Postnatal development of type I and type II hair cells in the mouse utricle: Acquisition of voltage-gated conductances and differentiated morphology

Abstract

The type I and type II hair cells of mature amniote vestibular organs have been classified according to their afferent nerve terminals: calyx and bouton, respectively. Mature type I and type II cells also have different complements of voltage-gated channels. Type I cells alone express a delayed rectifier, g(K,L), that is activated at resting potential. We report that in mouse utricles this electrophysiological differentiation occurs during the first postnatal week. Whole-cell currents were recorded from hair cells in denervated organotypic cultures and in acutely excised epithelia. From postnatal day 1 (P1) to P3, most hair cells expressed a delayed rectifier that activated positive to resting potential and a fast inward rectifier, g(K1). Between P4 and P8, many cells acquired the type I-specific conductance g(K,L) and/or a slow inward rectifier, g(h). By P8, the percentages of cells expressing g(K,L) and g(h) were at mature levels. To investigate whether the electrophysiological differentiation correlated with morphological changes, we fixed utricles at different times between P0 and P28. Ultrastructural criteria were developed to classify cells when calyces were not present, as in cultures and neonatal organs. The morphological and electrophysiological differentiation followed different time courses, converging by P28. At P0, when no hair cells expressed g(K,L), 33% were classified as type I by ultrastructural criteria. By P28, ~60% of hair cells in acute preparations received calyx terminals and expressed g(K,L). Data from the denervated cultures showed that neither electrophysiological nor morphological differentiation depended on ongoing innervation.