scholarly journals An Integrated Perspective of Evolution and Development: From Genes to Function to Ear, Lateral Line and Electroreception

Diversity ◽  
2021 ◽  
Vol 13 (8) ◽  
pp. 364
Author(s):  
Bernd Fritzsch

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.

2015 ◽  
Vol 112 (9) ◽  
pp. E1000-E1009 ◽  
Author(s):  
Joshua D. Salvi ◽  
Dáibhid Ó Maoiléidigh ◽  
Brian A. Fabella ◽  
Mélanie Tobin ◽  
A. J. Hudspeth

Hair cells, the sensory receptors of the internal ear, subserve different functions in various receptor organs: they detect oscillatory stimuli in the auditory system, but transduce constant and step stimuli in the vestibular and lateral-line systems. We show that a hair cell's function can be controlled experimentally by adjusting its mechanical load. By making bundles from a single organ operate as any of four distinct types of signal detector, we demonstrate that altering only a few key parameters can fundamentally change a sensory cell’s role. The motions of a single hair bundle can resemble those of a bundle from the amphibian vestibular system, the reptilian auditory system, or the mammalian auditory system, demonstrating an essential similarity of bundles across species and receptor organs.


2021 ◽  
Vol 22 (8) ◽  
pp. 4189
Author(s):  
Karen L. Elliott ◽  
Gabriela Pavlínková ◽  
Victor V. Chizhikov ◽  
Ebenezer N. Yamoah ◽  
Bernd Fritzsch

We review the molecular basis of several transcription factors (Eya1, Sox2), including the three related genes coding basic helix–loop–helix (bHLH; see abbreviations) proteins (Neurog1, Neurod1, Atoh1) during the development of spiral ganglia, cochlear nuclei, and cochlear hair cells. Neuronal development requires Neurog1, followed by its downstream target Neurod1, to cross-regulate Atoh1 expression. In contrast, hair cells and cochlear nuclei critically depend on Atoh1 and require Neurod1 expression for interactions with Atoh1. Upregulation of Atoh1 following Neurod1 loss changes some vestibular neurons’ fate into “hair cells”, highlighting the significant interplay between the bHLH genes. Further work showed that replacing Atoh1 by Neurog1 rescues some hair cells from complete absence observed in Atoh1 null mutants, suggesting that bHLH genes can partially replace one another. The inhibition of Atoh1 by Neurod1 is essential for proper neuronal cell fate, and in the absence of Neurod1, Atoh1 is upregulated, resulting in the formation of “intraganglionic” HCs. Additional genes, such as Eya1/Six1, Sox2, Pax2, Gata3, Fgfr2b, Foxg1, and Lmx1a/b, play a role in the auditory system. Finally, both Lmx1a and Lmx1b genes are essential for the cochlear organ of Corti, spiral ganglion neuron, and cochlear nuclei formation. We integrate the mammalian auditory system development to provide comprehensive insights beyond the limited perception driven by singular investigations of cochlear neurons, cochlear hair cells, and cochlear nuclei. A detailed analysis of gene expression is needed to understand better how upstream regulators facilitate gene interactions and mammalian auditory system development.


PLoS ONE ◽  
2015 ◽  
Vol 10 (2) ◽  
pp. e0117041 ◽  
Author(s):  
Yuan-Hsiang Lin ◽  
Giun-Yi Hung ◽  
Liang-Chun Wu ◽  
Sheng-Wen Chen ◽  
Li-Yih Lin ◽  
...  

2002 ◽  
Vol 329 (2) ◽  
pp. 133-136 ◽  
Author(s):  
F Abbate ◽  
S Catania ◽  
A Germanà ◽  
T González ◽  
B Diaz-Esnal ◽  
...  

1980 ◽  
Vol 86 (1) ◽  
pp. 63-77
Author(s):  
ALFONS B. A. KROESE ◽  
JOHAN M. VAN DER ZALM ◽  
JOEP VAN DEN BERCKEN

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.


Author(s):  
Melanie Holmgren ◽  
Lavinia Sheets

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.


eLife ◽  
2018 ◽  
Vol 7 ◽  
Author(s):  
Eliot Dow ◽  
Adrian Jacobo ◽  
Sajjad Hossain ◽  
Kimberly Siletti ◽  
A J Hudspeth

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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