Vibration pattern of the organ of Corti up to 50 kHz: evidence for resonant electromechanical force

Abstract

Electromechanical force derived from the soma of the outer hair cell has long been postulated as the basis of the exquisite sensitivity of the cochlea. The problem with this postulate is that the electrical source and mechanical load for the electromechanical outer hair cell might be severely attenuated and phase-shifted by the electrical impedance of the cell and the mechanical impedance of the organ of Corti, respectively. Until now, it has not been possible to experimentally derive the high-frequency electrically induced force at the reticular lamina when the cells are embedded within the organ of Corti. In the study reported here, we succeeded in determining the frequency spectrum of the force up to 50 kHz. This was achieved by measuring both the electrically induced velocity and the mechanical impedance at different radial positions on the reticular lamina without tectorial membrane and with clamped basilar membrane. Velocity was measured with a laser interferometer and impedance, with a magnetically driven atomic force cantilever. The electromechanical force, normalized to the electric current density, exhibited a broad amplitude maximum at 7-20 kHz with a quality factor, Q(3dB), of 0.6 - 0.8. The displacement response was independent of frequency up to 10-20 kHz. The force response compensates for the viscoelastic impedance of the organ of Corti, extending the amplitude response of the organ to high frequencies. It is proposed that the electrical phase response of the cell is compensated with Zwislocki's original mechanism of a parallel resonance in the tectorial membrane-stereocilia complex.

Fig. 1.

Displacement amplitudes (Upper) and phases (Lower) for three preparations, at 12 (Left), 8(Center), and 4 (Right) mm from the basal end of the BM. Thin arrows: CFs calculated from the tonotopic map in Tsuji and Liberman (55): 1.2, 4.2, and 15.2 kHz. Data (symbols) and hypothetical responses (lines) are for IHCs (▾, full black line) and OHCs of the first (○, full gray line) and second (Δ, broken gray line) rows. The lines give the displacement responses to a hypothetical, frequency-independent force acting on the (measured) impedance at the respective position. The amplitude of this test force is scaled arbitrarily to match the measured displacement amplitudes at 480 Hz. Above 4–5 kHz for OHCs and 1–2 kHz for IHCs, the measured displacement is higher than expected for a constant force. The measured frequency responses correspond to a second-order low-pass filter. The appearance of inflection points (thick arrows) in the amplitude responses implies that the filter is not a resonant one. The cutoff frequency, f_c, quantifies the onset of the high-frequency amplitude roll-off and is defined as the intersection of two regression lines (thin lines illustrating the case for an IHC): one just below and the other above f_c, in the asymptotic high-frequency amplitude region. GPX, experiment identifier.

Fig. 2.

Displacement amplitudes (A, C, and E) and phases (B, D, and F) at different radial positions for three preparations. Distances are 11 (A and B), 6 (C and D), and 3 (E and F) mm from the basal end of the BM. Arrows, CFs calculated from the tonotopic map in Tsuji and Liberman (55): 1.6, 8, and 20.9 kHz. Radial positions are IHC, inner pillar cells (IPC), tunnel of Corti (ToC), outer pillar cells (OPC), first- to third-row OHCs, outer tunnel (OT), and Hensen's cells (HeC). Notice phase reversals between IPC and OPC and between second OHC and OT. Note that phase jumps randomly when amplitudes approach the noise level (typically, -30 to -40 dB). TierX, experiment identifier.

Fig. 3.

Force amplitudes (Upper) and phases (Lower) for three preparations at 12 (Left), 7 (Center), and 4 (Right) mm. Arrows, CFs calculated from the tonotopic map in Tsuji and Liberman (55): 1.2, 5.8, and 15.2 kHz. Data symbols are for IHCs (▾) and OHCs of the first (○), second (Δ), and third (+) rows. The maximum is most pronounced for the IHC. Above the frequency of the maximum, amplitudes and phases correspond to a low-pass filter of order between one and two. GPX, experiment identifier.