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. 2004 Nov 10;24(45):10057-63.
doi: 10.1523/JNEUROSCI.2711-04.2004.

Organ of Corti Potentials and the Motion of the Basilar Membrane

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Free PMC article

Organ of Corti Potentials and the Motion of the Basilar Membrane

Anders Fridberger et al. J Neurosci. .
Free PMC article

Abstract

During sound stimulation, receptor potentials are generated within the sensory hair cells of the cochlea. Prevailing theory states that outer hair cells use the potential-sensitive motor protein prestin to convert receptor potentials into fast alterations of cellular length or stiffness that boost hearing sensitivity almost 1000-fold. However, receptor potentials are attenuated by the filter formed by the capacitance and resistance of the membrane of the cell. This attenuation would limit cellular motility at high stimulus frequencies, rendering the above scheme ineffective. Therefore, Dallos and Evans (1995a) proposed that extracellular potential changes within the organ of Corti could drive cellular motor proteins. These extracellular potentials are not filtered by the membrane. To test this theory, both electric potentials inside the organ of Corti and basilar membrane vibration were measured in response to acoustic stimulation. Vibrations were measured at sites very close to those interrogated by the recording electrode using laser interferometry. Close comparison of the measured electrical and mechanical tuning curves and time waveforms and their phase relationships revealed that those extracellular potentials indeed could drive outer hair cell motors. However, to achieve the sharp frequency tuning that characterizes the basilar membrane, additional mechanical processing must occur inside the organ of Corti.

Figures

Figure 1.
Figure 1.
A, Schematic drawing showing major structures in a cross section of the organ of Corti. The white asterisk marks the fluid space where fast potential changes occur. TM, Tectorial membrane. B, Receptor current entering through transducer channels will be filtered by the parallel resistance and capacitance of the cell membrane of the outer hair cell. This filter has a frequency response similar to the one shown in C, causing substantial high-frequency attenuation. If extracellular potentials are assumed to drive prestin, the equivalent circuit is more complex, with the frequency response shown in D. In this case, the filter is almost flat throughout the entire frequency range [for parameters and additional details, see Dallos and Evans (1995a)].
Figure 2.
Figure 2.
Calibration of the recording system. Asterisks and squares denote, respectively, the measured amplitude and phase of the recording electrode and amplifier. Solid lines are fits of the amplitude data to a first-order filter that in this case had a cutoff frequency of 3.4 kHz. The input level was 10 mV; amplifier gain of 10.
Figure 4.
Figure 4.
The first 3 msec of the response to a 100 dB SPL tone burst at 2 kHz (stimulus rise time, 1 msec; cos2 envelope). BM velocity (leftmost y-scale; dashed line) is plotted together with organ of Corti potentials (OoC; right y-scale; solid line). Records were compensated for a 29 μsec delay introduced by the recording electrode and a 6 μsec delay introduced by the velocimeter. Both traces were low-pass filtered offline with a zero-phase fourth-order filter with a 10 kHz cutoff frequency. To prevent ringing artifacts introduced by filtering, amplitudes were reduced to zero at the beginning of the record using a Blackman window. In this sensitive preparation, technical problems prevented recording of the BM velocity after electrode penetration.
Figure 5.
Figure 5.
Response onset after a 100 dB SPL tone burst at 3 kHz. Signals were processed as in Figure 4. OoC, Organ of Corti.
Figure 3.
Figure 3.
BM displacement (left y-scale) and organ of Corti electric potentials (OoC; right y-scale) as a function of stimulus frequency for two different stimulus levels. Amplitudes were corrected for the response properties of the recording system. Recordings were from a relatively sensitive animal (total sensitivity loss of 10 dB after withdrawal of recording electrode).
Figure 6.
Figure 6.
Phase difference between potentials inside the organ of Corti and the BM displacement. Same preparation as in Figure 3. All data were corrected for electrode and velocimeter phase response. BF, Best frequency (the stimulus frequency evoking maximum BM response).
Figure 7.
Figure 7.
Phase difference between potentials recorded close to the BM and the BM displacement in an animal with a 5 dB loss of sensitivity at the time of the recording. Stimulus level is 60 dB SPL. The inset shows the normalized amplitude of the electric potentials (solid line) and the BM motion (dotted line). Q10dB values of 2.6 for electric potential and 3.7 for the BM. BF, Best frequency.
Figure 8.
Figure 8.
Phase differences between the organ of Corti potential and the BM displacement were predicted by the model described in the text. The dots show the measured phase difference; the solid line is the fitted curve. The inset shows the tuning curves for the BM (dots), the electric potential (solid line), and the fitted curve (dashed line). Note that the model accurately predicted the shape of the electric tuning curve in the frequency region below and slightly above the best frequency. At frequencies higher than this, substantial deviations were found. To verify these results, we also performed curve fits using guinea pig tuning curves mapped to specific cochlear locations using Greenwood's place-frequency map (Greenwood, 1990). Space constants obtained by this modified model were similar to those shown here.

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