A C Crawford

Université Victor Segalen Bordeaux 2, Burdeos, Aquitaine, France

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Publications (27)156.7 Total impact

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    ABSTRACT: Sound stimuli excite cochlear hair cells by vibration of each hair bundle, which opens mechanotransducer (MT) channels. We have measured hair-bundle mechanics in isolated rat cochleas by stimulation with flexible glass fibers and simultaneous recording of the MT current. Both inner and outer hair-cell bundles exhibited force-displacement relationships with a nonlinearity that reflects a time-dependent reduction in stiffness. The nonlinearity was abolished, and hair-bundle stiffness increased, by maneuvers that diminished calcium influx through the MT channels: lowering extracellular calcium, blocking the MT current with dihydrostreptomycin, or depolarizing to positive potentials. To simulate the effects of Ca(2+), we constructed a finite-element model of the outer hair cell bundle that incorporates the gating-spring hypothesis for MT channel activation. Four calcium ions were assumed to bind to the MT channel, making it harder to open, and, in addition, Ca(2+) was posited to cause either a channel release or a decrease in the gating-spring stiffness. Both mechanisms produced Ca(2+) effects on adaptation and bundle mechanics comparable to those measured experimentally. We suggest that fast adaptation and force generation by the hair bundle may stem from the action of Ca(2+) on the channel complex and do not necessarily require the direct involvement of a myosin motor. The significance of these results for cochlear transduction and amplification are discussed.
    Biophysical Journal 05/2008; 94(7):2639-53. · 3.67 Impact Factor
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    ABSTRACT: There is current debate about the origin of mechanical amplification whereby outer hair cells generate force to augment the sensitivity and frequency selectivity of the mammalian cochlea. To distinguish contributions to force production from the mechanotransducer (MET) channels and somatic motility, we have measured hair bundle motion during depolarization of individual outer hair cells in isolated rat cochleas. Depolarization evoked rapid positive bundle deflections that were reduced by perfusion with the MET channel blocker dihydrostreptomycin, with no effect on the nonlinear capacitance that is a manifestation of prestin-driven somatic motility. However, the movements were also diminished by Na salicylate and depended on the intracellular anion, properties implying involvement of the prestin motor. Furthermore, depolarization of one outer hair cell caused motion of neighboring hair bundles, indicating overall motion of the reticular lamina. Depolarization of solitary outer hair cells caused cell-length changes whose voltage-activation range depended on the intracellular anion but were insensitive to dihydrostreptomycin. These results imply that both the MET channels and the somatic motor participate in hair bundle motion evoked by depolarization. It is conceivable that the two processes can interact, a signal from the MET channels being capable of modulating the activity of the prestin motor.
    Journal of Neuroscience 04/2006; 26(10):2757-66. · 6.91 Impact Factor
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    ABSTRACT: In the first step in auditory transduction, sound-induced vibrations of the stereociliary bundles on the sensory hair cells are converted into electrical signals by opening of mechanotransducer channels. Faithful transduction and hence auditory performance will be limited by the kinetic properties of these channels. We have measured the time course of mechanotransducer currents in turtle and rat auditory hair cells during rapid deflections of the hair bundle. Current activation in the turtle had a time constant that decreased 10-fold with stimulus amplitude to a limiting value of approximately 50 micros. Lowering the external Ca2+ concentration slowed both activation and adaptation time constants. Similar effects were seen in hair cells tuned to low and high frequencies, but the overall kinetics was slower in low-frequency cells. In rat outer hair cells, the time courses of both activation and adaptation were at least 10-fold faster. Although activation kinetics was too fast to characterize accurately, the adaptation time constants in the rat, like the turtle, were Ca2+ dependent and faster in hair cells tuned to higher frequencies. The results imply that mechanotransducer channels operate similarly in turtle and rat but are faster in the mammal to accommodate its higher frequency range of hearing. We suggest that the kinetics of channel activation and adaptation imposes a bandpass filter on transduction, with a center frequency matched to the frequencies detected by the hair cell, which may improve the signal-to-noise ratio near threshold.
    Journal of Neuroscience 09/2005; 25(34):7831-9. · 6.91 Impact Factor
  • H J Kennedy, A C Crawford, R Fettiplace
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    ABSTRACT: It is generally accepted that the acute sensitivity and frequency discrimination of mammalian hearing requires active mechanical amplification of the sound stimulus within the cochlea. The prevailing hypothesis is that this amplification stems from somatic electromotility of the outer hair cells attributable to the motor protein prestin. Thus outer hair cells contract and elongate in synchrony with the sound-evoked receptor potential. But problems arise with this mechanism at high frequencies, where the periodic component of the receptor potential will be attenuated by the membrane time constant. On the basis of work in non-mammalian vertebrates, force generation by the hair bundles has been proposed as an alternative means of boosting the mechanical stimulus. Here we show that hair bundles of mammalian outer hair cells can also produce force on a submillisecond timescale linked to adaptation of the mechanotransducer channels. Because the bundle motor may ultimately be limited by the deactivation rate of the channels, it could theoretically operate at high frequencies. Our results show the existence of another force generator in outer hair cells that may participate in cochlear amplification.
    Nature 03/2005; 433(7028):880-3. · 38.60 Impact Factor
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    Anthony J Ricci, Andrew C Crawford, Robert Fettiplace
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    ABSTRACT: Hair cells in the vertebrate cochlea are arranged tonotopically with their characteristic frequency (CF), the sound frequency to which they are most sensitive, changing systematically with position. Single mechanotransducer channels of hair cells were characterized at different locations in the turtle cochlea. In 2.8 mM external Ca2+, the channel's chord conductance was 118 pS (range 80-163 pS), which nearly doubled (range 149-300 pS) on reducing Ca2+ to 50 microM. In both Ca2+ concentrations, the conductance was positively correlated with hair cell CF. Variation in channel conductance can largely explain the increases in size of the macroscopic transducer current and speed of adaptation with CF. It suggests diversity of transducer channel structure or environment along the cochlea that may be an important element of its tonotopic organization.
    Neuron 01/2004; 40(5):983-90. · 15.77 Impact Factor
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    ABSTRACT: Outer hair cells are centrally involved in the amplification and frequency tuning of the mammalian cochlea, but evidence about their transducing properties in animals with fully developed hearing is lacking. Here we describe measurements of mechanoelectrical transducer currents in outer hair cells of rats between postnatal days 5 and 18, before and after the onset of hearing. Deflection of hair bundles using a new rapid piezoelectric stimulator evoked transducer currents with ultra-fast activation and adaptation kinetics. Fast adaptation resembled the same process in turtle hair cells, where it is regulated by changes in stereociliary calcium. It is argued that sub-millisecond transducer adaptation can operate in outer hair cells under the ionic, driving force and temperature conditions that prevail in the intact mammalian cochlea.
    Nature Neuroscience 09/2003; 6(8):832-6. · 15.25 Impact Factor
  • R. Fettiplace, A. C. Crawford, A. J. Ricci
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    ABSTRACT: In the first step in auditory transduction, vibrations of the hair-cell stereociliary bundle are converted into an electrical signal by the gating of the mechanotransducer channels. Faithful transduction and hence cochlear performance will be limited by, among other things, the kinetic properties of these channels. We have measured the time course of mechanotransducer currents in turtle auditory hair cells during rapid deflections of the hair bundle. The current onset had a principal time constant that decreased 10-fold with stimulus amplitude up to saturation to a limiting value of ~40 microseconds. Lowering the external calcium concentration from 2.8 to 0.05 mM slowed both activation and adaptation time constants. Similar effects were seen in hair cells tuned to low and high frequencies, but the overall kinetics were slower in low frequency cells, which argues that transducer kinetics may be matched to the range of frequencies processed by the hair cell. The results suggest that calcium ions, along with bundle displacement, act directly on the mechanotransducer channels to modulate their probability of opening.
    01/2003;
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    A J Ricci, A C Crawford, R Fettiplace
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    ABSTRACT: Sound stimuli vibrate the hair bundles on auditory hair cells, but the resulting motion attributable to the mechanical stimulus may be modified by forces intrinsic to the bundle, which drive it actively. One category of active hair bundle motion has properties similar to fast adaptation of the mechanotransducer channels and is explicable if gating of the channels contributes significantly to the mechanics of the hair bundle. To explore this mechanism, we measured hair bundle compliance in turtle auditory hair cells under different conditions that alter the activation range of the channel. Force-displacement relationships were nonlinear, possessing a maximum slope compliance when approximately one-half of the transducer channels were open. When the external calcium concentration was reduced from 2.8 to 0.25 mm, the position of maximum compliance was shifted negative, reflecting a comparable shift in the transducer channel activation curve. Assuming that the nonlinearity represents the compliance attributable to channel gating, a single-channel gating force of 0.25 pN was calculated. By comparing bundle displacements with depolarization with and without an attached flexible fiber, the force contributed by each channel was independently estimated as 0.47 pN. These results are consistent with fast active bundle movements resulting from changes in mechanotransducer channel gating. However, several observations revealed additional components of hair bundle motion, with slower kinetics and opposite polarity to the fast movement but also linked to transducer adaptation. This finding argues for multiple mechanisms for controlling hair bundle position in auditory hair cells.
    Journal of Neuroscience 02/2002; 22(1):44-52. · 6.91 Impact Factor
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    A J Ricci, A C Crawford, R Fettiplace
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    ABSTRACT: During transduction in auditory hair cells, hair bundle deflection opens mechanotransducer channels that subsequently reclose or adapt to maintained stimuli, a major component of the adaptation occurring on a submillisecond time scale. Using a photodiode imaging technique, we measured hair bundle motion in voltage-clamped turtle hair cells to search for a mechanical correlate of fast adaptation. Excitatory force steps imposed by a flexible glass fiber attached to the bundle caused an initial movement toward the kinocilium, followed by a fast recoil equivalent to bundle stiffening. The recoil had a time course identical to adaptation of the transducer current, and like adaptation, was most prominent for small stimuli, was slowed by reducing extracellular calcium, and varied with hair cell resonant frequency. In free-standing hair bundles, depolarizations positive to 0 mV evoked an outward current attributable to opening of transducer channels, which was accompanied by a sustained bundle deflection toward the kinocilium. Both processes were sensitive to external calcium concentration and were abolished by blocking the transducer channels with dihydrostreptomycin. The similarity in properties of fast adaptation and the associated bundle motion indicates the operation of a rapid calcium-sensitive force generator linked to the gating of the transducer channels. This force generator may permit stimulus amplification during transduction in auditory hair cells.
    Journal of Neuroscience 11/2000; 20(19):7131-42. · 6.91 Impact Factor
  • R Fettiplace, A C Crawford, M G Evans
    Annals of the New York Academy of Sciences 06/1992; 656:1-11. · 4.38 Impact Factor
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    A C Crawford, M G Evans, R Fettiplace
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    ABSTRACT: 1. Mechano-electrical transducer currents evoked by deflections of the hair bundle were recorded in turtle isolated hair cells under whole-cell voltage clamp. The outcome of perfusing with solutions of reduced Ca2+ concentration was investigated. 2. The transducer current was roughly doubled by lowering the concentration of divalent cations from normal (2.2 mM-Mg2+, 2.8 mM-Ca2+) to 0 Mg2+, 0.5 mM-Ca2+. No significant effects on the current's kinetics or reversal potential, or on the current-displacement relationship, were noted. 3. If the Ca2+ concentration was lowered to 50 microM (with no Mg2+), there was about a threefold increase in the maximum current but other changes, including loss of adaptation and a decreased slope and negative shift in the current-displacement relationship, were also observed. As a result, more than half the peak transducer current became activated at the resting position of the hair bundle compared to about a tenth in the control solution. 4. The extra changes manifest during perfusion with 50 microM-Ca2+ had also been seen when the cell was held at positive potentials near the Ca2+ equilibrium potential. This supports the view that some consequences of reduced external Ca2+ stem from a decline in its intracellular concentration. 5. With 20 microM-Ca2+, a standing inward current developed and the cell became unresponsive to mechanical stimuli, which may be explained by the transducer channels being fully activated at the resting position of the bundle. 6. The results are interpreted in terms of a dual action of Ca2+: an external block of the transducer channel which reduces the maximum current, and an intracellular effect on the position and slope of the current-displacement relationship; the latter effect can be modelled by internal Ca2+ stabilizing one of the closed states of the channel. 7. During perfusion with 1 microM-Ca2+, the holding current transiently increased but then returned to near its control level. There was a concomitant irreversible loss of sensitivity to hair bundle displacements which we suggest is due to rupture of the mechanical linkages to the transducer channel. 8. Following treatment with 1 microM-Ca2+, single-channel currents with an amplitude of -9 pA at -85 mV were sometimes visible in the whole-cell recording. The probability of such channels being open could be modulated by small deflections of the hair bundle which indicates that they may be the mechano-electrical transducer channels or conductance about 100 pS. 9. Open- and closed-time distributions for the channel were fitted by single exponentials, the mean open time at rest being approximately 1 ms. The mean open time was increased and the mean closed time decreased for movements of the hair bundle towards the kinocilium.(ABSTRACT TRUNCATED AT 400 WORDS)
    The Journal of Physiology 04/1991; 434:369-98. · 4.38 Impact Factor
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    A C Crawford, M G Evans, R Fettiplace
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    ABSTRACT: 1. Transducer currents were recorded in turtle cochlear hair cells during mechanical stimulation of the hair bundle. The currents were measured under whole-cell voltage clamp in isolated cells that were firmly stuck to the floor of the recording chamber. 2. Stimuli were calibrated by projecting the image of the hair bundle onto a rapidly scanned 128 photodiode array. This technique showed that, while the cell body was immobilized, the tip of the bundle would follow faithfully the motion of an attached glass probe up to frequencies of more than 1 kHz. 3. The relationship between inward transducer current and bundle displacement was sigmoidal. Maximum currents of 200-400 pA were observed for deflections of the tip of the bundle of 0.5 microns, equivalent to rotating the bundle by about 5 deg. 4. In response to a step deflection of the bundle, the current developed with a time constant (about 0.4 ms for small stimuli) that decreased with the size of displacement. This suggests that the onset of the current was limited by the gating kinetics of the transduction channel. The onset time course was slowed about fourfold for a 20 degrees C drop in temperature. 5. For small maintained displacements, the current relaxed to about a quarter of the peak level with a time constant of 3-5 ms. This adaptation was associated with a shift of the current-displacement relationship in the direction of the stimulus. The rate and extent of adaptation were decreased by lowering external Ca2+. 6. Adaptation was strongly voltage sensitive, and was abolished at holding potentials positive to the reversal potential of the transducer current of about 0 mV. It was also diminished by loading cells with 10 mM of the Ca2+ chelator BAPTA. These observations suggest that adaptation may be partly controlled by influx of Ca2+ through the transducer channels. 7. Removal of adaptation produced asymmetric responses, with fast onsets but slow decays following return of the bundle to its resting position; the offset time course depended on both the magnitude and duration of the prior displacement. 8. In some experiments, hair bundles were deflected with a flexible glass fibre whose motion was monitored using a dual photodiode arrangement. Positive holding potentials abolished adaptation of the transducer currents, but had no influence on the time course of motion of the fibre. We have no evidence therefore that adaptation is caused by a mechanical reorganization within the bundle.
    The Journal of Physiology 01/1990; 419:405-34. · 4.38 Impact Factor
  • J J Art, A C Crawford, R Fettiplace
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    ABSTRACT: The electrical and mechanical properties of single hair cells from the turtle's cochlea were examined to investigate the basis of their electrical resonance. Receptor potentials were measured with intracellular micropipettes in the isolated basilar papilla. At the onset and termination of a step displacement of the ciliary bundle the receptor potential showed a damped oscillation reflecting the frequency selectivity of the cell. Resonance frequencies increased systematically from apex to base of the cochlea. Similar oscillations could be elicited by a current step injected through the recording electrode. Solitary hair cells enzymatically isolated from the papilla were investigated with the tight-seal whole-cell recording method. Cells retained their properties in response to current steps and had resonance frequencies between 10 and 350 Hz. In voltage clamp such cells displayed a large outward K+ current and an inward Ca2+ current both activated by depolarization from the resting potential. The relaxation time constant of the K+ current was inversely correlated with the resonance frequency of the cell, varying from 150 ms in the lowest frequency cells to less than 1 ms in the highest ones. It is argued that variation in the kinetics of this current is the major factor responsible for the range of resonance frequencies. In preparations of the isolated papilla a flexible glass fibre, attached to the tip of a ciliary bundle, was used to deliver constant force steps to the bundle and to monitor its displacement. Receptor potentials were simultaneously recorded. At the beginning and end of a force step towards the kinocilium, the bundle vibrated at a frequency which coincided with the electrical resonance frequency of the cell.(ABSTRACT TRUNCATED AT 250 WORDS)
    Hearing Research 02/1986; 22:31-6. · 2.54 Impact Factor
  • A CRAWFORD, R FETTIPLACE
    Hearing Research - HEAR RES. 01/1986; 22:91-91.
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    A C Crawford, R Fettiplace
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    ABSTRACT: The mechanical behaviour of the ciliary bundles of hair cells in the turtle cochlea was examined by deflecting them with flexible glass fibres of known compliance during simultaneous intracellular recording of the cell's membrane potential. Bundle motion was monitored through the attached fibre partially occluding a light beam incident on a photodiode array. The change in photocurrent was assumed to be proportional to bundle displacement. For deflexions of 1-100 nm towards the kinocilium, the stiffness of the ciliary bundles was estimated as about 6 X 10(-4) N/m, with the fibre attached to the top of the bundle. When the fibre was placed at different positions up the bundle, the stiffness decreased approximately as the inverse square of the distance from the ciliary base. This suggests that the bundles rotate about an axis close to the apical pole of the cell and have a rotational stiffness of about 2 X 10(-14) N. m/rad. Step displacements of the fixed end of the flexible fibre caused the hair cell's membrane potential to execute damped oscillations; the frequency of the oscillations in different cells ranged from 20 to 320 Hz. Displacements towards the kinocilium always produced membrane depolarization. The amplitude of the initial oscillation increased with displacements up to 100 nm and then saturated. For small displacements of a few nanometres, the hair cell's mechanoelectrical sensitivity was estimated as about 0.2 mV/nm. Force steps delivered by the flexible fibre caused the bundle position to undergo damped oscillations in synchrony with the receptor potential. The mechanical oscillations could be abolished with large depolarizing currents that attenuated the receptor potential. When placed against a bundle, a fibre's spontaneous motion increased and became quasi-sinusoidal with an amplitude several times that expected from the compliance of the system. It is suggested that the hair bundle drives the fibre. We conclude that turtle cochlear hair cells contain an active force generating mechanism.
    The Journal of Physiology 08/1985; 364:359-79. · 4.38 Impact Factor
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    J J Art, A C Crawford, R Fettiplace, P A Fuchs
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    ABSTRACT: 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. 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. 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. 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. 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. Perfusion with perilymphs containing 0.5-15 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. 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. We conclude that the efferent modification of the shape of the tuning curve may be a composite result of the synaptic conductance and the hyperpolarization of the hair cell membrane.
    The Journal of Physiology 04/1985; 360:397-421. · 4.38 Impact Factor
  • A C Crawford, R Fettiplace
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    ABSTRACT: Impulse activity of single auditory nerve fibres was recorded in the isolated half-head of the turtle in response to displacements of a piezoelectric probe placed on the basilar membrane. The temporal pattern of firing in response to sinusoidal displacements of amplitude 0.1-1.0 nm r.m.s. at a fibre's characteristic frequency could be matched to that generated by low-level tonal stimuli delivered to the tympanum. Frequency-threshold curves for acoustic and mechanical stimuli had similar shapes and differed only at frequencies above 500 Hz where the middle ear should filter acoustic but not direct mechanical stimuli. Step displacements of the basilar membrane gave a transient periodic discharge which resembled the responses to acoustic clicks. Most fibres initially increased their firing rate for rarefaction clicks and displacements towards the scala tympani.
    Hearing Research 12/1983; 12(2):199-208. · 2.54 Impact Factor
  • J J Art, A C Crawford, R Fettiplace, P A Fuchs
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    ABSTRACT: Intracellular recordings were made from hair cells in the isolated cochlea of the turtle to characterize the inhibition achieved by the cochlea's efferent innervation. A short train of shocks delivered to the efferent axons produced in the hair cells slow hyperpolarizing synaptic potentials which could be reversed by shifting the membrane potential more negative than about -80 mV. Throughout the efferent hyperpolarization, there was a reduction of up to 25-fold in the amplitude of the receptor potential for tones presented at the hair cell's characteristic frequency. Efferent stimulation also was shown to degrade the cell's tuning properties. It is argued that the combined effects of the hyperpolarization and the loss in hair cell sensitivity could account for a threshold elevation of at least 70 dB in the auditory nerve fibres.
    Proceedings of the Royal Society of London. Series B, Containing papers of a Biological character. Royal Society (Great Britain) 11/1982; 216(1204):377-84.
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    A C Crawford, R Fettiplace
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    ABSTRACT: 1. Intracellular recordings were made from single cochlear hair cells in the isolated half-head of the turtle. Receptor potentials were recorded while the ear was stimulated with high-intensity tones in order to examine the cochlear non-linearities which shape the hair cell responses.2. The size of a hair cell's voltage response to a tone burst was reduced, abolished and then reversed by steady depolarizing currents of increasing strength. The average current needed to produce reversal was about 0.3 nA, the reversal potential being close to zero with respect to the scala tympani.3. Short current pulses injected on the peaks and dips of the receptor potential showed that the membrane resistance and time constant were decreased on the depolarizing phase of the receptor potential. These changes were not due to non-linearity in the hair cell's current-voltage curve in the absence of acoustic stimulation. The results are consistent with the idea that the transducer causes the cell to depolarize by increasing the membrane conductance to ions with an equilibrium potential close to zero.4. Saturated receptor potentials from poorly tuned cells exhibited a pronounced asymmetry, with the maximum depolarizing excursion being several times the maximum hyperpolarizing excursion. This asymmetry was not seen in sharply tuned cells. It is proposed that the asymmetry is present in the transducer conductance change and in sharply tuned cells is reduced in the receptor potential by subsequent filtering.5. For high sound pressures which produced close to a saturated response, the hair cell voltage wave form displayed a number of non-linear features dependent upon the frequency of stimulation relative to the characteristic frequency (c.f.). The most prominent feature occurred at very low frequencies where the potential exhibited damped oscillations on the depolarizations and hyperpolarizations; these ;ringing frequencies' lay above and below the c.f. of the cell respectively.6. The ;ringing frequencies' varied with the c.f. of the cell but for a given cell were largely independent of the frequency of stimulation. The ;ringing frequencies' could be changed by injecting steady currents into the cell during acoustic stimulation; depolarizing currents increased the ringing frequencies and hyperpolarizing currents decreased the frequencies.7. The hair cell's response to a continuous test tone at the c.f. of the cell could be suppressed by simultaneous addition of a second tone whose sound presure was comparable to, or greater than, the test tone. The degree of suppression varied with the intensity and frequency of the second tone, and was maximal close to the c.f. of the cell. The sound pressure required to produce a constant suppression as a function of frequency was sharply tuned, and the tuning of the suppression showed similarities to the frequency selectivity of two-tone suppression described in the auditory nerve.8. An attempt was made to reconstruct the main features of the receptor potential at high intensities.
    The Journal of Physiology 07/1981; 315:317-38. · 4.38 Impact Factor
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    A C Crawford, R Fettiplace
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    ABSTRACT: 1. Intracellular recordings were made from single cochlear hair cells in the isolated half-head of the turtle. The electrical responses of the cells were recorded under two conditions: (a) when the ear was stimulated with low-intensity tones of different frequencies and (b) when current steps were injected through the intracellular electrode. The aim of the experiments was to evaluate the extent to which the cochlea's frequency selectivity could be accounted for by the electrical properties of the hair cells.2. At low levels of acoustic stimulation, the amplitude of the hair cell's receptor potential was proportional to sound pressure. The linear tuning curve, which is defined as the sensitivity of the cell as a function of frequency when the cell is operating in its linear range, was measured for a number of hair cells with characteristic frequencies from 86 Hz to 425 Hz.3. A rectangular current passed into a hair cell elicited a membrane potential change consisting of a damped oscillation superimposed on a step. Small currents produced symmetrical oscillations at the beginning and end of the pulse. Larger currents increased the initial ringing frequency if depolarizing and decreased it if hyperpolarizing.4. For small currents the frequency of the oscillations and the quality factor (Q) of the electrical resonance derived from the decay of the oscillations were close to the characteristic frequency and Q of the hair-cell linear tuning curve obtained from sound presentations.5. The hair cell's membrane potential change to small-current pulses or low-intensity tone bursts could be largely described by representing the hair cell as a simple electrical resonator consisting of an inductance, resistor and capacitor.6. When step displacements of 29-250 nm were applied to a micropipette, placed just outside a hair cell in the basilar papilla, an initial periodic firing of impulses could be recorded from single fibres in the auditory nerve. Currents of up to 1 nA, injected through the same micropipette, failed to produce any change in the auditory nerve discharge. The experiment demonstrates that current injection does not produce gross movements of the electrode tip.7. The contribution of the electrical resonance to hair-cell tuning was assessed by dividing the linear tuning curve by the cell's impedance as a function of frequency. The procedure assumes that the electrical resonance is independent of other filtering stages, and on this assumption the resonance can account for the tip of the acoustical tuning curve.8. The residual filter produced by the division was broad; it exhibited a high-frequency roll-off with a corner frequency at 500-600 Hz, similar in all cells, and a low-frequency roll-off, with a corner frequency from 30 to 350 Hz which varied from cell to cell but was uncorrelated with the characteristic frequency of the cell.9. The phase of the receptor potential relative to the sound pressure at the tympanum was measured in ten cells. For low intensities the phase characteristic was independent of the sound pressure. At low frequencies the receptor potential led the sound by 270-360 degrees , and in the region of the characteristic frequency there was an abrupt phase lag of 90-180 degrees ; the abruptness of the phase change depended upon the Q of the cell.10. The calculated phase shift of the electrical resonator as a function of frequency was subtracted from the phase characteristic of the receptor potential. The subtraction removed the sharp phase transition around the characteristic frequency, and in this frequency region the residual phase after subtraction was approximately constant at +180 degrees . This is consistent with the idea that the hair cells depolarize in response to displacements of the basilar membrane towards the scala vestibuli. The high-frequency region of the residual phase characteristic was similar in all cells.11. It is concluded that each hair cell contains its own electrical resonance mechanism which accounts for most of the frequency selectivity of the receptor potential. All cells also show evidence of a broad band-pass filter, the high frequency portion of which may be produced by the action of the middle ear.
    The Journal of Physiology 04/1981; 312:377-412. · 4.38 Impact Factor

Publication Stats

2k Citations
156.70 Total Impact Points

Institutions

  • 2008
    • UniversitĂ© Victor Segalen Bordeaux 2
      Burdeos, Aquitaine, France
  • 1980–2008
    • University of Cambridge
      • Department of Physiology, Development and Neuroscience
      Cambridge, England, United Kingdom
  • 2000–2006
    • University of Wisconsin–Madison
      Madison, Wisconsin, United States
  • 2002–2005
    • Louisiana State University Health Sciences Center New Orleans
      • Center for Neuroscience
      New Orleans, LA, United States
  • 2003
    • University of Bristol
      Bristol, England, United Kingdom