Coupling Active Hair Bundle Mechanics, Fast Adaptation, and Somatic Motility in a Cochlear Model

Overview

Journal Biophys J

Publisher Cell Press

Specialty Biophysics

Date 2011 Jun 7

PMID 21641302

Citations 29

Authors

Julien Meaud

Karl Grosh

Affiliations

Soon will be listed here.

Abstract

One of the central questions in the biophysics of the mammalian cochlea is determining the contributions of the two active processes, prestin-based somatic motility and hair bundle (HB) motility, to cochlear amplification. HB force generation is linked to fast adaptation of the transduction current via a calcium-dependent process and somatic force generation is driven by the depolarization caused by the transduction current. In this article, we construct a global mechanical-electrical-acoustical mathematical model of the cochlea based on a three-dimensional fluid representation. The global cochlear model is coupled to linearizations of nonlinear somatic motility and HB activity as well as to the micromechanics of the passive structural and electrical elements of the cochlea. We find that the active HB force alone is not sufficient to power high frequency cochlear amplification. However, somatic motility can overcome resistor-capacitor filtering by the basolateral membrane and deliver sufficient mechanical energy for amplification at basal locations. The results suggest a new theory for high frequency active cochlear mechanics, in which fast adaptation controls the transduction channel sensitivity and thereby the magnitude of the energy delivered by somatic motility.

Citing Articles

Gating-spring stiffness increases outer-hair-cell bundle stiffness, damping, and receptor current.

Zhu Z, Reid W, O Maoileidigh D Sci Rep. 2024; 14(1):29904.

PMID: 39622900 PMC: 11612202. DOI: 10.1038/s41598-024-81355-5.

3D morphology of an outer-hair-cell hair bundle increases its displacement and dynamic range.

Zhu Z, Reid W, George S, Ou V, O Maoileidigh D Biophys J. 2024; 123(19):3433-3451.

PMID: 39161094 PMC: 11480765. DOI: 10.1016/j.bpj.2024.08.009.

Rate-dependent cochlear outer hair cell force generation: Models and parameter estimation.

Cai W, Grosh K Biophys J. 2024; 123(19):3421-3432.

PMID: 39148291 PMC: 11480764. DOI: 10.1016/j.bpj.2024.08.007.

Something in Our Ears Is Oscillating, but What? A Modeller's View of Efforts to Model Spontaneous Emissions.

Wit H, Bell A J Assoc Res Otolaryngol. 2024; 25(4):313-328.

PMID: 38710871 PMC: 11349976. DOI: 10.1007/s10162-024-00940-7.

Cochlear outer hair cell electromotility enhances organ of Corti motion on a cycle-by-cycle basis at high frequencies in vivo.

Dewey J, Altoe A, Shera C, Applegate B, Oghalai J Proc Natl Acad Sci U S A. 2021; 118(43).

PMID: 34686590 PMC: 8639341. DOI: 10.1073/pnas.2025206118.

References

Kros C, Rusch A, Richardson G . Mechano-electrical transducer currents in hair cells of the cultured neonatal mouse cochlea. Proc Biol Sci. 1992; 249(1325):185-93. DOI: 10.1098/rspb.1992.0102. View

Kennedy H, Crawford A, Fettiplace R . Force generation by mammalian hair bundles supports a role in cochlear amplification. Nature. 2005; 433(7028):880-3. DOI: 10.1038/nature03367. View

Reichenbach T, Hudspeth A . A ratchet mechanism for amplification in low-frequency mammalian hearing. Proc Natl Acad Sci U S A. 2010; 107(11):4973-8. PMC: 2841936. DOI: 10.1073/pnas.0914345107. View

Peng A, Ricci A . Somatic motility and hair bundle mechanics, are both necessary for cochlear amplification?. Hear Res. 2010; 273(1-2):109-22. PMC: 2943979. DOI: 10.1016/j.heares.2010.03.094. View

Fridberger A, de Monvel J, Zheng J, Hu N, Zou Y, Ren T . Organ of Corti potentials and the motion of the basilar membrane. J Neurosci. 2004; 24(45):10057-63. PMC: 6730184. DOI: 10.1523/JNEUROSCI.2711-04.2004. View

Ricci A, Kennedy H, Crawford A, Fettiplace R . The transduction channel filter in auditory hair cells. J Neurosci. 2005; 25(34):7831-9. PMC: 6725256. DOI: 10.1523/JNEUROSCI.1127-05.2005. View

Santos-Sacchi J, Song L, Zheng J, Nuttall A . Control of mammalian cochlear amplification by chloride anions. J Neurosci. 2006; 26(15):3992-8. PMC: 6673883. DOI: 10.1523/JNEUROSCI.4548-05.2006. View

Iwasa K . A two-state piezoelectric model for outer hair cell motility. Biophys J. 2001; 81(5):2495-506. PMC: 1301719. DOI: 10.1016/S0006-3495(01)75895-X. View

Davis H . An active process in cochlear mechanics. Hear Res. 1983; 9(1):79-90. DOI: 10.1016/0378-5955(83)90136-3. View

10.

Fridberger A, Flock A, Ulfendahl M, Flock B . Acoustic overstimulation increases outer hair cell Ca2+ concentrations and causes dynamic contractions of the hearing organ. Proc Natl Acad Sci U S A. 1998; 95(12):7127-32. PMC: 22763. DOI: 10.1073/pnas.95.12.7127. View

11.

Tinevez J, Julicher F, Martin P . Unifying the various incarnations of active hair-bundle motility by the vertebrate hair cell. Biophys J. 2007; 93(11):4053-67. PMC: 2084239. DOI: 10.1529/biophysj.107.108498. View

12.

Cai H, Manoussaki D, Chadwick R . Effects of coiling on the micromechanics of the mammalian cochlea. J R Soc Interface. 2006; 2(4):341-8. PMC: 1578277. DOI: 10.1098/rsif.2005.0049. View

13.

Meaud J, Grosh K . The effect of tectorial membrane and basilar membrane longitudinal coupling in cochlear mechanics. J Acoust Soc Am. 2010; 127(3):1411-21. PMC: 2856508. DOI: 10.1121/1.3290995. View

14.

Van Netten S, Kros C . Gating energies and forces of the mammalian hair cell transducer channel and related hair bundle mechanics. Proc Biol Sci. 2000; 267(1455):1915-23. PMC: 1690752. DOI: 10.1098/rspb.2000.1230. View

15.

Ashmore J, Avan P, Brownell W, Dallos P, Dierkes K, Fettiplace R . The remarkable cochlear amplifier. Hear Res. 2010; 266(1-2):1-17. PMC: 6366996. DOI: 10.1016/j.heares.2010.05.001. View

16.

Chan D, Hudspeth A . Ca2+ current-driven nonlinear amplification by the mammalian cochlea in vitro. Nat Neurosci. 2005; 8(2):149-55. PMC: 2151387. DOI: 10.1038/nn1385. View

17.

Kennedy H, Evans M, Crawford A, Fettiplace R . Fast adaptation of mechanoelectrical transducer channels in mammalian cochlear hair cells. Nat Neurosci. 2003; 6(8):832-6. DOI: 10.1038/nn1089. View

18.

Markin V, Hudspeth A . Gating-spring models of mechanoelectrical transduction by hair cells of the internal ear. Annu Rev Biophys Biomol Struct. 1995; 24:59-83. DOI: 10.1146/annurev.bb.24.060195.000423. View

19.

Nam J, Fettiplace R . Force transmission in the organ of Corti micromachine. Biophys J. 2010; 98(12):2813-21. PMC: 2884234. DOI: 10.1016/j.bpj.2010.03.052. View

20.

Howard J, Hudspeth A . Compliance of the hair bundle associated with gating of mechanoelectrical transduction channels in the bullfrog's saccular hair cell. Neuron. 1988; 1(3):189-99. DOI: 10.1016/0896-6273(88)90139-0. View