Minimal basilar membrane motion in low-frequency hearing

Abstract

Low-frequency hearing is critically important for speech and music perception, but no mechanical measurements have previously been available from inner ears with intact low-frequency parts. These regions of the cochlea may function in ways different from the extensively studied high-frequency regions, where the sensory outer hair cells produce force that greatly increases the sound-evoked vibrations of the basilar membrane. We used laser interferometry in vitro and optical coherence tomography in vivo to study the low-frequency part of the guinea pig cochlea, and found that sound stimulation caused motion of a minimal portion of the basilar membrane. Outside the region of peak movement, an exponential decline in motion amplitude occurred across the basilar membrane. The moving region had different dependence on stimulus frequency than the vibrations measured near the mechanosensitive stereocilia. This behavior differs substantially from the behavior found in the extensively studied high-frequency regions of the cochlea.

Keywords: basilar membrane; hair cells; hearing; optical coherence tomography.

Fig. 1.

Sound-evoked movements of the lateral segment of the basilar membrane are small in isolated preparations. (A) Schematic drawing of the organ of Corti indicating the approximate measurement locations on the basilar membrane and the Hensen cells. (Lower Left) Basilar membrane is identified with confocal microscopy, revealing a honeycomb-like pattern of cells. (Lower Right) Hensen cells are found near the stereocilia of the outer hair cells. (B) Three-dimensional reconstructions obtained from confocal image stacks with 4-μm section spacing were used for determining the spatial relations between measurement sites. (C) Absolute location of the measurement spot was determined by confocal imaging of the focused measurement beam (red dots, here focused on the basilar membrane). (D) Peak basilar membrane displacement is smaller than peak Hensen cell vibration. The stimulus level is 59 dB SPL. Note that all sound pressures given in this figure were corrected for attenuation caused by immersion of the preparation in tissue culture medium (Methods). (E) At 59 dB SPL, basilar membrane vibrations peak at higher frequencies in most preparations. (F) Frequency difference ranges from 0 to 150 Hz. In no case was the basilar membrane tuned to a lower frequency than the Hensen cells. BF, best frequency. (G and H) Mechanical tuning curves are of similar shape as the tuning of the cochlear microphonic potentials. Sound pressure in G was 59 dB SPL. Amp, amplitude. (I) Sharpness of tuning does not differ between the basilar membrane and the Hensen cells. (J) Hensen cells show compressive nonlinearity at levels >85 dB SPL.

Fig. 2.

Minimal basilar membrane movement during electrical stimulation in isolated preparations. (A, Upper) Current ramps going from −5 to +5 μA (Inset) result in no apparent motion at the basilar membrane. (A, Lower) Lack of electrically evoked motions of bone, the stimulus electrode, and Reissner’s membrane. (B) Current-evoked displacement (Displ) measured from three separate sites on the basilar membrane (A–C in the schematic drawing). The motion of each site is separately plotted, as indicated by the label on each graph. (C) In contrast to the basilar membrane, Hensen cells show large motion during electrical stimulation (−5 to +5 μA). (D, Lower Left) Current-evoked motion of Hensen cells is reversibly abolished by salicylate (10 mM, stimulus amplitude of −5 to + 5 μA). The basilar membrane is not affected by salicylate (Upper Left) or FM1-43 (Upper Right), but Hensen cell motion is sharply reduced after application of FM1-43 (Lower Right). Disp, displacement.

Fig. 3.

In vivo motion of the basilar membrane and reticular lamina in closed cochleae. (A) Color-coded displacement data were superimposed on a morphological scan (grayscale). The stimulus is a 175-Hz tone at 90 dB SPL. (B) Tuning curves at the reticular lamina and at the basilar membrane were similar in shape, but the amplitude at the basilar membrane was smaller. The thick lines show the mean amplitude ± SEM in six preparations, and the thin lines show the corresponding phase values ± SEM. The measurement location is ∼1.5 mm from the helicotrema. (C) Tuning curves from the reticular lamina (blue solid line) and basilar membrane (red solid line) in a single preparation. The dashed lines show a reticular lamina tuning curve acquired in vivo (blue dashed line) and postmortem (black dashed line) from a different preparation, where the measurement location was closer to the base of the cochlea than the preparations included in the averaged data in B. (D) Averaged vibrations of structures in the organ of Corti, from the reticular lamina (RL) toward the basilar membrane (n = 6). (E) Basilar membrane vibrations peak in an area 30–50 μm medial to the edge of the organ of Corti, but decline rapidly on either side of the peak. The thick red lines are fits to the exponential function given in the main text, and the vertical line and gray zone indicate the average position (±SEM) of the lateral edge of the organ of Corti (OoC) relative to the location of peak vibration. (F) Reticular lamina displacement at the best frequency. Thick red lines are fits to the functions 502 − 2 × distance and 475 − 6.5 × distance. (G) Phase is invariant with distance from the peak for both the reticular lamina and the basilar membrane. diff., difference. (H) Reissner’s membrane shows behavior qualitatively similar to the basilar membrane, but the length scale of the exponential decay is different. All vibration data in this figure were acquired at a stimulus level of 90 dB SPL. The thin red lines in E, F, and H show data from the preparation plotted with solid lines in C.

Fig. 4.

Morphological differences between the basal and apical turns may contribute to the sound-evoked motion of the basilar membrane. (A) In the basal cochlear turn, the basilar membrane has a dense core surrounded on both sides by layers of cells. (B) In the apical turn, the dense core is replaced by a thin layer of tissue that runs through the width of the basilar membrane.