Origin of the receptor potential in inner hair cells of the mammalian cochlea—evidence for Davis' theory

Abstract

The primary sensory hair cells of the mammalian cochlea are located in the organ of Corti, a sensory epithelium which separates fluids of widely differing chemical composition. The apical, sensory surfaces of the hair cells are exposed to the potassium-rich endolymph of the scala media and their lateral and ventral surfaces are exposed to the perilymph of the scala tympani whose chemical composition resembles that of other extracellular fluids^1–3. The high potassium concentration of the endolymph (150 mM) is believed to result from the activity of electrogenic potassium pumps located in the stria vascularis which lines the lateral walls of the cochlea³. These pumps are also the source of the positive endocochlear potential of about +80 mV which can be recorded from the scala media^4–6. When the ear is stimulated with sound, receptor potentials may be recorded extracellularly from the fluid-filled spaces of the cochlea^7,8, and intracellularly from the rows of inner and outer hair cells^9–11. According to the ‘resistance microphone’ theory of Davis¹², these receptor potentials are derived from the preexisting polarization of the hair cells by a change in the ohmic resistance of the mechanosensitive portion of the cell membrane (Fig. 1). This produces potential changes in the scala tympani and scala media of opposite phase, thus giving rise to the cochlear microphonic (CM). Evidence is presented here to support this theory. When sufficient depolarizing current is injected into inner hair cells to cancel the polarizing voltage, the receptor potentials disappear, and their phase is reversed when the polarizing voltage across the apical membranes of the hair cells is reversed.