Structures, Mechanisms, and Energetics in Temporal Processing

Chapter
Part of the Springer Handbook of Auditory Research book series (SHAR, volume 50)

Abstract

The ability of mammals to discriminate which ear is the first to receive acoustic stimuli with a resolution of approximately 10 μS is remarkable. It requires precise detection of the acoustic signal by the inner ear and equally precise communication and refinement of the information through at least three synapses prior to dichotic integration in the superior olive. The Jeffress place theory for sound localization was introduced in 1948 and remains a touchstone for research in the area. At its heart are assumptions about the ability of the auditory system to detect, transmit, and process temporal information. More than a half century of research has established that rapid processing of acoustic information in hair cells and brain stem auditory neurons is achieved with surprisingly similar mechanisms having high metabolic demands. Short electrical time constants are required for rapid temporal processing. Hair cells and auditory brain stem neurons have a high conductance at their resting potential that contributes to short time constants, but at the same time leads to large resting currents that have high metabolic demands. The membrane proteins that modulate these currents have a shallow, nonuniform, voltage dependence that results in a broad dynamic range, and further increases metabolic demand. High-speed performance is energetically costly, as is the case with automobiles, and provides the rationale for the high metabolic activity associated with auditory structures. Energetic considerations provide a conceptual bridge between the peripheral and brain stem auditory system.

Keywords

Cholesterol Permeability Depression Pyridine Retina 

Notes

Acknowledgments

This work was supported by the Baylor College of Medicine Jake and Nina Kamin Chair of Otorhinolaryngology and Communicative Sciences and NIH/NIDCD grants R01 DC000354 and DC002775 (WEB) and the Univeristy of North Carolina at Chapel Hill Thomas J. Dark Distinguished Research Professorship and NIH/NIDCD grants R01 DC004551 and DC009809 (PBM).

References

  1. Adams, P. R., Brown, D. A., & Constanti, A. (1982). M-currents and other potassium currents in bullfrog sympathetic neurones. The Journal of Physiology, 330, 537–572.PubMedCentralPubMedGoogle Scholar
  2. Adamson, C. L., Reid, M. A., Mo, Z. L., Bowne-English, J., & Davis, R. L. (2002). Firing features and potassium channel content of murine spiral ganglion neurons vary with cochlear location. The Journal of Comparative Neurology, 447(4), 331–350.PubMedGoogle Scholar
  3. Ashida, G., & Carr, C. E. (2010). Effect of sampling frequency on the measurement of phase-locked action potentials. Frontiers in Neuroscience, 4(100), 1–9.Google Scholar
  4. Ashmore, J. (2008). Cochlear outer hair cell motility. Physiological Review, 88(1), 173–210.Google Scholar
  5. Ashmore, J., Avan, P., Brownell, W. E., Dallos, P., Dierkes, K., Fettiplace, R., Grosh, K., Hackney, C. M., Hudspeth, A. J., Julicher, F., Lindner, B., Martin, P., Meaud, J., Petit, C., Santos-Sacchi, J., & Canlon, B. (2010). The remarkable cochlear amplifier. Hearing Research, 266(1–2), 1–17.PubMedGoogle Scholar
  6. Ashmore, J. F. (1987). A fast motile response in guinea-pig outer hair cells: The cellular basis of the cochlear amplifier. The Journal of Physiology, 388, 323–347.PubMedCentralPubMedGoogle Scholar
  7. Ashmore, J. F., & Brownell, W. E. (1986). Kilohertz movements induced by electrical stimulation in outer hair cells isolated from the guinea pig cochlea. The Journal of Physiology, 376, 49P.Google Scholar
  8. Attwell, D., & Laughlin, S. B. (2001). An energy budget for signaling in the grey matter of the brain. Journal of Cerebral Blood Flow and Metabolism, 21(10), 1133–1145.PubMedGoogle Scholar
  9. Avissar, M., Furman, A. C., Saunders, J. C., & Parsons, T. D. (2007). Adaptation reduces spike-count reliability, but not spike-timing precision, of auditory nerve responses. The Journal of Neuroscience, 27(24), 6461–6472.PubMedGoogle Scholar
  10. Bal, R., & Oertel, D. (2001). Potassium currents in octopus cells of the mammalian cochlear nucleus. Journal of Neurophysiology, 86(5), 2299–2311.PubMedGoogle Scholar
  11. Bal, R., Baydas, G., & Naziroglu, M. (2009). Electrophysiological properties of ventral cochlear nucleus neurons of the dog. Hearing Research, 256(1–2), 93–103.PubMedGoogle Scholar
  12. Barela, A. J., Waddy, S. P., Lickfett, J. G., Hunter, J., Anido, A., Helmers, S. L., Goldin, A. L., & Escayg, A. (2006). An epilepsy mutation in the sodium channel SCN1A that decreases channel excitability. The Journal of Neuroscience, 26(10), 2714–2723.PubMedGoogle Scholar
  13. Baylor, D. A., Matthews, G., & Nunn, B. J. (1984). Location and function of voltage-sensitive conductances in retinal rods of the salamander, Ambystoma tigrinum. The Journal of Physiology, 354, 203–223.PubMedCentralPubMedGoogle Scholar
  14. Beisel, K. W., Nelson, N. C., Delimont, D. C., & Fritzsch, B. (2000). Longitudinal gradients of KCNQ4 expression in spiral ganglion and cochlear hair cells correlate with progressive hearing loss in DFNA2. Brain Research. Molecular Brain Research, 82(1–2), 137–149.PubMedGoogle Scholar
  15. 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.PubMedGoogle Scholar
  16. Békésy, G. von (1952). DC resting potentials inside the cochlear partition. Journal Acoustical Society of America, 24(1), 72–76.Google Scholar
  17. Borst, J. G., & Soria van Hoeve, J. (2012). The calyx of held synapse: From model synapse to auditory relay. Annual Review of Physiology, 74, 199–224.PubMedGoogle Scholar
  18. Bourk, T. R. (1976). Electrical responses of neural units in the anteroventral cochlear nucleus of the cat. Ph.D. dissertation, Massachusetts Institute of Technology.Google Scholar
  19. Brand, A., Behrend, O., Marquardt, T., McAlpine, D., & Grothe, B. (2002). Precise inhibition is essential for microsecond interaural time difference coding. Nature, 417(6888), 543–547.PubMedGoogle Scholar
  20. Breneman, K. D., Brownell, W. E., & Rabbitt, R. D. (2009). Hair cell bundles: Flexoelectric motors of the inner ear. PLoS One, 4(4), e5201.PubMedCentralPubMedGoogle Scholar
  21. Brownell, W. E. (1975). Organization of the cat trapezoid body and the discharge characteristics of its fibers. Brain Research, 94(3), 413–433.PubMedGoogle Scholar
  22. Brownell, W. E. (1982). Cochlear transduction: An integrative model and review. Hearing Research, 6(3), 335–360.PubMedCentralPubMedGoogle Scholar
  23. Brownell, W. E. (1983). Observations on a motile response in isolated outer hair cells. In W. R. Webster & L. M. Aitken (Eds.), Mechanisms of hearing (pp. 5–10). Monash: Monash University Press.Google Scholar
  24. Brownell, W. E. (1984). Microscopic observation of cochlear hair cell motility. Scanning Electron Microscopy(Pt 3), 1401–1406.Google Scholar
  25. Brownell, W. E. (1990). Outer hair cell electromotility and otoacoustic emissions. Ear and Hearing, 11(2), 82–92.PubMedCentralPubMedGoogle Scholar
  26. Brownell, W. E. (2006). The piezoelectric outer hair cell. In R. A. Eatock, R. R. Fay, & A. N. Popper (Eds.), Vertebrate hair cells (pp. 313–347). New York: Springer Science+Business Media.Google Scholar
  27. Brownell, W. E., & Kachar, B. (1986). Outer hair cell motility: A possible electro-kinetic mechanism. In J. B. Allen, J. L. Hall, A. E. Hubbard, S. T. Neely & A. Tubis (Eds.), Peripheral auditory mechanisms (pp. 369–376).New York: Springer-Verlag.Google Scholar
  28. Brownell, W. E., Zidanic, M., & Spirou, G. A. (1986). Standing currents and their modulation in the Cochlea. In R. A. Altschuler, D. W. Hoffman, & R. P. Bobbin (Eds.), Neurobiology of hearing: The cochlea (pp. 91–107). New York: Raven Press.Google Scholar
  29. Brownell, W. E., Manis, P. B., Zidanic, M., & Spirou, G. A. (1983). Acoustically evoked radial current densities in scala tympani. Journal Acoustical Society of America, 74(3), 792–800.Google Scholar
  30. Brownell, W. E., Bader, C. R., Bertrand, D., & de Ribaupierre, Y. (1985). Evoked mechanical responses of isolated cochlear outer hair cells. Science, 227(4683), 194–196.PubMedGoogle Scholar
  31. Brownell, W. E., Qian, F., & Anvari, B. (2010). Cell membrane tethers generate mechanical force in response to electrical stimulation. Biophysical Journal, 99(3), 845–852.PubMedCentralPubMedGoogle Scholar
  32. Brownell, W. E., Jacob, S., Hakizimana, P., Ulfendahl, M., & Fridberger, A. (2011). Membrane cholesterol modulates cochlear electromechanics. Pflugers Archive: European Journal of Physiology, 461(6), 677–686.Google Scholar
  33. Cant, N. B., & Morest, D. K. (1979). The bushy cells in the anteroventral cochlear nucleus of the cat. A study with the electron microscope. Neuroscience, 4(12), 1925–1945.Google Scholar
  34. Cao, X. J., & Oertel, D. (2011). The magnitudes of hyperpolarization-activated and low-voltage-activated potassium currents co-vary in neurons of the ventral cochlear nucleus. Journal of Neurophysiology, 106(2), 630–640.PubMedCentralPubMedGoogle Scholar
  35. Cao, X. J., Shatadal, S., & Oertel, D. (2007). Voltage-sensitive conductances of bushy cells of the mammalian ventral cochlear nucleus. Journal of Neurophysiology, 97(6), 3961–3975.PubMedGoogle Scholar
  36. Carlyon, R. P., Long, C. J., & Micheyl, C. (2012). Across-channel timing differences as a potential code for the frequency of pure tones. Journal of the Association for Research in Otolaryngology: JARO, 13(2), 159–171.Google Scholar
  37. Carney, L. H. (1990). Sensitivities of cells in anteroventral cochlear nucleus of cat to spatiotemporal discharge patterns across primary afferents. Journal of Neurophysiology, 64(2), 437–456.PubMedGoogle Scholar
  38. Caspary, D. M., Backoff, P. M., Finlayson, P. G., & Palombi, P. S. (1994). Inhibitory inputs modulate discharge rate within frequency receptive fields of anteroventral cochlear nucleus neurons. Journal of Neurophysiology, 72(5), 2124–2133.PubMedGoogle Scholar
  39. Chambard, J. M., & Ashmore, J. F. (2005). Regulation of the voltage-gated potassium channel KCNQ4 in the auditory pathway. Pflugers Archive: European Journal of Physiology, 450(1), 34–44.Google Scholar
  40. Chertoff, M. E., & Brownell, W. E. (1994). Characterization of cochlear outer hair cell turgor. American Journal of Physiology, 266(2 Pt 1), C467–479.PubMedGoogle Scholar
  41. Chirila, F. V., Rowland, K. C., Thompson, J. M., & Spirou, G. A. (2007). Development of gerbil medial superior olive: Integration of temporally delayed excitation and inhibition at physiological temperature. The Journal of Physiology, 584(Pt 1), 167–190.PubMedCentralPubMedGoogle Scholar
  42. Corbitt, C., Farinelli, F., Brownell, W. E., & Farrell, B. (2012). Tonotopic relationships reveal the charge density varies along the lateral wall of outer hair cells. Biophysical Journal, 102(12), 2715–2724.PubMedCentralPubMedGoogle Scholar
  43. Dallos, P., Popper, A. N., & Fay, R. R. (Eds.). (1996). The cochlea (Vol. 8). New York: Springer-Verlag.Google Scholar
  44. Davis, H. (1983). An active process in cochlear mechanics. Hearing Research, 9(1), 79–90.PubMedGoogle Scholar
  45. Davis, H., Tasaki, I., & Goldstein, R. (1952). The peripheral origin of activity, with reference to the ear. Cold Spring Harbor Symposium Quantitative Biology, 17, 143–154.Google Scholar
  46. Dieler, R., Shehata-Dieler, W. E., & Brownell, W. E. (1991). Concomitant salicylate-induced alterations of outer hair cell subsurface cisternae and electromotility. Journal of Neurocytology, 20(8), 637–653.PubMedGoogle Scholar
  47. Evans, B. N. (1990). Fatal contractions: ultrastructural and electromechanical changes in outer hair cells following transmembraneous electrical stimulation. Hearing Research, 45(3), 265–282.PubMedGoogle Scholar
  48. Francis, H. W., & Manis, P. B. (2000). Effects of deafferentation on the electrophysiology of ventral cochlear nucleus neurons. Hearing Research, 149(1–2), 91–105.PubMedGoogle Scholar
  49. Frank, G., Hemmert, W., & Gummer, A. W. (1999). Limiting dynamics of high-frequency electromechanical transduction of outer hair cells. Proceedings of the National Academy of Sciences of the USA, 96(8), 4420–4425.PubMedCentralPubMedGoogle Scholar
  50. Friauf, E., & Ostwald, J. (1988). Divergent projections of physiologically characterized rat ventral cochlear nucleus neurons as shown by intra-axonal injection of horseradish peroxidase. Experimental Brain Research, 73(2), 263–284.PubMedGoogle Scholar
  51. Fukui, I., & Ohmori, H. (2004). Tonotopic gradients of membrane and synaptic properties for neurons of the chicken nucleus magnocellularis. The Journal of Neuroscience, 24(34), 7514–7523.PubMedGoogle Scholar
  52. Gai, Y., & Carney, L. H. (2008). Influence of inhibitory inputs on rate and timing of responses in the anteroventral cochlear nucleus. Journal of Neurophysiology, 99(3), 1077–1095.PubMedCentralPubMedGoogle Scholar
  53. Gardner, S. M., Trussell, L. O., & Oertel, D. (1999). Time course and permeation of synaptic AMPA receptors in cochlear nuclear neurons correlate with input. The Journal of Neuroscience, 19(20), 8721–8729.PubMedGoogle Scholar
  54. Geiger, J. R., Melcher, T., Koh, D. S., Sakmann, B., Seeburg, P. H., Jonas, P., & Monyer, H. (1995). Relative abundance of subunit mRNAs determines gating and Ca2+ permeability of AMPA receptors in principal neurons and interneurons in rat CNS. Neuron, 15(1), 193–204.PubMedGoogle Scholar
  55. Ghaffari, R., Aranyosi, A. J., & Freeman, D. M. (2007). Longitudinally propagating traveling waves of the mammalian tectorial membrane. Proceedings of the National Academy of Sciences of the USA, 104(42), 16510–16515.PubMedCentralPubMedGoogle Scholar
  56. Gittelman, J. X., & Tempel, B. L. (2006). Kv1.1–containing channels are critical for temporal precision during spike initiation. Journal of Neurophysiology, 96(3), 1203–1214.PubMedGoogle Scholar
  57. Glowatzki, E., & Fuchs, P. A. (2002). Transmitter release at the hair cell ribbon synapse. Nature Neuroscience, 5(2), 147–154.PubMedGoogle Scholar
  58. Gold, T. (1948). Hearing. II. The physical basis of the action of the cochlea. Proceedings of the Royal Society London B: Biological Science, 135, 492–498.Google Scholar
  59. Goldberg, J. M., & Brown, P. B. (1969). Response of binaural neurons of dog superior olivary complex to dichotic tonal stimuli: some physiological mechanisms of sound localization. Journal of Neurophysiology, 32(4), 613–636.PubMedGoogle Scholar
  60. Goldberg, J. M., & Brownell, W. E. (1973). Discharge characteristics of neurons in anteroventral and dorsal cochlear nuclei of cat. Brain Research, 64, 35–54.PubMedGoogle Scholar
  61. Gomez-Nieto, R., & Rubio, M. E. (2011). Ultrastructure, synaptic organization, and molecular components of bushy cell networks in the anteroventral cochlear nucleus of the rhesus monkey. Neuroscience, 179, 188–207.PubMedCentralPubMedGoogle Scholar
  62. Guinan, J. J., Jr., & Li, R. Y. (1990). Signal processing in brainstem auditory neurons which receive giant endings (calyces of Held) in the medial nucleus of the trapezoid body of the cat. Hearing Research, 49(1–3), 321–334.PubMedGoogle Scholar
  63. Gulley, R. L., Landis, D. M., & Reese, T. S. (1978). Internal organization of membranes at end bulbs of Held in the anteroventral cochlear nucleus. The Journal of Comparative Neurology, 180(4), 707–741.PubMedGoogle Scholar
  64. Hackett, J. T., Jackson, H., & Rubel, E. W. (1982). Synaptic excitation of the second and third order auditory neurons in the avian brain stem. Neuroscience, 7(6), 1455–1469.PubMedGoogle Scholar
  65. Hagins, W. A., Penn, R. D., & Yoshikami, S. (1970). Dark current and photocurrent in retinal rods. Biophysical Journal, 10(5), 380–412.PubMedCentralPubMedGoogle Scholar
  66. Hakizimana, P., Brownell, W. E., Jacob, S., & Fridberger, A. (2012). Sound-induced length changes in outer hair cell stereocilia. Nature Communications, 3(1094), 10 pages.Google Scholar
  67. Hallermann, S., de Kock, C. P., Stuart, G. J., & Kole, M. H. (2012). State and location dependence of action potential metabolic cost in cortical pyramidal neurons. Nature Neuroscience, 15(7), 1007–1014.PubMedGoogle Scholar
  68. Hallworth, R., & Jensen-Smith, H. (2008). The morphological specializations and electromotility of the mammalian outer hair cell. In G. A. Manley, R. R. Fay, & A. N. Popper (Eds.), Active processes and otoacoustic emissions (Vol. 30, pp. 145–189). New York: Springer Science+Business Media.Google Scholar
  69. Heinz, M. G., Colburn, H. S., & Carney, L. H. (2001). Rate and timing cues associated with the cochlear amplifier: level discrimination based on monaural cross-frequency coincidence detection. The Journal of the Acoustical Society of America, 110(4), 2065–2084.PubMedGoogle Scholar
  70. Henkel, C. K., & Brunso-Bechtold, J. K. (1990). Dendritic morphology and development in the ferret medial superior olivary nucleus. The Journal of Comparative Neurology, 294(3), 377–388.PubMedGoogle Scholar
  71. Hestrin, S. (1992). Developmental regulation of NMDA receptor-mediated synaptic currents at a central synapse. Nature, 357(6380), 686–689.PubMedGoogle Scholar
  72. Holt, A. G., Asako, M., Duncan, R. K., Lomax, C. A., Juiz, J. M., & Altschuler, R. A. (2006). Deafness associated changes in expression of two-pore domain potassium channels in the rat cochlear nucleus. [Research Support, N.I.H., Extramural]. Hearing Research, 216–217, 146–153.PubMedGoogle Scholar
  73. Housley, G. D., & Ashmore, J. F. (1992). Ionic currents of outer hair cells isolated from the guinea-pig cochlea. [Research Support, Non-U.S. Gov’t]. The Journal of Physiology, 448, 73–98.Google Scholar
  74. Huang, H., & Trussell, L. O. (2011). KCNQ5 channels control resting properties and release probability of a synapse. Nature Neuroscience, 14(7), 840–847.PubMedCentralPubMedGoogle Scholar
  75. Isaacson, J. S., & Walmsley, B. (1996). Amplitude and time course of spontaneous and evoked excitatory postsynaptic currents in bushy cells of the anteroventral cochlear nucleus. Journal of Neurophysiology, 76(3), 1566–1571.PubMedGoogle Scholar
  76. Jeffress, L. A. (1948). A place theory of sound localization. Journal of Comparative and Physiological Psychology, 41(1), 35–39.PubMedGoogle Scholar
  77. Johnson, D. H. (1980). The relationship between spike rate and synchrony in responses of auditory-nerve fibers to single tones. Journal Acoustical Society of America, 68(4), 1115–1122.Google Scholar
  78. Johnson, S. L., Beurg, M., Marcotti, W., & Fettiplace, R. (2011). Prestin-driven cochlear amplification is not limited by the outer hair cell membrane time constant. Neuron, 70(6), 1143–1154.PubMedCentralPubMedGoogle Scholar
  79. Joris, P. X., Smith, P. H., & Yin, T. C. (1994a). Enhancement of neural synchronization in the anteroventral cochlear nucleus. II. Responses in the tuning curve tail. Journal of Neurophysiology, 71(3), 1037–1051.PubMedGoogle Scholar
  80. Joris, P. X., Carney, L. H., Smith, P. H., & Yin, T. C. (1994b). Enhancement of neural synchronization in the anteroventral cochlear nucleus. I. Responses to tones at the characteristic frequency. Journal of Neurophysiology, 71(3), 1022–1036.PubMedGoogle Scholar
  81. Kachar, B., Brownell, W. E., Altschuler, R., & Fex, J. (1986). Electrokinetic shape changes of cochlear outer hair cells. Nature, 322(6077), 365–368.PubMedGoogle Scholar
  82. Kemp, D. T. (1978). Stimulated acoustic emissions from within the human auditory system. Journal Acoustical Society of America, 64(5), 1386–1391.Google Scholar
  83. Khatibzadeh, N., Gupta, S., Farrell, B., Brownell, W. E., & Anvari, B. (2012). Effects of cholesterol on nano-mechanical properties of the living cell plasma membrane. Soft Matter, 8(32), 8350–8360.PubMedCentralPubMedGoogle Scholar
  84. Khurana, S., Liu, Z., Lewis, A. S., Rosa, K., Chetkovich, D., & Golding, N. L. (2012). An essential role for modulation of hyperpolarization-activated current in the development of binaural temporal precision. The Journal of Neuroscience, 32(8), 2814–2823.PubMedCentralPubMedGoogle Scholar
  85. Kiang, N. Y., Watanabe, T., Thomas, E. C., & Clark, L. F. (1962). Stimulus coding in the cat’s auditory nerve. Preliminary report. Transactions of the American Otological Society, 50, 264–283.PubMedGoogle Scholar
  86. Kim, J. H., Kushmerick, C., & von Gersdorff, H. (2010). Presynaptic resurgent Na+ currents sculpt the action potential waveform and increase firing reliability at a CNS nerve terminal. The Journal of Neuroscience, 30(46), 15479–15490.PubMedCentralPubMedGoogle Scholar
  87. Kopp-Scheinpflug, C., Dehmel, S., Dorrscheidt, G. J., & Rubsamen, R. (2002). Interaction of excitation and inhibition in anteroventral cochlear nucleus neurons that receive large endbulb synaptic endings. The Journal of Neuroscience, 22(24), 11004–11018.PubMedGoogle Scholar
  88. Kopp-Scheinpflug, C., Steinert, J. R., & Forsythe, I. D. (2011). Modulation and control of synaptic transmission across the MNTB. Hearing Research, 279(1–2), 22–31.PubMedGoogle Scholar
  89. Koppl, C. (1997). Phase locking to high frequencies in the auditory nerve and cochlear nucleus magnocellularis of the barn owl, Tyto alba. The Journal of Neuroscience, 17(9), 3312–3321.PubMedGoogle Scholar
  90. Kossl, M., & Vater, M. (1989). Noradrenaline enhances temporal auditory contrast and neuronal timing precision in the cochlear nucleus of the mustached bat. The Journal of Neuroscience, 9(12), 4169–4178.PubMedGoogle Scholar
  91. Koyano, K., Funabiki, K., & Ohmori, H. (1996). Voltage-gated ionic currents and their roles in timing coding in auditory neurons of the nucleus magnocellularis of the chick. Neuroscience Research, 26(1), 29–45.PubMedGoogle Scholar
  92. Kros, C. J., & Crawford, A. C. (1990). Potassium currents in inner hair cells isolated from the guinea-pig cochlea. The Journal of Physiology, 421, 263–291.PubMedCentralPubMedGoogle Scholar
  93. Kuwabara, N., & Zook, J. M. (1991). Classification of the principal cells of the medial nucleus of the trapezoid body. The Journal of Comparative Neurology, 314(4), 707–720.PubMedGoogle Scholar
  94. Leao, R. N., Leao, R. M., da Costa, L. F., Rock Levinson, S., & Walmsley, B. (2008). A novel role for MNTB neuron dendrites in regulating action potential amplitude and cell excitability during repetitive firing. The European Journal of Neuroscience, 27(12), 3095–3108.PubMedGoogle Scholar
  95. Levic, S., & Yamoah, E. N. (2011). Plasticity in membrane cholesterol contributes toward electrical maturation of hearing. The Journal of Biological Chemistry, 286(7), 5768–5773.PubMedCentralPubMedGoogle Scholar
  96. Liberman, M. C. (1991). Central projections of auditory-nerve fibers of differing spontaneous rate. I. Anteroventral cochlear nucleus. The Journal of Comparative Neurology, 313(2), 240–258.PubMedGoogle Scholar
  97. Lin, K. H., Oleskevich, S., & Taschenberger, H. (2011). Presynaptic Ca2+ influx and vesicle exocytosis at the mouse endbulb of Held: a comparison of two auditory nerve terminals. The Journal of Physiology, 589(Pt 17), 4301–4320.PubMedCentralPubMedGoogle Scholar
  98. Lorente de Nó, R. (1981). The primary acoustic nuclei. New York: Raven Press.Google Scholar
  99. Lorteije, J. A., Rusu, S. I., Kushmerick, C., & Borst, J. G. (2009). Reliability and precision of the mouse calyx of Held synapse. The Journal of Neuroscience, 29(44), 13770–13784.PubMedGoogle Scholar
  100. Louage, D. H., van der Heijden, M., & Joris, P. X. (2004). Temporal properties of responses to broadband noise in the auditory nerve. Journal of Neurophysiology, 91(5), 2051–2065.PubMedGoogle Scholar
  101. Ludwig, J., Oliver, D., Frank, G., Klocker, N., Gummer, A. W., & Fakler, B. (2001). Reciprocal electromechanical properties of rat prestin: The motor molecule from rat outer hair cells. Proceedings of the National Academy of Sciences of the USA, 98(7), 4178–4183.Google Scholar
  102. Manis, P. B., & Brownell, W. E. (1983). Synaptic organization of eighth nerve afferents to cat dorsal cochlear nucleus. Journal of Neurophysiology, 50(5), 1156–1181.PubMedGoogle Scholar
  103. Manis, P. B., & Marx, S. O. (1991). Outward currents in isolated ventral cochlear nucleus neurons. The Journal of Neuroscience, 11(9), 2865–2880.PubMedGoogle Scholar
  104. Manis, P. B., Xie, R., Wang, Y., Marrs, G. S., & Spirou, G. A. (2011). The Endbulbs of Held. In L. O. Trussell, A. N. Popper & R. R. Fay (Eds.), Synaptic mechanisms in the auditory system (Vol. 41, pp. 61–94). New York: Springer Science+Business Media.Google Scholar
  105. Manley, G. A., Fay, R. R., & Popper, A. N. (2008). Active processes and otoacoustic emissions in hearing (Vol. 30). New York: Springer Science+Business Media.Google Scholar
  106. Mathews, P. J., Jercog, P. E., Rinzel, J., Scott, L. L., & Golding, N. L. (2010). Control of submillisecond synaptic timing in binaural coincidence detectors by K(v)1 channels. Nature Neuroscience, 13(5), 601–609.PubMedCentralPubMedGoogle Scholar
  107. Mistrik, P., & Ashmore, J. F. (2010). Reduced electromotility of outer hair cells associated with connexin-related forms of deafness: An in silico study of a cochlear network mechanism. Journal of the Association for Research in Otolaryngology : JARO, 11(4), 559–571.Google Scholar
  108. Moore, B. C., & Sek, A. (2009). Sensitivity of the human auditory system to temporal fine structure at high frequencies. The Journal of the Acoustical Society of America, 125(5), 3186–3193.PubMedGoogle Scholar
  109. Morimoto, N., Raphael, R. M., Nygren, A., & Brownell, W. E. (2002). Excess plasma membrane and effects of ionic amphipaths on mechanics of outer hair cell lateral wall. American Journal of Physiology, 282(5), C1076–1086.PubMedGoogle Scholar
  110. Mountain, D. C. (1980). Changes in endolymphatic potential and crossed olivocochlear bundle stimulation alter cochlear mechanics. Science, 210(4465), 71–72.PubMedGoogle Scholar
  111. Nguyen, T. V., & Brownell, W. E. (1998). Contribution of membrane cholesterol to outer hair cell lateral wall stiffness. Otolaryngology-Head and Neck Surgery, 119(1), 14–20.PubMedGoogle Scholar
  112. Nicol, M. J., & Walmsley, B. (2002). Ultrastructural basis of synaptic transmission between endbulbs of Held and bushy cells in the rat cochlear nucleus. The Journal of Physiology, 539(Pt 3), 713–723.PubMedCentralPubMedGoogle Scholar
  113. Oertel, D. (1983). Synaptic responses and electrical properties of cells in brain slices of the mouse anteroventral cochlear nucleus. The Journal of Neuroscience, 3(10), 2043–2053.PubMedGoogle Scholar
  114. Oghalai, J. S., Patel, A. A., Nakagawa, T., & Brownell, W. E. (1998). Fluorescence-imaged microdeformation of the outer hair cell lateral wall. The Journal of Neuroscience, 18(1), 48–58.PubMedGoogle Scholar
  115. Oleskevich, S., Clements, J., & Walmsley, B. (2000). Release probability modulates short-term plasticity at a rat giant terminal. The Journal of Physiology, 524 Pt 2, 513–523.PubMedCentralPubMedGoogle Scholar
  116. Oleskevich, S., Youssoufian, M., & Walmsley, B. (2004). Presynaptic plasticity at two giant auditory synapses in normal and deaf mice. The Journal of Physiology, 560(Pt 3), 709–719.PubMedCentralPubMedGoogle Scholar
  117. Pal, B., Rusznak, Z., Harasztosi, C., & Szucs, G. (2004). Depolarization-activated K+ currents of the bushy neurones of the rat cochlear nucleus in a thin brain slice preparation. Acta Physiologica Hungarica, 91(2), 83–98.PubMedGoogle Scholar
  118. Patuzzi, R. (2011). Ion flow in stria vascularis and the production and regulation of cochlear endolymph and the endolymphatic potential. Hearing Research, 277(1–2), 4–19.PubMedGoogle Scholar
  119. Purcell, E. K., Liu, L., Thomas, P. V., & Duncan, R. K. (2011). Cholesterol influences voltage-gated calcium channels and BK-type potassium channels in auditory hair cells. PLoS One, 6(10), e26289.PubMedCentralPubMedGoogle Scholar
  120. Quraishi, I. H., & Raphael, R. M. (2008). Generation of the endocochlear potential: A biophysical model. Biophysical Journal, 94(8), L64–66.PubMedCentralPubMedGoogle Scholar
  121. Rabbitt, R. D., Ayliffe, H. E., Christensen, D., Pamarthy, K., Durney, C., Clifford, S., & Brownell, W. E. (2005). Evidence of piezoelectric resonance in isolated outer hair cells. Biophysical Journal, 88(3), 2257–2265.PubMedCentralPubMedGoogle Scholar
  122. Rabbitt, R. D., Clifford, S., Breneman, K. D., Farrell, B., & Brownell, W. E. (2009). Power efficiency of outer hair cell somatic electromotility. PLoS Computational Biology, 5(7), e1000444.PubMedCentralPubMedGoogle Scholar
  123. Rajagopalan, L., Patel, N., Madabushi, S., Goddard, J. A., Anjan, V., Lin, F., Shope, C., Farrell, B., Lichtarge, O., Davidson, A. L., Brownell, W. E., & Pereira, F. A. (2006). Essential helix interactions in the anion transporter domain of prestin revealed by evolutionary trace analysis. The Journal of Neuroscience, 26(49), 12727–12734.PubMedCentralPubMedGoogle Scholar
  124. Rajagopalan, L., Greeson, J. N., Xia, A., Liu, H., Sturm, A., Raphael, R. M., Davidson, A. L., Oghalai, J. S., Pereira, F. A., & Brownell, W. E. (2007). Tuning of the outer hair cell motor by membrane cholesterol. The Journal of Biological Chemistry, 282(50), 36659–36670.PubMedCentralPubMedGoogle Scholar
  125. Raman, I. M., & Trussell, L. O. (1992). The kinetics of the response to glutamate and kainate in neurons of the avian cochlear nucleus. Neuron, 9(1), 173–186.PubMedGoogle Scholar
  126. Rao, D. (2011). Neuromodulation of intrinsic and synaptic plasticity in auditory cortex. Ph.D. thesis, The University of North Carolina, Chapel Hill.Google Scholar
  127. Raphael, R. M., Popel, A. S., & Brownell, W. E. (2000). A membrane bending model of outer hair cell electromotility. Biophysical Journal, 78(6), 2844–2862.PubMedCentralPubMedGoogle Scholar
  128. Rathouz, M., & Trussell, L. (1998). Characterization of outward currents in neurons of the avian nucleus magnocellularis. Journal of Neurophysiology, 80(6), 2824.PubMedGoogle Scholar
  129. Ratnanather, J. T., Zhi, M., Brownell, W. E., & Popel, A. S. (1996). Measurements and a model of the outer hair cell hydraulic conductivity. Hearing Research, 96(1–2), 33–40.Google Scholar
  130. Rautenberg, P. L., Grothe, B., & Felmy, F. (2009). Quantification of the three-dimensional morphology of coincidence detector neurons in the medial superior olive of gerbils during late postnatal development. The Journal of Comparative Neurology, 517(3), 385–396.Google Scholar
  131. Recio, A., & Rhode, W. S. (2000). Basilar membrane responses to broadband stimuli. Journal Acoustical Society of America, 108(5 Pt 1), 2281–2298.Google Scholar
  132. Recio-Spinoso, A., Temchin, A. N., van Dijk, P., Fan, Y. H., & Ruggero, M. A. (2005). Wiener-kernel analysis of responses to noise of chinchilla auditory-nerve fibers. Journal of Neurophysiology, 93(6), 3615–3634.Google Scholar
  133. Reyes, A. D., Rubel, E. W., & Spain, W. J. (1994). Membrane properties underlying the firing of neurons in the avian cochlear nucleus. The Journal of Neuroscience, 14(9), 5352.PubMedGoogle Scholar
  134. Rhode, W. S. (1971). Observations of the vibration of the basilar membrane in squirrel monkeys using the Mossbauer technique. Journal Acoustical Society of America, 49(4), Suppl 2:1218–1231.Google Scholar
  135. Rhode, W. S., Oertel, D., & Smith, P. H. (1983). Physiological response properties of cells labeled intracellularly with horseradish peroxidase in cat ventral cochlear nucleus. The Journal of comparative neurology, 213(4), 448–463.PubMedGoogle Scholar
  136. Ribrault, C., Sekimoto, K., & Triller, A. (2011). From the stochasticity of molecular processes to the variability of synaptic transmission. Nature reviews. Neuroscience, 12(7), 375–387.PubMedGoogle Scholar
  137. Romand, R. (1978). Survey of intracellular recording in the cochlear nucleus of the cat. Brain Research, 148(1), 43–65.PubMedGoogle Scholar
  138. Rothman, J. S., & Young, E. D. (1996). Enhancement of neural synchronization in computational models of ventral cochlear nucleus bushy cells. Auditory Neuroscience, 2, 47–62.Google Scholar
  139. Rothman, J. S., & Manis, P. B. (2003a). Kinetic analyses of three distinct potassium conductances in ventral cochlear nucleus neurons. Journal of Neurophysiology, 89(6), 3083–3096.PubMedGoogle Scholar
  140. Rothman, J. S., & Manis, P. B. (2003b). Differential expression of three distinct potassium currents in the ventral cochlear nucleus. Journal of Neurophysiology, 89(6), 3070–3082.PubMedGoogle Scholar
  141. Rothman, J. S., & Manis, P. B. (2003c). The roles potassium currents play in regulating the electrical activity of ventral cochlear nucleus neurons. Journal of Neurophysiology, 89(6), 3097–3113.PubMedGoogle Scholar
  142. Rothman, J. S., Young, E. D., & Manis, P. B. (1993). Convergence of auditory nerve fibers onto bushy cells in the ventral cochlear nucleus: Implications of a computational model. Journal of Neurophysiology, 70(6), 2562–2583.PubMedGoogle Scholar
  143. Rouiller, E. M., & Ryugo, D. K. (1984). Intracellular marking of physiologically characterized cells in the ventral cochlear nucleus of the cat. The Journal of Comparative Neurology, 225(2), 167–186.PubMedGoogle Scholar
  144. Rybalchenko, V., & Santos-Sacchi, J. (2003). Cl- flux through a non-selective, stretch-sensitive conductance influences the outer hair cell motor of the guinea-pig. The Journal of Physiology, 547(Pt 3), 873–891.PubMedCentralPubMedGoogle Scholar
  145. Santos-Sacchi, J. (1989). Asymmetry in voltage-dependent movements of isolated outer hair cells from the organ of Corti. The Journal of Neuroscience, 9(8), 2954–2962.PubMedGoogle Scholar
  146. Santos-Sacchi, J., & Dilger, J. P. (1988). Whole cell currents and mechanical responses of isolated outer hair cells. Hearing Research, 35(2–3), 143–150.PubMedGoogle Scholar
  147. Schwartz, I. R. (1977). Dendritic arrangements in the cat medial superior olive. Neuroscience, 2(1), 81–101.PubMedGoogle Scholar
  148. Schwarz, D. W., & Puil, E. (1997). Firing properties of spherical bushy cells in the anteroventral cochlear nucleus of the gerbil. Hearing Research, 114(1–2), 127–138.PubMedGoogle Scholar
  149. Scott, L. L., Hage, T. A., & Golding, N. L. (2007). Weak action potential backpropagation is associated with high-frequency axonal firing capability in principal neurons of the gerbil medial superior olive. The Journal of Physiology, 583(Pt 2), 647–661.PubMedCentralPubMedGoogle Scholar
  150. Scott, L. L., Mathews, P. J., & Golding, N. L. (2010). Perisomatic voltage-gated sodium channels actively maintain linear synaptic integration in principal neurons of the medial superior olive. The Journal of Neuroscience, 30(6), 2039–2050.PubMedCentralPubMedGoogle Scholar
  151. Sento, S., & Ryugo, D. K. (1989). Endbulbs of held and spherical bushy cells in cats: Morphological correlates with physiological properties. The Journal of Comparative Neurology, 280(4), 553–562.PubMedGoogle Scholar
  152. Sewell, W. F. (1984). The effects of furosemide on the endocochlear potential and auditory-nerve fiber tuning curves in cats. Hearing Research, 14(3), 305–314.PubMedGoogle Scholar
  153. Sfondouris, J., Rajagopalan, L., Pereira, F. A., & Brownell, W. E. (2008). Membrane composition modulates prestin-associated charge movement. The Journal of Biological Chemistry, 283(33), 22473–22481.PubMedCentralPubMedGoogle Scholar
  154. Shamma, S. A., Elhilali, M., & Micheyl, C. (2011). Temporal coherence and attention in auditory scene analysis. Trends in Neurosciences, 34(3), 114–123.PubMedCentralPubMedGoogle Scholar
  155. Shehata, W. E., Brownell, W. E., & Dieler, R. (1991). Effects of salicylate on shape, electromotility and membrane characteristics of isolated outer hair cells from guinea pig cochlea. Acta Oto-Laryngologica, 111(4), 707–718.PubMedGoogle Scholar
  156. Shera, C. A. (2001). Intensity-invariance of fine time structure in basilar-membrane click responses: implications for cochlear mechanics. The Journal of the Acoustical Society of America, 110(1), 332–348.PubMedGoogle Scholar
  157. Shera, C. A., & Olson, E. S. (2011). What fire is in mine ears: Progress in auditory biomechanics (Vol. 1403). Williamstown, MA: AIP Conference ProceedingsGoogle Scholar
  158. Shinn-Cunningham, B. G., & Wang, D. (2008). Influences of auditory object formation on phonemic restoration. The Journal of the Acoustical Society of America, 123(1), 295–301.PubMedGoogle Scholar
  159. Smith, P. H. (1995). Structural and functional differences distinguish principal from nonprincipal cells in the guinea pig MSO slice. Journal of Neurophysiology, 73(4), 1653–1667.PubMedGoogle Scholar
  160. Smith, P. H., Joris, P. X., & Yin, T. C. (1998). Anatomy and physiology of principal cells of the medial nucleus of the trapezoid body (MNTB) of the cat. Journal of Neurophysiology, 79(6), 3127–3142.PubMedGoogle Scholar
  161. Spector, A. A., Brownell, W. E., & Popel, A. S. (2003). Effect of outer hair cell piezoelectricity on high-frequency receptor potentials. The Journal of the Acoustical Society of America, 113(1), 453–461.PubMedGoogle Scholar
  162. Spector, A. A., Popel, A. S., Eatock, R. A., & Brownell, W. E. (2005). Mechanosensitive channels in the lateral wall can enhance the cochlear outer hair cell frequency response. Annals of Biomedical Engineering, 33(8), 991–1002.PubMedGoogle Scholar
  163. Spirou, G. A., Brownell, W. E., & Zidanic, M. (1990). Recordings from cat trapezoid body and HRP labeling of globular bushy cell axons. Journal of Neurophysiology, 63(5), 1169–1190.PubMedGoogle Scholar
  164. Spirou, G. A., Rager, J., & Manis, P. B. (2005). Convergence of auditory-nerve fiber projections onto globular bushy cells. Neuroscience, 136(3), 843–863.PubMedGoogle Scholar
  165. Street, S. E., & Manis, P. B. (2007). Action potential timing precision in dorsal cochlear nucleus pyramidal cells. Journal of Neurophysiology, 97(6), 4162–4172.PubMedCentralPubMedGoogle Scholar
  166. Strumbos, J. G., Polley, D. B., & Kaczmarek, L. K. (2010). Specific and rapid effects of acoustic stimulation on the tonotopic distribution of Kv3.1b potassium channels in the adult rat. Neuroscience, 167(3), 567–572.PubMedCentralPubMedGoogle Scholar
  167. Svirskis, G., Kotak, V., Sanes, D. H., & Rinzel, J. (2002). Enhancement of signal-to-noise ratio and phase locking for small inputs by a low-threshold outward current in auditory neurons. The Journal of Neuroscience, 22(24), 11019–11025.PubMedCentralPubMedGoogle Scholar
  168. Takahashi, S., & Santos-Sacchi, J. (2001). Non-uniform mapping of stress-induced, motility-related charge movement in the outer hair cell plasma membrane. Pflugers Archive: European Journal of Physiology, 441(4), 506–513.Google Scholar
  169. Typlt, M., Englitz, B., Sonntag, M., Dehmel, S., Kopp-Scheinpflug, C., & Ruebsamen, R. (2012). Multidimensional characterization and differentiation of neurons in the anteroventral cochlear nucleus. PLoS One, 7(1), e29965.PubMedCentralPubMedGoogle Scholar
  170. Tzounopoulos, T., Kim, Y., Oertel, D., & Trussell, L. O. (2004). Cell-specific, spike timing-dependent plasticities in the dorsal cochlear nucleus. Nature Neuroscience, 7(7), 719–725.PubMedGoogle Scholar
  171. Wang, Y., & Manis, P. B. (2005). Synaptic transmission at the cochlear nucleus endbulb synapse during age-related hearing loss in mice. Journal of Neurophysiology, 94(3), 1814–1824.PubMedCentralPubMedGoogle Scholar
  172. Wang, Y. X., Wenthold, R. J., Ottersen, O. P., & Petralia, R. S. (1998). Endbulb synapses in the anteroventral cochlear nucleus express a specific subset of AMPA-type glutamate receptor subunits. The Journal of Neuroscience, 18(3), 1148–1160.PubMedGoogle Scholar
  173. Weitzel, E. K., Tasker, R., & Brownell, W. E. (2003). Outer hair cell piezoelectricity: Frequency response enhancement and resonance behavior. The Journal of the Acoustical Society of America, 114(3), 1462–1466.PubMedCentralPubMedGoogle Scholar
  174. 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.PubMedCentralPubMedGoogle Scholar
  175. Wen, B., Wang, G. I., Dean, I., & Delgutte, B. (2012). Time course of dynamic range adaptation in the auditory nerve. Journal of Neurophysiology, 108(1), 69–82.PubMedCentralPubMedGoogle Scholar
  176. Wenthold, R. J., Zempel, J. M., Parakkal, M. H., Reeks, K. A., & Altschuler, R. A. (1986). Immunocytochemical localization of GABA in the cochlear nucleus of the guinea pig. Brain Research, 380(1), 7–18.PubMedGoogle Scholar
  177. Wenthold, R. J., Huie, D., Altschuler, R. A., & Reeks, K. A. (1987). Glycine immunoreactivity localized in the cochlear nucleus and superior olivary complex. Neuroscience, 22(3), 897–912.PubMedGoogle Scholar
  178. Wu, S. H., & Oertel, D. (1984). Intracellular injection with horseradish peroxidase of physiologically characterized stellate and bushy cells in slices of mouse anteroventral cochlear nucleus. The Journal of Neuroscience, 4(6), 1577–1588.PubMedGoogle Scholar
  179. Wu, S. H., & Oertel, D. (1986). Inhibitory circuitry in the ventral cochlear nucleus is probably mediated by glycine. The Journal of Neuroscience, 6(9), 2691–2706.PubMedGoogle Scholar
  180. Xie, R. & Manis, P.B. (2013). Target-specific IPSC kinetics promote temporal processing in auditory parallel pathways. The Journal of Neuroscience, 33(4), 1598–1614.PubMedCentralPubMedGoogle Scholar
  181. Yan, K., & Matthews, G. (1992). Blockers of potassium channels reduce the outward dark current in rod photoreceptor inner segments. Visual Neuroscience, 8(5), 479–481.PubMedGoogle Scholar
  182. Yang, H., & Xu-Friedman, M. A. (2012). Emergence of coordinated plasticity in the cochlear nucleus and cerebellum. The Journal of Neuroscience, 32(23), 7862–7868.PubMedCentralPubMedGoogle Scholar
  183. Yang, S., & Feng, A. S. (2007). Heterogeneous biophysical properties of frog dorsal medullary nucleus (cochlear nucleus) neurons. Journal of Neurophysiology, 98(4), 1953–1964.PubMedGoogle Scholar
  184. Zhang, R., Qian, F., Rajagopalan, L., Pereira, F. A., Brownell, W. E., & Anvari, B. (2007). Prestin modulates mechanics and electromechanical force of the plasma membrane. Biophysical Journal, 93(1), L07–09.PubMedCentralPubMedGoogle Scholar
  185. Zhang, X., & Carney, L. H. (2005). Response properties of an integrate-and-fire model that receives subthreshold inputs. Neural Computation, 17(12), 2571–2601.PubMedCentralPubMedGoogle Scholar
  186. Zheng, J., Shen, W., He, D. Z., Long, K. B., Madison, L. D., & Dallos, P. (2000). Prestin is the motor protein of cochlear outer hair cells. Nature, 405(6783), 149–155.PubMedGoogle Scholar
  187. Zidanic, M., & Brownell, W. E. (1989). Low-frequency modulation of the intracochlear potential field: An energy source for the cochlear amplifier. Il Valsalva, 65(Suppl. 1), 20–27.Google Scholar
  188. Zidanic, M., & Brownell, W. E. (1990). Fine structure of the intracochlear potential field. I. The silent current. Biophysical Journal, 57(6), 1253–1268.PubMedCentralPubMedGoogle Scholar
  189. Zidanic, M., & Brownell, W. E. (1992). Fine structure of the intracochlear potential field. II. Tone-evoked waveforms and cochlear microphonics. Journal of Neurophysiology, 67(1), 108–124.PubMedGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2014

Authors and Affiliations

  1. 1.Bobby R. Alford Department of Otolaryngology/Head and Neck Surgery, and the Departments of Neuroscience, Molecular Physiology and Biophysics, and the Structural and Computational Biology & Molecular Biophysics ProgramBaylor College of MedicineHoustonUSA
  2. 2.Departments of Otolaryngology/Head and Neck Surgery, Cell Biology and PhysiologyUniversity of North CarolinaChapel HillUSA

Personalised recommendations