A Delayed Rectifier Conductance Shapes the Voltage Response of Type I Hair Cells

1. Membrane currents of hair cells in acutely excised or cultured mouse utricles were recorded with the whole cell voltage-clamp method at temperatures between 23 and 36 degrees C. 2. Type I and II hair cells both had delayed rectifier conductances that activated positive to -55 mV. 3. Type I, but not type II, hair cells had an additional delayed rectifier conductance (gK,L) with an activation range that was unusually negative and variable. At 23-25 degrees C, V(1/2) values ranged from -88 to -62 mV in 57 cells. 4. gK,L was very large. At 23-25 degrees C, the average maximum chord conductance was 75 +/- 65 nS (mean +/- SD, n = 57; measured at -54 mV), or approximately 21 nS/pF of cell capacitance. 5. gK,L was highly selective for K+ over Na+ (permeability ratio PNa+/PK+:0.006), but unlike other delayed rectifiers, gK,L was significantly permeable to Cs+ (PCs+/PK+:0.31). gK,L was independent of extracellular Ca2+. 6. At -64 mV, Ba2+ and 4-aminopyridine blocked gK,L with apparent dissociation constants of 2.0 mM and 43 microM, respectively. Extracellular Cs+ (5 mM) blocked gK,L by 50% at -124 mV. Apamin (100 nM) and dendrotoxin (10 nM) has no effect. 7. The kinetic data of gK,L are consistent with a sequential gating model with at least two closed states and one open state. The slow activation kinetics (principal time constants at 23-25 degrees C:600-200 ms) had a thermal Q10 of 2.1. Inactivation (Q10:2.7) was partial at all temperatures. Deactivation followed a double-exponential time course and had a Q10 of 2.0. 8. At 23-25 degrees C, gK,L was appreciably activated at the mean resting potential of type I hair cells (-77 +/- 3.1 mV, n = 62), so that input conductances were often more than an order of magnitude larger than those of type II cells. If these conditions hold in vivo, type I cells would produce unusually small receptor potentials. Warming the cells to 36 degrees C produced parallel shifts in gK,L's activation range (0.8 +/- 0.3 mV/degrees C, n = 8), and in the resting potential (0.6 +/- 0.3 mV/degrees C, n = 4). Thus the high input conductances were not an artifact of unphysiological temperatures but remained high near body temperature. It remains possible that in vivo gK,L's activation range is less negative and input conductances are lower; the large variance in the voltage range of activation suggests that it may be subject to modulation.

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Membrane Properties of Chick Semicircular Canal Hair Cells In Situ During Embryonic Development

Journal of Neurophysiology ◽

10.1152/jn.2000.83.5.2740 ◽

2000 ◽

Vol 83 (5) ◽

pp. 2740-2756 ◽

Cited By ~ 31

Author(s):

S. Masetto ◽

P. Perin ◽

A. Malusà ◽

G. Zucca ◽

P. Valli

Keyword(s):

Hair Cell ◽

Hair Cells ◽

Central Zone ◽

Cell Voltage ◽

Peripheral Zone ◽

Membrane Properties ◽

Voltage Response ◽

Type I ◽

Electrophysiological Properties ◽

Different Types

The electrophysiological properties of developing vestibular hair cells have been investigated in a chick crista slice preparation, from embryonic day 10 ( E10) to E21 (when hatching would occur). Patch-clamp whole-cell experiments showed that different types of ion channels are sequentially expressed during development. An inward Ca2+ current and a slow outward rectifying K+current ( I K(V)) are acquired first, at or before E10, followed by a rapid transient K+current ( I K(A)) at E12, and by a small Ca-dependent K+ current ( I KCa) at E14. Hair cell maturation then proceeds with the expression of hyperpolarization-activated currents: a slow I h appears first, around E16, followed by the fast inward rectifier I K1around E19. From the time of its first appearance, I K(A) is preferentially expressed in peripheral ( zone 1) hair cells, whereas inward rectifying currents are preferentially expressed in intermediate ( zone 2) and central ( zone 3) hair cells. Each conductance conferred distinctive properties on hair cell voltage response. Starting from E15, some hair cells, preferentially located at the intermediate region, showed the amphora shape typical of type I hair cells. From E17 (a time when the afferent calyx is completed) these cells expressed I K, L, the signature current of mature type I hair cells. Close to hatching, hair cell complements and regional organization of ion currents appeared similar to those reported for the mature avian crista. By the progressive acquisition of different types of inward and outward rectifying currents, hair cell repolarization after both positive- and negative-current injections is greatly strengthened and speeded up.

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Potassium currents in mammalian and avian isolated type I semicircular canal hair cells

Journal of Neurophysiology ◽

10.1152/jn.1994.71.1.317 ◽

1994 ◽

Vol 71 (1) ◽

pp. 317-329 ◽

Cited By ~ 76

Author(s):

K. J. Rennie ◽

M. J. Correia

Keyword(s):

Membrane Potential ◽

Hair Cells ◽

Potassium Current ◽

Columba Livia ◽

Membrane Properties ◽

Delayed Rectifier ◽

Type I ◽

Type Ii ◽

Current Clamp ◽

Whole Cell

1. Type I vestibular hair cells were isolated from the cristae ampullares of the semicircular canals of the Mongolian gerbil (Meriones unguiculatus) and the white king pigeon (Columba livia). Dissociated type I cells were distinguished from type II hair cells by their neck to plate ratio (NPR) and their characteristic amphora shape. 2. The membrane properties of gerbil and pigeon type I hair cells were studied in whole-cell voltage- and current-clamp using the perforated patch technique with amphotericin B as the perforating agent. 3. In whole-cell current-clamp, the average zero-current potential, Vz, measured for pigeon type I hair cells, was -70 +/- 7 (SD) mV (n = 18) and -71 +/- 11 mV (n = 83) for gerbil type I hair cells. 4. At Vz, for both gerbil and pigeon type I hair cells, a potassium current (IKI) was > or = 50% activated. This current deactivated rapidly when the membrane potential was hyperpolarized below -90 mV. 5. IKI was blocked by externally applied 4-aminopyridine (4-AP) (5 mM) and by internally applied 20 mM tetraethylammonium (TEA). It was also reduced when 4 mM barium was present in the external solution. The degree of block by barium increased as the membrane potential became more positive. External cesium (5 mM) blocked the inward component of IKI. When IKI was pharmacologically blocked, Vz depolarized by approximately 40 mV. Therefore IKI appears to be a delayed rectifier and to set the more negative Vz noted for isolated type I hair cells when compared to isolated type II hair cells, which do not have IKI. 6. A second, smaller potassium current was present at membrane potential depolarizations above -40 mV. This current was blocked by 30-50 mM, externally applied TEA, 100 microM quinidine, 100 nM apamin, but not 100 nM charybdotoxin, indicating that this is a calcium-activated potassium current, IK(Ca), different from the maxi-K calcium-activated potassium current found in most other hair cells.

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The delayed rectifier, Ikh, is the major conductance in type i vestibular hair cells across vestibular end organs

Pflügers Archiv - European Journal of Physiology ◽

10.1007/s004240050102 ◽

1996 ◽

Vol 432 (1) ◽

pp. 34-42 ◽

Cited By ~ 32

Author(s):

Anthony J. Ricci ◽

Katherine J. Rennie ◽

Manning J. Correia

Keyword(s):

Hair Cells ◽

Delayed Rectifier ◽

Type I ◽

Vestibular Hair Cells

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Cyclic GMP inhibits and shifts the activation curve of the delayed-rectifier (IK1) of type I mammalian vestibular hair cells

Neuroreport ◽

10.1097/00001756-199708180-00010 ◽

1997 ◽

Vol 8 (12) ◽

pp. 2687-2690 ◽

Cited By ~ 27

Author(s):

O Behrend ◽

C Schwark ◽

T Kunihiro ◽

M Strupp

Keyword(s):

Cyclic Gmp ◽

Hair Cells ◽

Delayed Rectifier ◽

Type I ◽

Activation Curve ◽

Vestibular Hair Cells ◽

And Shifts

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Na+ Currents in Vestibular Type I and Type II Hair Cells of the Embryo and Adult Chicken

Journal of Neurophysiology ◽

10.1152/jn.01157.2002 ◽

2003 ◽

Vol 90 (2) ◽

pp. 1266-1278 ◽

Cited By ~ 20

Author(s):

S. Masetto ◽

M. Bosica ◽

M. J. Correia ◽

O. P. Ottersen ◽

G. Zucca ◽

...

Keyword(s):

Cell Membrane ◽

Hair Cells ◽

Regional Distribution ◽

Semicircular Canals ◽

Voltage Response ◽

Fast Time ◽

Type I ◽

Type Ii ◽

Adult Chicken ◽

Voltage Dependent

In birds, type I and type II hair cells differentiate before birth. Here we describe that chick hair cells, from the semicircular canals, begin expressing a voltage-dependent Na current ( INa) from embryonic day 14 (E14) and continue to express the current up to hatching (E21). During this period, INa was present in most (31/43) type I hair cells irrespective of their position in the crista, in most type II hair cells located far from the planum semilunatum (48/63), but only occasionally in type II hair cells close to the planum semilunatum (2/35). INa activated close to –60 mV, showed fast time- and voltage-dependent activation and inactivation, and was completely, and reversibly, blocked by submicromolar concentrations of tetrodotoxin ( Kd = 17 nM). One peculiar property of INa concerns its steady-state inactivation, which is complete at –60 mV (half-inactivating voltage = –96 mV). INa was found in type I and type II hair cells from the adult chicken as well, where it had similar, although possibly not identical, properties and regional distribution. Current-clamp experiments showed that INa could contribute to the voltage response provided that the cell membrane was depolarized from holding potentials more negative than –80 mV. When recruited, INa produced a significant acceleration of the cell membrane depolarization, which occasionally elicited a large rapid depolarization followed by a rapid repolarization (action-potential-like response). Possible physiological roles for INa in the embryo and adult chicken are discussed.

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Development of K+ and Na+ conductances in rodent postnatal semicircular canal type I hair cells

AJP Regulatory Integrative and Comparative Physiology ◽

10.1152/ajpregu.00460.2009 ◽

2010 ◽

Vol 298 (2) ◽

pp. R351-R358 ◽

Cited By ~ 14

Author(s):

Gang Q. Li ◽

Frances L. Meredith ◽

Katherine J. Rennie

Keyword(s):

Hair Cells ◽

Low Voltage ◽

Semicircular Canals ◽

Input Resistance ◽

Membrane Properties ◽

Delayed Rectifier ◽

Type I ◽

Adult Type ◽

Whole Cell Patch Clamp ◽

Ionic Changes

The rodent vestibular system is immature at birth. During the first postnatal week, vestibular type I and type II hair cells start to acquire their characteristic morphology and afferent innervation. We have studied postnatal changes in the membrane properties of type I hair cells acutely isolated from the semicircular canals (SCC) of gerbils and rats using whole cell patch clamp and report for the first time developmental changes in ionic conductances in these cells. At postnatal day (P) 5 immature hair cells expressed a delayed rectifier K+ conductance ( GDR) which activated at potentials above approximately −50 mV in both species. Hair cells also expressed a transient Na+ conductance ( GNa) with a mean half-inactivation of approximately −90 mV. At P6 in rat and P7 in gerbil, a low-voltage activated K+ conductance ( GK,L) was first observed and conferred a low-input resistance, typical of adult type I hair cells, on SCC type I hair cells. GK,L expression in hair cells increased markedly during the second postnatal week and was present in all rat type I hair cells by P14. In gerbil hair cells, GK,L appeared later and was present in all type I hair cells by P19. During the third postnatal week, GNa expression declined and was absent by the fourth postnatal week in rat and the sixth postnatal week in gerbils. Understanding the ionic changes associated with hair cell maturation could help elucidate development and regeneration mechanisms in the inner ear.

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