A differentially amplified motion in the ear for near-threshold sound detection

Abstract

The ear is a remarkably sensitive pressure fluctuation detector. In guinea pigs, behavioral measurements indicate a minimum detectable sound pressure of ∼20 μPa at 16 kHz. Such faint sounds produce 0.1-nm basilar membrane displacements, a distance smaller than conformational transitions in ion channels. It seems that noise within the auditory system would swamp such tiny motions, making weak sounds imperceptible. Here we propose a new mechanism contributing to a resolution of this problem and validate it through direct measurement. We hypothesized that vibration at the apical side of hair cells is enhanced compared with that at the commonly measured basilar membrane side. Using in vivo optical coherence tomography, we demonstrated that apical-side vibrations peaked at a higher frequency, had different timing and were enhanced compared with those at the basilar membrane. These effects depend nonlinearly on the stimulus sound pressure level. The timing difference and enhancement of vibrations are important for explaining how the noise problem is circumvented.

Figure 1

The cochlea and organ of Corti. a. Cross-section of the guinea pig cochlea showing the approach for vibration measurement. The panel on the right illustrates the scanning of the diode beam to obtain images of the hearing organ. b. Schematic organ of Corti cross-section. Arrows depict the direction of motion of different structures. c. OCT image of the organ of Corti in vivo. Asterisks mark the locations of vibration measurement.

Figure 2

Vibration of the basilar membrane (BM, -panel a) and reticular lamina (RL, -panel b) in a guinea pig cochlea. Displacement magnitudes of vibration are plotted as a function of stimulus frequency. An auditory sensitivity loss of 8 dB was caused by surgical procedures in the ear. Numbers against each curve represent sound levels of dB SPL (re 20 μPa) used to induce hearing organ vibration. At 30 dB SPL, the maximum amplitude of BM vibration was 0.21 nm at 18 kHz. RL vibration peaked at 18.75 kHz, with a displacement amplitude of 0.41 nm.

Figure 3

Displacement magnitude as a function of sound level (“input-output function”) measured from the basilar membrane (BM) and reticular lamina (RL). a, Input-output functions of BM (solid lines) and RL displacement (dashed lines); b, Postmortem input-output functions. Data plotted as mean ± standard error. Frequencies were normalized with respect to the best frequency of each animal. The frequency “0.9*BF” represents the frequency 0.9 times below the best frequency, and the frequency “1.05*BF” represents that 1.05 times above it. This compensates for slight variations in best frequencies in different experiments (best frequency range, 18.25-19.5 kHz). BF_P is the best frequency at postmortem and it is around 15 kHz in the experiments. The thin lines mark a linear relationship between the sound pressure level and vibration amplitude.

Figure 4

Sound-induced vibration of the basilar membrane (BM) and reticular lamina (RL) at the 19 kHz best frequency location in an animal with 7 dB sensitivity loss due to surgical preparation. a, b, Displacement amplitude versus frequency. c, d, Displacement phase relative to the speaker driving voltage versus frequency. e, f, Relative phase versus frequency at different sound levels with respect to the phase at 80 dB SPL. Numbers against the color lines in panels c and d represent the sound pressure level, which applies to all panels in this figure. Different sound levels were delivered in random order to avoid systematic errors. In panel b, the RL displacement magnitude at 70 dB SPL is affected by additional sensitivity loss of ~6 dB. This was the last measurement of the experiment.

Figure 5

Phase differences of RL displacement and organ of Corti receptor potential compared with BM motion. a, Phase of RL displacement minus phase of BM displacement at different sound levels plotted for a frequency range of 16-19 kHz and sound levels between 40 and 80 dB SPL. Numbers in the panel represent sound levels in dB SPL. The best frequency is 18 kHz for BM and 18.5 kHz for RL. b, Normalized relative phase of organ of Corti receptor potentials (RP) and BM velocity for sound levels between 40 and 110 dB SPL. The best frequency is 18.5 kHz. Potentials were recorded in the fluid spaces within the organ of Corti adjacent to the outer hair cells. The relative phase lead of electric potentials decreases with sound level as it does for the phase of RL-BM displacement. This is an expected result when the RL displacement is the “drive” to the OHC and the extracellular potential is the result of that displacement. Similar results were also obtained from two additional sensitive animals.