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Cellular Mechanisms for Information Coding in Auditory Brainstem Nuclei

  • Laurence O. Trussell
Part of the Springer Handbook of Auditory Research book series (SHAR, volume 15)

Abstract

The brainstem auditory nuclei carry out a wide variety of transformations of the signals carried by the auditory nerve. Although basic frequency and intensity information is first encoded in the cochlea, brainstem circuitry must perform further neural definitions and refinements of these parameters, as well as integrate the cues necessary for the localization of sounds in space. Each of these aspects is associated not just with certain cell types, morphologies, and synaptic connections, but with cells having characteristic electrical response profiles. Such response properties are an outcome of the complement of ion channels that the cells possess and of the dynamic properties of the synapses through which cells communicate.

Keywords

AMPA Receptor Auditory Nerve Cochlear Nucleus Auditory Nerve Fiber Dorsal Cochlear Nucleus 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

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References

  1. Agmon-Snir H, Carr CE, Rinzel J (1998) The role of dendrites in auditory coincidence detection. Nature 393: 268–272.PubMedCrossRefGoogle Scholar
  2. Bal R, Oertel D (2000) Hyperpolarization-activated, mixed-cation current (I(h)) in octopus cells of the mammalian cochlear nucleus. J Neurophysiol 84: 806–817.PubMedGoogle Scholar
  3. Banks MI, Sachs MB (1991) Regularity analysis in a compartmental model of chopper units in the anteroventral cochlear nucleus. J Neurophysiol 65: 606–629.PubMedGoogle Scholar
  4. Banks MI, Smith PH (1992) Intracellular recordings from neurobiotin-labeled cells in brain slices of the rat medial nucleus of the trapezoid body. J Neurosci 12: 2819–2837.PubMedGoogle Scholar
  5. Cai Y, McGee J, Walsh EJ (2000) Contributions of ion conductances to the onset responses of octopus cells in the ventral cochlear nucleus: simulation results. J Neurophysiol 83: 301–314.PubMedGoogle Scholar
  6. Carr CE (1993) Processing of temporal information in the brain. Annu Rev Neurosci 16: 223–243.PubMedCrossRefGoogle Scholar
  7. Carr CE, Konishi M (1990) A circuit for detection of interaural time differences in the brainstem of the barn owl. J Neurosci 10: 3227–3246.PubMedGoogle Scholar
  8. Caspary DM, Palombi PS, Backoff PM, Helfert RH, Finlayson PG (1993) GABA and glycine inputs control discharge rate within the excitatory response area of primary-like and phase-locked AVCN neurons. In: Merchan MA, Jiuz JM, Godfrey DA, Mugnaini E (eds) The mammalian cochlear nuclei. Organization and function. New York: Plenum, pp. 239–252.Google Scholar
  9. Caspary DM, Backoff PM, Finlayson PG, Palombi PS (1994) Inhibitory inputs modulate discharge rate within frequency receptive fields of anteroventral cochlear nucleus neurons. J Neurophysiol 72: 2124–2133.PubMedGoogle Scholar
  10. Covey E, Kauer JA, Casseday JH (1996) Whole-cell patch-clamp recording reveals subthreshold sound-evoked postsynaptic currents in the inferior colliculus of awake bats. J Neurosci 16: 3009–3018.PubMedGoogle Scholar
  11. Del Castillo J, Katz B (1954) Quantal components of the end-plate potential. J Physiol (Lond) 124: 560–573.Google Scholar
  12. Dittman JS, Regehr WG (1998) Calcium dependence and recovery kinetics of pre-synaptic depression at the climbing fiber to Purkinje cell synapse. J Neurosci 18: 6147–6162.PubMedGoogle Scholar
  13. Erisir A, Lau D, Rudy B, Leonard CS (1999) Function of specific K(+) channels in sustained high-frequency firing of fast-spiking neocortical interneurons. J Neurophysiol 82: 2476–2489.PubMedGoogle Scholar
  14. Evans EF, Zhao W (1993) Neuropharmacological and neurophysiological dissection of inhibition in the mammalian cochlear nuclei. In: Merchan MA, Jiuz JM, Godfrey DA, Mugnaini E (eds) The mammalian cochlear nuclei. Organization and function. New York: Plenum, pp. 253–266.Google Scholar
  15. Ferragamo MJ, Oertel D (1998) Shaping of synaptic responses and action potentials in octopus cells. Assoc Res Otolaryngol 21: 96.Google Scholar
  16. Ferragamo MJ, Golding NL, Oertel D (1998) Synaptic inputs to stellate cells in the ventral cochlear nucleus. J Neurophysiol 79: 51–63.PubMedGoogle Scholar
  17. Forsythe ID, Barnes-Davies M (1993) The binaural auditory pathway: excitatory amino acid receptors mediate dual timecourse excitatory postsynaptic currents in the rat medial nucleus of the trapezoid body. Proc R Soc Lond B Biol Sci 251: 151–157.CrossRefGoogle Scholar
  18. Funabiki K, Koyano K, Ohmori H (1998) The role of GABAergic inputs for coincidence detection in the neurones of nucleus laminaris of the chick. J Physiol (Lond) 508: 851–869.CrossRefGoogle Scholar
  19. Gardner SM, Trussell LO, Oertel D (1999) Time course and permeation of synaptic AMPA receptors in cochlear nuclear neurons correlate with input. J Neurosci 19: 8721–8729.PubMedGoogle Scholar
  20. Gardner SM, Trussell LO, Oertel D (2001) Comparison of AMPA receptors associated with different inputs in the cochlear nuclei. J Neurosci 21: 7428–7437.PubMedGoogle Scholar
  21. Geiger JR, Melcher T, Koh DS, Sakmann B, Seeburg PH, 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: 193–204.PubMedCrossRefGoogle Scholar
  22. Geisler CD, Greenberg S (1986) A two-stage nonlinear cochlear model possesses automatic gain control. J Acoust Soc Am 80: 1359–1363.PubMedCrossRefGoogle Scholar
  23. Godfrey DA, Kiang NY, Norris BE (1975) Single unit activity in the posteroventral cochlear nucleus of the cat. J Comp Neurol 162: 247–268.PubMedCrossRefGoogle Scholar
  24. Golding NL, Oertel D (1996) Context-dependent synaptic action of glycinergic and GABAergic inputs in the dorsal cochlear nucleus. J Neurosci 16: 2208–2219.PubMedGoogle Scholar
  25. Golding NL, Oertel D (1997) Physiological identification of the targets of cartwheel cells in the dorsal cochlear nucleus. J Neurophysiol 78: 248–260.PubMedGoogle Scholar
  26. Golding NL, Robertson D, Oertel D (1995) Recordings from slices indicate that octopus cells of the cochlear nucleus detect coincident firing of auditory nerve fibers with temporal precision. J Neurosci 15: 3138–3153.PubMedGoogle Scholar
  27. Grigg JJ, Brew HM, Tempel BL (2000) Differential expression of voltage-gated potassium channel genes in auditory nuclei of the mouse brainstem. Hear Res 140: 77–90.PubMedCrossRefGoogle Scholar
  28. Grothe B, Sanes DH (1993) Bilateral inhibition by glycinergic afferents in the medial superior olive. J Neurophysiol 69: 1192–1196.PubMedGoogle Scholar
  29. Guinan JJ, Jr., Li RY (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. Hear Res 49: 321–334.PubMedCrossRefGoogle Scholar
  30. Hamill OP, Marty A, Neher E, Sakmann B, Sigworth FJ (1981) Improved patch-clamp techniques for high-resolution current recording from cells and cell-free membrane patches. Pflugers Arch 391: 85–100.PubMedCrossRefGoogle Scholar
  31. Hirsch JA, Oertel D (1988) Intrinsic properties of neurones in the dorsal cochlear nucleus of mice, in vitro. J Physiol (Lond) 396: 535–548.Google Scholar
  32. Hollmann M (1999) Structure of ionotropic glutamate receptors. In: Jonas P, Monyer H (eds) Ionotropic glutamate receptors in the CNS. Berlin: Springer-Verlag, pp. 1–78.Google Scholar
  33. Hume RI, Dingledine R, Heinemann SF (1991) Identification of a site in glutamate receptor subunits that controls calcium permeability. Science 253: 1028–1031.PubMedCrossRefGoogle Scholar
  34. Hyson RL, Reyes AD, Rubel EW (1995) A depolarizing inhibitory response to GABA in brainstem auditory neurons of the chick. Brain Res 677: 117–126.PubMedCrossRefGoogle Scholar
  35. Isaacson JS, Walmsley B (1995) Receptors underlying excitatory synaptic transmission in slices of the rat anteroventral cochlear nucleus. J Neurophysiol 73: 964–973.PubMedGoogle Scholar
  36. Jhaveri S, Morest DK (1982) Neuronal architecture in nucleus magnocellularis of the chicken auditory system with observations on nucleus laminaris: a light and electron microscope study. Neuroscience 7: 809–836.PubMedCrossRefGoogle Scholar
  37. Joris PX, Carney LH, Smith PH, Yin TC (1994) Enhancement of neural synchronization in the anteroventral cochlear nucleus. I. Responses to tones at the characteristic frequency. J Neurophysiol 71: 1022–1036.PubMedGoogle Scholar
  38. Kane EC (1973) Octopus cells in the cochlear nucleus of the cat: heterotypic synapses upon homeotypic neurons. Int J Neurosci 5: 251–279.PubMedCrossRefGoogle Scholar
  39. Kanold PO, Manis PB (1999) Transient potassium currents regulate the discharge patterns of dorsal cochlear nucleus pyramidal cells. J Neurosci 19: 2195–2208.PubMedGoogle Scholar
  40. Klug A, Bauer EE, Pollak GD (1999) Multiple components of ipsilaterally evoked inhibition in the inferior colliculus. J Neurophysiol 82: 593–610.PubMedGoogle Scholar
  41. Kotak VC, Korada S, Schwartz IR, Sanes DH (1998) A developmental shift from GABAergic to glycinergic transmission in the central auditory system. J Neurosci 18: 4646–4655.PubMedGoogle Scholar
  42. Lawrence JJ, Trussell LO (2000) Long-term specification of AMPA receptor properties after synapse formation. J Neurosci 20: 4864–4870.PubMedGoogle Scholar
  43. Lester RA, Clements JD, Westbrook GL, Jahr CE (1990) Channel kinetics determine the time course of NMDA receptor-mediated synaptic currents. Nature 346: 565–567.PubMedCrossRefGoogle Scholar
  44. Liberman MC (1991) Central projections of auditory-nerve fibers of differing spontaneous rate. I. Anteroventral cochlear nucleus. J Comp Neurol 313: 240–258.PubMedCrossRefGoogle Scholar
  45. Lim R, Alvarez FJ, Walmsley B (2000) GABA mediates presynaptic inhibition at glycinergic synapses in a rat auditory brainstem nucleus. J Physiol 525: 447–459.PubMedCrossRefGoogle Scholar
  46. Lu T, Trussell LO (2000) Inhibitory transmission mediated by asynchronous transmitter release. Neuron 26: 683–694.PubMedCrossRefGoogle Scholar
  47. Manis PB (1990) Membrane properties and discharge characteristics of guinea pig dorsal cochlear nucleus neurons studied in vitro. J Neurosci 10: 2338–2351.PubMedGoogle Scholar
  48. Manis PB, Marx SO (1991) Outward currents in isolated ventral cochlear nucleus neurons. J Neurosci 11: 2865–2880.PubMedGoogle Scholar
  49. Martina M, Schultz JH, Ehmke H, Monyer H, Jonas P (1998) Functional and molecular differences between voltage-gated K+ channels of fast-spiking interneurons and pyramidal neurons of rat hippocampus. J Neurosci 18: 8111–8125.PubMedGoogle Scholar
  50. Mosbacher J, Schoepfer R, Monyer H, Burnashev N, Seeburg PH, Ruppersberg JP (1994) A molecular determinant for submillisecond desensitization in glutamate receptors. Science 266: 1059–1062.PubMedCrossRefGoogle Scholar
  51. Moser T, Beutner D (2000) Kinetics of exocytosis and endocytosis at the cochlear inner hair cell afferent synapse of the mouse. Proc Natl Acad Sci U S A 97: 883–888.PubMedCrossRefGoogle Scholar
  52. Oertel D (1983) Synaptic responses and electrical properties of cells in brain slices of the mouse anteroventral cochlear nucleus. J Neurosci 3: 2043–2053.PubMedGoogle Scholar
  53. Osen KK (1969) Cytoarchitecture of the cochlear nuclei in the cat. J Comp Neurol 136: 453–484.PubMedCrossRefGoogle Scholar
  54. Ostapoff EM, Morest DK, Potashner SJ (1990) Uptake and retrograde transport of [3H]GABA from the cochlear nucleus to the superior olive in the guinea pig. J Chem Neuroanat 3: 285–295.PubMedGoogle Scholar
  55. Otis T, Zhang S, Trussell LO (1996a) Direct measurement of AMPA receptor desensitization induced by glutamatergic synaptic transmission. J Neurosci 16: 7496–7504.Google Scholar
  56. Otis TS, Wu YC, Trussell LO (1996b) Delayed clearance of transmitter and the role of glutamate transporters at synapses with multiple release sites. J Neurosci 16: 1634–1644.Google Scholar
  57. Otis TS, Raman IM, Trussell LO (1995) AMPA receptors with high Ca2+ permeability mediate synaptic transmission in the avian auditory pathway. J Physiol (Lond) 482: 309–315.Google Scholar
  58. Parks TN (2000) The AMPA receptors of auditory neurons. Hear Res 147: 77–91.PubMedCrossRefGoogle Scholar
  59. Patneau DK, Mayer ML (1990) Structure-activity relationships for amino acid transmitter candidates acting at N-methyl-D-aspartate and quisqualate receptors. J Neurosci 10: 2385–2399.PubMedGoogle Scholar
  60. Perney TM, Kaczmarek LK (1997) Localization of a high threshold potassium channel in the rat cochlear nucleus. J Comp Neurol 386: 178–202.PubMedCrossRefGoogle Scholar
  61. Perney TM, Marshall J, Martin KA, Hockfield S, Kaczmarek LK (1992) Expression of the mRNAs for the Kv3.1 potassium channel gene in the adult and developing rat brain. J Neurophysiol 68: 756–766.PubMedGoogle Scholar
  62. Petralia RS, Wang YX, Zhao HM, Wenthold RJ (1996) Ionotropic and metabotropic glutamate receptors show unique postsynaptic, presynaptic, and glial localizations in the dorsal cochlear nucleus. J Comp Neurol 372: 356–383.PubMedCrossRefGoogle Scholar
  63. Pfeiffer RR (1966) Classification of response patterns of spike discharges for units in the cochlear nucleus: tone-burst stimulation. Exp Brain Res 1: 220–235.PubMedCrossRefGoogle Scholar
  64. Raman IM, Zhang S, Trussell LO (1994) Pathway-specific variants of AMPA receptors and their contribution to neuronal signaling. J Neurosci 14: 4998–5010.PubMedGoogle Scholar
  65. Rathouz M, Trussell L (1998) Characterization of outward currents in neurons of the avian nucleus magnocellularis. J Neurophysiol 80: 2824–2835.PubMedGoogle Scholar
  66. Ravindranathan A, Donevan SD, Sugden SG, Greig A, Rao MS, Parks TN (2000) Contrasting molecular composition and channel properties of AMPA receptors on chick auditory and brainstem motor neurons. J Physiol (Lond) 523: 667–684.CrossRefGoogle Scholar
  67. Reyes AD, Rubel EW, Spain WJ (1994) Membrane properties underlying the firing of neurons in the avian cochlear nucleus. J Neurosci 14: 5352–5364.PubMedGoogle Scholar
  68. Rhode WS, Greenberg S (1992) Physiology of the cochlear nuclei. In: Popper AN, Fay RR (eds) The Mammalian Auditory Pathway: Neurophysiology. New York: Springer-Verlag, pp. 94–152.CrossRefGoogle Scholar
  69. Rhode WS, Smith PH (1986) Encoding timing and intensity in the ventral cochlear nucleus of the cat. J Neurophysiol 56: 261–286.PubMedGoogle Scholar
  70. Rhode WS, Oertel D, Smith PH (1983a) Physiological response properties of cells labeled intracellularly with horseradish peroxidase in cat ventral cochlear nucleus. J Comp Neurol 213: 448–463.CrossRefGoogle Scholar
  71. Rhode WS, Smith PH, Oertel D (1983b) Physiological response properties of cells labeled intracellularly with horseradish peroxidase in cat dorsal cochlear nucleus. J Comp Neurol 213: 426–447.CrossRefGoogle Scholar
  72. Rodriguez-Moreno A, Herreras O, Lerma J (1997) Kainate receptors presynaptically downregulate GABAergic inhibition in the rat hippocampus. Neuron 19: 893–901.PubMedCrossRefGoogle Scholar
  73. Rothman JS, Young ED, Manis PB (1993) Convergence of auditory nerve fibers onto bushy cells in the ventral cochlear nucleus: implications of a computational model. J Neurophysiol 70: 2562–2583.PubMedGoogle Scholar
  74. Rouiller EM, Ryugo DK (1984) Intracellular marking of physiologically characterized cells in the ventral cochlear nucleus of the cat. J Comp Neurol 225: 167–186.PubMedCrossRefGoogle Scholar
  75. Rubel EW, Parks TN (1975) Organization and development of brainstem auditory nuclei of the chicken: tonotopic organization of n. magnocellularis and n. laminaris. J Comp Neurol 164: 411–433.PubMedCrossRefGoogle Scholar
  76. Rubio ME, Wenthold RJ (1997) Glutamate receptors are selectively targeted to postsynaptic sites in neurons. Neuron 18: 939–950.PubMedCrossRefGoogle Scholar
  77. Ruggero MA (1992) Physiology of the auditory nerve. In: Popper AN, Fay RR (eds) The Mammalian Auditory Pathway: Neurophysiology. New York: Springer-Verlag, pp. 34–93.CrossRefGoogle Scholar
  78. Saint Marie RL, Benson CG, Ostapoff EM, Morest DK (1991) Glycine immunoreactive projections from the dorsal to the anteroventral cochlear nucleus. Hear Res 51: 11–28.CrossRefGoogle Scholar
  79. Sanes DH, Friauf E (2000) Development and influence of inhibition in the lateral superior olivary nucleus. Hear Res 147: 46–58.PubMedCrossRefGoogle Scholar
  80. Sato K, Shiraishi S, Nakagawa H, Kuriyama H, Altschuler RA (2000) Diversity and plasticity in amino acid receptor subunits in the rat auditory brainstem. Hear Res 147: 137–144.PubMedCrossRefGoogle Scholar
  81. Schneggenburger R, Meyer AC, Neher E (1999) Released fraction and total size of a pool of immediately available transmitter quanta at a calyx synapse. Neuron 23: 399–409.PubMedCrossRefGoogle Scholar
  82. Schwarz DW, Tennigkeit F, Adam T, Finlayson P, Puil E (1998) Membrane properties that shape the auditory code in three nuclei of the central nervous system. J Otolaryngol 27: 311–317.PubMedGoogle Scholar
  83. Sento S, Ryugo DK (1989) Endbulbs of held and spherical bushy cells in cats: morphological correlates with physiological properties. J Comp Neurol 280: 553562.Google Scholar
  84. Sewell WF, Mroz EA (1990) Purification of a low-molecular-weight excitatory substance from the inner ears of goldfish. Hear Res 50: 127–137.PubMedCrossRefGoogle Scholar
  85. Smith PH, Rhode WS (1987) Characterization of HRP-labeled globular bushy cells in the cat anteroventral cochlear nucleus. J Comp Neurol 266: 360–375.PubMedCrossRefGoogle Scholar
  86. Smith PH, Rhode WS (1989) Structural and functional properties distinguish two types of multipolar cells in the ventral cochlear nucleus. J Comp Neurol 282: 595–616.PubMedCrossRefGoogle Scholar
  87. Smith PH, Joris PX, Yin TC (1993) Projections of physiologically characterized spherical bushy cell axons from the cochlear nucleus of the cat: evidence for delay lines to the medial superior olive. J Comp Neurol 331: 245–260.PubMedCrossRefGoogle Scholar
  88. Smith PH, Joris PX, Yin TC (1998) Anatomy and physiology of principal cells of the medial nucleus of the trapezoid body (MNTB) of the cat. J Neurophysiol 79: 3127–3142.PubMedGoogle Scholar
  89. Smith AJ, Owens S, Forsythe ID (2000) Characterisation of inhibitory and excitatory postsynaptic currents of the rat medial superior olive. J Physiol 529: 681–698.PubMedCrossRefGoogle Scholar
  90. Sommer B, Keinanen K, Verdoorn TA, Wisden W, Burnashev N, Herb A, Kohler M, Takagi T, Sakmann B, Seeburg PH (1990) Flip and flop: a cell-specific functional switch in glutamate-operated channels of the CNS. Science 249: 1580–1585.PubMedCrossRefGoogle Scholar
  91. Spruston N, Jaffe DB, Johnston D (1994) Dendritic attenuation of synaptic potentials and currents: the role of passive membrane properties. Trends Neurosci 17: 161–166.PubMedCrossRefGoogle Scholar
  92. Takahashi T, Forsythe ID, Tsujimoto T, Barnes-Davies M, Onodera K (1996) Pre-synaptic calcium current modulation by a metabotropic glutamate receptor. Science 274: 594–597.PubMedCrossRefGoogle Scholar
  93. Taschenberger H, von Gersdorff H (2000) Fine-tuning an auditory synapse for speed and fidelity: developmental changes in presynaptic waveform, EPSC kinetics, and synaptic plasticity. J Neurosci 20: 9162–9173.PubMedGoogle Scholar
  94. Trussell L (1998) Control of time course of glutamatergic synaptic currents. Prog Brain Res 116: 59–69.PubMedCrossRefGoogle Scholar
  95. Trussell LO, Zhang S, Raman IM (1993) Desensitization of AMPA receptors upon multiquantal neurotransmitter release. Neuron 10: 1185–1196.PubMedCrossRefGoogle Scholar
  96. Tsuchitani C, Boudreau JC (1967) Encoding of stimulus frequency and intensity by cat superior olive S- segment cells. J Acoust Soc Am 42: 794–805.PubMedCrossRefGoogle Scholar
  97. Turecek R, Trussell LO (2001) Presynaptic glycine receptors enhance transmitter release at a mammalian central synapse. Nature 411: 587–590.PubMedCrossRefGoogle Scholar
  98. Waldeck RF, Pereda A, Faber DS (2000) Properties and plasticity of paired-pulse depression at a central synapse. J Neurosci 20: 5312–5320.PubMedGoogle Scholar
  99. Wang LY, Kaczmarek LK (1998) High-frequency firing helps replenish the readily releasable pool of synaptic vesicles. Nature 394: 384–388.PubMedCrossRefGoogle Scholar
  100. Wang LY, Gan L, Forsythe ID, Kaczmarek LK (1998) Contribution of the Kv3.1 potassium channel to high-frequency firing in mouse auditory neurones. J Physiol (Lond) 509: 183–194.CrossRefGoogle Scholar
  101. Wang YX, Wenthold RJ, Ottersen OP, Petralia RS (1998) Endbulb synapses in the anteroventral cochlear nucleus express a specific subset of AMPA-type glutamate receptor subunits. J Neurosci 18: 1148–1160.PubMedGoogle Scholar
  102. Warchol ME, Dallos P (1990) Neural coding in the chick cochlear nucleus. J Comp Physiol [A] 166: 721–734.Google Scholar
  103. White JA, Young ED, Manis PB (1994) The electrotonic structure of regular-spiking neurons in the ventral cochlear nucleus may determine their response properties. J Neurophysiol 71: 1774–1786.PubMedGoogle Scholar
  104. Wickesberg RE, Oertel D (1990) Delayed, frequency-specific inhibition in the cochlear nuclei of mice: a mechanism for monaural echo suppression. J Neurosci 10: 1762–1768.PubMedGoogle Scholar
  105. Wickesberg RE, Whitton D, Oertel D (1991) Tuberculoventral neurons project to the multipolar cell area but not to the octopus cell area of the posteroventral cochlear nucleus. J Comp Neurol 313: 457–468.PubMedCrossRefGoogle Scholar
  106. Wu LG, Borst JG (1999) The reduced release probability of releasable vesicles during recovery from short-term synaptic depression. Neuron 23: 821–832.PubMedCrossRefGoogle Scholar
  107. Wu SH, Oertel D (1986) Inhibitory circuitry in the ventral cochlear nucleus is probably mediated by glycine. J Neurosci 6: 2691–2706.PubMedGoogle Scholar
  108. Wu SH, Oertel D (1987) Maturation of synapses and electrical properties of cells in the cochlear nuclei. Hear Res 30: 99–110.PubMedCrossRefGoogle Scholar
  109. Wu SH, Kelly JB (1992a) Binaural interaction in the lateral superior olive: time difference sensitivity studied in mouse brain slice. J Neurophysiol 68: 1151–1159.Google Scholar
  110. Wu SH, Kelly JB (1992b) Synaptic pharmacology of the superior olivary complex studied in mouse brain slice. J Neurosci 12: 3084–3097.Google Scholar
  111. Wu SH, Fu XW (1998) Glutamate receptors underlying excitatory synaptic transmission in the rat’s lateral superior olive studied in vitro. Hear Res 122: 47–59.PubMedCrossRefGoogle Scholar
  112. Yang L, Monsivais P, Rubel EW (1999) The superior olivary nucleus and its influence on nucleus laminaris: a source of inhibitory feedback for coincidence detection in the avian auditory brainstem. J Neurosci 19: 2313–2325.PubMedGoogle Scholar
  113. Yin TC, Chan JC (1990) Interaural time sensitivity in medial superior olive of cat. J Neurophysiol 64: 465–488.PubMedGoogle Scholar
  114. Young ED, Robert JM, Shofner WP (1988) Regularity and latency of units in ventral cochlear nucleus: implications for unit classification and generation of response properties. J Neurophysiol 60: 1–29.PubMedGoogle Scholar
  115. Zhang S, Trussell LO (1994a) Voltage clamp analysis of excitatory synaptic transmission in the avian nucleus magnocellularis. J Physiol (Lond) 480: 123–136.Google Scholar
  116. Zhang S, Trussell LO (1994b) A characterization of excitatory postsynaptic potentials in the avian nucleus magnocellularis. J Neurophysiol 72: 705–718.Google Scholar
  117. Zhou N, Taylor DA, Parks TN (1995) Cobalt-permeable non-NMDA receptors in developing chick brainstem auditory nuclei. Neuroreport 6: 2273–2276.PubMedCrossRefGoogle Scholar
  118. Zucker RS (1989) Short-term synaptic plasticity. Annu Rev Neurosci 12: 13–31.PubMedCrossRefGoogle Scholar

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© Springer Science+Business Media New York 2002

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  • Laurence O. Trussell

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