Relationship between Inner-Ear Fluid Pressure and Semicircular Canal Afferent Nerve Discharge

Abstract

The present study was designed to determine (1) the transcupular fluid pressure (ΔP) generated across the semicircular canal cupula in response to sinusoidal head rotation, (2) the translabyrinthine dilational pressure (P₀) generated across the membranous labyrinth in response to an increase in endolymph fluid volume (hydrops), (3) afferent nerve discharge patterns generated by these distinct pressure stimuli and, (4) threshold values of ΔP and P₀ required to elicit afferent neural responses. The experimental model was the oyster toadfish, Opsanus tau. Micromechanical indentation of the horizontal canal (HC) duct and utricular vestibule was used to simulate sinusoidal head rotation and fluid volume injection. Single-unit neural spike trains and endolymph pressure within the ampulla, on both sides of the cupula, were recorded simultaneously. ΔP averaged 0.013 Pa per 1°/s of sinusoidal angular head velocity and P₀ averaged 0.2 Pa per 1 nL of endolymph volume injection. The most responsive afferents had a threshold sensitivity to ΔP of 10^-3 Pa and to P₀ of 5 × 10^-2 Pa based on a discharge modulation criterion of 1 impulse/s per cycle for 2 Hz pressure stimuli. Neural sensitivity to ΔP was expected on the basis of transverse cupular and hair bundle deflections. Analysis of mechanics of the end organ, neuronal projections into the crista, and individual neural firing patterns indicates that P₀ sensitivity resulted from pressure-induced distension of the ampulla that led to a nonuniform cupular deformation pattern and hair bundle deflections. This explanation is consistent with predictions of a finite element model of the end organ. Results have implications regarding the role of ΔP in angular motion transduction and the role of P₀ under transient hydropic conditions.

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APPENDIX

FEM model construction

A simple finite element model of the toadfish HC ampulla and cupula was constructed for the purpose of directing experiments and interpreting results. The model geometry was based on a combination of microscopic observation of fresh tissue and histological sections of the ampulla (Ghanem et al. 1998; Silver et al. 1998). For simplicity, the geometry was reduced to a rectangular 3D domain, and hence the model results are limited to the central region of the crista. The finite element mesh was composed of 8-node brick elements projected to this fish geometry, as illustrated in Figure 12A. The ampullary walls and cupula were modeled as elastic materials. The elastic moduli of the cupula (shear modulus = 0.36 Pa, Poisson ratio = 0.5) and of the membranous duct (shear modulus = 300 Pa, Poisson ratio = 0.5) were selected to match the average cupular displacement and ampullary distension predicted by previous macromechanical models (Damiano and Rabbitt 1996; Rabbitt et al. 1999). In order to model the cupula as a totally incompressible material, an augmented Lagrangian method was used (Maker et al. 1990). The solution was constrained to a plane-strain problem. Motion of the side walls was constrained to the plane, and the bottom edge of the plane was fixed.

Figure 12.

FE model geometry. A Eight-node brick elements were used to construct a simplified rectangular model consisting of elastic elements for the crista and membranous labyrinth (light gray) and soft elastic elements for the cupula (dark gray). B A photomicrograph illustrating the geometry of the crista in the toadfish at the central cutting plane (Ghanem et al. 1998).

Two loading cases were studied: (1) transcupular pressure ΔP and (2) dilational pressure P₀. The pressure for both the ΔP and P₀ cases were applied to all endolymph wetted surfaces including the sides of the crista, the cupular leaflets, and the interior surfaces of the ampulla. The magnitude of the pressure for the ΔP case was taken to be ΔP = 0.01 Pa. The magnitude of pressure used in the P₀ case was taken from the present experimental measurements to be 0.12 Pa. Since the model is linear, displacement magnitudes and shear strains scale with the elastic moduli and pressure but the spatial distribution remains constant.

The FE model presented here for the toadfish cupula is similar to the human model presented by Njeugna et al. (1992). They modeled a two-dimensional slice of the human cupula as a thick, soft, elastic material that spanned the cross section of the ampulla and extended down the sides of a stiff elastic crista. The present model is slightly more general in that we included elasticity of the membranous duct and solved for the resulting ampullary distension. Although differences in geometry between the species cause some differences in the cupular deformation fields, the general trends for both P₀ loading and ΔP loading are similar for the two models.