Human cochlear microanatomy – an electron microscopy and super-resolution structured illumination study and review

References

• Engström H, Sjöstrand FS. The structure and innervation of the cochlear hair cells. Acta Otolaryngol. 1954;44(5–6):490–501.
   PubMed Web of Science ®Google Scholar
• Lim DJ. Three dimensional observation of the inner ear with the scanning electron microscope. Acta Otolaryngol Suppl. 1969;255:1–38.
   PubMedGoogle Scholar
• Bredberg G, Lindeman HH, Ades HW, et al. Scanning electron microscopy of the organ of corti. Science. 1970;170(3960):861–863.
   PubMed Web of Science ®Google Scholar
• Spoendlin H, Schrott A. The spiral ganglion and the innervation of the human organ of corti. Acta Otolaryngol. 1988;105(5–6):403–410.
   PubMed Web of Science ®Google Scholar
• Liu W, Li H, Edin F, et al. Molecular composition and distribution of gap junctions in the sensory epithelium of the human cochlea—a super-resolution structured illumination microscopy (SR-SIM) study. Ups J Med Sci. 2017;122(3):160–170.
   PubMed Web of Science ®Google Scholar
• Liu W, Luque M, Glueckert R, et al. Expression of Na/K-ATPase subunits in the human cochlea: a confocal and super-resolution microscopy study with special reference to auditory nerve excitation and cochlear implantation. Ups J Med Sci. 2019;124(3):168–179.
   PubMed Web of Science ®Google Scholar
• Rask-Andersen H, Liu W, Boström M, et al. Audiological Medicine Immunolocalization of prestin in the human cochlea Immunolocalization of prestin in the human cochlea. Audiol Med. 2010;8(2):56–62.
   Google Scholar
• Zheng J, Shen W, He DZ, et al. Prestin is the motor protein of cochlear outer hair cells. Nature. 2000;405(6783):149–155.
   PubMed Web of Science ®Google Scholar
• Pollock LM, Gupta N, Chen X, et al. Supervillin is a component of the hair cell’s cuticular plate and the head plates of organ of Corti supporting cells. PLoS One. 2016;11(7):e0158349.
   PubMed Web of Science ®Google Scholar
• Slepecky NB, Ulfendahl M. Actin-binding and microtubule-associated proteins in the organ of Corti. Hear Res. 1992;57(2):201–215.
   PubMed Web of Science ®Google Scholar
• Griffith LM, Pollard TD. Evidence for actin filament-microtubule interaction mediated by microtubule-associated proteins. J Cell Biol. 1978;78(3):958–965.
   PubMed Web of Science ®Google Scholar
• Flock Å, Bretscher A, Weber K. Immunohistochemical localization of several cytoskeletal proteins in inner ear sensory and supporting cells. Hear Res. 1982;7:75–89.
   PubMed Web of Science ®Google Scholar
• Henderson CG, Tucker JB, Mogensen MM, et al. Three microtubule-organizing centres collaborate in a mouse cochlear epithelial cell during supracellularly coordinated control of microtubule positioning. 1995:108(Pt 1):37–50.
   Google Scholar
• Slepecky NB, Savage JE. Expression of actin isoforms in the guinea pig organ of Corti: muscle isoforms are not detected. Hear Res. 1994;73(1):16–26.
   PubMed Web of Science ®Google Scholar
• Mahendrasingam S, Furness D, Hackney C. Ultrastructural localisation of spectrin in sensory and supporting cells of guinea-pig organ of Corti. Hear Res. 1998;126(1–2):151–160.
   PubMed Web of Science ®Google Scholar
• Liu W, Löwenheim H, Santi PA, et al. Expression of trans-membrane serine protease 3 (TMPRSS3) in the human organ of Corti. Cell Tissue Res. 2018;372(3):445–456.
   PubMed Web of Science ®Google Scholar
• Kelsell DP, Dunlop J, Stevens HP, et al. Connexin 26 mutations in hereditary non-syndromic sensorineural deafness. Nature. 1997;387(6628):80–83.
   PubMed Web of Science ®Google Scholar
• del Castillo I, Villamar M, Moreno-Pelayo MA, et al. A deletion involving the connexin 30 gene in nonsyndromic hearing impairment. N Engl J Med. 2002;346(4):243–249.
   PubMed Web of Science ®Google Scholar
• Teubner B, Michel V, Pesch J, et al. Connexin30 (Gjb6)-deficiency causes severe hearing impairment and lack of endocochlear potential. Hum Mol Genet. 2003;12(1):13–21.
   PubMed Web of Science ®Google Scholar
• Harris LA. Emerging issues of connexin channels: biophysics fills the gap. Q Rev Biophys. 2001;34(3):325–472.
   PubMed Web of Science ®Google Scholar
• Jagger DJ, Forge A. Compartmentalized and signal-selective gap junctional coupling in the hearing cochlea. J Neurosci. 2006;26(4):1260–1268.
   PubMed Web of Science ®Google Scholar
• Schick B, Praetorius M, Eigenthaler M, et al. Expression of VASP and zyxin in cochlear pillar cells: indication for actin-based dynamics?. Cell Tissue Res. 2003;311(3):315–323.
   PubMed Web of Science ®Google Scholar
• Guipponi M, Vuagniaux G, Wattenhofer M, et al. The transmembrane serine protease (TMPRSS3) mutated in deafness DFNB8/10 activates the epithelial sodium channel (ENaC) in vitro. Hum Mol Genet. 2002;11(23):2829–2836.
   PubMed Web of Science ®Google Scholar
• Fasquelle L, Scott HS, Lenoir M, et al. Tmprss3, a transmembrane serine protease deficient in human DFNB8/10 deafness, is critical for cochlear hair cell survival at the onset of hearing. J Biol Chem. 2011;286(19):17383–17397.
   PubMed Web of Science ®Google Scholar
• Molina L, Fasquelle L, Nouvian R, et al. Tmprss3 loss of function impairs cochlear inner hair cell Kcnma1 channel membrane expression. Hum Mol Genet. 2013;22(7):1289–1299.
   PubMed Web of Science ®Google Scholar
• Mammano F, Ashmore JF. Differential expression of outer hair cell potassium currents in the isolated cochlea of the guinea-pig. J Physiol. 1996;496(3):639–646.
   PubMed Web of Science ®Google Scholar
• Ghaffari R, Aranyosi AJ, Freeman DM. Longitudinally propagating traveling waves of the mammalian tectorial membrane. Proc Natl Acad Sci USA. 2007;104(42):16510–16515.
   PubMed Web of Science ®Google Scholar
• Richardson GP, Lukashkin AN, Russell IJ. The tectorial membrane: one slice of a complex cochlear sandwich. Curr Opin Otolaryngol Head Neck Surg. 2008;16(5):458–464.
   PubMed Web of Science ®Google Scholar
• Lim DJ. Fine morphology of the tectorial membrane. Its relationship to the organ of corti. Arch Otolaryngol. 1972;96(3):199–215.
   PubMedGoogle Scholar
• Hoshino T. Contact between the tectorial membrane and the cochlear sensory hairs in the human and the monkey. Arch Otorhinolaryngol. 1977;217(1):53–60.
   PubMedGoogle Scholar
• Kawabata I, Nomura Y. Extra internal hair cells. A scanning electron microscopic study. Acta Otolaryngol. 1978;85(5–6):342–348.
   PubMed Web of Science ®Google Scholar
• Rask-Andersen H, Liu W, Erixon E, et al. Human cochlea: anatomical characteristics and their relevance for cochlear implantation. Anat Rec. 2012;295(11):1791–1811.
   Google Scholar
• Hayashi H, Schrott-Fischer A, Glueckert R, et al. Molecular organization and fine structure of the human tectorial membrane: is it replenished? Cell Tissue Res. 2015;362(3):513–527.
   PubMed Web of Science ®Google Scholar
• Richardson GP, Russell IJ, Duance VC, et al. Polypeptide composition of the mammalian tectorial membrane. Hear Res. 1987;25(1):45–60.
   PubMed Web of Science ®Google Scholar
• Thalmann I, Thallinger G, Comegys TH, et al. Composition and supramolecular organization of the tectorial membrane. Laryngoscope. 1987;97(3 Pt 1):357–367.
   PubMed Web of Science ®Google Scholar
• Slepecky NB, Savage JE, Cefaratti LK, et al. Electron-microscopic localization of type II, IX, and V collagen in the organ of Corti of the gerbil. Cell Tissue Res. 1992;267(3):413–418.
   PubMed Web of Science ®Google Scholar
• Goodyear RJ, Richardson GP. Structure, function, and development of the tectorial membrane: an extracellular matrix essential for hearing. Curr Top Dev Biol. 2018;130:217–244.
   PubMed Web of Science ®Google Scholar
• Iurato S. Submicroscopic structure of the membranous labyrinth. 1. The tectorial membrane. Z Zellforsch Mikrosk Anat. 1960;52(1):105–128.
   PubMedGoogle Scholar
• Thorn L, Arnold W, Schinko I, et al. Light and electron microscopic studies of the greater epithelial ridge and its relationship to the developing tectorial membrane in the cochlear duct of the guinea pig (author's transl). Arch Otorhinolaryngol. 1978;221(2):123–133.
   PubMedGoogle Scholar
• Prieto JJ, Rueda J, Merchan JA. Two different secretion mechanisms in the inner ear’s interdental cells. Hear Res. 1990;45(1–2):51–61.
   PubMed Web of Science ®Google Scholar
• Pfister M, Thiele H, Van Camp G, et al. A genotype-phenotype correlation with gender-effect for hearing impairment caused by TECTA mutations. Cell Physiol Biochem. 2004;14(4–6):369–376.
   PubMedGoogle Scholar
• Verhoeven K, Laer L, Van Kirschhofer K, et al. Mutations in the human alpha-tectorin gene cause autosomal dominant non-syndromic hearing impairment. Nat Genet. 1998;19(1):60–62.
   PubMed Web of Science ®Google Scholar
• Alasti F, Sanati MH, Behrouzifard AH, et al. A novel TECTA mutation confirms the recognizable phenotype among autosomal recessive hearing impairment families. Int J Pediatr Otorhinolaryngol. 2008;72(2):249–255.
   PubMed Web of Science ®Google Scholar
• Lukashkin AN, Legan PK, Weddell TD, et al. A mouse model for human deafness DFNB22 reveals that hearing impairment is due to a loss of inner hair cell stimulation. Proc Natl Acad Sci USA. 2012;109(47):19351–19356.
   PubMed Web of Science ®Google Scholar
• Legan PK, Lukashkina VA, Goodyear RJ, et al. A targeted deletion in alpha-tectorin reveals that the tectorial membrane is required for the gain and timing of cochlear feedback. Neuron. 2000;28(1):273–285.
   PubMed Web of Science ®Google Scholar
• Sellon JB, Ghaffari R, Farrahi S, et al. Porosity controls spread of excitation in tectorial membrane traveling waves. Biophys J. 2014;106(6):1406–1413.
   PubMed Web of Science ®Google Scholar
• Meaud J, Grosh K. The effect of tectorial membrane and basilar membrane longitudinal coupling in cochlear mechanics. J Acoust Soc Am. 2010;127(3):1411–1421.
   PubMed Web of Science ®Google Scholar
• Teudt IU, Richter CP. Basilar membrane and tectorial membrane stiffness in the CBA/CaJ mouse. J Assoc Res Otolaryngol. 2014;15(5):675–694.
   PubMed Web of Science ®Google Scholar
• Gueta R, Barlam D, Shneck RZ, et al. Measurement of the mechanical properties of isolated tectorial membrane using atomic force microscopy. Proc Natl Acad Sci USA. 2006;103(40):14790–14795.
   PubMed Web of Science ®Google Scholar
• Gavara N, Chadwick RS, Gribble PL. Collagen-based mechanical anisotropy of the tectorial membrane: implications for inter-row coupling of outer hair cell bundles. PLoS One. 2009;4(3):e4877.
   PubMed Web of Science ®Google Scholar
• Kimura RS. Hairs of the cochlear sensory cells and their attachment to the tectorial membrane. Acta Otolaryngol. 1966;61(1):55–72.
   PubMedGoogle Scholar
• Nowotny M, Gummer AW. Nanomechanics of the subtectorial space caused by electromechanics of cochlear outer hair cells. Proc Natl Acad Sci USA. 2006;103(7):2120–2125.
   PubMed Web of Science ®Google Scholar
• Zwaenepoel I, Mustapha M, Leibovici M, et al. Otoancorin, an inner ear protein restricted to the interface between the apical surface of sensory epithelia and their overlying acellular gels, is defective in autosomal recessive deafness DFNB22. Proc Natl Acad Sci USA. 2002;99(9):6240–6245.
   PubMed Web of Science ®Google Scholar
• Schuknecht HF, Gacek MR. Cochlear pathology in presbycusis. Ann Otol Rhinol Laryngol. 1993;102(1 Pt 2):1–16.
   PubMed Web of Science ®Google Scholar
• Békésy GV, Sy GVB. DC resting potentials inside the cochlear partition exploration of cochlear potentials in guinea pig with a microelectrode DC resting potentials inside the cochlear partition. Cit J Acoust Soc Am. 1952;24(1):72.
   Web of Science ®Google Scholar
• Schulte BA, Schmiedt RA. Lateral wall Na, K-ATPase and endocochlear potentials decline with age in quiet-reared gerbils. Hear Res. 1992;61(1–2):35–46.
   PubMed Web of Science ®Google Scholar
• Iizuka T, Kamiya K, Gotoh S, et al. Perinatal Gjb2 gene transfer rescues hearing in a mouse model of hereditary deafness. Hum Mol Genet. 2015;24(13):3651–3661.
   PubMed Web of Science ®Google Scholar
• Salt AN, Melichar I, Thalmann R. Mechanisms of endocochlear potential generation by stria vascularis. Laryngoscope. 1987;97(8 Pt 1):984–991.
   PubMed Web of Science ®Google Scholar
• Takeuchi S, Ando M, Kakigi A. Mechanism generating endocochlear potential: role played by intermediate cells in stria vascularis. Biophys J. 2000;79(5):2572–2582.
   PubMed Web of Science ®Google Scholar
• Nin F, Hibino H, Doi K, et al. Y. The endocochlear potential depends on two K + diffusion potentials and an electrical barrier in the stria vascularis of the inner ear. Proc Natl Acad Sci USA. 2008;105(5):1751–1756.
   PubMed Web of Science ®Google Scholar
• Wangemann P, Liu J, Marcus DC. Ion transport mechanisms responsible for K + secretion and the transepithelial voltage across marginal cells of stria vascularis in vitro. Hear Res. 1995;84(1–2):19–29.
   PubMed Web of Science ®Google Scholar
• Shen Z, Marcus DC, Sunose H, et al. I(sK) channel in strial marginal cells. Voltage-dependence, ion-selectivity, inhibition by 293B and sensitivity to clofilium. Aud Neurosci. 1997;3(3):215–230.
   Web of Science ®Google Scholar
• Gow A, Davies C, Southwood CM, et al. Deafness in Claudin 11-null mice reveals the critical contribution of basal cell tight junctions to stria vascularis function. J Neurosci. 2004;24(32):7051–7062.
   PubMed Web of Science ®Google Scholar
• Kitajiri SI, Miyamoto T, Mineharu A, et al. Compartmentalization established by claudin-11-based tight junctions in stria vascularis is required for hearing through generation of endocochlear potential. J Cell Sci. 2004;117(Pt 21):5087–5096.
   PubMed Web of Science ®Google Scholar
• Hibino H, Horio Y, Inanobe A, et al. An ATP-dependent inwardly rectifying potassium channel, KAB-2 (Kir4. 1), in cochlear stria vascularis of inner ear: its specific subcellular localization and correlation with the formation of endocochlear potential. J Neurosci. 1997;17(12):4711–4721.
   PubMed Web of Science ®Google Scholar
• 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. 2010;459(4):521–533.
   PubMed Web of Science ®Google Scholar
• Nin F, Yoshida T, Sawamura S, et al. The unique electrical properties in an extracellular fluid of the mammalian cochlea; their functional roles, homeostatic processes, and pathological significance. Pflugers Arch Eur J Physiol. 2016;4(10):1637–1649.
   Google Scholar
• Marcus DC, Wu T, Wangemann P, et al. KCNJ10 (kir4.1) potassium channel knockout abolishes endocochlear potential. Am J Physiol Cell Physiol. 2002;282(2):C403–C407.
   PubMed Web of Science ®Google Scholar
• Liu W, Schrott-Fischer A, Glueckert R, et al. The human “Cochlear Battery” - claudin-11 barrier and ion transport proteins in the lateral wall of the cochlea. Front Mol Neurosci. 2017;10:239.
   PubMed Web of Science ®Google Scholar
• Kikuchi T, Adams JC, Miyabe Y, et al. Potassium ion recycling pathway via gap junction systems in the mammalian cochlea and its interruption in hereditary nonsyndromic deafness. Med Electron Microsc. 2000;33(2):51–56.
   PubMedGoogle Scholar
• Forge A, Becker D, Casalotti S, et al. Connexins and gap junctions in the inner ear. Audiol Neurootol. 2002;7(3):141–145.
   PubMed Web of Science ®Google Scholar
• Zhang Y, Tang W, Ahmad S, et al. Gap junction-mediated intercellular biochemical coupling in cochlear supporting cells is required for normal cochlear functions. Proc Natl Acad Sci USA. 2005;102(42):15201–15206.
   PubMed Web of Science ®Google Scholar
• Linthicum FH, Fayad JN. Spiral ganglion cell loss is unrelated to segmental cochlear sensory system degeneration in humans. Otol Neurotol. 2009;30(3):418–422.
   PubMed Web of Science ®Google Scholar
• Liu W, Glueckert R, Linthicum FH, et al. Possible role of gap junction intercellular channels and connexin 43 in satellite glial cells (SGCs) for preservation of human spiral ganglion neurons: a comparative study with clinical implications. Cell Tissue Res. 2014;355(2):267–278.
   PubMed Web of Science ®Google Scholar
• Rask-Andersen H, Tylstedt S, Kinnefors A, et al. Synapses on human spiral ganglion cells: A transmission electron microscopy and immunohistochemical study. Hear Res. 2000;141(1–2):1–2.
   PubMed Web of Science ®Google Scholar
• Tylstedt S, Rask-Andersen H. A 3-D model of membrane specializations between human auditory spiral ganglion cells. J Neurocytol. 2001;30(6):465–473.
   PubMedGoogle Scholar
• Rask-Andersen H, Tylstedt S, Kinnefors A, et al. Nerve fibre interaction with large ganglion cells in the human spiral ganglion: a TEM study. Auris Nasus Larynx. 1997;24(1):1–11.
   PubMedGoogle Scholar
• Zong L, Zhu Y, Liang R, et al. Gap junction mediated miRNA intercellular transfer and gene regulation: a novel mechanism for intercellular genetic communication. Sci Rep. 2016;6:19884.
   PubMed Web of Science ®Google Scholar
• Tokhtaeva E, Clifford RJ, Kaplan JH, et al. Subunit isoform selectivity in assembly of Na,K. ATPase α-β Heterodimers. J Biol Chem. 2012;287(31):26115–26125.
   PubMed Web of Science ®Google Scholar
• Geering K. The functional role of the β-subunit in the maturation and intracellular transport of Na,K-ATPase. FEBS Lett. 1991;285:189–193.
   PubMed Web of Science ®Google Scholar