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.
This is a preview of subscription content, log in via an institution.
Buying options
Tax calculation will be finalised at checkout
Purchases are for personal use only
Learn about institutional subscriptionsReferences
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.
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.
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.
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.]
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.
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].
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].
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.
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.
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.
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.
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].
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.
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.
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.
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.
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.
Curtis, D. R., & Eccles, J. C. (1959). The time courses of excitatory and inhibitory synaptic actions. Journal of Physiology, 145(3), 529–546.
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.
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.
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.
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.
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].
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.
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.
Fatt, P., & Katz, B. (1953). The effect of inhibitory nerve impulses on a crustacean muscle fibre. Journal of Physiology, 121(2), 374–389.
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.
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.
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.
Grothe, B. (2003). New roles for synaptic inhibition in sound localization. Nature Reviews Neuroscience, 4(7), 540–550. doi: 10.1038/nrn1136nrn1136[pii].
Gulledge, A. T., & Stuart, G. J. (2003). Excitatory actions of GABA in the cortex. Neuron, 37(2), 299–309. doi: S0896627302011467[pii].
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.
Jonas, P., Bischofberger, J., & Sandkuhler, J. (1998). Corelease of two fast neurotransmitters at a central synapse. Science, 281(5375), 419–424.
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.
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.
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.
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.
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.
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].
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.
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].
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.
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.
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].
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.
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].
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.
Lorente de No, V. (1981). The Primary Acoustic Nuclei. New York: Raven Press.
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].
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].
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.
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.
McBain, C. J., & Fisahn, A. (2001). Interneurons unbound. Nature Reviews Neuroscience, 2(1), 11–23. doi: 10.1038/35049047.
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.
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].
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.
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].
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.
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].
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].
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.
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.
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.
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].
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.
Osen, K. K. (1969). The intrinsic organization of the cochlear nuclei. Acta Otolaryngologica, 67(2), 352–359.
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].
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.
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.
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.
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].
Rhode, W. S. (1999). Vertical cell responses to sound in cat dorsal cochlear nucleus. Journal of Neurophysiology, 82(2), 1019–1032.
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.
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.
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.
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.
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.
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.
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.
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.
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].
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].
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.
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.
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.
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.
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].
Tollin, D. J. (2003). The lateral superior olive: A functional role in sound source localization. Neuroscientist, 9(2), 127–143.
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.
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.
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].
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].
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.
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.
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.
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.
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].
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.
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.
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.
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.
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.
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.
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.
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.
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.
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).
Author information
Authors and Affiliations
Corresponding author
Editor information
Editors and Affiliations
Rights and permissions
Copyright information
© 2012 Springer Science+Business Media, LLC
About this chapter
Cite this chapter
Trussell, L.O. (2012). Inhibitory Neurons in the Auditory Brainstem. In: Trussell, L., Popper, A., Fay, R. (eds) Synaptic Mechanisms in the Auditory System. Springer Handbook of Auditory Research, vol 41. Springer, New York, NY. https://doi.org/10.1007/978-1-4419-9517-9_7
Download citation
DOI: https://doi.org/10.1007/978-1-4419-9517-9_7
Published:
Publisher Name: Springer, New York, NY
Print ISBN: 978-1-4419-9516-2
Online ISBN: 978-1-4419-9517-9
eBook Packages: Biomedical and Life SciencesBiomedical and Life Sciences (R0)