Electrochemical properties of the non-excitable tissue stria vascularis of the mammalian cochlea are sensitive to sounds.

Autor: Zhang Q; Division of Glocal Pharmacology, Department of Pharmacology, Graduate School of Medicine, Osaka University, Suita, Osaka, Japan.; Department of Molecular Physiology, Niigata University Graduate School of Medical and Dental Sciences, Asahimachi-dori, Niigata, Japan.; Department of Otolaryngology Head and Neck Surgery, Niigata University Graduate School of Medical and Dental Sciences, Asahimachi-dori, Niigata, Japan., Ota T; Division of Glocal Pharmacology, Department of Pharmacology, Graduate School of Medicine, Osaka University, Suita, Osaka, Japan., Yoshida T; Department of Otorhinolaryngology, Graduate School of Medical Sciences, Kyushu University, Maidashi, Fukuoka, Japan., Ino D; Division of Glocal Pharmacology, Department of Pharmacology, Graduate School of Medicine, Osaka University, Suita, Osaka, Japan., Sato MP; Department of Otolaryngology, Kindai University Faculty of Medicine, Osaka, Japan., Doi K; Department of Otolaryngology, Kindai University Faculty of Medicine, Osaka, Japan., Horii A; Department of Otolaryngology Head and Neck Surgery, Niigata University Graduate School of Medical and Dental Sciences, Asahimachi-dori, Niigata, Japan., Nin F; Department of Physiology, Division of Biological Principles, Graduate School of Medicine, Gifu University, Yanagido, Gifu, Japan., Hibino H; Division of Glocal Pharmacology, Department of Pharmacology, Graduate School of Medicine, Osaka University, Suita, Osaka, Japan.; AMED, AMED-CREST, Osaka, Japan.
Jazyk: angličtina
Zdroj: The Journal of physiology [J Physiol] 2021 Oct; Vol. 599 (19), pp. 4497-4516. Date of Electronic Publication: 2021 Sep 16.
DOI: 10.1113/JP281981
Abstrakt: Excitable cochlear hair cells convert the mechanical energy of sounds into the electrical signals necessary for neurotransmission. The key process is cellular depolarization via K + entry from K + -enriched endolymph through hair cells' mechanosensitive channels. Positive 80 mV potential in endolymph accelerates the K + entry, thereby sensitizing hearing. This potential represents positive extracellular potential within the epithelial-like stria vascularis; the latter potential stems from K + equilibrium potential (E K ) across the strial membrane. Extra- and intracellular [K + ] determining E K are likely maintained by continuous unidirectional circulation of K + through a putative K + transport pathway containing hair cells and stria. Whether and how the non-excitable tissue stria vascularis responds to acoustic stimuli remains unclear. Therefore, we analysed a cochlear portion for the best frequency, 1 kHz, by theoretical and experimental approaches. We have previously developed a computational model that integrates ion channels and transporters in the stria and hair cells into a circuit and described a circulation current composed of K + . Here, in this model, mimicking of hair cells' K + flow induced by a 1 kHz sound modulated the circulation current and affected the strial ion transport mechanisms; the latter effect resulted in monotonically decreasing potential and increasing [K + ] in the extracellular strial compartment. Similar results were obtained when the stria in acoustically stimulated animals was examined using microelectrodes detecting the potential and [K + ]. Measured potential dynamics mirrored the E K change. Collectively, because stria vascularis is electrically coupled to hair cells by the circulation current in vivo too, the strial electrochemical properties respond to sounds. KEY POINTS: A highly positive potential of +80 mV in K + -enriched endolymph in the mammalian cochlea accelerates sound-induced K + entry into excitable sensory hair cells, a process that triggers hearing. This unique endolymphatic potential represents an E K -based battery for a non-excitable epithelial-like tissue, the stria vascularis. To examine whether and how the stria vascularis responds to sounds, we used our computational model, in which strial channels and transporters are serially connected to those hair cells in a closed-loop circuit, and found that mimicking hair cell excitation by acoustic stimuli resulted in increased extracellular [K + ] and decreased the battery's potential within the stria. This observation was overall verified by electrophysiological experiments using live guinea pigs. The sensitivity of electrochemical properties of the stria to sounds indicates that this tissue is electrically coupled to hair cells by a radial ionic flow called a circulation current.
(© 2021 The Authors. The Journal of Physiology © 2021 The Physiological Society.)
Databáze: MEDLINE