Abstract
Glutamate signaling in the auditory brainstem is a dynamic process. ItĀ involves the perfect coordination of pre- and postsynaptic factors that reliably permit the transfer of information between neurons. When compared to other brain regions, glutamate signaling in the auditory brainstem is unique in that it provides the initial mechanisms underlying the perception of behaviorally relevant communication signals. Disruptions in such mechanisms are thought to underlie several hearing-related disorders. Relying on the foundation of work by Dr. Edwin Rubel and colleagues, this chapter offers a conceptual overview of factors that regulate glutamate signaling in the auditory brainstem, as well as determinants responsible for development, activity-dependent regulation, pathophysiology, and neuromodulation.
This is a preview of subscription content, log in via an institution to check access.
Access this chapter
Tax calculation will be finalised at checkout
Purchases are for personal use only
Abbreviations
- [Ca2+]i :
-
Intracellular free calcium concentration
- AMPA-R:
-
Ī±-Amino-3-hydroxy-5-methyl-4-isoxazolepropionic acid receptor
- AP:
-
Action potential
- AVCN:
-
Anteroventral cochlear nucleus
- CN:
-
Cochlear nucleus
- CNS:
-
Central nervous system
- DCN:
-
Dorsal cochlear nucleus
- EPSC:
-
Excitatory postsynaptic current
- EPSP:
-
Excitatory postsynaptic potential
- GABABR:
-
Ī³-Aminobutyric acid receptor
- GPCR:
-
G proteinācoupled receptor
- IC:
-
Inferior colliculus
- iGluR:
-
Ionotropic glutamate receptors
- ILD:
-
Interaural level difference
- IPSC:
-
Inhibitory postsynaptic current
- ITD:
-
Interaural time difference
- LSO:
-
Lateral superior olive
- LTD:
-
Long-term depression
- LTP:
-
Long-term potentiation
- mGluR:
-
Metabotropic glutamate receptor
- MNTB:
-
Medial nucleus of trapezoid body
- MSO:
-
Medial superior olive
- NL:
-
Nucleus laminaris
- NM:
-
Cochlear nucleus magnocellularis
- NMDA-R:
-
Ī-Methyl-d-aspartate receptor
- SOC:
-
Superior olivary complex
- TTX:
-
Tetrodotoxin
- VCN:
-
Ventral cochlear nucleus
- VGCC:
-
Voltage-gated calcium channel
References
Anderson, C. T., Radford, R. J., Zastrow, M. L., Zhang, D. Y., et al. (2015). Modulation of extrasynaptic NMDA receptors by synaptic and tonic zinc. Proceedings of the National Academy of Sciences of the USA, 112(20), 2705ā2714.
Barnes-Davies, M., & Forsythe, I. D. (1995). Pre- and postsynaptic glutamate receptors at a giant excitatory synapse in rat auditory brainstem slices. The Journal of Physiology, 488 (Pt 2), 387ā406.
Bartlett, T. E., & Wang, Y. T. (2013). The intersections of NMDAR-dependent synaptic plasticity and cell survival. Neuropharmacology, 74, 59ā68.
Berridge, M. J. (2014). Calcium regulation of neural rhythms, memory and Alzheimerās disease. The Journal of Physiology, 592 (Pt 2), 281ā293.
Bilak, M. M., Bilak, S. R., & Morest, D. K. (1996). Differential expression of N-methyl-d-aspartate receptor in the cochlear nucleus of the mouse. Neuroscience, 75(4), 1075ā1097.
Billups, B., Graham, B. P., Wong, A. Y., & Forsythe, I. D. (2005). Unmasking group III metabotropic glutamate autoreceptor function at excitatory synapses in the rat CNS. The Journal of Physiology, 565(Pt 3), 885ā896.
Blackmer, T., Kuo, S. P., Bender, K. J., Apostolides, P. F., & Trussell, L. O. (2009). Dendritic calcium channels and their activation by synaptic signals in auditory coincidence detector neurons. The Journal of Neurophysiology, 102(2), 1218ā1226.
Born, D. E., & Rubel, E. W. (1985). Afferent influences on brain stem auditory nuclei of the chicken: Neuron number and size following cochlea removal. The Journal of Comparative Neurology, 231(4), 435ā445.
Born, D. E., & Rubel, E. W. (1988). Afferent influences on brain stem auditory nuclei of the chicken: Presynaptic action potentials regulate protein synthesis in nucleus magnocellularis neurons. The Journal of Neuroscience, 8(3), 901ā919.
Brenowitz, S., & Trussell, L. O. (2001). Maturation of synaptic transmission at end-bulb synapses of the cochlear nucleus. The Journal of Neuroscience, 21(23), 9487ā9498.
Brenowitz, S., David, J., & Trussell, L. (1998). Enhancement of synaptic efficacy by presynaptic GABA(B) receptors. Neuron, 20(1), 135ā141.
Carzoli, K. L., & Hyson, R. L. (2011). In vivo analysis of the role of metabotropic glutamate receptors in the afferent regulation of chick cochlear nucleus neurons. Hearing Research, 272(1ā2), 49ā57.
Chalifoux, J. R., & Carter, A. G. (2011). GABAB receptor modulation of synaptic function. Current Opinion in Neurobiology, 21(2), 339ā344.
Chanda, S., & Xu-Friedman, M. A. (2010). A low-affinity antagonist reveals saturation and desensitization in mature synapses in the auditory brain stem. Journal of Neurophysiology, 103(4), 1915ā1926.
Chanda, S., & Xu-Friedman, M. A. (2011). Excitatory modulation in the cochlear nucleus through group I metabotropic glutamate receptor activation. The Journal of Neuroscience, 31(20), 7450ā7455.
Code, R. A., & Carr, C. E. (1994). Choline acetyltransferase-immunoreactive cochlear efferent neurons in the chick auditory brainstem. The Journal of Comparative Neurology, 340(2), 161ā173.
Couchman, K., Grothe, B., & Felmy, F. (2012). Functional localization of neurotransmitter receptors and synaptic inputs to mature neurons of the medial superior olive. Journal of Neurophysiology, 107(4), 1186ā1198.
Cramer, K. S., Bermingham-McDonogh, O., Krull, C. E., & Rubel, E. W. (2004). EphA4 signaling promotes axon segregation in the developing auditory system. Developmental Biology, 269(1), 26ā35.
Cramer, K. S., Cerretti, D. P., & Siddiqui, S. A. (2006). EphB2 regulates axonal growth at the midline in the developing auditory brainstem. Developmental Biology, 295(1), 76ā89.
Denker, A., & Rizzoli, S. O. (2010). Synaptic vesicle pools: An update. Frontiers in Synaptic Neuroscience, 2, 135.
Dietz, B., Jovanovic, S., Wielsch, B., Nerlich, J., et al. (2012). Purinergic modulation of neuronal activity in developing auditory brainstem. The Journal of Neuroscience, 32(31), 10699ā10712.
Dingledine, R., Borges, K., Bowie, D., & Traynelis, S. F. (1999). The glutamate receptor ion channels. Pharmacology Reviews, 51(1), 7ā61.
Ebert, U., & Ostwald, J. (1995). GABA can improve acoustic contrast in the rat ventral cochlear nucleus. Experimental Brain Research, 104(2), 310ā322.
Ene, F. A., Kullmann, P. H., Gillespie, D. C., & Kandler, K. (2003). Glutamatergic calcium responses in the developing lateral superior olive: Receptor types and their specific activation by synaptic activity patterns. Journal of Neurophysiology, 90(4), 2581ā2591.
Ene, F. A., Kalmbach, A., & Kandler, K. (2007). Metabotropic glutamate receptors in the lateral superior olive activate TRP-like channels: Age- and experience-dependent regulation. Journal of Neurophysiology, 97(5), 3365ā3375.
Farazifard, R., & Wu, S. H. (2010). Metabotropic glutamate receptors modulate glutamatergic and GABAergic synaptic transmission in the central nucleus of the inferior colliculus. Brain Research, 1325, 28ā40.
Feldman, D. E., & Knudsen, E. I. (1994). NMDA and non-NMDA glutamate receptors in auditory transmission in the barn owl inferior colliculus. The Journal of Neuroscience, 14(10), 5939ā5958.
Feldman, D. E., & Knudsen, E. I. (1997). An anatomical basis for visual calibration of the auditory space map in the barn owl's midbrain. The Journal of Neuroscience, 17(17), 6820ā6837.
Feldman, D. E., & Knudsen, E. I. (1998). Pharmacological specialization of learned auditory responses in the inferior colliculus of the barn owl. The Journal of Neuroscience, 18(8), 3073ā3087.
Fioravante, D., & Regehr, W. G. (2011). Short-term forms of presynaptic plasticity. Current Opinion in Neurobiology, 21(2), 269ā274.
Flint, A. C., Maisch, U. S., Weishaupt, J. H., Kriegstein, A. R., & Monyer, H. (1997). NR2A subunit expression shortens NMDA receptor synaptic currents in developing neocortex. The Journal of Neuroscience, 17(7), 2469ā2476.
Forsythe, I. D. (1994). Direct patch recording from identified presynaptic terminals mediating glutamatergic EPSCs in the rat CNS, in vitro. The Journal of Physiology, 479 (Pt 3), 381ā387.
Fortune, E. S., & Rose, G. J. (2001). Short-term synaptic plasticity as a temporal filter. Trends in Neuroscience, 24(7), 381ā385.
Franken, T. P., Roberts, M. T., Wei, L., Golding, N. L., & Joris, P. X. (2015). In vivo coincidence detection in mammalian sound localization generates phase delays. Nature Neuroscience, 18(3), 444ā452.
Fujino, K., & Oertel, D. (2003). Bidirectional synaptic plasticity in the cerebellum-like mammalian dorsal cochlear nucleus. Proceedings of the National Academy of Sciences of the USA, 100(1), 265ā270.
Gambrill, A. C., & Barria, A. (2011). NMDA receptor subunit composition controls synaptogenesis and synapse stabilization. Proceedings of the National Academy of Sciences of the USA, 108(14), 5855ā5860.
Gillespie, D. C., Kim, G., & Kandler, K. (2005). Inhibitory synapses in the developing auditory system are glutamatergic. Nature Neuroscience, 8(3), 332ā338.
Hall, B. J., & Ghosh, A. (2008). Regulation of AMPA receptor recruitment at developing synapses. Trends in Neuroscience, 31(2), 82ā89.
Hall, B. J., Ripley, B., & Ghosh, A. (2007). NR2B signaling regulates the development of synaptic AMPA receptor current. The Journal of Neuroscience, 27(49), 13446ā13456.
Harris, J. A., & Rubel, E. W. (2006). Afferent regulation of neuron number in the cochlear nucleus: Cellular and molecular analyses of a critical period. Hearing Research, 216ā217, 127ā137.
Harris, J. A., Iguchi, F., Seidl, A. H., Lurie, D. I., & Rubel, E. W. (2008). Afferent deprivation elicits a transcriptional response associated with neuronal survival after a critical period in the mouse cochlear nucleus. The Journal of Neuroscience, 28(43), 10990ā11002.
Hassfurth, B., Grothe, B., & Koch, U. (2010). The mammalian interaural time difference detection circuit is differentially controlled by GABAB receptors during development. The Journal of Neuroscience, 30(29), 9715ā9727.
He, S., Wang, Y. X., Petralia, R. S., & Brenowitz, S. D. (2014). Cholinergic modulation of large-conductance calcium-activated potassium channels regulates synaptic strength and spine calcium in cartwheel cells of the dorsal cochlear nucleus. The Journal of Neuroscience, 34(15), 5261ā5272.
Henley, J. M., Barker, E. A., & Glebov, O. O. (2011). Routes, destinations and delays: Recent advances in AMPA receptor trafficking. Trends in Neuroscience, 34(5), 258ā268.
Hoffpauir, B. K., Grimes, J. L., Mathers, P. H., & Spirou, G. A. (2006). Synaptogenesis of the calyx of Held: Rapid onset of function and one-to-one morphological innervation. The Journal of Neuroscience, 26(20), 5511ā5523.
Hollmann, M., & Heinemann, S. (1994). Cloned glutamate receptors. Annual Review of Neuroscience, 17, 31ā108.
Hyson, R. L. (1997). Transneuronal regulation of ribosomes after blockade of ionotropic excitatory amino acid receptors. Brain Research, 749(1), 61ā70.
Hyson, R. L. (1998). Activation of metabotropic glutamate receptors is necessary for transneuronal regulation of ribosomes in chick auditory neurons. Brain Research, 809(2), 214ā220.
Hyson, R. L., & Rubel, E. W. (1989). Transneuronal regulation of protein synthesis in the brain-stem auditory system of the chick requires synaptic activation. The Journal of Neuroscience, 9(8), 2835ā2845.
Irie, T., & Ohmori, H. (2008). Presynaptic GABA(B) receptors modulate synaptic facilitation and depression at distinct synapses in fusiform cells of mouse dorsal cochlear nucleus. Biochemical and Biophysical Research Communications, 367(2), 503ā508.
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), 1566ā1571.
Juiz, J. M., Albin, R. L., Helfert, R. H., & Altschuler, R. A. (1994). Distribution of GABAA and GABAB binding sites in the cochlear nucleus of the guinea pig. Brain Research, 639(2), 193ā201.
Kalmbach, A., Kullmann, P. H., & Kandler, K. (2010). NMDAR-mediated calcium transients elicited by glutamate co-release at developing inhibitory synapses. Frontiers in Synaptic Neuroscience, 2, 27.
Kandler, K., & Friauf, E. (1995). Development of glycinergic and glutamatergic synaptic transmission in the auditory brainstem of perinatal rats. The Journal of Neuroscience, 15(10), 6890ā6904.
Kandler, K., & Gillespie, D. C. (2005). Developmental refinement of inhibitory sound-localization circuits. Trends in Neuroscience, 28(6), 290ā296.
Kantamneni, S. (2015). Cross-talk and regulation between glutamate and GABAB receptors. Frontiers in Cellular Neuroscience, 9, 135.
Kato, B. M., & Rubel, E. W. (1999). Glutamate regulates IP3-type and CICR stores in the avian cochlear nucleus. Journal of Neurophysiology, 81(4), 1587ā1596.
Kato, B. M., Lachica, E. A., & Rubel, E. W. (1996). Glutamate modulates intracellular Ca2+ stores in brain stem auditory neurons. Journal of Neurophysiology, 76(1), 646ā650.
Kim, S. J., Kim, Y. S., Yuan, J. P., Petralia, R. S., et al. (2003). Activation of the TRPC1 cation channel by metabotropic glutamate receptor mGluR1. Nature, 426(6964), 285ā291.
Kopp-Scheinpflug, C., Steinert, J. R., & Forsythe, I. D. (2011). Modulation and control of synaptic transmission across the MNTB. Hearing Research, 279(1ā2), 22ā31.
Kotak, V. C., & Sanes, D. H. (1995). Synaptically evoked prolonged depolarizations in the developing auditory system. Journal of Neurophysiology, 74(4), 1611ā1620.
Kotak, V. C., & Sanes, D. H. (1997). Deafferentation weakens excitatory synapses in the developing central auditory system. European Journal of Neuroscience, 9(11), 2340ā2347.
Kuba, H., Koyano, K., & Ohmori, H. (2002). Synaptic depression improves coincidence detection in the nucleus laminaris in brainstem slices of the chick embryo. European Journal of Neuroscience, 15(6), 984ā990.
Kuba, H., Oichi, Y., & Ohmori, H. (2010). Presynaptic activity regulates Na(+) channel distribution at the axon initial segment. Nature, 465(7301), 1075ā1078.
Kushmerick, C., Price, G. D., Taschenberger, H., Puente, N., et al. (2004). Retroinhibition of presynaptic Ca2+ currents by endocannabinoids released via postsynaptic mGluR activation at a calyx synapse. The Journal of Neuroscience, 24(26), 5955ā5965.
Lachica, E. A., Rubsamen, R., Zirpel, L., & Rubel, E. W. (1995). Glutamatergic inhibition of voltage-operated calcium channels in the avian cochlear nucleus. The Journal of Neuroscience, 15(3 Pt 1), 1724ā1734.
Lachica, E. A., Kato, B. M., Lippe, W. R., & Rubel, E. W. (1998). Glutamatergic and GABAergic agonists increase [Ca2+]i in avian cochlear nucleus neurons. Journal of Neurobiology, 37(2), 321ā337.
Levi-Montalcini, R. (1949). The development to the acoustico-vestibular centers in the chick embryo in the absence of the afferent root fibers and of descending fiber tracts. The Journal of Comparative Neurology, 91(2), 209ā241.
Lu, T., & Trussell, L. O. (2007). Development and elimination of endbulb synapses in the chick cochlear nucleus. The Journal of Neuroscience, 27(4), 808ā817.
Lu, Y. (2014). Metabotropic glutamate receptors in auditory processing. Neuroscience, 274, 429ā445.
Lu, Y., & Rubel, E. W. (2005). Activation of metabotropic glutamate receptors inhibits high-voltage-gated calcium channel currents of chicken nucleus magnocellularis neurons. Journal of Neurophysiology, 93(3), 1418ā1428.
Lu, Y., Harris, J. A., & Rubel, E. W. (2007). Development of spontaneous miniature EPSCs in mouse AVCN neurons during a critical period of afferent-dependent neuron survival. Journal of Neurophysiology, 97(1), 635ā646.
Luscher, C., Nicoll, R. A., Malenka, R. C., & Muller, D. (2000). Synaptic plasticity and dynamic modulation of the postsynaptic membrane. Nature Neuroscience, 3(6), 545ā550.
Ma, C. L., Kelly, J. B., & Wu, S. H. (2002). AMPA and NMDA receptors mediate synaptic excitation in the rat's inferior colliculus. Hearing Research, 168(1ā2), 25ā34.
Magnusson, A. K., Park, T. J., Pecka, M., Grothe, B., & Koch, U. (2008). Retrograde GABA signaling adjusts sound localization by balancing excitation and inhibition in the brainstem. Neuron, 59(1), 125ā137.
Malenka, R. C. (1994). Synaptic plasticity in the hippocampus: LTP and LTD. Cell, 78(4), 535ā538.
Martinez-Galan, J. R., Perez-Martinez, F. C., & Juiz, J. M. (2012). Signalling routes and developmental regulation of group I metabotropic glutamate receptors in rat auditory midbrain neurons. Journal of Neuroscience Research, 90(10), 1913ā1923.
Mayer, F., Albrecht, O., Dondzillo, A., & Klug, A. (2014). Glycinergic inhibition to the medial nucleus of the trapezoid body shows prominent facilitation and can sustain high levels of ongoing activity. Journal of Neurophysiology, 112(11), 2901ā2915.
Nicholas, A. H., & Hyson, R. L. (2004). Group I and II metabotropic glutamate receptors are necessary for the activity-dependent regulation of ribosomes in chick auditory neurons. Brain Research, 1014(1ā2), 110ā119.
Nicoletti, F., Wroblewski, J. T., Novelli, A., Alho, H., et al. (1986). The activation of inositol phospholipid metabolism as a signal-transducing system for excitatory amino acids in primary cultures of cerebellar granule cells. The Journal of Neuroscience, 6(7), 1905ā1911.
Nicoletti, F., Bruno, V., Ngomba, R. T., Gradini, R., & Battaglia, G. (2015). Metabotropic glutamate receptors as drug targets: Whatās new? Current Opinion in Pharmacology, 20, 89ā94.
Niedzielski, A. S., & Wenthold, R. J. (1995). Expression of AMPA, kainate, and NMDA receptor subunits in cochlear and vestibular ganglia. The Journal of Neuroscience, 15(3 Pt 2), 2338ā2353.
Nishimaki, T., Jang, I. S., Ishibashi, H., Yamaguchi, J., & Nabekura, J. (2007). Reduction of metabotropic glutamate receptor-mediated heterosynaptic inhibition of developing MNTB-LSO inhibitory synapses. European Journal of Neuroscience, 26(2), 323ā330.
Niswender, C. M., & Conn, P. J. (2010). Metabotropic glutamate receptors: Physiology, pharmacology, and disease. Annual Review of Pharmacology and Toxicology, 50, 295ā322.
Okuda, H., Yamada, R., Kuba, H., & Ohmori, H. (2013). Activation of metabotropic glutamate receptors improves the accuracy of coincidence detection by presynaptic mechanisms in the nucleus laminaris of the chick. The Journal of Physiology, 591(Pt 1), 365ā378.
Oleskevich, S., & Walmsley, B. (2002). Synaptic transmission in the auditory brainstem of normal and congenitally deaf mice. The Journal of Physiology, 540(Pt 2), 447ā455.
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), 709ā719.
Otis, T. S., & Trussell, L. O. (1996). Inhibition of transmitter release shortens the duration of the excitatory synaptic current at a calyceal synapse. Journal of Neurophysiology, 76(5), 3584ā3588.
Otis, T. S., Raman, I. M., & Trussell, L. O. (1995). AMPA receptors with high Ca2+ permeability mediate synaptic transmission in the avian auditory pathway. The Journal of Physiology, 482 (Pt 2), 309ā315.
Paoletti, P., Bellone, C., & Zhou, Q. (2013). NMDA receptor subunit diversity: Impact on receptor properties, synaptic plasticity and disease. Nature Reviews Neuroscience, 14(6), 383ā400.
Parks, T. N. (2000). The AMPA receptors of auditory neurons. Hearing Research, 147(1ā2), 77ā91.
Petralia, R. S., Wang, Y. X., Mayat, E., & Wenthold, R. J. (1997). Glutamate receptor subunit 2-selective antibody shows a differential distribution of calcium-impermeable AMPA receptors among populations of neurons. The Journal of Comparative Neurology, 385(3), 456ā476.
Petralia, R. S., Rubio, M. E., Wang, Y. X., & Wenthold, R. J. (2000). Differential distribution of glutamate receptors in the cochlear nuclei. Hearing Research, 147(1ā2), 59ā69.
Pliss, L., Yang, H., & Xu-Friedman, M. A. (2009). Context-dependent effects of NMDA receptors on precise timing information at the endbulb of Held in the cochlear nucleus. Journal of Neurophysiology, 102(5), 2627ā2637.
Raman, I. M., Zhang, S., & Trussell, L. O. (1994). Pathway-specific variants of AMPA receptors and their contribution to neuronal signaling. The Journal of Neuroscience, 14(8), 4998ā5010.
Ravindranathan, A., Parks, T. N., & Rao, M. S. (1997). New isoforms of the chick glutamate receptor subunit GluR4: Molecular cloning, regional expression and developmental analysis. Brain Research Molecular Brain Research, 50(1ā2), 143ā153.
Ravindranathan, A., Donevan, S. D., Sugden, S. G., Greig, A., et al. (2000). Contrasting molecular composition and channel properties of AMPA receptors on chick auditory and brainstem motor neurons. The Journal of Physiology, 523(Pt 3), 667ā684.
Rondard, P., & Pin, J. P. (2015). Dynamics and modulation of metabotropic glutamate receptors. Current Opinion in Pharmacology, 20, 95ā101.
Rubel, E. W., & Fritzsch, B. (2002). Auditory system development: Primary auditory neurons and their targets. Annual Review of Neuroscience, 25, 51ā101.
Sahley, T. L., Hammonds, M. D., & Musiek, F. E. (2013). Endogenous dynorphins, glutamate and N-methyl-d-aspartate (NMDA) receptors may participate in a stress-mediated type-I auditory neural exacerbation of tinnitus. Brain Research, 1499, 80ā108.
Sanchez, J. T., Gans, D., & Wenstrup, J. J. (2007). Contribution of NMDA and AMPA receptors to temporal patterning of auditory responses in the inferior colliculus. The Journal of Neuroscience, 27(8), 1954ā1963.
Sanchez, J. T., Wang, Y., Rubel, E. W., & Barria, A. (2010). Development of glutamatergic synaptic transmission in binaural auditory neurons. Journal of Neurophysiology, 104(3), 1774ā1789.
Sanchez, J. T., Seidl, A. H., Rubel, E. W., & Barria, A. (2012). Control of neuronal excitability by NMDA-type glutamate receptors in early developing binaural auditory neurons. The Journal of Physiology, 590(Pt 19), 4801ā4818.
Sanchez, J. T., Ghelani, S., & Otto-Meyer, S. (2015). From development to disease: Diverse functions of NMDA-type glutamate receptors in the lower auditory pathway. Neuroscience, 285, 248ā259.
Sanes, D. H., McGee, J., & Walsh, E. J. (1998). Metabotropic glutamate receptor activation modulates sound level processing in the cochlear nucleus. Journal of Neurophysiology, 80(1), 209ā217.
Sanz-Clemente, A., Nicoll, R. A., & Roche, K. W. (2013). Diversity in NMDA receptor composition: Many regulators, many consequences. Neuroscientist, 19(1), 62ā75.
Schneggenburger, R., Sakaba, T., & Neher, E. (2002). Vesicle pools and short-term synaptic depression: Lessons from a large synapse. Trends in Neuroscience, 25(4), 206ā212.
Shore, S. E. (2011). Plasticity of somatosensory inputs to the cochlear nucleus: Implications for tinnitus. Hearing Research, 281(1ā2), 38ā46.
Sladeczek, F., Pin, J. P., Recasens, M., Bockaert, J., & Weiss, S. (1985). Glutamate stimulates inositol phosphate formation in striatal neurones. Nature, 317(6039), 717ā719.
Stange, A., Myoga, M. H., Lingner, A., Ford, M. C., et al. (2013). Adaptation in sound localization: From GABA(B) receptor-mediated synaptic modulation to perception. Nature Neuroscience, 16(12), 1840ā1847.
Steinert, J. R., Postlethwaite, M., Jordan, M. D., Chernova, T., et al. (2010). NMDAR-mediated EPSCs are maintained and accelerate in time course during maturation of mouse and rat auditory brainstem in vitro. The Journal of Physiology, 588(Pt 3), 447ā463.
Stincic, T. L., & Hyson, R. L. (2011). The localization and physiological effects of cannabinoid receptor 1 in the brain stem auditory system of the chick. Neuroscience, 194, 150ā159.
Sun, H., Ma, C. L., Kelly, J. B., & Wu, S. H. (2006). GABAB receptor-mediated presynaptic inhibition of glutamatergic transmission in the inferior colliculus. Neuroscience Letters, 399(1ā2), 151ā156.
Takahashi, T., Forsythe, I. D., Tsujimoto, T., Barnes-Davies, M., & Onodera, K. (1996). Presynaptic calcium current modulation by a metabotropic glutamate receptor. Science, 274(5287), 594ā597.
Tang, Y. Z., & Carr, C. E. (2004). Development of NMDA R1 expression in chicken auditory brainstem. Hearing Research, 191(1ā2), 79ā89.
Tang, Y. Z., & Carr, C. E. (2007). Development of N-methyl-d-aspartate receptor subunits in avian auditory brainstem. The Journal of Comparative Neurology, 502(3), 400ā413.
Tang, Z. Q., Liu, Y. W., Shi, W., Dinh, E. H., et al. (2013). Activation of synaptic group II metabotropic glutamate receptors induces long-term depression at GABAergic synapses in CNS neurons. The Journal Neuroscience, 33(40), 15964ā15977.
Tomita, S., Chen, L., Kawasaki, Y., Petralia, R. S., et al. (2003). Functional studies and distribution define a family of transmembrane AMPA receptor regulatory proteins. The Journal of Cell Biology, 161(4), 805ā816.
Traynelis, S. F., Wollmuth, L. P., McBain, C. J., Menniti, F. S., et al. (2010). Glutamate receptor ion channels: structure, regulation, and function. Pharmacology Review, 62(3), 405ā496.
Trussell, L. (1998). Control of time course of glutamatergic synaptic currents. Progress in Brain Research, 116, 59ā69.
Trussell, L. O. (1999). Synaptic mechanisms for coding timing in auditory neurons. Annual Review of Physiology, 61, 477ā496.
Trussell, L. O. (2002). Transmission at the hair cell synapse. Nature Neuroscience, 5(2), 85ā86.
Trussell, L. O., & Fischbach, G. D. (1989). Glutamate receptor desensitization and its role in synaptic transmission. Neuron, 3(2), 209ā218.
Turecek, R., & Trussell, L. O. (2001). Presynaptic glycine receptors enhance transmitter release at a mammalian central synapse. Nature, 411(6837), 587ā590.
Tzounopoulos, T. (2008). Mechanisms of synaptic plasticity in the dorsal cochlear nucleus: plasticity-induced changes that could underlie tinnitus. American Journal of Audiology, 17(2), S170ā175.
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), 719ā725.
Vale, C., & Sanes, D. H. (2002). The effect of bilateral deafness on excitatory and inhibitory synaptic strength in the inferior colliculus. European Journal of Neuroscience, 16(12), 2394ā2404.
Voytenko, S. V., & Galazyuk, A. V. (2011). mGluRs modulate neuronal firing in the auditory midbrain. Neuroscience Letters, 492(3), 145ā149.
Walmsley, B., Berntson, A., Leao, R. N., & Fyffe, R. E. (2006). Activity-dependent regulation of synaptic strength and neuronal excitability in central auditory pathways. The Journal of Physiology, 572(Pt 2), 313ā321.
Wang, L. C., Tang, Z. Q., & Lu, Y. (2012). Synaptic activity-induced Ca(2+) signaling in avian cochlear nucleus magnocellularis neurons. Neuroscience Reseatch, 72(2), 129ā139.
Wang, Y., Cunningham, D. E., Tempel, B. L., & Rubel, E. W. (2009). Compartment-specific regulation of plasma membrane calcium ATPase type 2 in the chick auditory brainstem. The Journal of Comparative Neurology, 514(6), 624ā640.
Wenzel, A., Villa, M., Mohler, H., & Benke, D. (1996). Developmental and regional expression of NMDA receptor subtypes containing the NR2D subunit in rat brain. Journal of Neurochemistry, 66(3), 1240ā1248.
Wong, A. Y., Billups, B., Johnston, J., Evans, R. J., & Forsythe, I. D. (2006). Endogenous activation of adenosine A1 receptors, but not P2X receptors, during high-frequency synaptic transmission at the calyx of Held. Journal of Neurophysiology, 95(6), 3336ā3342.
Wu, S. H., & Fu, X. W. (1998). Glutamate receptors underlying excitatory synaptic transmission in the rat's lateral superior olive studied in vitro. Hearing Research, 122(1ā2), 47ā59.
Wu, S. H., Ma, C. L., Sivaramakrishnan, S., & Oliver, D. L. (2002). Synaptic modification in neurons of the central nucleus of the inferior colliculus. Hearing Research, 168(1ā2), 43ā54.
Xu-Friedman, M. A., & Regehr, W. G. (2004). Structural contributions to short-term synaptic plasticity. Physiological Reviews, 84(1), 69ā85.
Yang, Y. M., Aitoubah, J., Lauer, A. M., Nuriya, M., et al. (2011). GluA4 is indispensable for driving fast neurotransmission across a high-fidelity central synapse. The Journal of Physiology, 589(Pt 17), 4209ā4227.
Youssoufian, M., Oleskevich, S., & Walmsley, B. (2005). Development of a robust central auditory synapse in congenital deafness. Journal of Neurophysiology, 94(5), 3168ā3180.
Zhang, H., & Kelly, J. B. (2001). AMPA and NMDA receptors regulate responses of neurons in the rat's inferior colliculus. Journal of Neurophysiology, 86(2), 871ā880.
Zhang, S., & Trussell, L. O. (1994). Voltage clamp analysis of excitatory synaptic transmission in the avian nucleus magnocellularis. The Journal of Physiology, 480(Pt 1), 123ā136.
Zirpel, L., & Parks, T. N. (2001). Zinc inhibition of group I mGluR-mediated calcium homeostasis in auditory neurons. Journal of the Association of Research in Otolaryngology, 2(2), 180ā187.
Zirpel, L., & Rubel, E. W. (1996). Eighth nerve activity regulates intracellular calcium concentration of avian cochlear nucleus neurons via a metabotropic glutamate receptor. Journal of Neurophysiology, 76(6), 4127ā4139.
Zirpel, L., Nathanson, N. M., Rubel, E. W., & Hyson, R. L. (1994). Glutamate-stimulated phosphatidylinositol metabolism in the avian cochlear nucleus. Neuroscience Letters, 168(1ā2), 163ā166.
Zirpel, L., Lachica, E. A., & Rubel, E. W. (1995). Activation of a metabotropic glutamate receptor increases intracellular calcium concentrations in neurons of the avian cochlear nucleus. The Journal of Neuroscience, 15(1 Pt 1), 214ā222.
Zirpel, L., Lippe, W. R., & Rubel, E. W. (1998). Activity-dependent regulation of [Ca2+]i in avian cochlear nucleus neurons: Roles of protein kinases A and C and relation to cell death. Journal of Neurophysiolology, 79(5), 2288ā2302.
Zirpel, L., Janowiak, M. A., Taylor, D. A., & Parks, T. N. (2000). Developmental changes in metabotropic glutamate receptor-mediated calcium homeostasis. The Journal of Comparative Neurology, 421(1), 95ā106.
Zucker, R. S., & Regehr, W. G. (2002). Short-term synaptic plasticity. Annual Review in Physiology, 64, 355ā405.
Compliance with Ethics Requirements
Jason Tait Sanchez declares that he has no conflict of interest.
Yong Lu declares that he has no conflict of interest.
Author information
Authors and Affiliations
Corresponding author
Editor information
Editors and Affiliations
Rights and permissions
Copyright information
Ā© 2017 Springer International Publishing AG
About this chapter
Cite this chapter
Sanchez, J.T., Lu, Y. (2017). Glutamate Signaling in the Auditory Brainstem. In: Cramer, K., Coffin, A., Fay, R., Popper, A. (eds) Auditory Development and Plasticity. Springer Handbook of Auditory Research, vol 64. Springer, Cham. https://doi.org/10.1007/978-3-319-21530-3_4
Download citation
DOI: https://doi.org/10.1007/978-3-319-21530-3_4
Published:
Publisher Name: Springer, Cham
Print ISBN: 978-3-319-21529-7
Online ISBN: 978-3-319-21530-3
eBook Packages: Biomedical and Life SciencesBiomedical and Life Sciences (R0)