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Published in: Journal of the Association for Research in Otolaryngology 1/2015

01-02-2015 | Research Article

Cytoarchitecture of the Mouse Organ of Corti from Base to Apex, Determined Using In Situ Two-Photon Imaging

Authors: Joris A. M. Soons, Anthony J. Ricci, Charles R. Steele, Sunil Puria

Published in: Journal of the Association for Research in Otolaryngology | Issue 1/2015

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ABSTRACT

The cells in the organ of Corti are highly organized, with a precise 3D microstructure hypothesized to be important for cochlear function. Here we provide quantitative data on the mouse organ of Corti cytoarchitecture, as determined using a new technique that combines the imaging capabilities of two-photon microscopy with the autofluorescent cell membranes of the genetically modified mTmG mouse. This combination allowed us to perform in situ imaging on freshly excised tissue, thus minimizing any physical distortions to the tissue that extraction from the cochlea and chemical fixation and staining might have caused. 3D image stacks of the organ of Corti were obtained from base to apex in the cochlear duct, from which 3D lengths and relative angles for inner and outer hair cells, Deiters’ cells, phalangeal processes, and inner and outer pillars were measured. In addition, intercellular distances, diameters, and stereocilia shapes were obtained. An important feature of this study is the quantitative reporting of the longitudinal tilts of the outer hair cells towards the base of the cochlea, the tilt of phalangeal processes towards the apex, and Deiters’ cells that collectively form a Y-shaped building block that is thought to give rise to the lattice-like organization of the organ of Corti. The variations of this Y-shaped element along the cochlear duct and between the rows of outer hair cells are shown with the third row morphologically different from the other rows, and their potential importance for the cochlear amplifier is discussed.
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Literature
go back to reference Angelborg C, Engstrom H (1972) Supporting elements in the organ of Corti. I. Fibrillar structures in the supporting cells of the organ of Corti of mammals. Acta Otolaryngol. Suppl 73:49–60 Angelborg C, Engstrom H (1972) Supporting elements in the organ of Corti. I. Fibrillar structures in the supporting cells of the organ of Corti of mammals. Acta Otolaryngol. Suppl 73:49–60
go back to reference Berens P (2009) CircStat: a Matlab toolbox for circular statistics. J Stat Softw 31–10 Berens P (2009) CircStat: a Matlab toolbox for circular statistics. J Stat Softw 31–10
go back to reference Brownell WE, Bader CR, Bertrand D, de Ribaupierre Y (1985) Evoked mechanical responses of isolated cochlear outer hair cells. Science (New York, N.Y.) 227(4683):194–6 Brownell WE, Bader CR, Bertrand D, de Ribaupierre Y (1985) Evoked mechanical responses of isolated cochlear outer hair cells. Science (New York, N.Y.) 227(4683):194–6
go back to reference Buytaert JAN, Johnson SB, Dierick M, Salih WHM, Santi PA (2013) MicroCT versus sTSLIM 3D imaging of the mouse cochlea. J Histochem Cytoc 61:382–395CrossRef Buytaert JAN, Johnson SB, Dierick M, Salih WHM, Santi PA (2013) MicroCT versus sTSLIM 3D imaging of the mouse cochlea. J Histochem Cytoc 61:382–395CrossRef
go back to reference Cooper NP, Rhode WS (1997) Mechanical responses to two-tone distortion products in the apical and basal turns of the mammalian cochlea. J Neurophysiol 78:261–270PubMed Cooper NP, Rhode WS (1997) Mechanical responses to two-tone distortion products in the apical and basal turns of the mammalian cochlea. J Neurophysiol 78:261–270PubMed
go back to reference Dannhof BJ, Roth B, Bruns V (1991) Length of hair cells as a measure of frequency representation in the mammalian inner ear? Die Naturwissenschaften 78(12):570–573PubMedCrossRef Dannhof BJ, Roth B, Bruns V (1991) Length of hair cells as a measure of frequency representation in the mammalian inner ear? Die Naturwissenschaften 78(12):570–573PubMedCrossRef
go back to reference Drobizhev M, Tillo S, Makarov NS, Hughes TE, Rebane A (2009) Absolute two-photon absorption spectra and two-photon brightness of orange and red fluorescent proteins. J Phys Chem B 113(4):855–859PubMedCentralPubMedCrossRef Drobizhev M, Tillo S, Makarov NS, Hughes TE, Rebane A (2009) Absolute two-photon absorption spectra and two-photon brightness of orange and red fluorescent proteins. J Phys Chem B 113(4):855–859PubMedCentralPubMedCrossRef
go back to reference Drobizhev M, Makarov NS, Tillo S, Hughes TE, Rebane A (2011) Two-photon absorption properties of fluorescent proteins. Nat Methods 8(5):393–399PubMedCrossRef Drobizhev M, Makarov NS, Tillo S, Hughes TE, Rebane A (2011) Two-photon absorption properties of fluorescent proteins. Nat Methods 8(5):393–399PubMedCrossRef
go back to reference Gao SS, Xia A, Yuan T et al (2011) Quantitative imaging of cochlear soft tissues in wild-type and hearing-impaired transgenic mice by spectral domain optical coherence tomography. Opt Express 19:15415–15428PubMedCentralPubMedCrossRef Gao SS, Xia A, Yuan T et al (2011) Quantitative imaging of cochlear soft tissues in wild-type and hearing-impaired transgenic mice by spectral domain optical coherence tomography. Opt Express 19:15415–15428PubMedCentralPubMedCrossRef
go back to reference Geisler D, Sang C (1995) A cochlear model using feed-forward outer-hair-cell forces. Hear Res 86:132–146PubMedCrossRef Geisler D, Sang C (1995) A cochlear model using feed-forward outer-hair-cell forces. Hear Res 86:132–146PubMedCrossRef
go back to reference Hartman BH, Reh T, Bermingham-McDonogh O (2010) Notch signaling specifies prosensory domains via lateral induction in the developing mammalian inner ear. PNAS 107:15792–15797PubMedCentralPubMedCrossRef Hartman BH, Reh T, Bermingham-McDonogh O (2010) Notch signaling specifies prosensory domains via lateral induction in the developing mammalian inner ear. PNAS 107:15792–15797PubMedCentralPubMedCrossRef
go back to reference Karavitaki KD (2002). Measurements and models of electrically-evoked motion in the gerbil organ of Corti. Ph.D. Thesis, MIT, Cambridge Karavitaki KD (2002). Measurements and models of electrically-evoked motion in the gerbil organ of Corti. Ph.D. Thesis, MIT, Cambridge
go back to reference Keiler S, Richter C-P (2001) Cochlear dimensions obtained in hemicochleae of four different strains of mice: CBA/CaJ, 129/CD1, 129/SvEv and C57BL/6J. Hear Res 162:91–104PubMedCrossRef Keiler S, Richter C-P (2001) Cochlear dimensions obtained in hemicochleae of four different strains of mice: CBA/CaJ, 129/CD1, 129/SvEv and C57BL/6J. Hear Res 162:91–104PubMedCrossRef
go back to reference Kolmer W (1913) Studien am Labyrinth von Insectivoren, Sitzungsberichte Akademie der Wissenschaften, Abteilung III, pp. 29–57 Kolmer W (1913) Studien am Labyrinth von Insectivoren, Sitzungsberichte Akademie der Wissenschaften, Abteilung III, pp. 29–57
go back to reference Liberman MC, Dodds LW, Pierce S (1990) Afferent and efferent innervation of the cat cochlea: quantitative analysis with light and electron microscopy. J Comp Neurol Liberman MC, Dodds LW, Pierce S (1990) Afferent and efferent innervation of the cat cochlea: quantitative analysis with light and electron microscopy. J Comp Neurol
go back to reference Liu CC, Gao SS, Yuan T, Steele C, Puria S, Oghalai JS (2011) Biophysical mechanisms underlying outer hair cell loss associated with a shortened tectorial membrane. JARO 12(5):577–594PubMedCentralPubMedCrossRef Liu CC, Gao SS, Yuan T, Steele C, Puria S, Oghalai JS (2011) Biophysical mechanisms underlying outer hair cell loss associated with a shortened tectorial membrane. JARO 12(5):577–594PubMedCentralPubMedCrossRef
go back to reference Maison SF, Adams JC, Liberman MC (2003) Olivocochlear innervation in the mouse: immunocytochemical maps, crossed versus uncrossed contributions, and transmitter colocalization. J Comp Neurol 455:406–416PubMedCentralPubMedCrossRef Maison SF, Adams JC, Liberman MC (2003) Olivocochlear innervation in the mouse: immunocytochemical maps, crossed versus uncrossed contributions, and transmitter colocalization. J Comp Neurol 455:406–416PubMedCentralPubMedCrossRef
go back to reference Mikaelian D, Ruben RJ (1965) Development of hearing in the normal CBA-J mouse: Correlation of physiological observations with behavioral responses and with cochlear anatomy. Acta Oto-Laryngologica 59.2–6:451–461. Mikaelian D, Ruben RJ (1965) Development of hearing in the normal CBA-J mouse: Correlation of physiological observations with behavioral responses and with cochlear anatomy. Acta Oto-Laryngologica 59.2–6:451–461.
go back to reference Müller M, von Hünerbein K, Hoidis S, Smolders JWT (2005) A physiological place-frequency map of the cochlea in the CBA/J mouse. Hear Res 202:63–73PubMedCrossRef Müller M, von Hünerbein K, Hoidis S, Smolders JWT (2005) A physiological place-frequency map of the cochlea in the CBA/J mouse. Hear Res 202:63–73PubMedCrossRef
go back to reference Muzumdar MD, Tasic B, Miyamichi K, Li L, Luo L (2007) A global double-fluorescent Cre reporter mouse. Genesis (New York, NY: 2000) 45(9):593–605CrossRef Muzumdar MD, Tasic B, Miyamichi K, Li L, Luo L (2007) A global double-fluorescent Cre reporter mouse. Genesis (New York, NY: 2000) 45(9):593–605CrossRef
go back to reference Nam JH (2014) Microstructures in the Organ of Corti help outer hair cells form traveling waves along the cochlear coil. Biophys J 106(11):2426–2433PubMedCrossRef Nam JH (2014) Microstructures in the Organ of Corti help outer hair cells form traveling waves along the cochlear coil. Biophys J 106(11):2426–2433PubMedCrossRef
go back to reference Neely ST, Kim DO (1983) An active cochlear model showing sharp tuning and high sensitivity. Hear Res 9:123–130PubMedCrossRef Neely ST, Kim DO (1983) An active cochlear model showing sharp tuning and high sensitivity. Hear Res 9:123–130PubMedCrossRef
go back to reference Puria S, Hartman B, Kim J, Oghalai JS, Ricci AJ, Liberman MC (2011) Three-dimensional imaging of the mouse organ of Corti cytoarchitecture for mechanical modeling. AIP Conf. Proc. pp 356–362 Puria S, Hartman B, Kim J, Oghalai JS, Ricci AJ, Liberman MC (2011) Three-dimensional imaging of the mouse organ of Corti cytoarchitecture for mechanical modeling. AIP Conf. Proc. pp 356–362
go back to reference Ren T, He W (2011) Measurement of basilar membrane, reticular lamina, and tectorial membrane vibrations in the intact mouse cochlea. AIP Conf. Proc 1403, 423 Ren T, He W (2011) Measurement of basilar membrane, reticular lamina, and tectorial membrane vibrations in the intact mouse cochlea. AIP Conf. Proc 1403, 423
go back to reference Retzius G (1884) Das Gehörorgan der Wirbeltiere, vol. 2. Samson & Wallin, Stockholm Retzius G (1884) Das Gehörorgan der Wirbeltiere, vol. 2. Samson & Wallin, Stockholm
go back to reference Shera CA, Guinan JJ (2003) Stimulus-frequency-emission group delay: a test of coherent reflection filtering and a window on cochlear tuning. J Acoust Soc Am 113:2762PubMedCrossRef Shera CA, Guinan JJ (2003) Stimulus-frequency-emission group delay: a test of coherent reflection filtering and a window on cochlear tuning. J Acoust Soc Am 113:2762PubMedCrossRef
go back to reference Shera CA, Zweig (1993) Order from chaos: resolving the paradox of periodicity in evoked otoacoustic emission. Biophys Hair Cell Sens Syst 54–63 Shera CA, Zweig (1993) Order from chaos: resolving the paradox of periodicity in evoked otoacoustic emission. Biophys Hair Cell Sens Syst 54–63
go back to reference Slepecky NB (1996) Structure of the mammalian cochlea, chapter 2 in the cochlea. In: Dallos PJ, Popper AN, Fay RR (Eds.) (Springer handbook of auditory research) Slepecky NB (1996) Structure of the mammalian cochlea, chapter 2 in the cochlea. In: Dallos PJ, Popper AN, Fay RR (Eds.) (Springer handbook of auditory research)
go back to reference So PT (2002) Two-photon fluorescence light microscopy. Encyclopedia of Life Sciences, Nature Publishing Group 1–5 So PT (2002) Two-photon fluorescence light microscopy. Encyclopedia of Life Sciences, Nature Publishing Group 1–5
go back to reference Soons J, Dirckx JJJ, Puria S, and Steele CR (2014) Basilar membrane and reticular lamina motion in a multi-scale finite element model of the mouse cochlea. In: Mechanics of Hearing 2014, AIP proceedings (submitted) Soons J, Dirckx JJJ, Puria S, and Steele CR (2014) Basilar membrane and reticular lamina motion in a multi-scale finite element model of the mouse cochlea. In: Mechanics of Hearing 2014, AIP proceedings (submitted)
go back to reference Spicer SS, Schulte BA (1994) Differences along the place-frequency map in the structure of supporting cells in the gerbil cochlea. Hear Res 79:161–177PubMedCrossRef Spicer SS, Schulte BA (1994) Differences along the place-frequency map in the structure of supporting cells in the gerbil cochlea. Hear Res 79:161–177PubMedCrossRef
go back to reference Steele CR, Baker G, Tolomeo J, Zetes D (1993) Electro-mechanical models of the outer hair cell. In: Duifhuis H, Horst JW, van Dijk P, van Netten SM (eds) Biophysics of hair cell sensory systems. World Scientific, Singapore, pp 207–215 Steele CR, Baker G, Tolomeo J, Zetes D (1993) Electro-mechanical models of the outer hair cell. In: Duifhuis H, Horst JW, van Dijk P, van Netten SM (eds) Biophysics of hair cell sensory systems. World Scientific, Singapore, pp 207–215
go back to reference Szalai R, Epp B, Champneys A, Homer M (2011) On time-delayed and feed-forward transmission line models of the cochlea. J Mech Mat Struct 6(1):557–568CrossRef Szalai R, Epp B, Champneys A, Homer M (2011) On time-delayed and feed-forward transmission line models of the cochlea. J Mech Mat Struct 6(1):557–568CrossRef
go back to reference Tiedemann H (1970) A new approach to theory of hearing. Acta Otolaryngol Suppl 277:1–50PubMed Tiedemann H (1970) A new approach to theory of hearing. Acta Otolaryngol Suppl 277:1–50PubMed
go back to reference Voldřich L (1983) Experimental and topographic morphology in cochlear mechanics. In: de Boer E, Viergever MA (eds) Mechanics of hearing. Delft University Press, Delft, pp 163–167CrossRef Voldřich L (1983) Experimental and topographic morphology in cochlear mechanics. In: de Boer E, Viergever MA (eds) Mechanics of hearing. Delft University Press, Delft, pp 163–167CrossRef
go back to reference Wen B, Boahen K (2003) A linear cochlear model with active bi-directional coupling. The 25th Annual International Conference of the IEEE Engineering in Medicine and Biology Society (EMBC 2003), pp. 2013–2016 Wen B, Boahen K (2003) A linear cochlear model with active bi-directional coupling. The 25th Annual International Conference of the IEEE Engineering in Medicine and Biology Society (EMBC 2003), pp. 2013–2016
go back to reference Yoon Y-J, Puria S, Steele CR (2009) A cochlear model using the time-averaged Lagrangian and the push-pull mechanism in the organ of Corti. J Mech Mater Struct 4(5):977–986PubMedCentralPubMedCrossRef Yoon Y-J, Puria S, Steele CR (2009) A cochlear model using the time-averaged Lagrangian and the push-pull mechanism in the organ of Corti. J Mech Mater Struct 4(5):977–986PubMedCentralPubMedCrossRef
Metadata
Title
Cytoarchitecture of the Mouse Organ of Corti from Base to Apex, Determined Using In Situ Two-Photon Imaging
Authors
Joris A. M. Soons
Anthony J. Ricci
Charles R. Steele
Sunil Puria
Publication date
01-02-2015
Publisher
Springer US
Published in
Journal of the Association for Research in Otolaryngology / Issue 1/2015
Print ISSN: 1525-3961
Electronic ISSN: 1438-7573
DOI
https://doi.org/10.1007/s10162-014-0497-1

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