damaged by noise, aging, and ototoxic drugs. This damage often results in permanent sensorineural hearing loss. Hair cells have high energy demands and rely on mitochondria to produce ATP as well as contribute to intracellular calcium homeostasis. In addition to generating ATP, mitochondria produce reactive oxygen species, which can lead to oxidative stress, and regulate cell death pathways. Zebrafish lateral-line hair cells are structurally and functionally analogous to cochlear hair cells but are optically and pharmacologically accessible within an intact specimen, making the zebrafish a good model in which to study hair-cell mitochondrial activity. Moreover, the ease of genetic manipulation of zebrafish embryos allows for the study of mutations implicated in human deafness, as well as the generation of transgenic models to visualize mitochondrial calcium transients and mitochondrial activity in live organisms. Studies of the zebrafish lateral line have shown that variations in mitochondrial activity can predict hair-cell susceptibility to damage by aminoglycosides or noise exposure. In addition, antioxidants have been shown to protect against noise trauma and ototoxic drug–induced hair-cell death. In this review, we discuss the tools and findings of recent investigations into zebrafish hair-cell mitochondria and their involvement in cellular processes, both under homeostatic conditions and in response to noise or ototoxic drugs. The zebrafish lateral line is a valuable model in which to study the roles of mitochondria in hair-cell pathologies and to develop therapeutic strategies to prevent sensorineural hearing loss in humans.

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Connectomics of the zebrafish's lateral-line neuromast reveals wiring and miswiring in a simple microcircuit

eLife ◽

10.7554/elife.33988 ◽

2018 ◽

Vol 7 ◽

Cited By ~ 11

Author(s):

Eliot Dow ◽

Adrian Jacobo ◽

Sajjad Hossain ◽

Kimberly Siletti ◽

A J Hudspeth

Keyword(s):

Hair Cell ◽

Lateral Line ◽

Hair Cells ◽

Planar Cell Polarity ◽

Developmental Stages ◽

Notch Signaling Pathway ◽

Nerve Fibers ◽

Directional Sensitivity ◽

Efferent Nerve ◽

Polarity Gene

The lateral-line neuromast of the zebrafish displays a restricted, consistent pattern of innervation that facilitates the comparison of microcircuits across individuals, developmental stages, and genotypes. We used serial blockface scanning electron microscopy to determine from multiple specimens the neuromast connectome, a comprehensive set of connections between hair cells and afferent and efferent nerve fibers. This analysis delineated a complex but consistent wiring pattern with three striking characteristics: each nerve terminal is highly specific in receiving innervation from hair cells of a single directional sensitivity; the innervation is redundant; and the terminals manifest a hierarchy of dominance. Mutation of the canonical planar-cell-polarity gene vangl2, which decouples the asymmetric phenotypes of sibling hair-cell pairs, results in randomly positioned, randomly oriented sibling cells that nonetheless retain specific wiring. Because larvae that overexpress Notch exhibit uniformly oriented, uniformly innervating hair-cell siblings, wiring specificity is mediated by the Notch signaling pathway.

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