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The Electrophysiological Signature of Spiral Ganglion Neurons

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

Abstract

Examination of the basic features of primary sensory afferents has revealed much about the fundamental principles of neural encoding. This approach has been particularly valuable in the auditory system, which is systematically organized according to sound frequency and has a multiplicity of tonotopic specializations. The first neural element of the auditory pathway, the type I spiral ganglion neurons, consists of unique primary afferents that, unlike other sensory afferents, have their somata positioned directly in the axonal conduction pathway and display both graded and heterogeneous morphological properties. Electrophysiological specializations are also evident, exemplified by multifaceted voltage-gated ionic currents carried by diverse ion channel subunits that likely fine-tune neuronal firing patterns. Ion channel subunit density and the resulting characteristic firing patterns are not uniform throughout the ganglion, but instead show specific distribution patterns, some of which are related to the frequency-specific contour of the cochlear endorgan. Moreover, these properties can be regulated by neurotrophins such that fast firing electrophysiological features predominate in primary afferents innervating the high-frequency regions, whereas slow firing features are prevalent within primary afferents innervating the low-frequency regions. Thus, the complex electrophysiological properties of the spiral ganglion neurons and their regulation suggest that the primary auditory afferents are capable of shaping the electrophysiological signals that they transmit into the brain.

Keywords

  • Accommodation
  • Brain-derived neurotrophic factor
  • Membrane potential
  • Neurotrophin 3
  • Primary auditory afferents
  • Threshold
  • Voltage-gated ion channels

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References

  • Adamson, C. L., Reid, M. A., & Davis, R. L. (2002a). Opposite actions of brain-derived neurotrophic factor and neurotrophin-3 on firing features and ion channel composition of murine spiral ganglion neurons. The Journal of Neuroscience, 22(4), 1385–1396.

    Google Scholar 

  • Adamson, C. L., Reid, M. A., Mo, Z. L., Bowne-English, J., & Davis, R. L. (2002b). Firing features and potassium channel content of murine spiral ganglion neurons vary with cochlear location. The Journal of Comparative Neurology, 447(4), 331–350.

    Google Scholar 

  • Ahmad, K. M., Klug, K., Herr, S., Sterling, P., & Schein, S. (2003). Cell density ratios in a foveal patch in macaque retina. Visual Neuroscience, 20(2), 189–209.

    Google Scholar 

  • Altschuler, R. A., Hoffman, D. W., Reeks, K. A., & Fex, J. (1985). Localization of dynorphin B-like and alpha-neoendorphin-like immunoreactivities in the guinea pig organ of Corti. Hearing Research, 17(3), 249–258.

    Google Scholar 

  • Banks, M. I., Pearce, R. A., & Smith, P. H. (1993). Hyperpolarization-activated cation current (Ih) in neurons of the medial nucleus of the trapezoid body: Voltage-clamp analysis and enhancement by norepinephrine and cAMP suggest a modulatory mechanism in the auditory brain stem. Journal of Neurophysiology, 70(4), 1420–1432.

    Google Scholar 

  • Barde, Y. A., Edgar, D., & Thoenen, H. (1982). Purification of a new neurotrophic factor from mammalian brain. EMBO Journal, 1(5), 549–553.

    Google Scholar 

  • Bean, B. P. (2007). The action potential in mammalian central neurons. Nature Reviews Neuroscience, 8(6), 451–465.

    Google Scholar 

  • Beisel, K. W., Rocha-Sanchez, S. M., Morris, K. A., Nie, L., Feng, F., Kachar, B., Yamoah, E. N., & Fritzsch, B. (2005). Differential expression of KCNQ4 in inner hair cells and sensory neurons is the basis of progressive high-frequency hearing loss. The Journal of Neuroscience, 25(40), 9285–9293.

    Google Scholar 

  • Bizley, J. K., & Walker, K. M. (2010). Sensitivity and selectivity of neurons in auditory cortex to the pitch, timbre, and location of sounds. Neuroscientist, 16(4), 453–469.

    Google Scholar 

  • Borst, J. G., & Sakmann, B. (1999). Effect of changes in action potential shape on calcium currents and transmitter release in a calyx-type synapse of the rat auditory brainstem. Philosophical Transactions of the Royal Society of London B: Biological Sciences, 354(1381), 347–355.

    Google Scholar 

  • Brödel, M., & Malone, P. D. (1946). Three unpublished drawings of the anatomy of the human ear. Philadelphia and London: W. B. Saunders Company.

    Google Scholar 

  • Brown, M. C. (1994). Antidromic responses of single units from the spiral ganglion. Journal of Neurophysiology, 71(5), 1835–1847.

    Google Scholar 

  • Burgess, B. J., Adams, J. C., & Nadol, J. B., Jr. (1997). Morphologic evidence for innervation of Deiters’ and Hensen’s cells in the guinea pig. Hearing Research, 108(1–2), 74–82.

    Google Scholar 

  • Carr, C. E., Soares, D., Parameshwaran, S., & Perney, T. (2001). Evolution and development of time coding systems. Current Opinion in Neurobiology, 11(6), 727–733.

    Google Scholar 

  • Catterall, W. A., Perez-Reyes, E., Snutch, T. P., & Striessnig, J. (2005). International Union of Pharmacology. XLVIII. Nomenclature and structure-function relationships of voltage-gated calcium channels. Pharmacological Reviews, 57(4), 411–425.

    Google Scholar 

  • Chen, C. (1997). Hyperpolarization-activated current (Ih) in primary auditory neurons. Hearing Research, 110(1–2), 179–190.

    Google Scholar 

  • Chen, W. C., Xue, H. Z., Hsu, Y. L., Liu, Q., Patel, S., & Davis, R. L. (2011). Complex distribution patterns of voltage-gated calcium channel alpha-subunits in the spiral ganglion. Hearing Research, 278(1–2), 52–68.

    Google Scholar 

  • Ciuman, R. R. (2010). The efferent system or olivocochlear function bundle—fine regulator and protector of hearing perception. International Journal of Biomedical Science, 6(4), 276–288.

    Google Scholar 

  • Cleland, B. G., Dubin, M. W., & Levick, W. R. (1971). Sustained and transient neurones in the cat’s retina and lateral geniculate nucleus. The Journal of Physiology, 217(2), 473–496.

    Google Scholar 

  • Collingridge, G. L., Olsen, R. W., Peters, J., & Spedding, M. (2009). A nomenclature for ligand-gated ion channels. Neuropharmacology, 56(1), 2–5.

    Google Scholar 

  • Crozier, R. A., & Davis, R. L. (2014). Unmasking of spiral ganglion neuron firing dynamics by membrane potential and neurotrophin-3. The Journal of Neuroscience, 34(29), 9688–9702.

    Google Scholar 

  • Davis, R. L. (1996). Differential distribution of potassium channels in acutely demyelinated, primary-auditory neurons in vitro. Journal of Neurophysiology, 76(1), 438–447.

    Google Scholar 

  • Debanne, D., Campanac, E., Bialowas, A., Carlier, E., & Alcaraz, G. (2011). Axon physiology. Physiological Reviews, 91(2), 555–602.

    Google Scholar 

  • Despres, G., Leger, G. P., Dahl, D., & Romand, R. (1994). Distribution of cytoskeletal proteins (neurofilaments, peripherin and MAP-tau) in the cochlea of the human fetus. Acta Oto-Laryngologica, 114(4), 377–381.

    Google Scholar 

  • Dulon, D., Jagger, D. J., Lin, X., & Davis, R. L. (2006). Neuromodulation in the spiral ganglion: shaping signals from the organ of corti to the CNS. The Journal of Membrane Biology, 209(2–3), 167–175.

    Google Scholar 

  • Echteler, S. M., & Nofsinger, Y. C. (2000). Development of ganglion cell topography in the postnatal cochlea. The Journal of Comparative Neurology, 425(3), 436–446.

    Google Scholar 

  • Farinas, I., Jones, K. R., Tessarollo, L., Vigers, A. J., Huang, E., Kirstein, M., de Caprona, D. C., Coppola, V., Backus, C., Reichardt, L. F., & Fritzsch, B. (2001). Spatial shaping of cochlear innervation by temporally regulated neurotrophin expression. The Journal of Neuroscience, 21(16), 6170–6180.

    Google Scholar 

  • Fekete, D. M., Rouiller, E. M., Liberman, M. C., & Ryugo, D. K. (1984). The central projections of intracellularly labeled auditory nerve fibers in cats. The Journal of Comparative Neurology, 229(3), 432–450.

    Google Scholar 

  • Flores-Otero, J., & Davis, R. L. (2011). Synaptic proteins are tonotopically graded in postnatal and adult type I and type II spiral ganglion neurons. The Journal of Comparative Neurology, 519(8), 1455–1475.

    Google Scholar 

  • Flores-Otero, J., Xue, H. Z., & Davis, R. L. (2007). Reciprocal regulation of presynaptic and postsynaptic proteins in bipolar spiral ganglion neurons by neurotrophins. The Journal of Neuroscience, 27(51), 14023–14034.

    Google Scholar 

  • Furshpan, E. J., & Furukawa, T. (1962). Intracellular and extracellular responses of the several regions of the Mauthner cell of the goldfish. Journal of Neurophysiology, 25, 732–771.

    Google Scholar 

  • Garcia-Diaz, J. F. (1999). Development of a fast transient potassium current in chick cochlear ganglion neurons. Hearing Research, 135(1–2), 124–134.

    Google Scholar 

  • Gray, H., & Lewis, W. H. (1918). Anatomy of the human body (20th ed.). Philadelphia and New York: Lea & Febiger.

    Google Scholar 

  • Greenberg, M. E., Xu, B., Lu, B., & Hempstead, B. L. (2009). New insights in the biology of BDNF synthesis and release: Implications in CNS function. The Journal of Neuroscience, 29(41), 12764–12767.

    Google Scholar 

  • Grothe, B., Pecka, M., & McAlpine, D. (2010). Mechanisms of sound localization in mammals. Physiological Reviews, 90(3), 983–1012.

    Google Scholar 

  • Guinan, J. (2011). Physiology of the medial and lateral olivocochlear systems. In D. K. Ryugo & R. R. Fay (Eds.), Auditory and vestibular efferents (pp. 39–81). New York: Springer Science+Business Media.

    Google Scholar 

  • Hafidi, A. (1998). Peripherin-like immunoreactivity in type II spiral ganglion cell body and projections. Brain Research, 805(1–2), 181–190.

    Google Scholar 

  • Heffner, R., & Heffner, H. (1980). Hearing in the elephant (Elephas maximus). Science, 208(4443), 518–520.

    Google Scholar 

  • Held, H. (1926). Die Cochlea der Säuger und der Vögel, ihre Entwicklung und ihr Bau. In W. Buddenbrock, M. H. Fischer, M. Frey, K. Frisch, M. Gildemeister, A. Goldscheider, K. Grahe, H. Held, H. Henning, H. Herter, F. B. Hofmann, E. M. Hornbostel, L. Jost, A. Kleyn, W. Koehler, W. Kolmer, A. Kreidl, W. Kümmel, R. Magnus, E. Mangold, T. Masuda, H. Rhese, F. Rohrer, H. Runge, A. Seybold, H. Sierp, E. Skramlik, P. Stark, J. Teufer, E. Waetzmann, V. Weizsaecker & C. Zarniko (Eds.), Receptionsorgane I (pp. 467–534). Munich: J. F. Bergmann-Verlag.

    Google Scholar 

  • Hille, B. (2001). Ion channels of excitable membranes, 3rd ed. Sunderland, MA: Sinauer.

    Google Scholar 

  • Hodgkin, A. L., & Huxley, A. F. (1952). Currents carried by sodium and potassium ions through the membrane of the giant axon of Loligo. The Journal of Physiology, 116(4), 449–472.

    Google Scholar 

  • Hodgkin, A. L., Huxley, A. F., & Katz, B. (1952). Measurement of current-voltage relations in the membrane of the giant axon of Loligo. The Journal of Physiology, 116(4), 424–448.

    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, E. J., & Reichardt, L. F. (2001). Neurotrophins: Roles in neuronal development and function. Annual Review of Neuroscience, 24, 677–736.

    Google Scholar 

  • Johnston, D., Wu, S. M.-S., & Gray, R. (1995). Foundations of cellular neurophysiology. Cambridge, MA: MIT Press.

    Google Scholar 

  • Kanold, P. O., & Manis, P. B. (1999). Transient potassium currents regulate the discharge patterns of dorsal cochlear nucleus pyramidal cells. The Journal of Neuroscience, 19(6), 2195–2208.

    Google Scholar 

  • Keithley, E. M., & Schreiber, R. C. (1987). Frequency map of the spiral ganglion in the cat. Journal of the Acoustic Society of America, 81(4), 1036–1042.

    Google Scholar 

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

    Google Scholar 

  • Kiang, N. Y. (1990). Curious oddments of auditory-nerve studies. Hearing Research, 49(1–3), 1–16.

    Google Scholar 

  • Kim, Y. H., & Holt, J. R. (2013). Functional contributions of HCN channels in the primary auditory neurons of the mouse inner ear. Journal of General Physiology, 142(3), 207–223.

    Google Scholar 

  • Klein, M., & Kandel, E. R. (1980). Mechanism of calcium current modulation underlying presynaptic facilitation and behavioral sensitization in Aplysia. Proceedings of the National Academy of Sciences of the USA, 77(11), 6912–6916.

    Google Scholar 

  • Kojima, S. (1990). Comparison of auditory functions in the chimpanzee and human. Folia Primatologica (Basel), 55(2), 62–72.

    Google Scholar 

  • Langer, P., Grunder, S., & Rusch, A. (2003). Expression of Ca2+-activated BK channel mRNA and its splice variants in the rat cochlea. The Journal of Comparative Neurology, 455(2), 198–209.

    Google Scholar 

  • Lawson, S. N., & Waddell, P. J. (1991). Soma neurofilament immunoreactivity is related to cell size and fibre conduction velocity in rat primary sensory neurons. The Journal of Physiology, 435, 41–63.

    Google Scholar 

  • Leake, P. A., & Snyder, R. L. (1989). Topographic organization of the central projections of the spiral ganglion in cats. The Journal of Comparative Neurology, 281(4), 612–629.

    Google Scholar 

  • Levine, E. S., Dreyfus, C. F., Black, I. B., & Plummer, M. R. (1995). Brain-derived neurotrophic factor rapidly enhances synaptic transmission in hippocampal neurons via postsynaptic tyrosine kinase receptors. Proceedings of the National Academy of Sciences of the USA, 92(17), 8074–8077.

    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 

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

    Google Scholar 

  • Liberman, M. C., & Oliver, M. E. (1984). Morphometry of intracellularly labeled neurons of the auditory nerve: Correlations with functional properties. Journal of Comparative Neurology, 223(2), 163–176.

    Google Scholar 

  • Liberman, M. C., Dodds, L. W., & Pierce, S. (1990). Afferent and efferent innervation of the cat cochlea: Quantitative analysis with light and electron microscopy. The Journal of Comparative Neurology, 301(3), 443–460.

    Google Scholar 

  • Liu, Q., & Davis, R. L. (2007). Regional specification of threshold sensitivity and response time in CBA/CaJ mouse spiral ganglion neurons. Journal of Neurophysiology, 98(4), 2215–2222.

    Google Scholar 

  • Liu, Q., Manis, P. B., & Davis, R. L. (2014a). I and HCN channels in murine spiral ganglion neurons: Tonotopic variation, local heterogeneity, and kinetic model. Journal of the Association for Research in Otolaryngology, 15(4), 585–599.

    Google Scholar 

  • Liu, Q., Lee, E., & Davis, R. L. (2014b). Heterogeneous intrinsic excitability of murine spiral ganglion neurons is determined by Kv1 and HCN channels. Neuroscience, 257, 96–110.

    Google Scholar 

  • Liu, W., & Davis, R. L. (2014). Calretinin and calbindin distribution patterns specify subpopulations of type I and type II spiral ganglion neurons in postnatal murine cochlea. The Journal of Comparative Neurology, 522, 2299–2318.

    Google Scholar 

  • Loewenstein, W. R., & Mendelson, M. (1965). Components of receptor adaptation in a Pacinian corpuscle. The Journal of Physiology, 177, 377–397.

    Google Scholar 

  • Lopez, C. A., Olson, E. S., Adams, J. C., Mou, K., Denhardt, D. T., & Davis, R. L. (1995). Osteopontin expression detected in adult cochleae and inner ear fluids. Hearing Research, 85(1–2), 210–222.

    Google Scholar 

  • Lopez, I., Ishiyama, G., Acuna, D., Ishiyama, A., & Baloh, R. W. (2003). Immunolocalization of voltage-gated calcium channel alpha1 subunits in the chinchilla cochlea. Cell and Tissue Research, 313(2), 177–186.

    Google Scholar 

  • Luscher, H. R., & Shiner, J. S. (1990). Simulation of action potential propagation in complex terminal arborizations. Biophysical Journal, 58(6), 1389–1399.

    Google Scholar 

  • Lv, P., Wei, D., & Yamoah, E. N. (2010). Kv7–type channel currents in spiral ganglion neurons: Involvement in sensorineural hearing loss. Journal of Biological Chemistry, 285(45), 34699–34707.

    Google Scholar 

  • Lv, P., Sihn, C. R., Wang, W., Shen, H., Kim, H. J., Rocha-Sanchez, S. M., & Yamoah, E. N. (2012). Posthearing Ca(2+) currents and their roles in shaping the different modes of firing of spiral ganglion neurons. The Journal of Neuroscience, 32(46), 16314–16330.

    Google Scholar 

  • Mason, W. T., & Leng, G. (1984). Complex action potential waveform recorded from supraoptic and paraventricular neurones of the rat: Evidence for sodium and calcium spike components at different membrane sites. Experimental Brain Research, 56(1), 135–143.

    Google Scholar 

  • McCormick, D. A., Connors, B. W., Lighthall, J. W., & Prince, D. A. (1985). Comparative electrophysiology of pyramidal and sparsely spiny stellate neurons of the neocortex. Journal of Neurophysiology, 54(4), 782–806.

    Google Scholar 

  • Merchan-Perez, A., & Liberman, M. C. (1996). Ultrastructural differences among afferent synapses on cochlear hair cells: Correlations with spontaneous discharge rate. The 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 

  • Mo, Z. L., & Davis, R. L. (1997a). Heterogeneous voltage dependence of inward rectifier currents in spiral ganglion neurons. Journal of Neurophysiology, 78(6), 3019–3027.

    Google Scholar 

  • Mo, Z. L., & Davis, R. L. (1997b). Endogenous firing patterns of murine spiral ganglion neurons. Journal of Neurophysiology, 77(3), 1294–1305.

    Google Scholar 

  • Mo, Z. L., Adamson, C. L., & Davis, R. L. (2002). Dendrotoxin-sensitive K(+) currents contribute to accommodation in murine spiral ganglion neurons. The Journal of Physiology, 542(Pt 3), 763–778.

    Google Scholar 

  • Mou, K., Adamson, C. L., & Davis, R. L. (1998). Time-dependence and cell-type specificity of synergistic neurotrophin actions on spiral ganglion neurons. The Journal of Comparative Neurology, 402(1), 129–139.

    Google Scholar 

  • Mountcastle, V. B., Talbot, W. H., & Kornhuber, H. H. (1966). The neural transformation of mechanical stimuli delivered to the monkey’s hand. In Ciba Foundation Symposium: Hormonal Factors in Carbohydrate Metabolism (Colloquia on Endocrinology) (pp. 325–351). Chichester, UK: John Wiley & Sons.

    Google Scholar 

  • Muller, M., von Hunerbein, K., Hoidis, S., & Smolders, J. W. (2005). A physiological place-frequency map of the cochlea in the CBA/J mouse. Hearing Research, 202(1–2), 63–73.

    Google Scholar 

  • Nadol, J. B., Jr. (1988). Comparative anatomy of the cochlea and auditory nerve in mammals. Hearing Research, 34(3), 253–266.

    Google Scholar 

  • Nadol, J. B., Jr., Burgess, B. J., & Reisser, C. (1990). Morphometric analysis of normal human spiral ganglion cells. Annals of Otology, Rhinology, and Laryngology, 99(5 Pt 1), 340–348.

    Google Scholar 

  • Orduz, D., Bischop, D. P., Schwaller, B., Schiffmann, S. N., & Gall, D. (2013). Parvalbumin tunes spike-timing and efferent short-term plasticity in striatal fast spiking interneurons. The Journal of Physiology, 591(Pt 13), 3215–3232.

    Google Scholar 

  • Peles, E., Nativ, M., Lustig, M., Grumet, M., Schilling, J., Martinez, R., Plowman, G. D., & Schlessinger, J. (1997). Identification of a novel contactin-associated transmembrane receptor with multiple domains implicated in protein-protein interactions. EMBO Journal, 16(5), 978–988.

    Google Scholar 

  • Perkins, R. E., & Morest, D. K. (1975). A study of cochlear innervation patterns in cats and rats with the Golgi method and Nomarkski optics. The Journal of Comparative Neurology, 163(2), 129–158.

    Google Scholar 

  • Puopolo, M., Raviola, E., & Bean, B. P. (2007). Roles of subthreshold calcium current and sodium current in spontaneous firing of mouse midbrain dopamine neurons. The Journal of Neuroscience, 27(3), 645–656.

    Google Scholar 

  • Rasband, M. N., & Trimmer, J. S. (2001). Developmental clustering of ion channels at and near the node of Ranvier. Developmental Biology, 236(1), 5–16.

    Google Scholar 

  • Reid, M. A., Flores-Otero, J., & Davis, R. L. (2004). Firing patterns of type II spiral ganglion neurons in vitro. The Journal of Neuroscience, 24(3), 733–742.

    Google Scholar 

  • Robertson, D. (1976). Possible relation between structure and spike shapes of neurones in guinea pig cochlear ganglion. Brain Research, 109(3), 487–496.

    Google Scholar 

  • Rosenblatt, K. P., Sun, Z. P., Heller, S., & Hudspeth, A. J. (1997). Distribution of Ca2+-activated K+ channel isoforms along the tonotopic gradient of the chicken’s cochlea. Neuron, 19(5), 1061–1075.

    Google Scholar 

  • Rosenbluth, J. (1962). The fine structure of acoustic ganglia in the rat. Journal of Cell Biology, 12, 329–359.

    Google Scholar 

  • Rosowski, J. J. (1991). The effects of external- and middle-ear filtering on auditory threshold and noise-induced hearing loss. Journal of the Acoustic Society of America, 90(1), 124–135.

    Google Scholar 

  • Rubel, E. W., & Fritzsch, B. (2002). Auditory system development: primary auditory neurons and their targets. Annual Review of Neuroscience, 25, 51–101

    Google Scholar 

  • Ruggero, M. A., & Temchin, A. N. (2002). The roles of the external, middle, and inner ears in determining the bandwidth of hearing. Proceedings of the National Academy of Sciences of the USA, 99(20), 13206–13210.

    Google Scholar 

  • Rusznak, Z., & Szucs, G. (2009). Spiral ganglion neurones: An overview of morphology, firing behaviour, ionic channels and function. Pflugers Archiv—European Journal of Physiology, 457(6), 1303–1325.

    Google Scholar 

  • Ryugo, D. (1992). The auditory nerve: Peripheral innervation, cell body morphology, and central projections. In D. Webster, A. Popper, & R. Fay (Eds.), The mammalian auditory pathway: Neuroanatomy (pp. 23–65). New York: Springer-Verlag.

    Google Scholar 

  • Safieddine, S., & Eybalin, M. (1992). Triple immunofluorescence evidence for the coexistence of acetylcholine, enkephalins and calcitonin gene-related peptide within efferent (olivocochlear) neurons of rats and guinea-pigs. European Journal of Neuroscience, 4(10), 981–992.

    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 

  • Schwaller, B., Meyer, M., & Schiffmann, S. (2002). ‘New’ functions for ‘old’ proteins: The role of the calcium-binding proteins calbindin D-28k, calretinin and parvalbumin, in cerebellar physiology. Studies with knockout mice. Cerebellum, 1(4), 241–258.

    Google Scholar 

  • Shibata, R., Nakahira, K., Shibasaki, K., Wakazono, Y., Imoto, K., & Ikenaka, K. (2000). A-type K+ current mediated by the Kv4 channel regulates the generation of action potential in developing cerebellar granule cells. The Journal of Neuroscience, 20(11), 4145–4155.

    Google Scholar 

  • Simmons, D., Duncan, J., de Caprona, D. C., & Fritzsch, B. (2011). Development of the inner ear efferent system. In D. K. Ryugo, R. R. Fay, & A. N. Popper (Eds.), Auditory and vestibular efferents (pp. 187–216). New York: Springer Science+Business Media.

    Google Scholar 

  • Spoendlin, H. (1973). The innervation of the cochlear receptor. In A.R. Møller (Ed.), Basic mechanisms in hearing (pp. 185–234). New York: Academic Press.

    Google Scholar 

  • Spoendlin, H., & Schrott, A. (1989). Analysis of the human auditory nerve. Hearing Research, 43(1), 25–38.

    Google Scholar 

  • Sudhof, T. C., Lottspeich, F., Greengard, P., Mehl, E., & Jahn, R. (1987). A synaptic vesicle protein with a novel cytoplasmic domain and four transmembrane regions. Science, 238(4830), 1142–1144.

    Google Scholar 

  • Sugawara, M., Murtie, J. C., Stankovic, K. M., Liberman, M. C., & Corfas, G. (2007). Dynamic patterns of neurotrophin 3 expression in the postnatal mouse inner ear. The Journal of Comparative Neurology, 501(1), 30–37.

    Google Scholar 

  • Sundgren-Andersson, A. K., & Johansson, S. (1998). Calcium spikes and calcium currents in neurons from the medial preoptic nucleus of rat. Brain Research, 783(2), 194–209.

    Google Scholar 

  • Szabo, Z. S., Harasztosi, C. S., Sziklai, I., Szucs, G., & Rusznak, Z. (2002). Ionic currents determining the membrane characteristics of type I spiral ganglion neurons of the guinea pig. European Journal of Neuroscience, 16(10), 1887–1895.

    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 

  • Thiers, F. A., Nadol, J. B., Jr., & Liberman, M. C. (2008). Reciprocal synapses between outer hair cells and their afferent terminals: Evidence for a local neural network in the mammalian cochlea. Journal of the Association for Research in Otolaryngology, 9(4), 477–489.

    Google Scholar 

  • Verheugen, J. A., Fricker, D., & Miles, R. (1999). Noninvasive measurements of the membrane potential and GABAergic action in hippocampal interneurons. The Journal of Neuroscience, 19(7), 2546–2555.

    Google Scholar 

  • Weisz, C. J., Glowatzki, E., & Fuchs, P. A. (2014). Excitability of type II cochlear afferents. The Journal of Neuroscience, 34(6), 2365–2373.

    Google Scholar 

  • Whitlon, D. S., Ketels, K. V., Coulson, M. T., Williams, T., Grover, M., Edpao, W., & Richter, C. P. (2006). Survival and morphology of auditory neurons in dissociated cultures of newborn mouse spiral ganglion. Neuroscience, 138(2), 653–662.

    Google Scholar 

  • Yamaguchi, K., & Ohmori, H. (1990). Voltage-gated and chemically gated ionic channels in the cultured cochlear ganglion neurone of the chick. The Journal of Physiology, 420, 185–206.

    Google Scholar 

  • Yang, Y. M., & Wang, L. Y. (2006). Amplitude and kinetics of action potential-evoked Ca2+ current and its efficacy in triggering transmitter release at the developing calyx of held synapse. The Journal of Neuroscience, 26(21), 5698–5708.

    Google Scholar 

  • Zhou, Z., Liu, Q., & Davis, R. L. (2005). Complex regulation of spiral ganglion neuron firing patterns by neurotrophin-3. The Journal of Neuroscience, 25(33), 7558–7566.

    Google Scholar 

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Acknowledgments

We thank Dr. Mark R. Plummer for discussions and a critical reading of the manuscript. This work is supported by NIH NIDCD RO1 DC01856.

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Correspondence to Robin L. Davis .

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Davis, R.L., Crozier, R.A. (2016). The Electrophysiological Signature of Spiral Ganglion Neurons. 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_4

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