Ionic basis of the receptor potential in a vertebrate hair cell

Abstract

Vertebrate hair cells, the primary receptors of auditory, vestibular and lateral-line organs, occur in epithelia which separate fluids of differing ionic composition. The apical surfaces of hair cells, on which the mechanosensitive hair bundles are situated, face a high-K⁺ fluid (termed endolymph in the inner ear); the basolateral surfaces instead contact fluid (perilymph or a related substance) of a composition similar to that of other extracellular fluids^1–3. The universal occurrence of high-K⁺ fluid on the apical surfaces of hair cells in vertebrates has been taken as evidence that it is important for the transduction process, in particular that it relates to the ionic specificity⁴ of the conductance change⁵ underlying the receptor potential. There is, however, conflicting experimental evidence regarding this specificity. K⁺ has generally been thought to carry the receptor current, as replacement of endolymph with perilymph in the guinea pig cochlea abolishes the extracellularly recorded microphonic potential⁶. Yet microphonic potentials, as well as intracellular receptor potentials, have been recorded in other preparations when the apical surfaces of the hair cells faced instead a high-Na⁺ saline, and thus when the electrochemical gradient for K⁺ was near zero^5,7. Ca²⁺ has also been proposed to carry the receptor current⁸, but its concentration is quite low in endolymph³, particularly that of the mammalian cochlea⁹. We present evidence here that the receptor current in a vertebrate hair cell is carried in vivo by K⁺, but that the transduction channel is in fact nonspecific, being permeable to Li⁺, Na⁺, K⁺, Rb⁺, Cs⁺, Ca²⁺, and at least one small organic cation.