Two resting potential levels regulated by the inward-rectifier potassium channel in the guinea-pig spiral modiolar artery

Zhi-Gen Jiang, Jun Qiang Si, Michael R. Lasarev, Alfred Nuttall

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Abstract

1. Intracellular in vitro recordings were made from 771 cells from the spiral modiolar artery (SMA). The initial resting potentials (RPs) displayed a bimodal distribution that was well modelled as a mixture of two Gaussian distributions. About half of the cells had an average RP of -74 mV, and were termed high-RP cells, whereas the other half had an average RP around -41 mV, and were termed low-RP cells. Preparations that were incubated for longer than 24 h contained significantly more high-RP cells than those incubated for less than 8 h. 2. When labelled with the fluorescent dye propidium iodide, 68 and 36 cells were identified as smooth muscle cells (SMC) and endothelial cells (EC), respectively. The RP and input resistance were not significantly different between these two types of cell. Dye coupling was observed only in ECs. Dual cell recordings with 0.2-1.0 mm separation demonstrated the simultaneous existence of high- and low-RP cells and a heterogeneous low-strength electrical coupling. 3. The high-RP cells were depolarized by ACh and by high extracellular potassium concentration (high K+). The low-RP cells were usually hyperpolarized by moderately high K+ (7.5-20 mM) and by ACh. The high K+-induced hyperpolarization was suppressed by barium (Ba2+, 10-50 μM). The putative gap junction blocker 18β-glycyrrhetinic acid suppressed the ACh-induced responses in SMCs, but not in ECs. 4. Low-RP cells could rapidly shift the membrane potential to a permanent high-RP state spontaneously or, more often, after a brief application of hyperpolarizing agents including high K+, ACh, nitric oxide and pinacidil. Once shifted to a high-RP state, the responses of these cells to high K+ and ACh became similar to those of the original high-RP cells. 5. High-RP cells occasionally shifted their potentials to a low-RP state either spontaneously or after a brief application of 10-50 μM Ba2+ or 100 μM ouabain. Once shifted to the low-RP state, the response of these cells to high K+ and ACh became a hyperpolarization. The shift between high- and low-RP states was largely mimicked by wash-in and wash-out of low concentrations of Ba2+. The shift often showed a regenerative process as a fast phase in its middle course. 6. It is concluded that the cochlear SMA in vitro is composed of poorly and heterogeneously coupled SMCs and ECs, simultaneously resting in one of two distinct states, one a high-RP state and the other a low-RP state. The two RP states are exchangeable mainly due to all-or-none- like conductance changes of the inward-rectifier K+ channel.

Original languageEnglish (US)
Pages (from-to)829-842
Number of pages14
JournalJournal of Physiology
Volume537
Issue number3
DOIs
StatePublished - Dec 15 2001

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Inwardly Rectifying Potassium Channel
Membrane Potentials
Guinea Pigs
Arteries

ASJC Scopus subject areas

  • Physiology

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Two resting potential levels regulated by the inward-rectifier potassium channel in the guinea-pig spiral modiolar artery. / Jiang, Zhi-Gen; Si, Jun Qiang; Lasarev, Michael R.; Nuttall, Alfred.

In: Journal of Physiology, Vol. 537, No. 3, 15.12.2001, p. 829-842.

Research output: Contribution to journalArticle

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N2 - 1. Intracellular in vitro recordings were made from 771 cells from the spiral modiolar artery (SMA). The initial resting potentials (RPs) displayed a bimodal distribution that was well modelled as a mixture of two Gaussian distributions. About half of the cells had an average RP of -74 mV, and were termed high-RP cells, whereas the other half had an average RP around -41 mV, and were termed low-RP cells. Preparations that were incubated for longer than 24 h contained significantly more high-RP cells than those incubated for less than 8 h. 2. When labelled with the fluorescent dye propidium iodide, 68 and 36 cells were identified as smooth muscle cells (SMC) and endothelial cells (EC), respectively. The RP and input resistance were not significantly different between these two types of cell. Dye coupling was observed only in ECs. Dual cell recordings with 0.2-1.0 mm separation demonstrated the simultaneous existence of high- and low-RP cells and a heterogeneous low-strength electrical coupling. 3. The high-RP cells were depolarized by ACh and by high extracellular potassium concentration (high K+). The low-RP cells were usually hyperpolarized by moderately high K+ (7.5-20 mM) and by ACh. The high K+-induced hyperpolarization was suppressed by barium (Ba2+, 10-50 μM). The putative gap junction blocker 18β-glycyrrhetinic acid suppressed the ACh-induced responses in SMCs, but not in ECs. 4. Low-RP cells could rapidly shift the membrane potential to a permanent high-RP state spontaneously or, more often, after a brief application of hyperpolarizing agents including high K+, ACh, nitric oxide and pinacidil. Once shifted to a high-RP state, the responses of these cells to high K+ and ACh became similar to those of the original high-RP cells. 5. High-RP cells occasionally shifted their potentials to a low-RP state either spontaneously or after a brief application of 10-50 μM Ba2+ or 100 μM ouabain. Once shifted to the low-RP state, the response of these cells to high K+ and ACh became a hyperpolarization. The shift between high- and low-RP states was largely mimicked by wash-in and wash-out of low concentrations of Ba2+. The shift often showed a regenerative process as a fast phase in its middle course. 6. It is concluded that the cochlear SMA in vitro is composed of poorly and heterogeneously coupled SMCs and ECs, simultaneously resting in one of two distinct states, one a high-RP state and the other a low-RP state. The two RP states are exchangeable mainly due to all-or-none- like conductance changes of the inward-rectifier K+ channel.

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