MECHANICAL INDENTATION OF THE VESTIBULAR LABYRINTH AND ITS RELATIONSHIP TO HEAD ROTATION IN THE TOADFISH, OPSANUS-TAU

1. In the present study we examine the response of the semicircular ca nal of the toadfish (Opsanus tail) to head rotation and to mechanical indentation of the membranous labyrinth. The relationship between the two stimuli is described by a new elastohydrodynamic model that deline ates the three-dimensional (3-D) spatio-temporal distribution of endol ymph pressure and flow. In vivo electrophysiological recordings of pri mary afferents supplying the horizontal canal (HC) were employed to va lidate the model predictions. Data were collected from 213 afferents i n 18 fish during independent head rotation, HC indentation, utricle (U ) indentation, and paired stimuli. To quantify the afferent response a nd the relationship between the applied sinusoidal stimuli, the magnit ude (gain) and temporal relationship (phase) of the first harmonic of modulation were calculated and compared with theoretical predictions. 2. A mathematical based extensively on the 3-D morphology of a toadfis h labyrinth and the physical properties of endolymph is presented to d escribe the relationship between head rotation and mechanical indentat ion. All model parameters specifying labyrinthine morphology and physi cal properties of endolymph are known; the model contains no free para meters. New results are independent of the structural properties of th e cupula. The analysis employs an asymptotic solution of the Navier-St okes equations in the three toroidal ducts that includes the 3-D fluid -structure interaction taking place within the enlarged ampulla. The s olution addresses the differential pressure (Delta P) acting across th e cupula and the dilatational pressure acting on both sides of the cup ula. The analysis quantifies the hydrodynamics of the HC for mechanica l indentations of the long and slender portion of the canal duct (HC i ndentation) and the U (U indentation). Results specifically relate the indentation stimuli to head rotation. Linear commutations of HC inden tation, U indentation, and rotation stimuli are analyzed by matching D elta P acting across the cupula for the three stimulus modalities. 3. HC afferents show a linear correspondence between KC indentation, U in dentation, and rotation stimuli. Specific experimental results for sin usoidal stimuli at frequencies <2 Hz show 1) +/-1 mu m-HC indentation commutates with -/+4 degrees/s rotation, 2) +/-1-mu m HC indentation c ommutates with -/+5-mu m U indentation, and 3) -/+15-mu m U indentatio n commutates with +/-4 degrees/s rotation. These results were obtained by adjusting the relative amplitude and phase of two stimuli presente d simultaneously to achieve destructive interaction that minimizes the afferent modulation (balanced). Equivalent results were obtained usin g afferent responses to the stimuli applied independently. Neural resu lts are in quantitative agreement with the 3-D analysis of the labyrin thine elastohydrodynamics, supporting the conclusion that the correspo ndence between mechanical indentations and head rotation is due to the intrinsic biomechanics of the labyrinth. 4. As predicted by the theor y, afferent recordings show that the simple linear correspondence betw een HC indentation and head rotation (see above) does not extend to hi gh frequencies. The theory quantifies this in terms of differences in the inertial forces arising within the endolymph. At high frequencies, the amplitude of HC indentation must be reduced and the phase retarde d to match the response to head rotation. For the toadfish, this frequ ency dependence occurs at >2 Hz. Also owing to endolymph inertia, theo retical results show that the mass-induced upper corner frequency asso ciated with head rotation does not exist during HC indentation. This p rediction was confirmed experimentally using afferent responses to sim ultaneous HC and U indentation stimuli. 5. In agreement with the theor y, the magnitude of afferent modulation decreases as the distance from the sensory epithelium to the position of the indenter is increased. Position sensitivity was measured by adjusting the amplitude and phase of HC indentation relative to simultaneous U indentation, or a second HC indentation at a different location, to achieve maximum constructi ve and destructive interference of the afferent response. The phase of the response is insensitive to the location of HC indentation, but re verses 180 degrees during U indentation. Gain of afferent modulation e licited by U indentation is similar to 15 times less than that elicite d by HC indentation similar to 3 mm from the ampulla. This position se nsitivity is quantitatively predicted by the elastohydrodynamic theory and at <2 Hz is due to the viscous drag in the long and slender regio n of the canal. The theory also shows that the gain is 0 for indentati on in the distal vicinity of the posterior canal (PC) bifurcation and that the response to U indentation is insensitive to the position of t he indenter.