Bidirectional transduction in vertebrate hair cells: A mechanism for coupling mechanical and electrical processes

Weiß, Thomas

doi:10.1016/0378-5955(82)90045-4

Cited by 112 publications

(30 citation statements)

References 18 publications

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“…Resonance phenomena arising from voltage-and time-dependent conductances certainly can be shunt damped in this way, and the recent demonstration that the principal conductance in frog saccular hair cells is a calcium-sensitive potassium conductance (Lewis & Hudspeth, 1983 a, b) is consistent with this view. The possibility remains, however, that other voltagecontrolled feed-back loops, perhaps involving the transduction process or mechanical properties of the ciliary apparatus, play a part in the apparent electrical resonance (see, for example, the suggestions by Weiss, 1982;Mountain, Hubbard & McMullen, 1983). Provided that such feed-back mechanisms place the membrane potential in the feed-back loop, they are potentially capable of being shunt damped in the way we have proposed.…”

Section: Discussionmentioning

confidence: 82%

Efferent modulation of hair cell tuning in the cochlea of the turtle.

Art

Crawford

Fettiplace

et al. 1985

The Journal of Physiology

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SUMMARY1. Intracellular recordings were made from turtle cochlear hair cells in order to study the changes in their tuning properties resulting from electrical stimulation of the efferent axons.2. Efferent stimulation caused a reduction in the amplitude of the receptor potential at the hair cell's most sensitive or characteristic frequency, an increased amplitude at frequencies more than an octave below the characteristic frequency, and no change at very high frequencies.3. These differential effects resulted in a broadening of each cell's tuning curve, which, during maximal efferent stimulation degenerated from a sharply tuned resonance to a critically damped low-pass filter.4. Efferent alterations in tuning were also inferred from the oscillations in membrane potential produced by acoustic clicks or extrinsic currents. The quality factor (Q) of tuning, derived from the decay of the oscillations, was progressively reduced with synaptic hyperpolarizations up to about 5 mV in amplitude. A consequence of efferent action was that the wave forms of transient pressure changes were more faithfully encoded as changes in hair cell membrane potential.5. Hyperpolarization of a hair cell by steady current injection resulted in a lowering of its characteristic frequency and quality factor, and an increase in steady-state resistance. By comparison, for a given reduction in quality factor, efferent stimulation was associated with a smaller change in characteristic frequency. This difference is expected if the resonance is also damped by the shunting action of the synaptic conductance.6. Perfusion with perilymphs containing 05-15 mm of the potassium channel blocker, tetraethylammonium bromide (TEA) reduced the hair cell's frequency selectivity, whether assayed acoustically or with extrinsic currents. Lower TEA concentrations abolished the efferent inhibitory post-synaptic potential with only a minor change in tuning.7. TEA produced other effects different from efferent stimulation including (i) a lowering of the characteristic frequency, and (ii) a highly asymmetric receptor potential. These observations suggest that the efferents do not simply block membrane conductances associated with tuning.

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Section: Discussionmentioning

confidence: 82%

Efferent modulation of hair cell tuning in the cochlea of the turtle.

Art

Crawford

Fettiplace

et al. 1985

The Journal of Physiology

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“…Nonlinear mechanisms for the generation of hair cell potentials and nerve spike trains, considered here and in other theoretical studies (Engebretson and Eldredge, 1968;Pfeitfer, 1970;Schroeder and Hall, 1974) have been shown capable of accounting for the various nonlinear phenomena such as two-tone suppression, saturation, and rectification. However, propagating combination tones and the possible active tuning (Kim, 1980;Siegel and Kim, 1982;Weiss, 1982) are two phenomena that could involve nonlinearities at the basilar membrane (or its coupling properties to the hair cells). Some descriptive models without explicit biophysical components have been proposed to account for these phenomena (de Boer, 1983;Neely and Kim, 1982).…”

Section: (B) ] and Can Be Traced To The Combined Influences Of The Nomentioning

confidence: 99%

A biophysical model of cochlear processing: Intensity dependence of pure tone responses

et al. 1986

The Journal of the Acoustical Society of America

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A mathematical model of cochlear processing is developed to account for the nonlinear dependence of frequency selectivity on intensity in inner hair cell and auditory nerve fiber responses. The model describes the transformation from acoustic stimulus to intracellular hair cell potentials in the cochlea. It incorporates a linear formulation of basilar membrane mechanics and subtectorial fluid-cilia displacement coupling, and a simplified description of the inner hair cell nonlinear transduction process. The analysis at this stage is restricted to low-frequency single tones. The computed responses to single tone inputs exhibit the experimentally observed nonlinear effects of increasing intensity such as the increase in the bandwidth of frequency selectivity and the downward shift of the best frequency. In the model, the first effect is primarily due to the saturating effect of the hair cell nonlinearity. The second results from the combined effects of both the nonlinearity and of the inner hair cell low-pass transfer function. In contrast to these shifts along the frequency axis, the model does not exhibit intensity dependent shifts of the spatial location along the cochlea of the peak response for a given single tone. The observed shifts therefore do not contradict an intensity invariant tonotopic code.

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“…Because both the V1 and V0 components of the receptor potential exhibit this non-linearity, it is unlikely to be generated by a mechanism which occurs after the non-linear mechanism that produces the V0 component. If we make the reasonable assumption that the V0 component of the receptor potential is produced by the asymmetric rectification of stereocilia displacement into membrane conductance change, then the non-linearity must be localized to the micromechanics of the stereocilia and/or to the mechanoelectric transduction of these displacements into membrane conductance changes or perhaps to some mechanism that couples these processes (Weiss, 1982 (Goodman, Smith & Chamberlain, 1982), and in discharges of cochlear nerve fibres (Sachs & Abbas, 1974;Harrison, 1981) in mammals. Such non-linearities can be produced by models of cochlear macromechanics that include non-linear damping of the cochlear partition (Hubbard & Geisler, 1972;Kim, Molnar & Pfeiffer, 1973;Hall, 1974Hall, , 1977a (Crawford & Fettiplace, 1980a, b, 1981 Fettiplace & Crawford, 1978& Crawford, , 1980; and in vivo in inner hair cells in the organ of Corti in the guinea-pig, Caviaporcellus, (Russell & Sellick, 1977, 1978Sellick, 1979;Brown, Nuttall, Masta & Lawrence, 1981) and in the Mongolian gerbil, Meriones unguiculatus, (Goodman, Smith & Chamberlain, 1982 Crawford & Fettiplace (1980a have interpreted this result to indicate that a substantial fraction of the frequency selectivity of responses to acoustic stimuli is due to resonant electrical properties of the hair-cell membrane.…”

Section: Frequency-dependent Compressive Non-linearitymentioning

confidence: 99%

Receptor potentials of lizard cochlear hair cells with free‐standing stereocilia in response to tones.

Holton¹,

Weiß²

1983

The Journal of Physiology

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SUMMARY1. Intracellular potentials were recorded with micropipettes from hair cells with free-standing stereocilia in the cochleae of anaesthetized alligator lizards.2. Wave forms of intracellular responses to click stimuli were classified into three types: hair cells, supporting cells, and untuned cells. We studied primarily the responses of hair cells to tonal stimuli.3. For most frequencies, f, and levels, P, of tone-burst stimuli, the response envelope of the receptor potential increases monotonically at the tone-burst onset, and decreases monotonically at tone-burst offset. Overshoot in the envelope of the response at the onset and offset of tone bursts is observed only for tone bursts of low f, high P, and short ( and V' components was measured by means of iso-voltage (iso-V0 and iso-V,)contours. Iso-V0 and iso-V' contours are V-shaped: the maximum sensitivity occurs at a characteristic frequency (c.f. ). The shapes of these contours near the c.f. depend on the values of V0 and V1 at which the contours were measured and are sharper for lower values of V1 and V1. The mean slopes of the low-and high-frequency sides of these contours are: -45-0 and + 85-1 dB/decade for iso-V0 contours (n = 26), and -33'6 and + 103'8 dB/decade for iso-V1 contours (n = 28).6. The receptor potential has non-linear properties. The magnitudes and phase angles of V0, 'l, V2, and V3 receptor-potential components were measured as a function of P for different f. The slopes of level functions (the dependence of log V0 and log V1I on log P) were measured at low levels for different f. T. HOLTON AND T. F. WEISSdiffering from c.f. by more than a half-octave, the slope for VT is between 1 and 2 with a mean of 1P3; the slope for V1 is about 1, i.e. V11 increases approximately linearly with P. For frequencies near c.f., the slopes for V0 and V1 are approximately 0-8 and 0 5, respectively, indicating the presence of a compressive non-linearity. An effect of this frequency-dependent non-linearity is to sharpen the frequency selectivity at lower response magnitudes for f near c.f.7. The receptor potential shows low-pass filtering. Whereas the maximum response magnitude of V0 (i.e. the saturation value measured at high P) does not depend on f, the maximum Vj decreases by approximately 20 dB/decade with increasing f. Values of IIJ1I measured at a constant value of V0 also decline by approximately 20 dB/decade.8. Many of the results are consistent with the predictions of a three-stage model of the generation of the receptor potential. The first stage, which represents the mechanical properties ofthe middle and inner ear, is a linear, time-invariant, band-pass filter; the second stage, which represents mechanoelectric transduction in hair cells, is a zero-memory non-linearity; the third stage, which represents the electrical properties of hair cells, is a linear, time-invariant, low-pass filter. However, the results differ from the model predictions for low-level acoustic stimuli near c.f., and indicate the presence of a frequency-dependent compr...

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Bidirectional transduction in vertebrate hair cells: A mechanism for coupling mechanical and electrical processes

Cited by 112 publications

References 18 publications

Efferent modulation of hair cell tuning in the cochlea of the turtle.

Efferent modulation of hair cell tuning in the cochlea of the turtle.

A biophysical model of cochlear processing: Intensity dependence of pure tone responses

Receptor potentials of lizard cochlear hair cells with free‐standing stereocilia in response to tones.

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