Evidence for outer hair cell driven oscillatory fluid flow in the tunnel of corti

Abstract

Outer hair cell (OHC) somatic motility plays a key role in mammalian cochlear frequency selectivity and hearing sensitivity, but the mechanism of cochlear amplification is not well understood and remains a matter of controversy. We have visualized and quantified the effects of electrically evoked OHC somatic motility within the gerbil organ of Corti using an excised cochlear preparation. We found that OHC motility induces oscillatory motion of the medial olivocochlear fibers where they cross the tunnel of Corti (ToC) in their course to innervate the OHCs. We show that this motion is present at physiologically relevant frequencies and remains at locations distal to the OHC excitation point. We interpret this fiber motion to be the result of oscillatory fluid flow in the ToC. We show, using a simple one-dimensional hydromechanical model of the ToC, that a fluid wave within the tunnel can travel without significant attenuation for distances larger than the wavelength of the cochlear traveling wave at its peak. This ToC fluid wave could interact with the cochlear traveling wave to amplify the motion of the basilar membrane. The ToC wave could also provide longitudinal coupling between adjacent sections of the basilar membrane, and such coupling may be critical for cochlear amplification.

FIGURE 1

Anatomical cross sections of the OC. (A) A cartoon of the OC emphasizing some of the major structures: the three rows of OHCs (OHC1, OHC2, OHC3), the IHCs, the inner pillar cells (IPC), the outer pillar cells (OPC), the arcuate zone (AZ) of the BM, the MOC fibers, and the ToC. The ToC has a triangular cross sectional area and is filled with fluid. The anatomical structures that form the three sides of the tunnel are the IPC, the OPC, and the AZ of the BM. The tunnel communicates with the spaces of Nuel (the fluid space that surrounds the basolateral membrane of the OHCs) via the space between the OPCs. Three axes of optical coordinates are shown: 1) the vertical axis, which is parallel to the optical axis of the microscope objective; 2) the radial axis, extending from the spiral lamina (LAM) to the spiral ligament (LIG); and 3) the longitudinal axis, extending from base to apex. Both the radial and the longitudinal axis are parallel to the surface of the objective. (B and C) Optical cross sections at the levels close to the basal end of the OHCs and the MOC fibers, respectively. Depending on the preparation, the bottom of the image leads toward either the apex or the base of the cochlea. For the experiment illustrated in this figure the bottom of the image leads toward the base. (D and E) The boxed regions of B and C are shown magnified in D and E, respectively. Scale bar for B, 44 μm and for D, 22 μm.

FIGURE 2

Images of OHCs and MOC fibers taken at different times within one stimulus period. (A and D) No stimulus condition. (B and E) Phase 90°. (C and F) Phase 270°. The dotted line in each of the images is added as a reference to emphasize the observation that during the stimulus period the OHCs are displaced in the radial direction (also longitudinal in most of the experiments), and the MOC fibers are displaced in the longitudinal direction. Also note that the MOC fibers are displaced without significant shape changes. In this figure the bottom of the images leads toward the base of the cochlea.

FIGURE 3

Frequency response of OHC1 (solid symbols) and MOC fibers (open symbols) for experiment 131R (A–C) and 213R (D–F). Each data point represents the average of several cells of the corresponding structures. Specifically, the data in panels A and B are the average of eight OHC1 (solid symbols) and eight MOC fibers (open symbols) and the data in panels D and F are the average of eight OHC1 (solid symbols) and two MOC fibers (open symbols). The error bars indicate the standard deviation. For OHC1 the displacement shown is in the radial direction, whereas for the MOC fibers the displacement is in the longitudinal direction. For both experiments, zero phase for the OHCs corresponds to motion toward the spiral ligament and for the MOC fibers corresponds to motion toward the base. The noise floor in these experiments is ∼60 nm peak-to-peak (PP).

FIGURE 4

OHC3 total displacement and resulting ToC flow as a function of longitudinal position for experiments 1011R (A and B) and 1026R (C and D). The stimulus frequency is 60 Hz. Each point in the graph represents the average displacement/flow along a 200-μm cochlea length. Different locations were measured in random order, and their time sequence is indicated by the number next to the data point, i.e., data point 1 was collected first, data point 2 was collected second, etc. The arrows indicate the location of the basal cut (B), the electrode (E), and the apical cut (A). The noise level for experiment 1011R is ∼40 nm and for experiment 1026R it is ∼30 nm.

FIGURE 5

One-dimensional hydromechanical model of the ToC. The fluid mass in the ToC per unit length is represented by an inductor (L_ToC), the tube resistance per unit length is represented by a resistor (R_ToC), and the volume compliance of the AZ per unit length is represented by a capacitor (C_AZ). Parameter values were calculated as follows: L_ToC = ρ/A_ToC from Benade (35), from Benade (35), C_AZ from Naidu and Mountain (18), where the density of water ρ = 10⁻¹² g/μm³, the coefficient of shear viscosity in water σ = 10 ⁻⁶ g/(μm s), the cross sectional area of the ToC A_ToC = H_ToC W_ToC/2, H_ToC is the ToC height estimated as the height of IPC from Edge et al. (15), W_ToC is the ToC width estimated as the width of AZ from Edge et al. (15). H_ToC varied from 55 μm to 76 μm and W_ToC varied from 42 μm to 52 μm from base to apex. The resulting values for R_ToC varied from 19 × 10⁻¹² g/(μm⁵ s) at the base to 6.5 × 10⁻¹² g/(μm⁵ s) at the apex. The values for L_ToC varied from 8.7 × 10⁻¹⁶ g/(μm⁵ s) at the base to 5.1 × 10⁻¹⁶ g/(μm⁵ s) at the apex. The input to the model is the oscillatory fluid flow generated per section from the contractions of the OHCs (U_OHC(y)). The output of the model is the oscillatory ToC flow (U_ToC(y)) which by convention is positive if directed toward the apex.

FIGURE 6

Model input (“OHC flow”) and output (“ToC flow”) for two electrode positions (indicated by the arrows in panel A): 2 mm from the base (E1, gray line) and 8 mm from the base (E2, black line). “OHC flow” represents the flow generated from the OHCs per section and is the input to our model. “ToC flow” represents the flow in the ToC that results from the “OHC flow”. The location where the “ToC flow” shifts direction depends on both the electrode location and the impedance of the tunnel on each side of the electrode.