Inhibitory Neurons in the Auditory Brainstem

Chapter
Part of the Springer Handbook of Auditory Research book series (SHAR, volume 41)

Abstract

Most chapters in this volume address the function of the major excitatory synapses in the lower auditory pathways, with respect to coincidence detection, the ion channels that determine neuronal firing, and the control of excitation through modulation and plasticity. However, none of these processes can be understood at a functional level without considering synaptic inhibition. Indeed, inhibition through GABAergic and glycinergic interneurons is likely to play an essential role in controlling the excitation at every level of central auditory processing. The present chapter examines inhibitory interneurons in several contexts in order to illustrate the diversity of their cellular mechanisms and circuit-level function, with a focus on the auditory brainstem. The term “interneuron” is used loosely; in fact, inhibitory cells are so fundamental to auditory processing that individual neurons may act as both proper interneurons (intrinsic neurons, i.e., those inhibiting within a local circuit) and inhibitory projection neurons (inhibiting across brainstem nuclei or regions). After introducing the study of interneurons and their general function, the chapter examines two prominent examples from the cochlear nucleus and superior olivary complex, rather than provide an exhaustive summary of all known auditory interneurons. Then four aspects of interneuron physiology are explored: the control of the reversal potential for Cl, the gating properties of the receptor-channel complex, the role of corelease of the transmitters GABA and glycine from interneuronal synapses; and, lastly, mechanisms for prolonging the action of the transmitter.

Keywords

Depression Boron Glycine Oligomerization Bicarbonate 

Notes

Acknowledgments

I wish to thank Mr. Dan Yaeger and Dr. Donata Oertel for comments on the manuscript. Dr. Gareth Price provided data for Fig. 7.5. Support was provided by the NIH (grants NS028901 and DC004450).

References

  1. Alibardi, L. (1998). Ultrastructural and immunocytochemical characterization of commissural neurons in the ventral cochlear nucleus of the rat. Annals of Anatomy, 180(5), 427–438.PubMedGoogle Scholar
  2. Alibardi, L. (2006). Review: Cytological characteristics of commissural and tuberculo-ventral neurons in the rat dorsal cochlear nucleus. Hearing Research, 216–217, 73–80. doi: S0378-5955(06)00010-4[pii] 10.1016/j.heares.2006.01.005. PubMedCrossRefGoogle Scholar
  3. Araki, T., & Terzuolo, C. A. (1962). Membrane currents in spinal motoneurons associated with the action potential and synaptic activity. Journal of Neurophysiology, 25, 772–789.PubMedGoogle Scholar
  4. Awatramani, G. B., Turecek, R., & Trussell, L. O. (2005). Staggered development of GABAergic and glycinergic transmission in the MNTB. Journal of Neurophysiology, 93(2), 819–828. doi:  10.1152/jn.00798.200400798.2004[pii.]PubMedCrossRefGoogle Scholar
  5. Backoff, P. M., Palombi, P. S., & Caspary, D. M. (1997). Glycinergic and GABAergic inputs affect short-term suppression in the cochlear nucleus. Hearing Research, 110(1–2), 155–163.PubMedCrossRefGoogle Scholar
  6. Backoff, P. M., Shadduck Palombi, P., & Caspary, D. M. (1999). Gamma-aminobutyric acidergic and glycinergic inputs shape coding of amplitude modulation in the chinchilla cochlear nucleus. Hearing Research, 134(1–2), 77–88. doi: S0378-5955(99)00071-4 [pii].PubMedCrossRefGoogle Scholar
  7. Balakrishnan, V., Becker, M., Lohrke, S., Nothwang, H. G., Guresir, E., & Friauf, E. (2003). Expression and function of chloride transporters during development of inhibitory neurotransmission in the auditory brainstem. Journal of Neuroscience, 23(10), 4134–4145. doi: 23/10/4134[pii].PubMedGoogle Scholar
  8. Balakrishnan, V., Kuo, S. P., Roberts, P. D., & Trussell, L. O. (2009). Slow glycinergic transmission mediated by transmitter pooling. Nature Neuroscience, 12(3), 286–294. doi: nn.2265[pii] 10.1038/nn.2265. PubMedCrossRefGoogle Scholar
  9. Beato, M., & Sivilotti, L. G. (2007). Single-channel properties of glycine receptors of juvenile rat spinal motoneurones in vitro. Journal of Physiology, 580(Pt. 2), 497–506. doi: jphysiol.2006.125740[pii] 10.1113/jphysiol.2006.125740. PubMedGoogle Scholar
  10. Blaesse, P., Guillemin, I., Schindler, J., Schweizer, M., Delpire, E., Khiroug, L., Friauf, E., & Nothwang, H. G. (2006). Oligomerization of KCC2 correlates with development of inhibitory neurotransmission. Journal of Neuroscience, 26(41), 10407–10419. doi: 26/41/10407[pii] 10.1523/JNEUROSCI.3257-06.2006. PubMedCrossRefGoogle Scholar
  11. Boron, W. F., Chen, L., & Parker, M. D. (2009). Modular structure of sodium-coupled bicarbonate transporters. Journal of Experimental Biology, 212(Pt. 11), 1697–1706. doi: 212/11/1697[pii] 10.1242/jeb.028563. PubMedCrossRefGoogle Scholar
  12. 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. doi:  10.1038/417543a417543a[pii].PubMedCrossRefGoogle Scholar
  13. Brawer, J. R., Morest, D. K., & Kane, E. C. (1974). The neuronal architecture of the cochlear nucleus of the cat. Journal of Comparative Neurology, 155(3), 251–300. doi:  10.1002/cne.901550302. PubMedCrossRefGoogle Scholar
  14. Burger, R. M., Cramer, K. S., Pfeiffer, J. D., & Rubel, E. W. (2005). Avian superior olivary nucleus provides divergent inhibitory input to parallel auditory pathways. Journal of Comparative Neurology, 481(1), 6–18. doi:  10.1002/cne.20334. PubMedCrossRefGoogle Scholar
  15. Butt, S. J., Fuccillo, M., Nery, S., Noctor, S., Kriegstein, A., Corbin, J. G., & Fishell, G. (2005). The temporal and spatial origins of cortical interneurons predict their physiological subtype. Neuron, 48(4), 591–604. doi: S0896-6273(05)00934-7[pii] 10.1016/j.neuron.2005.09.034. PubMedCrossRefGoogle Scholar
  16. Cant, N. B., & Casseday, J. H. (1986). Projections from the anteroventral cochlear nucleus to the lateral and medial superior olivary nuclei. Journal of Comparative Neurology, 247(4), 457–476. doi:  10.1002/cne.902470406. PubMedCrossRefGoogle Scholar
  17. Cant, N. B., & Gaston, K. C. (1982). Pathways connecting the right and left cochlear nuclei. Journal of Comparative Neurology, 212(3), 313–326. doi:  10.1002/cne.902120308. PubMedCrossRefGoogle Scholar
  18. Curtis, D. R., & Eccles, J. C. (1959). The time courses of excitatory and inhibitory synaptic actions. Journal of Physiology, 145(3), 529–546.PubMedGoogle Scholar
  19. Davis, K. A., & Young, E. D. (2000). Pharmacological evidence of inhibitory and disinhibitory neuronal circuits in dorsal cochlear nucleus. Journal of Neurophysiology, 83(2), 926–940.PubMedGoogle Scholar
  20. de la Rocha, J., Marchetti, C., Schiff, M., & Reyes, A. D. (2008). Linking the response properties of cells in auditory cortex with network architecture: Cotuning versus lateral inhibition. Journal of Neuroscience, 28(37), 9151–9163. doi: 28/37/9151[pii] 10.1523/JNEUROSCI.1789-08.2008. PubMedCrossRefGoogle Scholar
  21. Doucet, J. R., & Ryugo, D. K. (2003). Axonal pathways to the lateral superior olive labeled with biotinylated dextran amine injections in the dorsal cochlear nucleus of rats. Journal of Comparative Neurology, 461(4), 452–465. doi:  10.1002/cne.10722. PubMedCrossRefGoogle Scholar
  22. Doucet, J. R., & Ryugo, D. K. (2006). Structural and functional classes of multipolar cells in the ventral cochlear nucleus. Anatomical Record Part A: Discoveries in Molecular, Cellular, and Evolutionary Biology, 288(4), 331–344. doi:  10.1002/ar.a.20294. CrossRefGoogle Scholar
  23. Doucet, J. R., Ross, A. T., Gillespie, M. B., & Ryugo, D. K. (1999). Glycine immunoreactivity of multipolar neurons in the ventral cochlear nucleus which project to the dorsal cochlear nucleus. Journal of Comparative Neurology, 408(4), 515–531. doi:  10.1002/(SICI)1096-9861(19990614)408:4<515::AID-CNE6>3.0.CO;2-O[pii<515::AID-CNE6>3.0.CO;2-O[pii].PubMedCrossRefGoogle Scholar
  24. Doucet, J. R., Lenihan, N. M., & May, B. J. (2009). Commissural neurons in the rat ventral cochlear nucleus. Journal of the Association for Research in Otolaryngology, 10(2), 269–280. doi:  10.1007/s10162-008-0155-6. PubMedCrossRefGoogle Scholar
  25. Farrant, M., & Nusser, Z. (2005). Variations on an inhibitory theme: Phasic and tonic activation of GABA(A) receptors. Nature Reviews Neuroscience, 6(3), 215–229. doi: nrn1625[pii] 10.1038/nrn1625. PubMedCrossRefGoogle Scholar
  26. Fatt, P., & Katz, B. (1953). The effect of inhibitory nerve impulses on a crustacean muscle fibre. Journal of Physiology, 121(2), 374–389.PubMedGoogle Scholar
  27. Ferragamo, M. J., Golding, N. L., & Oertel, D. (1998). Synaptic inputs to stellate cells in the ventral cochlear nucleus. Journal of Neurophysiology, 79(1), 51–63.PubMedGoogle Scholar
  28. Gillespie, D. C., Kim, G., & Kandler, K. (2005). Inhibitory synapses in the developing auditory system are glutamatergic. Nature Neuroscience, 8(3), 332–338. doi: nn1397[pii] 10.1038/nn1397. PubMedCrossRefGoogle Scholar
  29. Golding, N. L., & Oertel, D. (1996). Context-dependent synaptic action of glycinergic and GABAergic inputs in the dorsal cochlear nucleus. Journal of Neuroscience, 16(7), 2208–2219.PubMedGoogle Scholar
  30. Grothe, B. (2003). New roles for synaptic inhibition in sound localization. Nature Reviews Neuroscience, 4(7), 540–550. doi:  10.1038/nrn1136nrn1136[pii].PubMedCrossRefGoogle Scholar
  31. Gulledge, A. T., & Stuart, G. J. (2003). Excitatory actions of GABA in the cortex. Neuron, 37(2), 299–309. doi: S0896627302011467[pii].PubMedCrossRefGoogle Scholar
  32. Irvine, D. R., Park, V. N., & McCormick, L. (2001). Mechanisms underlying the sensitivity of neurons in the lateral superior olive to interaural intensity differences. Journal of Neurophysiology, 86(6), 2647–2666.PubMedGoogle Scholar
  33. Jonas, P., Bischofberger, J., & Sandkuhler, J. (1998). Corelease of two fast neurotransmitters at a central synapse. Science, 281(5375), 419–424.PubMedCrossRefGoogle Scholar
  34. Joris, P. X., & Yin, T. C. (1995). Envelope coding in the lateral superior olive. I. Sensitivity to interaural time differences. Journal of Neurophysiology, 73(3), 1043–1062.PubMedGoogle Scholar
  35. Joris, P., & Yin, T. C. (2007). A matter of time: Internal delays in binaural processing. Trends in Neurosciences, 30(2), 70–78. doi: S0166-2236(06)00275-X[pii] 10.1016/j.tins.2006.12.004. PubMedCrossRefGoogle Scholar
  36. Kadner, A., & Berrebi, A. S. (2008). Encoding of temporal features of auditory stimuli in the medial nucleus of the trapezoid body and superior paraolivary nucleus of the rat. Neuroscience, 151(3), 868–887. doi: S0306-4522(07)01408-X[pii] 10.1016/j.neuroscience.2007.11.008. PubMedCrossRefGoogle Scholar
  37. Kadner, A., Kulesza, R. J. Jr., & Berrebi, A. S. (2006). Neurons in the medial nucleus of the trapezoid body and superior paraolivary nucleus of the rat may play a role in sound duration coding. Journal of Neurophysiology, 95(3), 1499–1508. doi: 00902.2005[pii] 10.1152/jn.00902.2005. PubMedCrossRefGoogle Scholar
  38. Kakazu, Y., Akaike, N., Komiyama, S., & Nabekura, J. (1999). Regulation of intracellular chloride by cotransporters in developing lateral superior olive neurons. Journal of Neuroscience, 19(8), 2843–2851.PubMedGoogle Scholar
  39. Kim, G., & Kandler, K. (2003). Elimination and strengthening of glycinergic/GABAergic connections during tonotopic map formation. Nature Neuroscience, 6(3), 282–290. doi:  10.1038/nn1015nn1015[pii].PubMedCrossRefGoogle Scholar
  40. Kim, Y., & Trussell, L. O. (2009). Negative shift in the glycine reversal potential mediated by a Ca2  +  − and pH-dependent mechanism in interneurons. Journal of Neuroscience, 29(37), 11495–11510. doi: 29/37/11495[pii] 10.1523/JNEUROSCI.1086-09.2009. PubMedCrossRefGoogle Scholar
  41. Klug, A., Khan, A., Burger, R. M., Bauer, E. E., Hurley, L. M., Yang, L., Grothe, B., Halvorsen, M. B., & Park, T. J. (2000). Latency as a function of intensity in auditory neurons: Influences of central processing. Hearing Research, 148(1–2), 107–123. doi: S0378-5955(00)00146-5[pii].PubMedCrossRefGoogle Scholar
  42. Kolston, J., Osen, K. K., Hackney, C. M., Ottersen, O. P., & Storm-Mathisen, J. (1992). An atlas of glycine- and GABA-like immunoreactivity and colocalization in the cochlear nuclear complex of the guinea pig. Anatomy and Embryology, 186(5), 443–465.PubMedCrossRefGoogle Scholar
  43. Kotak, V. C., & Sanes, D. H. (2003). Gain adjustment of inhibitory synapses in the auditory system. Biological Cybernetics, 89(5), 363–370. doi:  10.1007/s00422-003-0441-7. PubMedCrossRefGoogle Scholar
  44. Kulesza, R. J. Jr., Spirou, G. A., & Berrebi, A. S. (2003). Physiological response properties of neurons in the superior paraolivary nucleus of the rat. Journal of Neurophysiology, 89(4), 2299–2312. doi:  10.1152/jn.00547.200200547.2002[pii].PubMedCrossRefGoogle Scholar
  45. Kulesza, R. J. Jr., Kadner, A., & Berrebi, A. S. (2007). Distinct roles for glycine and GABA in shaping the response properties of neurons in the superior paraolivary nucleus of the rat. Journal of Neurophysiology, 97(2), 1610–1620. doi: 00613.2006[pii] 10.1152/jn.00613.2006. PubMedCrossRefGoogle Scholar
  46. Kullmann, P. H., Ene, F. A., & Kandler, K. (2002). Glycinergic and GABAergic calcium responses in the developing lateral superior olive. European Journal of Neuroscience, 15(7), 1093–1104. doi: 1946[pii].PubMedCrossRefGoogle Scholar
  47. Kuo, S. P., Bradley, L. A., & Trussell, L. O. (2009). Heterogeneous kinetics and pharmacology of synaptic inhibition in the chick auditory brainstem. Journal of Neuroscience, 29(30), 9625–9634. doi: 29/30/9625[pii] 10.1523/JNEUROSCI.0103-09.2009. PubMedCrossRefGoogle Scholar
  48. Lorente de No, V. (1981). The Primary Acoustic Nuclei. New York: Raven Press.Google Scholar
  49. Lu, T., & Trussell, L. O. (2000). Inhibitory transmission mediated by asynchronous transmitter release. Neuron, 26(3), 683–694. doi: S0896-6273(00)81204-0[pii].PubMedCrossRefGoogle Scholar
  50. Lu, T., & Trussell, L. O. (2001). Mixed excitatory and inhibitory GABA-mediated transmission in chick cochlear nucleus. Journal of Physiology, 535(Pt. 1), 125–131. doi: PHY_12754 [pii].PubMedCrossRefGoogle Scholar
  51. Lu, T., Rubio, M. E., & Trussell, L. O. (2008). Glycinergic transmission shaped by the corelease of GABA in a mammalian auditory synapse. Neuron, 57(4), 524–535. doi: S0896-6273(07)01010-0[pii] 10.1016/j.neuron.2007.12.010. PubMedCrossRefGoogle Scholar
  52. Magnusson, A. K., Kapfer, C., Grothe, B., & Koch, U. (2005). Maturation of glycinergic inhibition in the gerbil medial superior olive after hearing onset. Journal of Physiology, 568(Pt. 2), 497–512. doi: jphysiol.2005.094763[pii] 10.1113/jphysiol.2005.094763. PubMedCrossRefGoogle Scholar
  53. McBain, C. J., & Fisahn, A. (2001). Interneurons unbound. Nature Reviews Neuroscience, 2(1), 11–23. doi:  10.1038/35049047. PubMedCrossRefGoogle Scholar
  54. Miller, P. S., & Smart, T. G. (2010). Binding, activation and modulation of Cys-loop receptors. Trends in Pharmacological Sciences, 31(4), 161–174. doi: S0165-6147(09)00211-9[pii] 10.1016/j.tips.2009.12.005. PubMedCrossRefGoogle Scholar
  55. Monsivais, P., & Rubel, E. W. (2001). Accommodation enhances depolarizing inhibition in central neurons. Journal of Neuroscience, 21(19), 7823–7830. doi: 21/19/7823[pii].PubMedGoogle Scholar
  56. Monsivais, P., Yang, L., & Rubel, E. W. (2000). GABAergic inhibition in nucleus magnocellularis: Implications for phase locking in the avian auditory brainstem. Journal of Neuroscience, 20(8), 2954–2963.PubMedGoogle Scholar
  57. Moore, J. K., Osen, K. K., Storm-Mathisen, J., & Ottersen, O. P. (1996). Gamma-aminobutyric acid and glycine in the baboon cochlear nuclei: An immunocytochemical colocalization study with reference to interspecies differences in inhibitory systems. Journal of Comparative Neurology, 369(4), 497–519. doi:  10.1002/(SICI)1096-9861(19960610)369:4<497::AID-CNE2>3.0.CO;2-#[pii4<497::AID-CNE2>3.0.CO;2-#[pii].PubMedCrossRefGoogle Scholar
  58. Mugnaini, E. (1985). GABA neurons in the superficial layers of the rat dorsal cochlear nucleus: Light and electron microscopic immunocytochemistry. Journal of Comparative Neurology, 235(1), 61–81. doi:  10.1002/cne.902350106. PubMedCrossRefGoogle Scholar
  59. Nabekura, J., Katsurabayashi, S., Kakazu, Y., Shibata, S., Matsubara, A., Jinno, S., Mizoguchi, Y., Sasaki, A., & Ishibashi, H. (2004). Developmental switch from GABA to glycine release in single central synaptic terminals. Nature Neuroscience, 7(1), 17–23. doi:  10.1038/nn1170nn1170[pii].PubMedCrossRefGoogle Scholar
  60. Needham, K., & Paolini, A. G. (2003). Fast inhibition underlies the transmission of auditory information between cochlear nuclei. Journal of Neuroscience, 23(15), 6357–6361. doi: 23/15/6357[pii].PubMedGoogle Scholar
  61. Needham, K., & Paolini, A. G. (2007). The commissural pathway and cochlear nucleus bushy neurons: An in vivo intracellular investigation. Brain Research, 1134(1), 113–121. doi: S0006-8993(06)03459-7[pii] 10.1016/j.brainres.2006.11.058. PubMedCrossRefGoogle Scholar
  62. Nelken, I., & Young, E. D. (1994). Two separate inhibitory mechanisms shape the responses of dorsal cochlear nucleus type IV units to narrowband and wideband stimuli. Journal of Neurophysiology, 71(6), 2446–2462.PubMedGoogle Scholar
  63. Noh, J., Seal, R. P., Garver, J. A., Edwards, R. H., & Kandler, K. (2010). Glutamate co-release at GABA/glycinergic synapses is crucial for the refinement of an inhibitory map. Nature Neuroscience, 13(2), 232–238. doi: nn.2478[pii] 10.1038/nn.2478. PubMedCrossRefGoogle Scholar
  64. Oertel, D., & Young, E. D. (2004). What’s a cerebellar circuit doing in the auditory system? Trends in Neurosciences, 27(2), 104–110. doi:  10.1016/j.tins.2003.12.001S0166223603003862[pii].PubMedCrossRefGoogle Scholar
  65. Oertel, D., Wu, S. H., Garb, M. W., & Dizack, C. (1990). Morphology and physiology of cells in slice preparations of the posteroventral cochlear nucleus of mice. Journal of Comparative Neurology, 295(1), 136–154. doi:  10.1002/cne.902950112. PubMedCrossRefGoogle Scholar
  66. Osen, K. K. (1969). The intrinsic organization of the cochlear nuclei. Acta Otolaryngologica, 67(2), 352–359.CrossRefGoogle Scholar
  67. Ostapoff, E. M., Benson, C. G., & Saint Marie, R. L. (1997). GABA- and glycine-immunoreactive projections from the superior olivary complex to the cochlear nucleus in guinea pig. Journal of Comparative Neurology, 381(4), 500–512. doi:  10.1002/(SICI)1096-9861(19970519)381:4<500::AID-CNE9>3.0.CO;2–6 <500::AID-CNE9>3.0.CO;2–6 [pii].PubMedCrossRefGoogle Scholar
  68. Palombi, P. S., & Caspary, D. M. (1992). GABAA receptor antagonist bicuculline alters response properties of posteroventral cochlear nucleus neurons. Journal of Neurophysiology, 67(3), 738–746.PubMedGoogle Scholar
  69. Park, T. J., Grothe, B., Pollak, G. D., Schuller, G., & Koch, U. (1996). Neural delays shape selectivity to interaural intensity differences in the lateral superior olive. Journal of Neuroscience, 16(20), 6554–6566.PubMedGoogle Scholar
  70. Pecka, M., Zahn, T. P., Saunier-Rebori, B., Siveke, I., Felmy, F., Wiegrebe, L., Klug, A., Pollak, G. D., & Grothe, B. (2007). Inhibiting the inhibition: A neuronal network for sound localization in reverberant environments. Journal of Neuroscience, 27(7), 1782–1790. doi: 27/7/1782[pii] 10.1523/JNEUROSCI.5335-06.2007. PubMedCrossRefGoogle Scholar
  71. Piechotta, K., Weth, F., Harvey, R. J., & Friauf, E. (2001). Localization of rat glycine receptor alpha1 and alpha2 subunit transcripts in the developing auditory brainstem. Journal of Comparative Neurology, 438(3), 336–352. doi:  10.1002/cne.1319[pii].PubMedCrossRefGoogle Scholar
  72. Rhode, W. S. (1999). Vertical cell responses to sound in cat dorsal cochlear nucleus. Journal of Neurophysiology, 82(2), 1019–1032.PubMedGoogle Scholar
  73. Rhode, W. S., Oertel, D., & Smith, P. H. (1983a). Physiological response properties of cells labeled intracellularly with horseradish peroxidase in cat ventral cochlear nucleus. Journal of Comparative Neurology, 213(4), 448–463. doi:  10.1002/cne.902130408. PubMedCrossRefGoogle Scholar
  74. Rhode, W. S., Smith, P. H., & Oertel, D. (1983b). Physiological response properties of cells labeled intracellularly with horseradish peroxidase in cat dorsal cochlear nucleus. Journal of Comparative Neurology, 213(4), 426–447. doi:  10.1002/cne.902130407. PubMedCrossRefGoogle Scholar
  75. Rivera, C., Voipio, J., Payne, J. A., Ruusuvuori, E., Lahtinen, H., Lamsa, K., Pirvola, U., Saarma, M., & Kaila, K. (1999). The K+/Cl- co-transporter KCC2 renders GABA hyperpolarizing during neuronal maturation. Nature, 397(6716), 251–255. doi:  10.1038/16697. PubMedCrossRefGoogle Scholar
  76. Roberts, M. T., & Trussell, L. O. (2010). Molecular layer inhibitory interneurons provide feedforward and lateral inhibition in the dorsal cochlear nucleus. Journal of Neurophysiology. doi: jn.00312.2010[pii] 10.1152/jn.00312.2010.
  77. Roberts, M. T., Bender, K. J., & Trussell, L. O. (2008). Fidelity of complex spike-mediated synaptic transmission between inhibitory interneurons. Journal of Neuroscience, 28(38), 9440–9450. doi: 28/38/9440[pii] 10.1523/JNEUROSCI.2226-08.2008. PubMedCrossRefGoogle Scholar
  78. Rodrigues, A. R., & Oertel, D. (2006). Hyperpolarization-activated currents regulate excitability in stellate cells of the mammalian ventral cochlear nucleus. Journal of Neurophysiology, 95(1), 76–87. doi: 00624.2005[pii] 10.1152/jn.00624.2005. PubMedCrossRefGoogle Scholar
  79. Rubio, M. E., & Juiz, J. M. (2004). Differential distribution of synaptic endings containing glutamate, glycine, and GABA in the rat dorsal cochlear nucleus. Journal of Comparative Neurology, 477(3), 253–272. doi:  10.1002/cne.20248. PubMedCrossRefGoogle Scholar
  80. Sanes, D. H. (1990). An in vitro analysis of sound localization mechanisms in the gerbil lateral superior olive. Journal of Neuroscience, 10(11), 3494–3506.PubMedGoogle Scholar
  81. Schofield, B. R., & Cant, N. B. (1996). Origins and targets of commissural connections between the cochlear nuclei in guinea pigs. Journal of Comparative Neurology, 375(1), 128–146. doi:  10.1002/(SICI)1096-9861(19961104)375:1<128::AID-CNE8>3.0.CO;2-5[pii<128::AID-CNE8>3.0.CO;2-5[pii].PubMedCrossRefGoogle Scholar
  82. Semyanov, A., Walker, M. C., Kullmann, D. M., & Silver, R. A. (2004). Tonically active GABA A receptors: Modulating gain and maintaining the tone. Trends in Neurosciences, 27(5), 262–269. doi:  10.1016/j.tins.2004.03.005S0166223604000906[pii].PubMedCrossRefGoogle Scholar
  83. Shore, S. E., Sumner, C. J., Bledsoe, S. C., & Lu, J. (2003). Effects of contralateral sound stimulation on unit activity of ventral cochlear nucleus neurons. Experimental Brain Research, 153(4), 427–435. doi:  10.1007/s00221-003-1610-6. CrossRefGoogle Scholar
  84. Simat, M., Parpan, F., & Fritschy, J. M. (2007). Heterogeneity of glycinergic and gabaergic interneurons in the granule cell layer of mouse cerebellum. Journal of Comparative Neurology, 500(1), 71–83. doi:  10.1002/cne.21142. PubMedCrossRefGoogle Scholar
  85. Smith, P. H., & Rhode, W. S. (1989). Structural and functional properties distinguish two types of multipolar cells in the ventral cochlear nucleus. Journal of Comparative Neurology, 282(4), 595–616. doi:  10.1002/cne.902820410. PubMedCrossRefGoogle Scholar
  86. Street, S. E., & Manis, P. B. (2007). Action potential timing precision in dorsal cochlear nucleus pyramidal cells. Journal of Neurophysiology, 97(6), 4162–4172. doi: 00469.2006[pii] 10.1152/jn.00469.2006. PubMedCrossRefGoogle Scholar
  87. Thompson, A. M. (1998). Heterogeneous projections of the cat posteroventral cochlear nucleus. Journal of Comparative Neurology, 390(3), 439–453. doi:  10.1002/(SICI)1096-9861(19980119)390:3<439::AID-CNE10>3.0.CO;2-J[pii<439::AID-CNE10>3.0.CO;2-J[pii].PubMedCrossRefGoogle Scholar
  88. Tollin, D. J. (2003). The lateral superior olive: A functional role in sound source localization. Neuroscientist, 9(2), 127–143.PubMedCrossRefGoogle Scholar
  89. Trussell, L. O. (1999). Synaptic mechanisms for coding timing in auditory neurons. Annual Review of Physiology, 61, 477–496. doi:  10.1146/annurev.physiol.61.1.477. PubMedCrossRefGoogle Scholar
  90. Voigt, H. F., & Young, E. D. (1988). Neural correlations in the dorsal cochlear nucleus: Pairs of units with similar response properties. Journal of Neurophysiology, 59(3), 1014–1032.PubMedGoogle Scholar
  91. Wenthold, R. J. (1987). Evidence for a glycinergic pathway connecting the two cochlear nuclei: An immunocytochemical and retrograde transport study. Brain Research, 415(1), 183–187. doi: 0006-8993(87)90285-X[pii].PubMedCrossRefGoogle Scholar
  92. 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. doi: 0306-4522(87)92968-X[pii].PubMedCrossRefGoogle Scholar
  93. Wenz, M., Hartmann, A. M., Friauf, E., & Nothwang, H. G. (2009). CIP1 is an activator of the K  +  −Cl- cotransporter KCC2. Biochemical and Biophysical Research Communications, 381(3), 388–392. doi: S0006-291X(09)00311-8[pii] 10.1016/j.bbrc.2009.02.057. PubMedCrossRefGoogle Scholar
  94. Wickesberg, R. E., & Oertel, D. (1990). Delayed, frequency-specific inhibition in the cochlear nuclei of mice: A mechanism for monaural echo suppression. Journal of Neuroscience, 10(6), 1762–1768.PubMedGoogle Scholar
  95. Wickesberg, R. E., Whitlon, D., & Oertel, D. (1991). Tuberculoventral neurons project to the multipolar cell area but not to the octopus cell area of the posteroventral cochlear nucleus. Journal of Comparative Neurology, 313(3), 457–468. doi:  10.1002/cne.903130306. PubMedCrossRefGoogle Scholar
  96. Wojcik, S. M., Katsurabayashi, S., Guillemin, I., Friauf, E., Rosenmund, C., Brose, N., & Rhee, J. S. (2006). A shared vesicular carrier allows synaptic corelease of GABA and glycine. Neuron, 50(4), 575–587. doi: S0896-6273(06)00307-2[pii] 10.1016/j.neuron.2006.04.016. PubMedCrossRefGoogle Scholar
  97. Wollmuth, L. P., & Sobolevsky, A. I. (2004). Structure and gating of the glutamate receptor ion channel. Trends in Neurosciences, 27(6), 321–328. doi:  10.1016/j.tins.2004.04.005S0166223604001250[pii].PubMedCrossRefGoogle Scholar
  98. Wouterlood, F. G., Mugnaini, E., Osen, K. K., & Dahl, A. L. (1984). Stellate neurons in rat dorsal cochlear nucleus studies with combined Golgi impregnation and electron microscopy: Synaptic connections and mutual coupling by gap junctions. Journal of Neurocytology, 13(4), 639–664.PubMedCrossRefGoogle Scholar
  99. Wu, S. H., & Kelly, J. B. (1992a). Binaural interaction in the lateral superior olive: Time difference sensitivity studied in mouse brain slice. Journal of Neurophysiology, 68(4), 1151–1159.PubMedGoogle Scholar
  100. Wu, S. H., & Kelly, J. B. (1992b). Synaptic pharmacology of the superior olivary complex studied in mouse brain slice. Journal of Neuroscience, 12(8), 3084–3097.PubMedGoogle Scholar
  101. Wu, S. H., & Kelly, J. B. (1994). Physiological evidence for ipsilateral inhibition in the lateral superior olive: Synaptic responses in mouse brain slice. Hearing Research, 73(1), 57–64.PubMedCrossRefGoogle Scholar
  102. Yang, L., Monsivais, P., & Rubel, E. W. (1999). The superior olivary nucleus and its influence on nucleus laminaris: A source of inhibitory feedback for coincidence detection in the avian auditory brainstem. Journal of Neuroscience, 19(6), 2313–2325.PubMedGoogle Scholar
  103. Yin, T. C. T. (2002). Neural mechanisms of encoding binaural localization cue in the audutory brainstem. In D. Oertel, R. R. Fay, & A. N. Popper (Eds.), Integrative Functions in the Mammalian Auditory Pathway (pp. 99–159). New York: Springer.Google Scholar
  104. Young, E. D., & Davis, K. A. (2002). Circuitry and function of the dorsal cochlear nucleus. In D. Oertel, R. R. Fay, & A. N. Popper (Eds.), Integrative Functions in the Mammalian Auditory Pathway (pp. 160–206). New York: Springer.Google Scholar
  105. Zhang, S., & Oertel, D. (1993). Cartwheel and superficial stellate cells of the dorsal cochlear nucleus of mice: Intracellular recordings in slices. Journal of Neurophysiology, 69(5), 1384–1397.PubMedGoogle Scholar
  106. Zhang, S., & Oertel, D. (1994). Neuronal circuits associated with the output of the dorsal cochlear nucleus through fusiform cells. Journal of Neurophysiology, 71(3), 914–930.PubMedGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2012

Authors and Affiliations

  1. 1.Vollum Institute, Oregon Hearing Research CenterOregon Health and Science UniversityPortlandUSA

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