Hearing benefits from an active process that amplifies acoustic inputs by more than a hundred-fold, sharpens frequency discrimination to facilitate the comprehension of speech and the recognition of sound sources, and compresses responses so that we can resolve sounds over a million-fold range in amplitude.
The gating of transduction channels endows a mechanically sensitive hair bundle with negative stiffness, an instability that interacts with the motor protein myosin 1c to produce a mechanical amplifier and oscillator. This active hair-bundle motility constitutes the active process of some non-mammalian tetrapods.
An outer hair cell of the mammalian cochlea displays somatic motility, in which changes in the transmembrane voltage alter the membrane area occupied by the piezoelectric protein prestin. Depolarization causes the cell body to contract and hyperpolarization causes it to extend at frequencies that can exceed 100 kHz.
Acoustic stimulation evokes on the elastic basilar membrane a travelling wave that progresses from the cochlear base towards the apex, peaking at a specific position determined by the stimulus frequency. As this wave advances, the active process of successive hair cells adds energy to counter viscous dissipation.
The active process of the mammalian cochlea combines active hair-bundle motility and somatic motility; the former mechanism probably regulates the phase of responsiveness, whereas the latter provides most of the mechanical power.
The characteristics of the active process reflect the operation of hair cells near a dynamical instability, the Hopf bifurcation, the generic properties of which explain various phenomena associated with hearing. When extreme quiet excites the active process sufficiently, hair cells traverse the bifurcation and — even in most individuals with normal hearing — produce spontaneous oscillations that emerge from the ears.
Uniquely among human senses, hearing is not simply a passive response to stimulation. Our auditory system is instead enhanced by an active process in cochlear hair cells that amplifies acoustic signals several hundred-fold, sharpens frequency selectivity and broadens the ear's dynamic range. Active motility of the mechanoreceptive hair bundles underlies the active process in amphibians and some reptiles; in mammals, this mechanism operates in conjunction with prestin-based somatic motility. Both individual hair bundles and the cochlea as a whole operate near a dynamical instability, the Hopf bifurcation, which accounts for the cardinal features of the active process.
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An investigator of Howard Hughes Medical Institute, the author thanks T. Reichenbach for the programme used to generate figure 1d and the members of his research group for comments on the manuscript.
The author declares no competing financial interests.
An abrupt, qualitative change in the character of a dynamical system in response to a continuous change in the value of a particular variable, the control parameter.
In sensory neuroscience, the term refers to the representation of a physical stimulus — for example, light, sound, acceleration, touch and chemicals — as electrical activity in an appropriate receptor cell.
- Hair bundles
Mechanically sensitive organelles of a hair cell, each consisting of an upright cluster of cylindrical stereocilia that extend from the cell's apical surface.
- Basilar membrane
A flat strip of connective tissue that spirals along the mammalian cochlea and supports the organ of Corti, which is the receptor for acoustic stimuli.
- Travelling wave
A mechanical disturbance that propagates along the basilar membrane from the base towards the apex of the cochlea in response to acoustic stimulation.
The phenomenon whereby application of a mechanical force to a substance produces an electrical potential difference across that substance, or vice versa, such as the application of changes in voltage to the piezoelectric protein prestin, which causes it to undergo a conformational change that results in an elongation or contraction of the cell.
- Gating compliance
A decrease in hair-bundle stiffness owing to the gating of transduction channels.
Resetting of the sensitivity in a sensory system. This involves an adjustment of the range of hair-bundle displacements over which a hair cell's electrical response varies.
- Limit-cycle oscillation
A stable pattern of oscillation in a non-linear dynamical system to which the system will return even if started in a different configuration.
- Distortion products
Oscillations at specific frequencies produced within a hearing organ by the non-linear properties of hair bundles exposed to acoustic stimuli at other frequencies. They are also called combination tones or phantom tones and are used in the medical diagnosis of hearing deficits.
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Hudspeth, A. Integrating the active process of hair cells with cochlear function. Nat Rev Neurosci 15, 600–614 (2014). https://doi.org/10.1038/nrn3786
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