A model for signal transmission in an ear having hair cells with free-standing stereocilia. I. Empirical basis for model structure

Abstract

No adequate theory for the signal-transmission properties of the peripheral auditory system exists for any vertebrate ear. Because the mammalian ear seems to pose conceptual and technical problems that complicate the development of an adequate theory, it is worthwhile to investigate simpler ears. The ear of the alligator lizard is simpler than mammalian ears in several respects: the motion of the basilar membrane is approximately independent of longitudinal position and is approximately linearly related to the sound pressure at the tympanic membrane; in a large region of the cochlea the hair cells have free-standing stereocilia that are not in contact with a tectorial membrane; the receptor potential of these hair cells is related to the sound pressure at the tympanic membrane in a relatively simple manner; the cochlear-nerve fiber responses from this region do not exhibit two-tone rate suppression. Also, the relative accessibility of this ear has enabled measurement of several response variables: tympanic-membrane volume velocity, extracolumella velocity, basilar-membrane velocity, hair-cell stereociliary displacement, hair-cell receptor potentials, and cochlearnerve-fiber discharges. A model is developed to represent these results in terms of underlying anatomical structures and physiological mechanisms. The model consists of four cascaded signal-processing stages: 1. (1) a macromechanical stage that relates the sound pressure at the tympanic membrane to the velocity of the basilar membrane by an acoustico-mechanical network model of the middle and inner ear and which acts as a bandpass, linear, time-invariant filter; 2. (2) a micromechanical stage that relates the velocity of the basilar membrane to the angular displacement of the hair-cell stereocilia by a hydrodynamic system that acts as a tonotopically-organized, bandpass, linear, time-invariant filter; 3. (3) a mechanoelectric transduction stage that relates the angular displacement of the stereocilia to a change in membrane resistance through a set of angular-displacement-controlled membrane ionic channels and which behaves as a memoryless nonlinear function; 4. (4) an electric stage that relates the change in resistance to the receptor potential by an electric network model of a hair cell that behaves approximately as a lowpass filter. This model predicts most — but not all — of the measured signal-transmission properties of this ear.