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  • Review Article
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The sensory and motor roles of auditory hair cells

Nature Reviews Neuroscience volume 7, pages 19–29 (2006)Cite this article

Key Points

  • Sound vibrations conducted to the cochlea are detected by inner and outer hair cells. Both types of hair cell transduce sound stimuli through minute displacements of their hair bundle, an array of modified microvilli known as stereocilia that project from their apical surface.

  • Outer hair cells, unlike inner hair cells, have a further role in generating force, known as the cochlear amplifier, which mechanically boosts the sound-induced vibrations and augments frequency tuning. Two mechanisms of force generation have been advanced: contractions of the cell soma and active motion of the hair bundle.

  • Many proteins found in the mechanosensory hair bundle have been isolated by studies of genetic mutations that cause deafness. Crucial proteins for hair bundle development and function include many myosin isoforms.

  • Myosin XVa is localized to the tips of the stereocilia and might regulate the rate of actin incorporation, and thereby specify stereociliary length. Myosin VIIa might control the interciliary linkages, whereas myosin 1c is proposed to modulate the force on the mechanotransducer channel imposed by stretch of the tip links.

  • Deflections of the hair bundle are detected by mechanoelectrical transduction (MET) channels, which are located at the tips of stereocilia and activated by tension in the tip links. The most likely candidate for the MET channels is a transient receptor potential (TRP) channel, possibly TRPA1, which has large unitary conductance and is highly permeable to Ca2+.

  • Elevation of intracellular Ca2+ by influx of the ion through MET channels controls adaptation by various routes, including fast channel re-closure and slower control of the force imposed on the channel through myosin 1c.

  • Fast adaptation of the MET channels occurs on a submillisecond timescale. Hair cells tuned to higher frequencies have MET channels with larger single-channel conductance, permitting a larger Ca2+ influx and faster adaptation matched to the frequency detected by the hair cell.

  • One mode of force generation by outer hair cells occurs by voltage-dependent contractions of the cell soma attributable to the chloride-binding protein prestin. However, prestin might not operate on a cycle-by-cycle basis at high frequencies because the receptor potential is attenuated by the membrane time constant.

  • Recent results indicate that changes in MET channel gating attributable to fast adaptation cause force generation by the hair bundle that could supplement prestin-driven somatic contractions. Prestin's role might then be to act as another form of adaptation, continuously resetting the operating range of the MET channels to maintain them in their most sensitive position.

Abstract

Cochlear hair cells respond with phenomenal speed and sensitivity to sound vibrations that cause submicron deflections of their hair bundle. Outer hair cells are not only detectors, but also generate force to augment auditory sensitivity and frequency selectivity. Two mechanisms of force production have been proposed: contractions of the cell body or active motion of the hair bundle. Here, we describe recently identified proteins involved in the sensory and motor functions of auditory hair cells and present evidence for each force generator. Both motor mechanisms are probably needed to provide the high sensitivity and frequency discrimination of the mammalian cochlea.

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Figure 1: The sound conduction pathway.
Figure 2: Cellular structure of the sound-detecting organ of Corti.
Figure 3: Structure and protein composition of the stereociliary bundle.
Figure 4: Mechanoelectrical tranduction currents in outer hair cells.
Figure 5: The putative motors of outer hair cells.
Figure 6: Mechanical properties of an outer hair cell bundle.

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Acknowledgements

This work was supported by a grant from the National Institute on Deafness and Other Communication Disorders, National Institutes of Health, USA. We thank Y. Katori and D. Furness for the electron micrograph in figure 3b, and C. Dizack for help with the artwork.

Author information

Authors and Affiliations

  1. Department of Physiology, University of Wisconsin Medical School, 185 Medical Sciences Building, 1300 University Avenue, Madison, 53706, Wisconsin, USA

    Robert Fettiplace

  2. MacKay Institute of Communication and Neuroscience, School of Life Sciences, Keele University, Staffordshire, ST5 5BG, UK

    Carole M. Hackney

Authors
  1. Robert Fettiplace
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  2. Carole M. Hackney
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Correspondence to Robert Fettiplace.

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The authors declare no competing financial interests.

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FURTHER INFORMATION

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Hackney's homepage

Hereditary Hearing Loss Homepage

Glossary

Electromechanical feedback

The electrical change in an OHC caused by basilar membrane vibration generates a movement of the OHC that, in turn, feeds back to or alters basilar membrane vibration.

Reverse transduction

In normal forward transduction, hair cells convert mechanical stimuli into electrical responses. In reverse transduction, the electrical signals of hair cells evoke a mechanical output.

Osmiophilic rootlet

The stem of a stereocilium that in electron micrographs is seen to be heavily stained by osmium, which probably indicates a dense concentration of protein.

Shaker 2 mouse

A congenitally deaf mouse with a mutation in myosin XV that results in abnormally short stereocilia.

PDZ domain

A peptide-binding domain that is important for the organization of membrane proteins, particularly at cell–cell junctions. It can bind to the carboxyl termini of proteins or can form dimers with other PDZ domains. PDZ domains are named after the proteins in which these sequence motifs were originally identified (PSD-95, Discs large, zona occludens 1).

Whirler mouse

A mouse mutant that is unresponsive to sound and shows circling and head-tossing behaviour, indicative of both auditory and vestibular dysfunction. The mutated protein is known as whirlin and is involved in stereocilia elongation.

Usher type I syndrome

One of three subtypes (I,II and III) of hereditary disorder characterized by sensorineural deafness of cochlear origin combined with loss of vision due to retinitis pigmentosa.

Adaptation

The decline in response, and therefore sensitivity, to a sustained stimulus. Adaptation is a property of many sensory receptors that enables them to adjust their sensitivity to prevailing conditions and respond only to changes in stimulus intensity.

Time constant

The time required for the response of a system to decline to 37% of its initial value. For the cell membrane, this is the product of its capacitance and resistance, setting the timescale over which membrane currents change the voltage. A small time constant means that a system's response can change rapidly.

Unitary conductance

The electrical conductance of a single ion channel: the current flowing through the channel divided by the voltage applied across the cell membrane. Unitary conductance is a characteristic channel property but varies according to the ion species present.

Ototoxic agents

Procedures or drugs that damage hearing, primarily by acting on the hair cells.

Varitint-waddler mouse

A mouse with deafness, vestibular and pigmentation defects due to mutation in the mucolipin 3 gene, which encodes the ion channel protein TRPML3. It is associated with progressive hair bundle disorganization and hair cell degeneration.

Photodiode imaging

The stimulator casts a shadow on a pair of photodiodes and, as it moves, the light on one photodiode increases while that on the other decreases. The difference in photocurrents can be used to measure displacements down to a few nanometres.

Low-pass filter

A filter that suppresses all frequencies above a certain point known as the cut-off frequency.

Periodic component

A repetitive waveform: for example, a sine wave.

Compliance

The inverse of stiffness; the displacement of an elastic element produced by a known force.

Sylgard bead

A drop of silicone rubber, a mixture of a base and a curing agent, that is deposited on the tip of a glass fibre while liquid, then polymerized and hardened by heating.

Piezoelectric actuator

A ceramic crystal that deforms when a potential difference is applied across it. Piezoelectric devices require large voltages to induce movements of a micron. Such devices are reversible and also generate a voltage in response to mechanical stress.

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Fettiplace, R., Hackney, C. The sensory and motor roles of auditory hair cells. Nat Rev Neurosci 7, 19–29 (2006). https://doi.org/10.1038/nrn1828

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