Mechanical Indentation of the Vestibular Labyrinth and its Relationship to Head Rotation in the Toadfish, Opsanus tau. Rabbitt, R. D., R. Boyle, and S. M. Highstein. Department of Bioengineering, 2480 Merrill Engineering Building, University of Utah, Salt Lake City, UT 84112, Departments of Otolaryngology/Head-Neck Surgery and Physiology, Oregon Health Sciences University, Portland, OR, 97201, Departments of Otolaryngology, Anatomy and Neurobiology, Washington University School of Medicine, St. Louis, MO 63110, Marine Biological Laboratory, Woods Hole, Massachusetts 02543.
APStracts 2:0013N, 1995.
SUMMARY AND CONCLUSIONS
1. The present study examines the response of the semicircular canal of the toadfish (Opsanus tau) to head rotation and to mechanical indentation of the membranous labyrinth. The relationship between the two stimuli is described by a new elasto-hydrodynamic model that delineates the three-dimensional (3-D) spatio-temporal distribution of endolymph pressure and flow. In-vivo electrophysiological recordings of primary afferents supplying the horizontal canal (HC) were employed to validate the model predictions. Data were collected from 213 afferents in 18 fish during independent head rotation, HC indentation, utricle (U) indentation and paired stimuli. To quantify the afferent response and the relationship between the applied sinusoidal stimuli the magnitude (gain) and temporal relationship (phase) of the first harmonic of modulation were calculated and compared to theoretical predictions. 2. Elasto-Hydrodynamic Theory. A mathematical model based extensively on the 3-D morphology of a model toadfish labyrinth and the physical properties of endolymph is presented to describe the relationship between head rotation and mechanical indentation. All model parameters specifying labyrinthine morphology and physical properties of endolymph are known; the model contains no free parameters. New results are independent of the structural properties of the cupula. The analysis employs an asymptotic solution of the Navier- Stokes equations in the three toroidal ducts that includes the 3-D fluid- structure interaction taking place within the enlarged ampulla. The solution addresses the differential pressure DP acting across the cupula and the dilatational pressure Po acting on both sides of the cupula. The analysis quantifies the hydrodynamics of the horizontal canal for mechanical indentations of the long-and-slender portion of the canal duct (HC indentation) and the utricle (U indentation). Results specifically relate the indentation stimuli to head rotation. Linear commutations of HC indentation, U indentation and rotation stimuli are analyzed by matching the differential component of the pressure DP acting across the cupula for the three stimulus modalities. 3. Low Frequency Relationship of Mechanical Indentation to Head Rotation. HC afferents show a linear correspondence between HC indentation, U indentation and rotation stimuli. Specific experimental results for sinusoidal stimuli at frequencies <2 Hz show: i) 1mm HC indentation commutates with 4 deg/s rotation, ii) 1mm HC indentation commutates with 15 mm U indentation, and iii) 15 mm U indentation commutates with 4 deg/s rotation. These results were obtained by adjusting the relative amplitude and phase of two stimuli presented simultaneously to achieve destructive interaction that minimizes the afferent modulation (balanced). Equivalent results were obtained using afferent responses to the stimuli applied independently. Neural results are in quantitative agreement with the 3-D analysis of the labyrinthine elasto- hydrodynamics, supporting the conclusion that the correspondence between mechanical indentations and head rotation is due to the intrinsic biomechanics of the labyrinth. 4. High Frequency Mechanical Indentation. As predicted by the theory, afferent recordings show that the simple linear correspondence between HC indentation and head rotation (point 3 above) does not extend to high 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 retarded in order to match the response to head rotation. For the toadfish, this frequency dependence occurs above 2 Hz. Also owing to endolymph inertia, theoretical results show that the mass-induced upper-corner frequency associated with head rotation does not exist during HC indentation. This prediction was confirmed experimentally using afferent responses to simultaneous HC and U indentation stimuli. 5. Sensitivity to Position of the Indenter. In agreement with the theory, 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 constructive and destructive interference of the afferent response. The phase of the response is insensitive to the location of HC indentation, but reverses 180o during U indentation. Gain of afferent modulation elicited by U indentation is 15 times less than that to HC indentation 3mm from the ampulla. This position sensitivity is quantitatively predicted by the elasto-hydrodynamic theory and below 2 Hz is due to the viscous drag in the long-and-slender region of the canal. The theory also shows that the gain is zero for indentation in the distal vicinity of the posterior canal (PC) bifurcation and that the response to U indentation is insensitive to the position of the indenter. 

Received 18 July 1994; accepted in final form 1 February 1995.
APS Manuscript Number J438-4.
Article publication pending J. Neurophysiol.
ISSN 1080-4757 Copyright 1995 The American Physiological Society.
Published in APStracts on  3 April 1995.