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How is the highly positive endocochlear potential formed? The specific architecture of the stria vascularis and the roles of the ion-transport apparatus

  • Sensory Physiology
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Abstract

Cochlear endolymph, an extracellular solution containing 150 mM K+, exhibits a positive potential of +80 mV. This is called the endocochlear potential (EP) and is essential for audition. The mechanism responsible for formation of the EP has been an enigma for the half century since its first measurement. A key element is the stria vascularis, which displays a characteristic tissue structure and expresses multiple ion-transport apparatus. The stria comprises two epithelial layers: a layer of marginal cells and one composed of intermediate and basal cells. Between the two layers lies an extracellular space termed the intrastrial space (IS), which is thus surrounded by the apical membranes of intermediate cells and the basolateral membranes of marginal cells. The fluid in the IS exhibits a low concentration of K+ and a positive potential similar to the EP. We have demonstrated that the IS is electrically isolated from the neighboring extracellular fluids, perilymph, and endolymph, which allows the IS to sustain its positive potential. This IS potential is generated by K+ diffusion across the apical membranes of intermediate cells, where inwardly rectifying Kir4.1 channels are localized. The low K+ concentration in the IS, which is mandatory for the large K+-diffusion potential, is maintained by Na+,K+-ATPases and Na+,K+,2Cl−-cotransporters expressed at the basolateral membranes of marginal cells. An additional K+-diffusion potential formed by KCNQ1/KCNE1-K+ channels at the apical membranes of marginal cells also contributes to the EP. Therefore, the EP depends on an electrically isolated space and two K+-diffusion potentials in the stria vascularis.

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Acknowledgments

We thank Dr. Bernd Nilius (KU Leuven) for providing us with an opportunity to write this review article and Dr. A. J. Hudspeth (The Rockefeller University) for his critical reading of the text. HH and YK are supported by the following research grants and funds: Grant-in-Aid for Scientific Research on Priority Areas 17081012 (to HH), Grant-in-Aid for Young Scientists (B) 19790188 (to HH), the Global COE Program “in silico medicine” at Osaka University (to HH, FN, and YK), and a grant for “Research and Development of Next-Generation Integrated Life Simulation Software” (to YK), from the Ministry of Education, Culture, Sport, Science and Technology of Japan, Senri Life Science Foundation (to HH), Japan Foundation for Applied Enzymology (to HH), and the Ichiro Kanehara Foundation for the Promotion of Medical Sciences and Medical care (to HH).

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  1. Division of Molecular and Cellular Pharmacology, Department of Pharmacology, Graduate School of Medicine, Osaka University, 2-2 Yamada-oka, Suita, Osaka, 565-0871, Japan

    Hiroshi Hibino, Fumiaki Nin, Chizuru Tsuzuki & Yoshihisa Kurachi

  2. Department of Otolaryngology—Head and Neck Surgery, Kyoto Prefectural University of Medicine, Kyoto, Japan

    Fumiaki Nin

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  1. Hiroshi Hibino
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  2. Fumiaki Nin
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  4. Yoshihisa Kurachi
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Correspondence to Yoshihisa Kurachi.

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Hibino, H., Nin, F., Tsuzuki, C. et al. How is the highly positive endocochlear potential formed? The specific architecture of the stria vascularis and the roles of the ion-transport apparatus. Pflugers Arch - Eur J Physiol 459, 521–533 (2010). https://doi.org/10.1007/s00424-009-0754-z

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  • DOI: https://doi.org/10.1007/s00424-009-0754-z

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