Amplifying effect of a release mechanism for fast adaptation in the hair bundle

Sul, Bora; Iwasa, Kuni H.

doi:10.1121/1.3143782

Cited by 7 publications

(6 citation statements)

References 13 publications

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“…After decades of research, the outer hair cells were found to provide the regenerative force for the power amplification in the cochlea (2)(3)(4). The outer hair cells should operate optimally to provide enough power to compensate for the power loss because of viscous friction (5)(6)(7)(8)(9). The power gain in the cochlea has been estimated/ measured to explain the operating principles of the cochlear amplifier (10)(11)(12).…”

Section: Introductionmentioning

confidence: 99%

“…A few studies considered the viscous friction in the STS as the primary cause of energy dissipation in the mammalian cochlea (26,27). The energy dissipation in the STS was estimated from the viscous friction of a Newtonian fluid between two parallel plates representing the tectorial membrane and the reticular lamina (7,8,27). However, the STS is more complex than a fluid layer between two parallel plates in shear motion because the IHCs' stereocilia may impede or interact with the flow.…”

Section: Introductionmentioning

confidence: 99%

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Power Dissipation in the Subtectorial Space of the Mammalian Cochlea Is Modulated by Inner Hair Cell Stereocilia

Prodanovic

Gracewski

Nam

2015

Biophysical Journal

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The stereocilia bundle is the mechano-transduction apparatus of the inner ear. In the mammalian cochlea, the stereocilia bundles are situated in the subtectorial space (STS)--a micrometer-thick space between two flat surfaces vibrating relative to each other. Because microstructures vibrating in fluid are subject to high-viscous friction, previous studies considered the STS as the primary place of energy dissipation in the cochlea. Although there have been extensive studies on how metabolic energy is used to compensate the dissipation, much less attention has been paid to the mechanism of energy dissipation. Using a computational model, we investigated the power dissipation in the STS. The model simulates fluid flow around the inner hair cell (IHC) stereocilia bundle. The power dissipation in the STS because of the presence IHC stereocilia increased as the stimulating frequency decreased. Along the axis of the stimulating frequency, there were two asymptotic values of power dissipation. At high frequencies, the power dissipation was determined by the shear friction between the two flat surfaces of the STS. At low frequencies, the power dissipation was dominated by the viscous friction around the IHC stereocilia bundle--the IHC stereocilia increased the STS power dissipation by 50- to 100-fold. There exists a characteristic frequency for STS power dissipation, CFSTS, defined as the frequency where power dissipation drops to one-half of the low frequency value. The IHC stereocilia stiffness and the gap size between the IHC stereocilia and the tectorial membrane determine the characteristic frequency. In addition to the generally assumed shear flow, nonshear STS flow patterns were simulated. Different flow patterns have little effect on the CFSTS. When the mechano-transduction of the IHC was tuned near the vibrating frequency, the active motility of the IHC stereocilia bundle reduced the power dissipation in the STS.

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Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Power Dissipation in the Subtectorial Space of the Mammalian Cochlea Is Modulated by Inner Hair Cell Stereocilia

Prodanovic

Gracewski

Nam

2015

Biophysical Journal

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“…The second benefit of this arrangement is that series viscosity can implement the release mechanism for fast adaptation. When coupled with negative stiffness, this mechanism can provide amplification (28). The third consequence involves masking the high phenomenological viscosity of the channels, which in the presence of viscoelasticity has little effect on hair-bundle motion.…”

Section: Discussionmentioning

confidence: 99%

Anomalous Brownian motion discloses viscoelasticity in the ear’s mechanoelectrical-transduction apparatus

Kozlov

Andor-Ardó

Hudspeth

2012

Proc. Natl. Acad. Sci. U.S.A.

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The ear detects sounds so faint that they produce only atomic-scale displacements in the mechanoelectrical transducer, yet thermal noise causes fluctuations larger by an order of magnitude. Explaining how hearing can operate when the magnitude of the noise greatly exceeds that of the signal requires an understanding both of the transducer's micromechanics and of the associated noise. Using microrheology, we characterize the statistics of this noise; exploiting the fluctuation-dissipation theorem, we determine the associated micromechanics. The statistics reveal unusual Brownian motion in which the mean square displacement increases as a fractional power of time, indicating that the mechanisms governing energy dissipation are related to those of energy storage. This anomalous scaling contradicts the canonical model of mechanoelectrical transduction, but the results can be explained if the micromechanics incorporates viscoelasticity, a salient characteristic of biopolymers. We amend the canonical model and demonstrate several consequences of viscoelasticity for sensory coding.auditory system | hair cell | interferometry | vestibular system T he development of experimental and analytical tools has made possible high-resolution studies of the mechanical properties of biological macromolecules on time scales ranging from the picosecond fluctuations of single amide bonds in proteins, through the submillisecond dynamics of ion-channel gating and enzyme catalysis, to the much slower events involved in cell division and motility (1,2). These studies reveal that the energy landscapes in proteins are complex and that the associated hierarchy of time scales produces nonexponential temporal correlations (3,4). The absence of a single characteristic time scale implies stochastic processes with memory and therefore distinct from simple diffusion.Auditory physiology offers a unique perspective on biological micromechanics. The conversion of a sound's energy into an electrical signal in the ear is a molecular event that involves an ion channel linked mechanically to a gating spring, an elastic element whose tension is modulated by sound. The weakest sounds that we can hear extend the gating spring by less than a nanometer (5,6). Under these conditions, separating the signal from the intrinsic thermal noise is a formidable task, but one facilitated by the periodic structure of most sounds. Although random fluctuations are known to dominate hair-bundle kinematics and to influence signal detection through stochastic resonance (7), their origin and statistical properties have remained obscure. In this work we have experimentally characterized the random fluctuations of hair bundles by dual-beam differential interferometry, a technique that has allowed us to make large-bandwidth, high-resolution measurements of the nanometer-scale thermal motions of stereocilia in living hair bundles from the inner ear. We have interpreted the measurements by introducing a theoretical framework that incorporates viscoelasticity and the known principl...

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“…In contrast, tall hair cells, which function as the sensor, are located away from the center of the basilar membrane, at a location seemingly unsuitable for sensing the motion of the basilar membrane directly. Thus it is likely short hair cells are involved in amplification by a hair bundle active process [27][28][29][30], transmitting the mechanical vibration of the basilar membrane to the hair bundles of tall hair cells. The problem is how that can happen?…”

Section: Motion Of Tectorial Membranementioning

confidence: 99%

Of Mice and Chickens: Revisiting the RC Time Constant Problem

Iwasa

2021

Preprint

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Avian hair cells depend on electrical resonance for frequency selectivity. The upper bound of the frequency range is limited by the RC time constant of hair cells because the sharpness of tuning requires that the resonance frequency must be lower than the RC roll-off frequency. In contrast, tuned mechanical vibration of the inner ear is the basis of frequency selectivity of the mammalian ear. This mechanical vibration is supported by outer hair cells (OHC) with their electromotility based on piezoelectricity, which is driven by the receptor potential. Thus it is also subjected to the RC time constant problem. Association of OHCs with a system with mechanical resonance leads to piezoelectric resonance. This resonance can nullify the membrane capacitance and solves the RC time constant problem for OHCs.

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Amplifying effect of a release mechanism for fast adaptation in the hair bundle

Cited by 7 publications

References 13 publications

Power Dissipation in the Subtectorial Space of the Mammalian Cochlea Is Modulated by Inner Hair Cell Stereocilia

Power Dissipation in the Subtectorial Space of the Mammalian Cochlea Is Modulated by Inner Hair Cell Stereocilia

Anomalous Brownian motion discloses viscoelasticity in the ear’s mechanoelectrical-transduction apparatus

Of Mice and Chickens: Revisiting the RC Time Constant Problem

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