Regional Analysis of Whole Cell Currents From Hair Cells of the Turtle Posterior Crista

Abstract

Regional analysis of whole cell currents from hair cells of the turtle posterior crista. J Neurophysiol 88: 3259 -3278, 2002; 10.1152/jn.00770.2001. The turtle posterior crista is made up of two hemicristae, each consisting of a central zone containing type I and type II hair cells and a surrounding peripheral zone containing only type II hair cells and extending from the planum semilunatum to the nonsensory torus. Afferents from various regions of a hemicrista differ in their discharge properties. To see if afferent diversity is related to the basolateral currents of the hair cells innervated, we selectively harvested type I and II hair cells from the central zone and type II hair cells from two parts of the peripheral zone, one near the planum and the other near the torus. Voltage-dependent currents were studied with the whole cell, ruptured-patch method and characterized in voltage-clamp mode. We found regional differences in both outwardly and inwardly rectifying voltage-sensitive currents. As in birds and mammals, type I hair cells have a distinctive outwardly rectifying current (I K,L ), which begins activating at more hyperpolarized voltages than do the outward currents of type II hair cells. Activation of I K,L is slow and sigmoidal. Maximal outward conductances are large. Outward currents in type II cells vary in their activation kinetics. Cells with fast kinetics are associated with small conductances and with partial inactivation during 200-ms depolarizing voltage steps. Almost all type II cells in the peripheral zone and many in the central zone have fast kinetics. Some type II cells in the central zone have large outward currents with slow kinetics and little inactivation. Although these currents resemble I K,L , they can be distinguished from the latter both electrophysiologically and pharmacologically. There are two varieties of inwardly rectifying currents in type II hair cells: activation of I K1 is rapid and monoexponential, whereas that of I h is slow and sigmoidal. Many type II cells either have both inward currents or only have I K1 ; very few cells only have I h . Inward currents are less conspicuous in type I cells. Type II cells near the torus have smaller outwardly rectifying currents and larger inwardly rectifying currents than those near the planum, but the differences are too small to account for variations in discharge properties of bouton afferents innervating the two regions of the peripheral zone. The large outward conductances seen in central cells, by lowering impedances, may contribute to the low rotational gains of some central-zone afferents.

Developmental Acquisition of Voltage-Dependent Conductances and Sensory Signaling in Hair Cells of the Embryonic Mouse Inner Ear

“…Estimates of reversal potential confirmed that the currents were carried primarily by potassium. In terms of kinetics, activation range, and potassium selectivity, these currents were similar to those carried by the fast inward rectifier G K1 found in postnatal mouse vestibular hair cells (Rüsch et al, 1998) and hair cells of other organs and species (Ohmori, 1984;Fuchs and Evans, 1990;Masetto et al, 1994;Holt and Eatock, 1995;Sugihara and Furukawa, 1996;Marcotti et al, 1999;Brichta et al, 2002). To estimate the inward rectifier conductance, we used the peak current at Ϫ124 mV divided by driving force (V M Ϫ E 1 ϭ 42 mV).…”

“…Because a systematic variation in single-channel conductance as a function of age is unlikely, the parsimonious interpretation suggests that the increased density results from an increase in the number of functional potassium channels. Therefore, we suggest that the data can be best explained by the developmental acquisition of a homogeneous variety of voltage-dependent potassium channels with properties similar to the delayed rectifier seen in mature postnatal type II hair cells (Lang and Correia, 1989;Rennie and Ashmore, 1991;Masetto and Correia, 1997;Rüsch et al, 1998;Masetto et al, 2000;Brichta et al, 2002). However, we cannot exclude the possibility that the channels consist of a consistent ratio of heterogeneous channel subunits whose stoichiometry is tightly regulated.…”

Mechanisms of Efferent-Mediated Responses in the Turtle Posterior Crista

“…Regardless of the explanation for the asymmetry, it seems reasonable to suppose that the relative sizes of the preblock inhibition and the postblock excitation reflect a balance between the density of nicotinic and SK channels. Other potential contributory factors include calcium buffering (Allbritton et al, 1992;Wu et al, 1996), the role of the cisterns and other internal stores in calcium regulation Lioudyno et al, 2004), and the presence of inward rectifiers (Brichta et al, 2002) that can limit hyperpolarizing responses (Robinson and Siegelbaum, 2003).…”

“…A T-type channel has not been seen in hair cells (Ló pez et al, 1999;Martini et al, 2000;Bao et al, 2003) (but see Nie et al, 2005). IRK channels are seen in both the turtle crista (Brichta et al, 2002) and frog vestibular organs (Holt and Eatock, 1995;Marcotti et al, 1999), but IRK currents do not show a depolarizing overshoot after a hyperpolarization (Marcotti et al, 1999). I H is a candidate in the turtle posterior crista because it is only present in type II hair cells that would synapse on BM units (Brichta et al, 2002) and can give rise to both a hyperpolarization sag and a posthyperpolarizing depolarization (Robinson and Siegelbaum, 2003).…”

“…IRK channels are seen in both the turtle crista (Brichta et al, 2002) and frog vestibular organs (Holt and Eatock, 1995;Marcotti et al, 1999), but IRK currents do not show a depolarizing overshoot after a hyperpolarization (Marcotti et al, 1999). I H is a candidate in the turtle posterior crista because it is only present in type II hair cells that would synapse on BM units (Brichta et al, 2002) and can give rise to both a hyperpolarization sag and a posthyperpolarizing depolarization (Robinson and Siegelbaum, 2003). A possible role in the frog vestibular labyrinth is less clear because an efferent-mediated postinhibitory excitation is seen in both posterior crista and saccular afferents (Sugai et al, 1991).…”