scholarly journals Control of a hair bundle’s mechanosensory function by its mechanical load

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.

2020 ◽  
Author(s):  
Y. Roongthumskul ◽  
J. Faber ◽  
D. Bozovic

ABSTRACTThe high sensitivity and effective frequency discrimination of sound detection performed by the auditory system rely on the dynamics of a system of hair cells. In the inner ear, these acoustic receptors are primarily attached to an overlying structure which provides mechanical coupling between the hair bundles. While the dynamics of individual hair bundles have been extensively investigated, the influence of mechanical coupling on the motility of the system of bundles remains underdetermined. We developed a technique of mechanically coupling two active hair bundles, enabling us to probe the dynamics of the coupled system experimentally. We demonstrated that the coupling could enhance the coherence of hair bundles’ spontaneous oscillation as well as their phase-locked response to sinusoidal stimuli, at the calcium concentration in the surrounding fluid near the physiological level. The empirical data were consistent with numerical results from a model of two coupled nonisochronous oscillators, each displaying a supercritical Hopf bifurcation. The model revealed that weak coupling can poise the system of unstable oscillators closer to the bifurcation by a shift in the critical point. In addition, the dynamics of strongly coupled oscillators far from criticality suggested that individual hair bundles may be regarded as nonisochronous oscillators. An optimal degree of nonisochronicity was required for the observed tuning behavior in the coherence of autonomous motion of the coupled system.STATEMENT OF SIGNIFICANCEHair cells of the inner ear transduce acoustic energy into electrical signals via a deflection of hair bundles. Unlike a passive mechanical antenna, a free-standing hair bundle behaves as an active oscillator that can sustain autonomous oscillations, as well as amplify a low-level stimulus. Hair bundles under physiological conditions are elastically coupled to each other via an extracellular matrix. Therefore, the dynamics of coupled nonlinear oscillators underlie the performance of the peripheral auditory system. Despite extensive theoretical investigations, there are limited experimental evidence that support the significance of coupling on hair bundle motility. We develop a technique to mechanically couple hair bundles and demonstrate the benefits of coupling on hair bundle spontaneous motility.


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.


2019 ◽  
Vol 29 (21) ◽  
pp. 3579-3587.e7 ◽  
Author(s):  
Adrian Jacobo ◽  
Agnik Dasgupta ◽  
Anna Erzberger ◽  
Kimberly Siletti ◽  
A.J. Hudspeth

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.


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