Skip to main content
SpringerLink
Log in
Book cover

The Primary Auditory Neurons of the Mammalian Cochlea pp 117–156Cite as

The Ribbon Synapse Between Type I Spiral Ganglion Neurons and Inner Hair Cells

  • Chapter
  • First Online:

Part of the book series: Springer Handbook of Auditory Research ((SHAR,volume 52))

Abstract

This chapter provides an overview of the first auditory synapses, in the cochlea where sound is encoded. We review insights into the development, structure, and function of the excitatory ribbon-type synapses between presynaptic inner hair cells and postsynaps on the type I spiral ganglion neurons. They convey all information about sound timing and intensity to the brain, via action potentials in the auditory nerve. Recordings from individual type I spiral ganglion neurons in vivo demonstrate remarkable diversity between neurons in their sound-response properties. Although much has been learned about the representation of acoustic information in the auditory nerve, relatively little is known about the synaptic mechanisms underlying diversity of encoding. The response properties of SGN determined by properties of SGN may be largely determined by the details of the 1:1 connection between each inner hair cell presynaptic active zone and its postsynaptic type I spiral ganglion neuron. This chapter covers (1) synaptogenesis as inner hair cells mature from pattern generators to sound receivers, (2) presynaptic mechanisms governing exocytosis, (3) synaptic transmission to the type 1 spiral ganglion neuron and subsequent action potential generation, and (4) how pre- and postsynaptic heterogeneities may contribute to the diversity of spiral ganglion neuron response properties that enable hearing over a broad range of sound pressure levels. Presynaptic stimulus-secretion coupling appears to operate in a nanodomain regime and the postsynaptic action potential generator is tightly coupled to synaptic input. Thus, opening of a single presynaptic Ca2+ channel may be sufficient to trigger a postsynaptic action potential.

This is a preview of subscription content, log in via an institution.

Chapter
USD   29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD   84.99
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD   109.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD   109.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Learn about institutional subscriptions

References

  • Augustine, G. J., Adler, E. M., & Charltonc, M. P. (1991). The calcium signal for transmitter secretion from presynaptic nerve terminals. Annals of the New York Academy of Sciences, 635(1), 365–381.

    Google Scholar 

  • Baig, S. M., Koschak, A., Lieb, A., Gebhart, M., Dafinger, C., Nürnberg, G., Ali, A., Ahmad, I., Sinnegger-Brauns, M. J., & Brandt, N. (2011). Loss of CaV1. 3 (CACNA1D) function in a human channelopathy with bradycardia and congenital deafness. Nature Neuroscience, 14(1), 77–84.

    Google Scholar 

  • Barnes, S., & Hille, B. (1989). Ionic channels of the inner segment of tiger salamander cone photoreceptors. The Journal of General Physiology (JGP), 94(4), 719–743.

    Google Scholar 

  • Beurg, M., Michalski, N., Safieddine, S., Bouleau, Y., Schneggenburger, R., Chapman, E. R., Petit, C., & Dulon, D. (2010). Control of exocytosis by synaptotagmins and otoferlin in auditory hair cells. The Journal of Neuroscience, 30(40), 13281–13290.

    Google Scholar 

  • Beutner, D., & Moser, T. (2001). The presynaptic function of mouse cochlear inner hair cells during development of hearing. The Journal of Neuroscience, 21(13), 4593–4599.

    Google Scholar 

  • Beutner, D., Voets, T., Neher, E., & Moser, T. (2001). Calcium dependence of exocytosis and endocytosis at the cochlear inner hair cell afferent synapse. Neuron, 29(3), 681–690.

    Google Scholar 

  • Bohne, B. A., Kenworthy, A., & Carr, C. D. (1982). Density of myelinated nerve fibers in the chinchilla cochlea. The Journal of the Acoustical Society of America, 72(1), 102–107.

    Google Scholar 

  • Brandt, A., Khimich, D., & Moser, T. (2005). Few CaV1.3 channels regulate the exocytosis of a synaptic vesicle at the hair cell ribbon synapse. The Journal of Neuroscience, 25(50), 11577–11585.

    Google Scholar 

  • Brandt, A., Striessnig, J., & Moser, T. (2003). CaV1.3 channels are essential for development and presynaptic activity of cochlear inner hair cells. The Journal of Neuroscience, 23(34), 10832–10840.

    Google Scholar 

  • Buran, B. N., Strenzke, N., Neef, A., Gundelfinger, E. D., Moser, T., & Liberman, M. C. (2010). Onset coding is degraded in auditory nerve fibers from mutant mice lacking synaptic ribbons. The Journal of Neuroscience, 30(22), 7587–7597.

    Google Scholar 

  • Chapochnikov, N. M., Takago, H., Huang, C. H., Pangršič, T., Khimich, D., Neef, J., Auge, E., Göttfert, F., Hell, S. W., Wichmann, C., Wolf, F., & Moser, T. (2014). Uniquantal release through a dynamic fusion pore is a candidate mechanism of hair cell exocytosis. Neuron, 83(6), 1389–1403.

    Google Scholar 

  • Cho, S., Li, G. L., & von Gersdorff, H. (2011). Recovery from short-term depression and facilitation is ultrafast and Ca2+-dependent at auditory hair cell synapses. The Journal of Neuroscience, 31(15), 5682–5692.

    Google Scholar 

  • Clause, A., Kim, G., Sonntag, M., Weisz, C. J. C., Vetter, D. E., Rűbsamen, R., & Kandler, K. (2014). The precise temporal pattern of prehearing spontaneous activity is necessary for tonotopic map refinement. Neuron, 82(4), 822–835.

    Google Scholar 

  • Corey, D. P., & Hudspeth, A. J. (1979). Ionic basis of the receptor potential in a vertebrate hair cell. Nature, 281(5733), 675–677.

    Google Scholar 

  • Cui, G., Meyer, A. C., Calin-Jageman, I., Neef, J., Haeseleer, F., Moser, T., & Lee, A. (2007). Ca2+-binding proteins tune Ca2+-feedback to CaV1.3 channels in mouse auditory hair cells. The Journal of Physiology, 585(3), 791–803.

    Google Scholar 

  • Dallos, P. (1985). Response characteristics of mammalian cochlear hair cells. The Journal of Neuroscience, 5(6), 1591–1608.

    Google Scholar 

  • Derbyshire, A. J., & Davis, H. (1935). The action potentials of the auditory nerve. Boston, MA: Department of Physiology, Harvard Medical School.

    Google Scholar 

  • Dou, H., Vazquez, A. E., Namkung, Y., Chu, H., Cardell, E. L., Nie, L., Parson, S., Shin, H. S., & Yamoah, E. N. (2004). Null mutation of α1D Ca2+ channel gene results in deafness but no vestibular defect in mice. Journal of the Association for Research in Otolaryngology (JARO), 5(2), 215–226.

    Google Scholar 

  • Duncker, S. V., Franz, C., Kuhn, S., Schulte, U., Campanelli, D., Brandt, N., Hirt, B., Fakler, B., Blin, N., & Ruth, P. (2013). Otoferlin couples to clathrin-mediated endocytosis in mature cochlear inner hair cells. The Journal of Neuroscience, 33(22), 9508–9519.

    Google Scholar 

  • Ehret, G. (1976). Development of absolute auditory thresholds in the house mouse (mus musculus). Ear and Hearing, 1(5), 179–184.

    Google Scholar 

  • Farris, H. E., Wells, G. B., & Ricci, A. J. (2006). Steady-state adaptation of mechanotransduction modulates the resting potential of auditory hair cells, providing an assay for endolymph [Ca2+]. The Journal of Neuroscience, 26(48), 12526–12536.

    Google Scholar 

  • Frank, T., Khimich, D., Neef, A., & Moser, T. (2009). Mechanisms contributing to synaptic Ca2+ signals and their heterogeneity in hair cells. Proceedings of the National Academy of Sciences of the USA, 106(11), 4483–4488.

    Google Scholar 

  • Frank, T., Rutherford, M. A., Strenzke, N., Neef, A., Pangršič, T., Khimich, D., Fejtova, A., Gundelfinger, E. D., Liberman, M. C., Harke, B., Bryan, K. E., Lee, A., Egner, A., Riedel, D., & Moser, T. (2010). Bassoon and the synaptic ribbon organize Ca2+ channels and vesicles to add release sites and promote refilling. Neuron, 68(4), 724–738.

    Google Scholar 

  • Fuchs, P. A. (2005). Time and intensity coding at the hair cell’s ribbon synapse. The Journal of Physiology, 566(1), 7–12.

    Google Scholar 

  • Fuchs, P. A., Evans, M. G., & Murrow, B. W. (1990). Calcium currents in hair cells isolated from the cochlea of the chick. The Journal of Physiology, 429(1), 553–568.

    Google Scholar 

  • Furukawa, T., & Matsuura, S. (1978). Adaptive rundown of excitatory post‐synaptic potentials at synapses between hair cells and eight nerve fibres in the goldfish. The Journal of Physiology, 276(1), 193–209.

    Google Scholar 

  • Furukawa, T., Kuno, M., & Matsuura, S. (1982). Quantal analysis of a decremental response at hair cell‐afferent fibre synapses in the goldfish sacculus. The Journal of Physiology, 322(1), 181–195.

    Google Scholar 

  • Galambos, R., & Davis, H. (1944). The response of single auditory-nerve fibers to acoustic stimulation. Boston, MA: Department of Physiology, Harvard Medical School.

    Google Scholar 

  • Gebhart, M., Juhasz-Vedres, G., Zuccotti, A., Brandt, N., Engel, J., Trockenbacher, A., Kaur, G., Obermair, G. J., Knipper, M., Koschak, A., & Striessnig, J. (2010). Modulation of cav1.3 ca2+ channel gating by rab3 interacting molecule. Molecular and Cellular Neuroscience, 44(3), 246–259.

    Google Scholar 

  • Géléoc, G. S., & Holt, J. R. (2003). Auditory amplification: Outer hair cells pres the issue. Trends in Neurosciences, 26(3), 115–117.

    Google Scholar 

  • Glowatzki, E., & Fuchs, P. A. (2000). Cholinergic synaptic inhibition of inner hair cells in the neonatal mammalian cochlea. Science, 288(5475), 2366–2368.

    Google Scholar 

  • Glowatzki, E., & Fuchs, P. A. (2002). Transmitter release at the hair cell ribbon synapse. Nature Neuroscience, 5(2), 147–154.

    Google Scholar 

  • Goutman, J. D. (2012). Transmitter release from cochlear hair cells is phase locked to cyclic stimuli of different intensities and frequencies. The Journal of Neuroscience, 32(47), 17025–17036.

    Google Scholar 

  • Goutman, J. D., & Glowatzki, E. (2007). Time course and calcium dependence of transmitter release at a single ribbon synapse. Proceedings of the National Academy of Sciences of the USA, 104(41), 16341–16346.

    Google Scholar 

  • Goutman, J. D., & Glowatzki, E. (2011). Short-term facilitation modulates size and timing of the synaptic response at the inner hair cell ribbon synapse. The Journal of Neuroscience, 31(22), 7974–7981.

    Google Scholar 

  • Grant, L., & Fuchs, P. (2008). Calcium-and calmodulin-dependent inactivation of calcium channels in inner hair cells of the rat cochlea. The Journal of Neurophysiology, 99(5), 2183–2193.

    Google Scholar 

  • Grant, L., Yi, E., & Glowatzki, E. (2010). Two modes of release shape the postsynaptic response at the inner hair cell ribbon synapse. The Journal of Neuroscience, 30(12), 4210–4220.

    Google Scholar 

  • Graydon, C. W., Cho, S., Li, G. L., Kachar, B., & von Gersdorff, H. (2011). Sharp Ca2+ nanodomains beneath the ribbon promote highly synchronous multivesicular release at hair cell synapses. The Journal of Neuroscience, 31(46), 16637–16650.

    Google Scholar 

  • Gregory, F. D., Bryan, K. E., Pangršič, T., Calin-Jageman, I. E., Moser, T., & Lee, A. (2011). Harmonin inhibits presynaptic CaV1.3 Ca2+ channels in mouse inner hair cells. Nature Neuroscience, 14(9), 1109–1111.

    Google Scholar 

  • Heidelberger, R., & Matthews, G. (1992). Calcium influx and calcium current in single synaptic terminals of goldfish retinal bipolar neurons. The Journal of Physiology, 447(1), 235–256.

    Google Scholar 

  • Heil, P., & Irvine, D. R. (1997). First-spike timing of auditory-nerve fibers and comparison with auditory cortex. Journal of Neurophysiology, 78(5), 2438–2454.

    Google Scholar 

  • Heil, P., & Neubauer, H. (2001). Temporal integration of sound pressure determines thresholds of auditory-nerve fibers. The Journal of Neuroscience, 21(18), 7404–7415.

    Google Scholar 

  • Heil, P., & Neubauer, H. (2003). A unifying basis of auditory thresholds based on temporal summation. Proceedings of the National Academy of Sciences of the USA, 100(10), 6151–6156.

    Google Scholar 

  • Heil, P., & Neubauer, H. (2010). Summing across different active zones can explain the quasi-linear Ca2+-dependencies of exocytosis by receptor cells. Frontiers in Synaptic Neuroscience, 2.

    Google Scholar 

  • Hibino, H., Pironkova, R., Onwumere, O., Vologodskaia, M., Hudspeth, A. J., & Lesage, F. (2002). Rim binding proteins (RBPs) couple rab3-interacting molecules (RIMs) to voltage-gated Ca2+ channels. Neuron, 34(3), 411–423.

    Google Scholar 

  • Hossain, W. A., Antic, S. D., Yang, Y., Rasband, M. N., & Morest, D. K. (2005). Where is the spike generator of the cochlear nerve? Voltage-gated sodium channels in the mouse cochlea. The Journal of Neuroscience, 25(29), 6857–6868.

    Google Scholar 

  • Huang, L. C., Thorne, P. R., Housley, G. D., & Montgomery, J. M. (2007). Spatiotemporal definition of neurite outgrowth, refinement and retraction in the developing mouse cochlea. Development, 134(16), 2925–2933.

    Google Scholar 

  • Huang, L. C., Barclay, M., Lee, K., Peter, S., Housley, G. D., Thorne, P. R., Montgomery, J. M., & others (2012). Synaptic profiles during neurite extension, refinement and retraction in the developing cochlea. Neural Development, 7 1–17.

    Google Scholar 

  • Hudspeth, A. J., & Lewis, R. S. (1988). Kinetic analysis of voltage-and ion-dependent conductances in saccular hair cells of the bull-frog, rana catesbeiana. The Journal of Physiology, 400(1), 237–274.

    Google Scholar 

  • Issa, N. P., & Hudspeth, A. J. (1996). The entry and clearance of Ca2+ at individual presynaptic active zones of hair cells from the bullfrog’s sacculus. Proceedings of the National Academy of Sciences of the USA, 93(18), 9527–9532.

    Google Scholar 

  • Jing, Z., Rutherford, M. A., Takago, H., Frank, T., Fejtova, A., Khimich, D., Moser, T., & Strenzke, N. (2013). Disruption of the presynaptic cytomatrix protein bassoon degrades ribbon anchorage, multiquantal release, and sound encoding at the hair cell afferent synapse. The Journal of Neuroscience, 33(10), 4456–4467.

    Google Scholar 

  • Johnson, S. L., Marcotti, W., & Kros, C. J. (2005). Increase in efficiency and reduction in Ca2+ dependence of exocytosis during development of mouse inner hair cells. The Journal of Physiology, 563(1), 177–191.

    Google Scholar 

  • Johnson, S. L., Forge, A., Knipper, M., Munkner, S., & Marcotti, W. (2008). Tonotopic variation in the calcium dependence of neurotransmitter release and vesicle pool replenishment at mammalian auditory ribbon synapses. The Journal of Neuroscience, 28(30), 7670–7678.

    Google Scholar 

  • Johnson, S. L., Franz, C., Kuhn, S., Furness, D. N., Rüttiger, L., Münkner, S., Rivolta, M. N., Seward, E. P., Herschman, H. R., & Engel, J. (2010). Synaptotagmin IV determines the linear Ca2+ dependence of vesicle fusion at auditory ribbon synapses. Nature Neuroscience, 13(1), 45–52.

    Google Scholar 

  • Johnson, S. L., Eckrich, T., Kuhn, S., Zampini, V., Franz, C., Ranatunga, K. M., Roberts, T. P., Masetto, S., Knipper, M., Kros, C. J., & Marcotti, W. (2011). Position-dependent patterning of spontaneous action potentials in immature cochlear inner hair cells. Nature Neuroscience, 14(6), 711–717.

    Google Scholar 

  • Kaeser, P. S., Deng, L., Wang, Y., Dulubova, I., Liu, X., Rizo, J., & Südhof, T. C. (2011). RIM proteins tether Ca2+ channels to presynaptic active zones via a direct PDZ-domain interaction. Cell, 144(2), 282–295.

    Google Scholar 

  • Kantardzhieva, A., Peppi, M., Lane, W. S., & Sewell, W. F. (2012). Protein composition of immunoprecipitated synaptic ribbons. Journal of Proteome Research, 11(2), 1163–1174.

    Google Scholar 

  • Kantardzhieva, A., Liberman, M. C., & Sewell, W. F. (2013). Quantitative analysis of ribbons, vesicles, and cisterns at the cat inner hair cell synapse: Correlations with spontaneous rate: hair cell synaptic ribbons. Journal of Comparative Neurology, 521(14), 3260–3271.

    Google Scholar 

  • Keen, E. C., & Hudspeth, A. J. (2006). Transfer characteristics of the hair cell’s afferent synapse. Proceedings of the National Academy of Sciences of the USA, 103(14), 5537–5542.

    Google Scholar 

  • Khimich, D., Nouvian, R., Pujol, R., tom Dieck, S., Egner, A., Gundelfinger, E. D., and Moser, T. (2005). Hair cell synaptic ribbons are essential for synchronous auditory signalling. Nature, 434, 889–894.

    Google Scholar 

  • Kiang, N. Y. S. (1965). Discharge patterns of single fibers in the cat’s auditory nerve. Cambridge, MA: MIT Press.

    Google Scholar 

  • Kim, M. H., Li, G. L., & von Gersdorff, H. (2013). Single Ca2+ channels and exocytosis at sensory synapses. The Journal of Physiology, 591(13), 3167–3178.

    Google Scholar 

  • Knudsen, E. I., & Konishi, M. (1979). Mechanisms of sound localization in the barn owl (tyto alba). Journal of Comparative Physiology, 133(1), 13–21.

    Google Scholar 

  • Koschak, A., Reimer, D., Huber, I., Grabner, M., Glossmann, H., Engel, J., & Striessnig, J. (2001). Alpha 1D (CaV1. 3) subunits can form L-type Ca2+ channels activating at negative voltages. The Journal of Biological Chemistry (jbc), 276(25), 22100–22106.

    Google Scholar 

  • Kros, C. J., Ruppersberg, J. P., & Rüsch, A. (1998). Expression of a potassium current in inner hair cells during development of hearing in mice. Nature, 394(6690), 281–284.

    Google Scholar 

  • Kubisch, C., Schroeder, B. C., Friedrich, T., Lütjohann, B., El-Amraoui, A., Marlin, S., Petit, C., & Jentsch, T. J. (1999). KCNQ4, a novel potassium channel expressed in sensory outer hair cells, is mutated in dominant deafness. Cell, 96(3), 437–446.

    Google Scholar 

  • Lacas-Gervais, S., Guo, J., Strenzke, N., Scarfone, E., Kolpe, M., Jahkel, M., De Camilli, P., Moser, T., Rasband, M. N., Solimena, M. (2004). βΙVΣ1 spectrin stabilizes the nodes of Ranvier and axon initial segments. The Journal of Cell Biology (JCB), 166(7), 983–990.

    Google Scholar 

  • Lee, A., Scheuer, T., & Catterall, W. A. (2000). Ca2+/calmodulin-dependent facilitation and inactivation of P/Q-type Ca2+ channels. The Journal of Neuroscience, 20(18), 6830–6838.

    Google Scholar 

  • Lenoir, M., Shnerson, A., & Pujol, R. (1980). Cochlear receptor development in the rat with emphasis on synaptogenesis. Anatomy and Embryology, 160(3), 253–262.

    Google Scholar 

  • Lenzi, D., & von Gersdorff, H. (2001). Structure suggests function: The case for synaptic ribbons as exocytotic nanomachines. Bioessays, 23(9), 831–840.

    Google Scholar 

  • Lenzi, D., Crum, J., Ellisman, M. H., & Roberts, W. M. (2002). Depolarization redistributes synaptic membrane and creates a gradient of vesicles on the synaptic body at a ribbon synapse. Neuron, 36(4), 649–659.

    Google Scholar 

  • Li, G. L., Keen, E., Andor-Ardo, D., Hudspeth, A. J., & von Gersdorff, H. (2009). The unitary event underlying multiquantal EPSCs at a hair cell’s ribbon synapse. The Journal of Neuroscience, 29(23), 7558–7568.

    Google Scholar 

  • Li, G. L., Cho, S., & von Gersdorff, H. (2014). Phase-locking precision is enhanced by multiquantal release at an auditory hair cell ribbon synapse. Neuron, 83(6), 1404–1417.

    Google Scholar 

  • Liberman, M. C. (1978). Auditory-nerve response from cats raised in a low-noise chamber. The Journal of the Acoustical Society of America, 63(2), 442–455.

    Google Scholar 

  • Liberman, M. C. (1980). Morphological differences among radial afferent fibers in the cat cochlea: An electron-microscopic study of serial sections. Hearing Research, 3(1), 45–63.

    Google Scholar 

  • Liberman, M. C. (1982). Single-neuron labeling in the cat auditory nerve. Science, 216(4551), 1239–1241.

    Google Scholar 

  • Liberman, L. D., Wang, H., & Liberman, M. C. (2011). Opposing gradients of ribbon size and AMPA receptor expression underlie sensitivity differences among cochlear-nerve/hair-cell synapses. The Journal of Neuroscience, 31(3), 801–808.

    Google Scholar 

  • Lysakowski, A., Gaboyard-Niay, S., Calin-Jageman, I., Chatlani, S., Price, S. D., & Eatock, R. A. (2011). Molecular microdomains in a sensory terminal, the vestibular calyx ending. The Journal of Neuroscience, 31(27), 10101–10114.

    Google Scholar 

  • Magupalli, V. G., Schwarz, K., Alpadi, K., Natarajan, S., Seigel, G. M., & Schmitz, F. (2008). Multiple ribeye-ribeye interactions create a dynamic scaffold for the formation of synaptic ribbons. The Journal of Neuroscience, 28(32), 7954–7967.

    Google Scholar 

  • Marcotti, W., Johnson, S. L., Rusch, A., & Kros, C. J. (2003). Sodium and calcium currents shape action potentials in immature mouse inner hair cells. The Journal of Physiology, 552(3), 743–761.

    Google Scholar 

  • Martinez-Dunst, C., Michaels, R. L., & Fuchs, P. A. (1997). Release sites and calcium channels in hair cells of the chick’s cochlea. The Journal of Neuroscience, 17(23), 9133–9144.

    Google Scholar 

  • Matthews, G., & Fuchs, P. (2010). The diverse roles of ribbon synapses in sensory neurotransmission. Nature Reviews Neuroscience, 11(12), 812–822.

    Google Scholar 

  • Matveev, V., Bertram, R., & Sherman, A. (2011). Calcium cooperativity of exocytosis as a measure of Ca2+ channel domain overlap. Brain Research, 1398 126–138.

    Google Scholar 

  • Meddis, R. (2006). Auditory-nerve first-spike latency and auditory absolute threshold: A computer model. The Journal of the Acoustical Society of America, 119(1), 406–417.

    Google Scholar 

  • Merchan-Perez, A., & Liberman, M. C. (1996). Ultrastructural differences among afferent synapses on cochlear hair cells: Correlations with spontaneous discharge rate. Journal of Comparative Neurology, 371(2), 208–221.

    Google Scholar 

  • Meyer, A. C., Frank, T., Khimich, D., Hoch, G., Riedel, D., Chapochnikov, N. M., Yarin, Y. M., Harke, B., Hell, S. W., Egner, A., & Moser, T. (2009). Tuning of synapse number, structure and function in the cochlea. Nature Neuroscience, 12(4), 444–453.

    Google Scholar 

  • Moser, T., & Beutner, D. (2000). Kinetics of exocytosis and endocytosis at the cochlear inner hair cell afferent synapse of the mouse. Proceedings of the National Academy of Sciences of the USA, 97(2), 883–888.

    Google Scholar 

  • Moser, T., Neef, A., & Khimich, D. (2006). Mechanisms underlying the temporal precision of sound coding at the inner hair cell ribbon synapse. The Journal of Physiology, 576(1), 55–62.

    Google Scholar 

  • Neef, J., Gehrt, A., Bulankina, A. V., Meyer, A. C., Riedel, D., Gregg, R. G., Strenzke, N., & Moser, T. (2009). The Ca2+ channel subunit β2 regulates Ca2+ channel abundance and function in inner hair cells and is required for hearing. The Journal of Neuroscience, 29(34), 10730–10740.

    Google Scholar 

  • Neef, J., Jung, S., Wong, A. B., Reuter, K., Pangrsic, T., Chakrabarti, R., Kugler, S., Lenz, C., Nouvian, R., Boumil, R. M., Frankel, W. N., Wichmann, C., & Moser, T. (2014). Modes and regulation of endocytic membrane retrieval in mouse auditory hair cells. The Journal of Neuroscience, 34(3), 705–716.

    Google Scholar 

  • Nouvian, R., Beutner, D., Parsons, T. D., & Moser, T. (2006). Structure and function of the hair cell ribbon synapse. Journal of Membrane Biology, 209(2–3), 153–165.

    Google Scholar 

  • Nouvian, R., Neef, J., Bulankina, A. V., Reisinger, E., Pangršič, T., Frank, T., Sikorra, S., Brose, N., Binz, T., & Moser, T. (2011). Exocytosis at the hair cell ribbon synapse apparently operates without neuronal snare proteins. Nature Neuroscience, 14(4), 411–413.

    Google Scholar 

  • Nusser, Z., Lujan, R., Laube, G., Roberts, J. D. B., Molnar, E., & Somogyi, P. (1998). Cell type and pathway dependence of synaptic AMPA receptor number and variability in the hippocampus. Neuron, 21(3), 545–559.

    Google Scholar 

  • Ohlemiller, K. K., Echteler, S. M., & Siegel, J. H. (1991). Factors that influence rate‐versus‐intensity relations in single cochlear nerve fibers of the gerbil. The Journal of the Acoustical Society of America, 90(1), 274–287.

    Google Scholar 

  • Oliver, D., Knipper, M., Derst, C., & Fakler, B. (2003). Resting potential and submembrane calcium concentration of inner hair cells in the isolated mouse cochlea are set by KCNQ-type potassium channels. The Journal of Neuroscience, 23(6), 2141–2149.

    Google Scholar 

  • Oliver, D., Taberner, A. M., Thurm, H., Sausbier, M., Arntz, C., Ruth, P., Fakler, B., & Liberman, M. C. (2006). The role of BKCa channels in electrical signal encoding in the mammalian auditory periphery. The Journal of Neuroscience, 26(23), 6181–6189.

    Google Scholar 

  • Palmer, A. R., & Russell, I. J. (1986). Phase-locking in the cochlear nerve of the guinea-pig and its relation to the receptor potential of inner hair cells. Hearing Research, 24(1), 1–15.

    Google Scholar 

  • Pangršič, T., Lasarow, L., Reuter, K., Takago, H., Schwander, M., Riedel, D., Frank, T., Tarantino, L. M., Bailey, J. S., Strenzke, N., Brose, N., Müller, U., Reisinger, E., & Moser, T. (2010). Hearing requires otoferlin-dependent efficient replenishment of synaptic vesicles in hair cells. Nature Neuroscience, 13(7), 869–876.

    Google Scholar 

  • Parsons, T. D., Lenzi, D., Almers, W., & Roberts, W. M. (1994). Calcium-triggered exocytosis and endocytosis in an isolated presynaptic cell: Capacitance measurements in saccular hair cells. Neuron, 13(4), 875–883.

    Google Scholar 

  • Platzer, J., Engel, J., Schrott-Fischer, A., Stephan, K., Bova, S., Chen, H., Zheng, H., & Striessnig, J. (2000). Congenital deafness and sinoatrial node dysfunction in mice lacking class D L-type Ca2+ channels. Cell, 102(1), 89–97.

    Google Scholar 

  • Ramakrishnan, N. A., Drescher, M. J., & Drescher, D. G. (2009). Direct interaction of otoferlin with syntaxin 1a, SNAP-25, and the L-type voltage-gated calcium channel CaV1.3. The Journal of Biological Chemistry (jbc), 284(3), 1364–1372.

    Google Scholar 

  • Raman, I. M., Sprunger, L. K., Meisler, M. H., & Bean, B. P. (1997). Altered subthreshold sodium currents and disrupted firing patterns in purkinje neurons of SCN8A mutant mice. Neuron, 19(4), 881–891.

    Google Scholar 

  • Reisinger, E., Bresee, C., Neef, J., Nair, R., Reuter, K., Bulankina, A., Nouvian, R., Koch, M., Buckers, J., Kastrup, L., Roux, I., Petit, C., Hell, S. W., Brose, N., Rhee, J. S., Kugler, S., Brigande, J. V., & Moser, T. (2011). Probing the functional equivalence of otoferlin and synaptotagmin 1 in exocytosis. The Journal of Neuroscience, 31(13), 4886–4895.

    Google Scholar 

  • Relkin, E. M., & Doucet, J. R. (1991). Recovery from prior stimulation. I: Relationship to spontaneous firing rates of primary auditory neurons. Hearing Research, 55(2), 215–222.

    Google Scholar 

  • Roberts, W. M. (1993). Spatial calcium buffering in saccular hair cells. Nature, 363, 74–76.

    Google Scholar 

  • Roberts, W. M., Jacobs, R. A., & Hudspeth, A. J. (1990). Colocalization of ion channels involved in frequency selectivity and synaptic transmission at presynaptic active zones of hair cells. The Journal of Neuroscience, 10(11), 3664–3684.

    Google Scholar 

  • Robertson, D., & Paki, B. (2002). Role of L-type Ca2+ channels in transmitter release from mammalian inner hair cells. II. Single-neuron activity. Journal of Neurophysiology, 87(6), 2734–2740.

    Google Scholar 

  • Rodriguez-Contreras, A., & Yamoah, E. N. (2001). Direct measurement of single-channel Ca2+ currents in bullfrog hair cells reveals two distinct channel subtypes. The Journal of Physiology, 534(3), 669–689.

    Google Scholar 

  • Rose, J. E., Brugge, J. F., Anderson, D. J., Hind, J. E., & others (1967). Phase-locked response to low-frequency tones in single auditory nerve fibers of the squirrel monkey. Journal of Neurophysiology, 30(4), 769–793.

    Google Scholar 

  • Roux, I., Safieddine, S., Nouvian, R., Simmler, M. C., Bahloul, A., Perfettini, I., Le Gall, M., Rostaing, P., Hamard, G., & Triller, A. (2006). Otoferlin, defective in a human deafness form, is essential for exocytosis at the auditory ribbon synapse. Cell, 127(2), 277–289.

    Google Scholar 

  • Ruel, J., Nouvian, R., d’ Aldin, C. G., Pujol, R., Eybalin, M., & Puel, J. L. (2001). Dopamine inhibition of auditory nerve activity in the adult mammalian cochlea. European Journal of Neuroscience, 14(6), 977–986.

    Google Scholar 

  • Ruel, J., Emery, S., Nouvian, R., Bersot, T., Amilhon, B., Van Rybroek, J. M., Rebillard, G., Lenoir, M., Eybalin, M., Delprat, B., Sivakumaran, T. A., Giros, B., El Mestikawy, S., Moser, T., Smith, R. J. H., Lesperance, M. M., & Puel, J. L. (2008). Impairment of SLC17A8 encoding vesicular glutamate transporter-3, VGLUT3, underlies nonsyndromic deafness DFNA25 and inner hair cell dysfunction in null mice. The American Journal of Human Genetics, 83(2), 278–292.

    Google Scholar 

  • Rüsch, A., Ng, L., Goodyear, R., Oliver, D., Lisoukov, I., Vennström, B., Richardson, G., Kelley, M. W., & Forrest, D. (2001). Retardation of cochlear maturation and impaired hair cell function caused by deletion of all known thyroid hormone receptors. The Journal of Neuroscience, 21(24), 9792–9800.

    Google Scholar 

  • Russell, I. J., & Sellick, P. M. (1978). Intracellular studies of hair cells in the mammalian cochlea. The Journal of Physiology, 284(1), 261–290.

    Google Scholar 

  • Rutherford, M. A., & Pangršič, T. (2012). Molecular anatomy and physiology of exocytosis in sensory hair cells. Cell Calcium, 52(3), 327–337.

    Google Scholar 

  • Rutherford, M. A., Chapochnikov, N. M., & Moser, T. (2012). Spike encoding of neurotransmitter release timing by spiral ganglion neurons of the cochlea. The Journal of Neuroscience, 32(14), 4773–4789.

    Google Scholar 

  • Rutherford, M. A. (2015). Resolving the structure of inner ear ribbon synapses with STED microscopy. Synapse, 69(5), 242-255.

    Google Scholar 

  • Sachs, M. B., Winslow, R. L., & Sokolowski, B. H. (1989). A computational model for rate-level functions from cat auditory-nerve fibers. Hearing Research, 41(1), 61–69.

    Google Scholar 

  • Safieddine, S., & Wenthold, R. J. (1999). SNARE complex at the ribbon synapses of cochlear hair cells: Analysis of synaptic vesicle‐and synaptic membrane‐associated proteins. European Journal of Neuroscience, 11(3), 803–812.

    Google Scholar 

  • Saito, K. (1990). Freeze-fracture organization of hair cell synapses in the sensory epithelium of guinea pig organ of corti. Journal of Electron Microscopy Technique, 15(2), 173–186.

    Google Scholar 

  • Santos-Sacchi, J. (1993). Voltage-dependent ionic conductances of type I spiral ganglion cells from the guinea pig inner ear. The Journal of Neuroscience, 13(8), 3599–3611.

    Google Scholar 

  • Schmitz, F., Königstorfer, A., & Südhof, T. C. (2000). RIBEYE, a component of synaptic ribbons: A protein’s journey through evolution provides insight into synaptic ribbon function. Neuron, 28(3), 857–872.

    Google Scholar 

  • Schnee, M. E., Lawton, D. M., Furness, D. N., Benke, T. A., & Ricci, A. J. (2005). Auditory hair cell-afferent fiber synapses are specialized to operate at their best frequencies. Neuron, 47(2), 243–254.

    Google Scholar 

  • Schnee, M. E., Castellano-Muñoz, M., & Ricci, A. J. (2013). Response properties from turtle auditory hair cell afferent fibers suggest spike generation is driven by synchronized release both between and within synapses. Journal of Neurophysiology, 110(1), 204–220.

    Google Scholar 

  • Schrauwen, I., Helfmann, S., Inagaki, A., Predoehl, F., Tabatabaiefar, M. A., Picher, M. M., Sommen, M., Seco, C. Z., Oostrik, J., Kremer, H., Dheedene, A., Claes, C., Fransen, E., Chaleshtori, M. H., Coucke, P., Lee, A., Moser, T., & Van Camp, G. (2012). A mutation in CaBP2, expressed in cochlear hair cells, causes autosomal-recessive hearing impairment. The American Journal of Human Genetics, 91(4), 636–645.

    Google Scholar 

  • Schwarz, K., Natarajan, S., Kassas, N., Vitale, N., & Schmitz, F. (2011). The synaptic ribbon is a site of phosphatidic acid generation in ribbon synapses. The Journal of Neuroscience, 31(44), 15996–16011.

    Google Scholar 

  • Sendin, G., Bulankina, A. V., Riedel, D., & Moser, T. (2007). Maturation of ribbon synapses in hair cells is driven by thyroid hormone. The Journal of Neuroscience, 27(12), 3163–3173.

    Google Scholar 

  • Sendin, G., Bourien, J., Rassendren, F., Puel, J. L., & Nouvian, R. (2014). Spatiotemporal pattern of action potential firing in developing inner hair cells of the mouse cochlea. Proceedings of the National Academy of Sciences of the USA, 111(5), 1999–2004.

    Google Scholar 

  • Sewell, W. F. (1984). The relation between the endocochlear potential and spontaneous activity in auditory nerve fibres of the cat. The Journal of Physiology, 347(1), 685–696.

    Google Scholar 

  • Sheets, L., Trapani, J. G., Mo, W., Obholzer, N., & Nicolson, T. (2011). Ribeye is required for presynaptic CaV1.3 channel localization and afferent innervation of sensory hair cells. Development, 138(7), 1309–1319.

    Google Scholar 

  • Shnerson, A., Devigne, C., & Pujol, R. (1981). Age-related changes in the C57Bl/6j mouse cochlea. II. ultrastructural findings. Developmental Brain Research, 2(1), 77–88.

    Google Scholar 

  • Siegel, J. H. (1992). Spontaneous synaptic potentials from afferent terminals in the guinea pig cochlea. Hearing Research, 59(1), 85–92.

    Google Scholar 

  • Siegel, J. H., & Relkin, E. M. (1987). Antagonistic effects of perilymphatic calcium and magnesium on the activity of single cochlear afferent neurons. Hearing Research, 28(2), 131–147.

    Google Scholar 

  • Slepecky, N. B., Galsky, M. D., Swartzentruber-Martin, H., & Savage, J. (2000). Study of afferent nerve terminals and fibers in the gerbil cochlea: Distribution by size. Hearing Research, 144(1), 124–134.

    Google Scholar 

  • Smith, C. A., & Sjöstrand, F. S. (1961). Structure of the nerve endings on the external hair cells of the guinea pig cochlea as studied by serial sections. Journal of Ultrastructure Research, 5(6), 523–556.

    Google Scholar 

  • Sobkowicz, H. M., Rose, J. E., Scott, G. E., & Slapnick, S. M. (1982). Ribbon synapses in the developing intact and cultured organ of corti in the mouse. The Journal of Neuroscience, 2(7), 942–957.

    Google Scholar 

  • Spassova, M., Eisen, M. D., Saunders, J. C., & Parsons, T. D. (2001). Chick cochlear hair cell exocytosis mediated by dihydropyridine-sensitive calcium channels. The Journal of Physiology, 535(3), 689–696.

    Google Scholar 

  • Spassova, M. A., Avissar, M., Furman, A. C., Crumling, M. A., Saunders, J. C., & Parsons, T. D. (2004). Evidence that rapid vesicle replenishment of the synaptic ribbon mediates recovery from short-term adaptation at the hair cell afferent synapse. Journal of the Association for Research in Otolaryngology, 5(4), 376–390.

    Google Scholar 

  • Spoendlin, H. (1972). Innervation densities of the cochlea. Acta Oto-Laryngologica, 73(2),–(6), 235–248.

    Google Scholar 

  • Stevens, S. S., & Davis, H. (1938/1983). Hearing: Its psychology and physiology. American Institute of Physics for the Acoustical Society of America.

    Google Scholar 

  • Strenzke, N., Chanda, S., Kopp-Scheinpflug, C., Khimich, D., Reim, K., Bulankina, A. V., Neef, A., Wolf, F., Brose, N., Xu-Friedman, M. A., & Moser, T. (2009). Complexin-I is required for high-fidelity transmission at the endbulb of held auditory synapse. The Journal of Neuroscience, 29(25), 7991–8004.

    Google Scholar 

  • Taberner, A. M. & Liberman, M. C. (2005). Response properties of single auditory nerve fibers in the mouse. Journal of Neurophysiology, 93(1), 557–569.

    Google Scholar 

  • Tachibana, M., Okada, T., Arimura, T., Kobayashi, K., & Piccolino, M. (1993). Dihydropyridine-sensitive calcium current mediates neurotransmitter release from bipolar cells of the goldfish retina. The Journal of Neuroscience, 13(7), 2898–2909.

    Google Scholar 

  • Tritsch, N. X., & Bergles, D. E. (2010). Developmental regulation of spontaneous activity in the mammalian cochlea. The Journal of Neuroscience, 30(4), 1539–1550.

    Google Scholar 

  • Tritsch, N. X., Yi, E., Gale, J. E., Glowatzki, E., & Bergles, D. E. (2007). The origin of spontaneous activity in the developing auditory system. Nature, 450(7166), 50–55.

    Google Scholar 

  • Tucker, T., & Fettiplace, R. (1995). Confocal imaging of calcium microdomains and calcium extrusion in turtle hair cells. Neuron, 15(6), 1323–1335.

    Google Scholar 

  • Uthaiah, R. C., & Hudspeth, A. J. (2010). Molecular anatomy of the hair cell’s ribbon synapse. The Journal of Neuroscience, 30(37), 12387–12399.

    Google Scholar 

  • Verpy, E., Leibovici, M., Zwaenepoel, I., Liu, X. Z., Gal, A., Salem, N., Mansour, A., Blanchard, S., Kobayashi, I., & Keats, B. J. (2000). A defect in harmonin, a PDZ domain-containing protein expressed in the inner ear sensory hair cells, underlies Usher syndrome type 1C. Nature Genetics, 26(1), 51–55.

    Google Scholar 

  • Vincent, P. F. Y., Bouleau, Y., Safieddine, S., Petit, C., & Dulon, D. (2014). Exocytotic machineries of vestibular type I and cochlear ribbon synapses display similar intrinsic otoferlin-dependent Ca2+ sensitivity but a different coupling to Ca2+ channels. The Journal of Neuroscience, 34(33), 10853–10869.

    Google Scholar 

  • Waites, C. L., Leal‐Ortiz, S. A., Okerlund, N., Dalke, H., Fejtova, A., Altrock, W. D., Gundelfinger, E. D., & Garner, C. C. (2013). Bassoon and piccolo maintain synapse integrity by regulating protein ubiquitination and degradation. The EMBO Journal, 32(7), 954–969.

    Google Scholar 

  • Walsh, E. J., & McGee, J. (1987). Postnatal development of auditory nerve and cochlear nucleus neuronal responses in kittens. Hearing Research, 28(1), 97–116.

    Google Scholar 

  • Walsh, E. J., & Romand, R. (1992). Functional development of the cochlea and the cochlear nerve. Development of Auditory and Vestibular Systems, 2 161–219.

    Google Scholar 

  • Walsh, B. T., Miller, J. B., Gacek, R., & Kiang, N. Y. S. (1972). Spontaneous activity in the eighth cranial nerve of the cat. International Journal of Neuroscience, 3(5), 221–235.

    Google Scholar 

  • Weiss, T. F. (1966). A model of the peripheral auditory system. Kybernetik, 3(4), 153–175.

    Google Scholar 

  • Wen, B., Wang, G. I., Dean, I., & Delgutte, B. (2009). Dynamic range adaptation to sound level statistics in the auditory nerve. The Journal of Neuroscience, 29(44), 13797–13808.

    Google Scholar 

  • Westerman, L. A., & Smith, R. L. (1984). Rapid and short-term adaptation in auditory nerve responses. Hearing Research, 15(3), 249–260.

    Google Scholar 

  • Wever, E. G., & Lawrence, M. (1954). Physiological acoustics. Princeton, NJ: Princeton University Press.

    Google Scholar 

  • Winter, I. M., Robertson, D., & Yates, G. K. (1990). Diversity of characteristic frequency rate-intensity functions in guinea pig auditory nerve fibres. Hearing Research, 45(3), 191–202.

    Google Scholar 

  • Wittig, J. H., & Parsons, T. D. (2008). Synaptic ribbon enables temporal precision of hair cell afferent synapse by increasing the number of readily releasable vesicles: A modeling study. The Journal of Neurophysiology, 100(4), 1724–1739.

    Google Scholar 

  • Wong, A. B., Jing, Z., Rutherford, M. A., Frank, T., Strenzke, N., & Moser, T. (2013). Concurrent maturation of inner hair cell synaptic Ca2+ influx and auditory nerve spontaneous activity around hearing onset in mice. The Journal of Neuroscience, 33(26), 10661–10666.

    Google Scholar 

  • Wong, A. B., Rutherford, M. A., Gabrielaitis, M., Pangršič, T., Göttfert, F., Frank, T., Michanski, S., Hell, S., Wolf, F., Wichmann, C., & Moser, T. (2014). Developmental refinement of hair cell synapses tightens the coupling of Ca 2+ influx to exocytosis. The EMBO Journal, 33(3), 247–264.

    Google Scholar 

  • Wu, X. S., Xue, L., Mohan, R., Paradiso, K., Gillis, K. D., & Wu, L. G. (2007). The origin of quantal size variation: Vesicular glutamate concentration plays a significant role. Journal of Neuroscience, 27(11), 3046–3056.

    Google Scholar 

  • Yang, P. S., Alseikhan, B. A., Hiel, H., Grant, L., Mori, M. X., Yang, W., Fuchs, P. A., & Yue, D. T. (2006). Switching of Ca2+-dependent inactivation of CaV1.3 channels by calcium binding proteins of auditory hair cells. The Journal of Neuroscience, 26(42), 10677–10689.

    Google Scholar 

  • Yasunaga, S., Grati, M., Cohen-Salmon, M., El-Amraoui, A., Mustapha, M., Salem, N., El-Zir, E., Loiselet, J., & Petit, C. (1999). A mutation in OTOF, encoding otoferlin, a FER-1-like protein, causes DFNB9, a nonsyndromic form of deafness. Nature Genetics, 21(4), 363–369.

    Google Scholar 

  • Yi, E., Roux, I., & Glowatzki, E. (2010). Dendritic HCN channels shape excitatory postsynaptic potentials at the inner hair cell afferent synapse in the mammalian cochlea. Journal of Neurophysiology, 103(5), 2532–2543.

    Google Scholar 

  • Zagaeski, M., Cody, A. R., Russell, I. J., & Mountain, D. C. (1994). Transfer characteristic of the inner hair cell synapse: Steady‐state analysis. The Journal of the Acoustical Society of America, 95(6), 3430–3434.

    Google Scholar 

  • Zampini, V., Johnson, S. L., Franz, C., Lawrence, N. D., Munkner, S., Engel, J., Knipper, M., Magistretti, J., Masetto, S., & Marcotti, W. (2010). Elementary properties of CaV1.3 Ca2+ channels expressed in mouse cochlear inner hair cells. The Journal of Physiology, 588(1), 187–199.

    Google Scholar 

  • Zampini, V., Johnson, S. L., Franz, C., Knipper, M., Holley, M. C., Magistretti, J., Masetto, S., & Marcotti, W. (2013). Burst activity and ultrafast activation kinetics of CaV1.3 Ca2+ channels support presynaptic activity in adult gerbil hair cell ribbon synapses. The Journal of Physiology, 591(16), 3811–3820.

    Google Scholar 

  • Zhang, S. Y., Robertson, D., Yates, G., & Everett, A. (1999). Role of L-type Ca2+ channels in transmitter release from mammalian inner hair cells I. Gross sound-evoked potentials. Journal of Neurophysiology, 82(6), 3307–3315.

    Google Scholar 

Download references

Acknowledgments

This work was supported by the Department of Otolaryngology at Washington University in St. Louis (M. A. R.) and a grant of the Deutsche Forschungsgemeinschaft to T. M. through the Collaborative Research Center 889.

Author information

Authors and Affiliations

  1. Department of Otolaryngology, Central Institute for the Deaf, Washington University School of Medicine, 660 South Euclid Ave, St. Louis, MO, 63110, USA

    Mark A. Rutherford

  2. Institute for Auditory Neuroscience and Inner Ear Lab, Collaborative Research Center 889, University Medical Center Göttingen, Robert-Kochstr. 40, 37075, Göttingen, Germany

    Tobias Moser

Authors
  1. Mark A. Rutherford
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Tobias Moser
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding authors

Correspondence to Mark A. Rutherford or Tobias Moser .

Editor information

Editors and Affiliations

  1. Department of Otolaryngology – Head and Neck Surgery, Sunnybrook Research Institute, University of Toronto, Toronto, Ontario, Canada

    Alain Dabdoub

  2. Department of Biology, University of Iowa, Iowa City, Iowa, USA

    Bernd Fritzsch

  3. Department of Biology, University of Maryland, College Park, Maryland, USA

    Arthur N. Popper

  4. Marine Biological Laboratory, Woods Hole, Massachusetts, USA

    Richard R. Fay

Rights and permissions

Reprints and permissions

Copyright information

© 2016 Springer Science+Business Media New York

About this chapter

Cite this chapter

Rutherford, M.A., Moser, T. (2016). The Ribbon Synapse Between Type I Spiral Ganglion Neurons and Inner Hair Cells. In: Dabdoub, A., Fritzsch, B., Popper, A., Fay, R. (eds) The Primary Auditory Neurons of the Mammalian Cochlea. Springer Handbook of Auditory Research, vol 52. Springer, New York, NY. https://doi.org/10.1007/978-1-4939-3031-9_5

Download citation

Publish with us

Policies and ethics

Search

Navigation