The effect of bilateral deafness on excitatory and inhibitory synaptic strength in the inferior colliculus

European Journal of Neuroscience

Volumn 16, Issue 12, 2002, Pages 2394-2404

  Vale, Carmen ^a,b   Sanes, Dan H ^a  

^a NEW YORK UNIVERSITY   (United States)

^b University of Castilla La Mancha   (Spain)

Author keywords

Chloride; Deafferentation; GABAA receptor; Gerbil; Inhibitory; NMDA receptor

Indexed keywords

AMPLITUDE MODULATION; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; AUDITORY STIMULATION; BRAIN SLICE; CELL DEATH; COCHLEAR NERVE; COCHLEAR NUCLEUS; CONTROLLED STUDY; EQUILIBRIUM CONSTANT; EXCITATORY POSTSYNAPTIC POTENTIAL; GERBIL; HEARING LOSS; INFERIOR COLLICULUS; INHIBITORY POSTSYNAPTIC POTENTIAL; NERVE CONDUCTION; NEUROTRANSMITTER RELEASE; NONHUMAN; PRIORITY JOURNAL; STIMULATION; SYNAPSE; SYNAPTIC TRANSMISSION; VOLTAGE CLAMP;

ANIMALS; ANIMALS, NEWBORN; AUDITORY PATHWAYS; COCHLEA; DEAFNESS; ELECTRIC STIMULATION; EXCITATORY POSTSYNAPTIC POTENTIALS; FUNCTIONAL LATERALITY; GERBILLINAE; INFERIOR COLLICULUS; MEMBRANE POTENTIALS; NEURAL INHIBITION; NEURONAL PLASTICITY; RECEPTORS, N-METHYL-D-ASPARTATE; SYNAPSES; SYNAPTIC TRANSMISSION;

EID: 0036927954     PISSN: 0953816X     EISSN: None     Source Type: Journal    
DOI: 10.1046/j.1460-9568.2002.02302.x     Document Type: Article

References (91)

1. Adams, J.C. (1979) Ascending projections to the inferior colliculus. J. Comp. Neurol., 183, 519-538.
2. Binns, K.E., Turner, J.P. & Salt, T.E. (1999) Visual experience alters the molecular profile of NMDA-receptor-mediated sensory transmission. Eur. J. Neurosci., 11, 1101-1104.
3. Bledsoe, S.C., Nagase, S., Miller, J.M. & Altschuler, R.A. (1995) Deafness-induced plasticity in the mature central auditory system. Neuroreport, 7, 225-229.
4. 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. J. Neurosci., 8, 901-919.
5. Carmignoto, C. & Vicini, S. (1992) Activity-dependent decrease in NMDA receptor responses during development of the visual cortex. Science, 258, 1007-1011.
6. Caspary, D.M., Holder, T.M., Hughes, L.F., Milbrandt, J.C., McKernan, R.M. & Naritoku, D.K. (1999) Age-related changes in GABA (A) receptor subunit composition and function in rat auditory system. Neuroscience, 93, 307-312.
7. Caspary, D.M., Milbrandt, J.C. & Helfert, R.H. (1995) Central auditory aging: GABA changes in the inferior colliculus. Exp. Gerontol., 30, 349-360.
8. Code, R.A., Durham, D. & Rubel, E.W. (1990) Effects of cochlea removal on GABAergic terminals in nucleus magnocellularis of the chicken. J. Comp. Neurol., 301, 643-654.
9. Coleman, J.R. & Clerici, W.J. (1987) Sources of projections to subdivisions of the inferior colliculus in the rat. J. Comp. Neurol., 262, 215-226.
10. Coleman, J.R. & O'Connor, P. (1979) Effects of monaural and binaural sound deprivation on cell development in the anteroventral cochlear nucleus of rats. Exp. Neurol., 64, 553-566.
11. Czepita, D., Reid, S.N. & Daw, N.W. (1994) Effect of longer periods of dark rearing on NMDA receptors in cat visual cortex. J. Neurophysiol., 72, 1220-1226.
12. Debanne, D., Guérineau, N.C., Gähwiler, B.H. & Thompson, S.M. (1996) Paired-pulse facilitation and depression at unitary synapses in rat hippoccampus: Quantal fluctuation affects subsequent release. J. Physiol. (Lond.), 491, 163-176.
13. Deitch, J.S. & Rubel, E.W. (1984) Afferent influences on brain stem auditory nuclei of the chicken: Time course and specificity of dendritic atrophy following deafferentation. J. Comp. Neurol., 229, 66-79.
14. Deitch, J.S. & Rubel, E.W. (1989) Rapid changes in ultrastructure during deafferentation-induced dendritic atrophy. J. Comp. Neurol., 281, 234-258.
15. Dobrunz, L.E. & Stevens, C.F. (1997) Heterogeneity of release probability, facilitation, and depletion at central synapses. Neuron, 18, 995-1008.
16. Durham, D. & Rubel, E.W. (1985) Afferent influences on brain stem auditory nuclei of the chicken: Succinate dehydrogenase activity following cochlea removal. J. Comp. Neurol., 231, 446-456.
17. Ebihara, S., Shirato, K., Harata, N. & Akaike, N. (1995) Gramicidin perforated patch recording: GABA response in mammalian neurones with intact intracellular chloride. J. Physiol. (Lond.), 484, 77-86.
18. Feng, A.S. & Rogowski, B.A. (1980) Effects of monaural and binaural occlusion on the morphology of neurons in the medial superior olivary nucleus of the rat. Brain Res., 189, 530-534.
19. Fox, K., Daw, N., Sato, H. & Czepita, D. (1992) The effect of visual experience on development of NMDA receptor synaptic transmission in kitten visual cortex. J. Neurosci., 12, 2672-2684.
20. Francis, H.W. & Manis, P.B. (2000) Effects of deafferentation on the electrophysiology of ventral cochlear nucleus neurons. Hear. Res., 149, 91-105.
21. Futai, K., Okada, M., Matsuyama, K. & Takahashi, T. (2001) High-fidelity transmission acquired via a developmental decrease in NMDA receptor expression at an auditory synapse. J. Neurosci., 21, 3342-3349.
22. Ganguly, K., Schinder, A.F., Wong, S.T. & Poo, M. (2001) GABA itself promotes the developmental switch of neuronal GABAergic responses from excitation to inhibition. Cell, 105, 521-532.
23. Gold, J.I. & Knudsen, E.I. (1999) Hearing impairment induces frequency-specific adjustments in auditory spatial tuning in the optic tectum of young owls. J. Neurophysiol., 82, 2197-2209.
24. Hashisaki, G.T. & Rubel, E.W. (1989) Effects of unilateral cochlea removal on anteroventral cochlear nucleus neurons in developing gerbils. J. Comp. Neurol., 283, 465-473.
25. Huang, L. & Pallas, S.L. (2001) NMDA antagonists in the superior colliculus prevent developmental plasticity but not visual transmission or map compression. J. Neurophysiol., 86, 1179-1194.
26. Hyson, R.L. & Rubel, E.W. (1989) Transneuronal regulation of protein synthesis in the brain stem auditory system of the chick requires synaptic activation. J. Neurosci., 9, 2835-2845.
27. Katz, L.C. & Shatz, C.J. (1996) Synaptic activity and the construction of cortical circuits. Science, 274, 1133-1138.
28. Kazaku, I., Akaike, N., Komiyama, S. & Nabekura, J. (1999) Regulation of intracellular chloride by cotransporters in developing lateral superior olive neurons. J. Neurosci., 19, 2843-2851.
29. Kelly, M.K., Carvell, G.E., Kodger, J.M. & Simons, D.J. (1999) Sensory loss by selected whisker removal produces immediate disinhibition in the somatosensory cortex of behaving rats. J. Neurosci., 19, 9117-9125.
30. Kilman, V., van Rossum, M.C.W. & Turrigiano, G.G. (2002) Activity deprivation reduces miniature IPSC amplitude by decreasing the number of postsynaptic GABAA receptors clustered at neocortical synapses. J. Neurosci., 22, 1328-1337.
31. Kitzes, L.M. (1984) Some physiological consequences of neonatal cochlear destruction in the inferior colliculus of the gerbil, Meriones unguiculatus. Brain Res., 306, 171-178.
32. Kitzes, L.M., Kageyama, G.H., Semple, M.N. & Kil, J. (1995) Development of ectopic projections from the ventral cochlear nucleus to the superior olivary complex induced by neonatal ablation of the contralateral cochlea. J. Comp. Neurol., 353, 341-363.
33. Kitzes, L.M. & Semple, M.N. (1985) Single-unit responses in the inferior colliculus: Effects of neonatal unilateral cochlear ablation. J. Neurophysiol., 53, 1483-1500.
34. Klinke, R., Kral, A., Heid, S., Tillein, J. & Hartmann, R. (1999) Recruitment of the auditory cortex in congenitally deaf cats by long-term cochlear electrostimulation. Science, 285, 1729-1733.
35. Kotak, V.C., DiMattina, C. & Sanes, D.H. (2001) GABA (B) and Trk receptor signaling mediates long-lasting inhibitory synaptic depression. J. Neurophysiol., 86, 536-540.
36. Kotak, V.C. & Sanes, D.H. (1995) Synaptically evoked prolonged depolarizations in the developing auditory system. J. Neurophysiol., 74, 1611-1620.
37. Kotak, V.C. & Sanes, D.H. (1996) Developmental influence of glycinergic transmission: Regulation of NMDA receptor-mediated EPSPs. J. Neurosci., 16, 1836-1843.
38. Kotak, V.C. & Sanes, D.H. (1997) Deafferentation weakens excitatory synapses in the developing central auditory system. Eur. J. Neurosci., 9, 2340-2347.
39. Kuwada, S., Batra, R., Yin, T.C.T., Oliver, D.L., Haberly, L.B. & Stanford, T.R. (1997) Intracellular recordings in response to monaural and binaural stimulation of neurons in the inferior colliculus of the cat. J. Neurosci., 17, 7565-7581.
40. Levi-Montalcini, R. (1949) The development of the acoustico-vestibular centers in the chick embryo in the absence of the afferent root fibers and of descending fiber tracts. J. Comp. Neurol., 91, 209-241.
41. Levitt, J.B., Schumer, R.A., Sherman, S.M., Spear, P.D. & Movshon, J.A. (2001) Visual response properties of neurons in the LGN of normally reared and visually deprived macaque monkeys. J. Neurophysiol., 85, 2111-2129.
42. Linden, R. (1994) The survival of developing neurons: A review of afferent control. Neuroscience, 58, 671-682.
43. Lo, Y.-J., Rao, S.C. & Sanes, D.H. (1998) Modulation of calcium by inhibitory systems in the developing auditory midbrain. Neuroscience, 83, 1075-1084.
44. Manabe, T., Wyllie, D.J.A., Perkel, D.J. & Nicoll, R.A. (1993) Modulation of synaptic transmission and long-term potentiation: Effects on paired pulse facilitation and EPSC variance in the CA1 region of the hippocampus. J. Neurophysiol., 70, 1451-1459.
45. McAlpine, D., Martin, R.L., Mossop, J.E. & Moore, D.R. (1997) Response properties of neurons in the inferior colliculus of the monaurally deafened ferret to acoustic stimulation of the intact ear. J. Neurophysiol., 78, 767-779.
46. McMullen, N.T., Goldberger, B., Suter, C.M. & Glaser, E.M. (1988) Neonatal deafening alters nonpyramidal dendrite orientation in auditory cortex: A computer microscopic study in the rabbit. J. Comp. Neurol., 267, 92-106.
47. Moore, D.R. & Kitzes, L.M. (1985) Projections from the cochlear nucleus to the inferior colliculus in normal and neonatally cochlea-ablated gerbils. J. Comp. Neurol., 240, 180-195.
48. Moore, D.R., Kotak, V.C. & Sanes, D.H. (1998) Commissural and Lemniscal synaptic input to the gerbil inferior colliculus. J. Neurophysiol., 80, 2229-2236.
49. Moore, D.R., Rogers, N.J. & O'Leary, S.J. (1998) Loss of cochlear nucleus neurons following aminoglycoside antibiotics or cochlea removal. Ann. Otol. Rhinol. Laringol., 107, 337-343.
50. Mossop, J.E., Wilson, M.J., Caspary, D.M. & Moore, D.R. (2000) Down-regulation of inhibition following unilateral deafening. Hear. Res., 147, 183-187.
51. Mostafapour, S.P., Cochran, S.L., Del Puerto, N.M. & Rubel, E.W. (2000) Patterns of cell death in mouse anteroventral cochlear nucleus neurons after unilateral cochlea removal. J. Comp. Neurol., 426, 561-571.
52. Nagase, S., Miller, J.M., Dupont, J., Lim, H.H., Sato, K. & Altschuler, R.A. (2000) Changes in cochlear electrical stimulation induced Fos expression in the rat inferior colliculus following deafness. Hear. Res., 147, 242-250.
53. Nordeen, K.W., Killackey, H.P. & Kitzes, L.M. (1983) Ascending auditory projections to the inferior colliculus in the adult gerbil, Meriones unguiculatus. J. Comp. Neurol., 214, 131-143.
54. Oleskevich, S. & Walmsley, B. (2002) Synaptic transmission in the auditory brainstem of normal and congenitally deaf mice. J. Physiol. (Lond.), 540, 447-455.
55. Oliver, D.L., Winer, J.A., Beckius, G.E. & Saint Marie, R.L. (1994) Morphology of GABAergic neurons in the inferior colliculus of the cat. J. Comp. Neurol., 340, 27-42.
56. Parks, T.N. (1979) Afferent influences on the development of the brain stem auditory nuclei of the chicken: Otocyst ablation. J. Comp. Neurol., 183, 665-678.
57. Parks, T.N. (1981) Changes in the length and organization of nucleus laminaris dendrites after unilateral otocyst ablation in chick embryos. J. Comp. Neurol., 202, 47-57.
58. Parks, T.N. (2000) The AMPA receptors of auditory neurons. Hear. Res., 147, 77-91.
59. Payne, J.A., Stevenson, T.J. & Donaldson, L.F. (1996) Molecular characterization of a putative K-Cl cotransporter in rat brain. J. Biol. Chem., 27, 16245-16252.
60. Plotkin, M.D., Snyder, E.Y., Hebert, S.C. & Delpire, E. (1997) Expression of the Na-K-Cl cotransporter is developmentally regulated in postnatal rat brains: A possible mechanism underlying GABA's excitatory role in immature brain. J. Neurobiol., 33, 781-795.
61. Potashner, S.J., Suneja, S.K. & Benson, C.G. (1997) Regulation of D-aspartate release and uptake in adult brain stem auditory nuclei after unilateral middle ear ossicle removal and cochlear ablation. Exp. Neurol., 148, 222-235.
62. Quinlan, E.M., Philpot, B.D., Huganir, R.L. & Bear, M.F. (1999) Rapid, experience-dependent expression of synaptic NMDA receptors in visual cortex in vivo. Nature Neurosci., 2, 352-357.
63. Rajan, R. (1998) Receptor organ damage causes loss of cortical surround inhibition without topographic map plasticity. Nature Neurosci., 1, 138-143.
64. Reetz, G. & Ehret, G. (1999) Inputs from three brainstem sources to identified neurons of the mouse inferior colliculus slice. Brain Res., 816, 527-543.
65. Reichling, D.B., Kyrozis, A., Wang. J. & McDermott, A.B. (1994) Mechanism of GABA and glycine depolarization-induced calcium transients in rat dorsal horn neurons. J. Physiol. (Lond.), 476, 411-421.
66. - cotransporter KCC2 renders GABA hyperpolarizing during neuronal maturation. Nature, 397, 251-255.
67. Russell, F.A. & Moore, D.R. (1995) Afferent reorganization within the superior olivary complex of the gerbil: Development and induction by neonatal, unilateral cochlear removal. J. Comp. Neurol., 352, 207-225.
68. Sanes, D.H., Markowitz, S., Bernstein, J. & Wardlow, J. (1992) The influence of inhibitory afferents on the development of postsynaptic dendritic arbors. J. Comp. Neurol., 321, 637-644.
69. Sato, K., Shiraishi, S., Nakagawa, H., Kuriyama, H. & Altschuler, R.A. (2000) Diversity and plasticity in amino acid receptor subunits in the rat auditory brain stem. Hear. Res., 147, 137-144.
70. Schomberg, S.L., Su, G., Haworth, R.A. & Sun, D. (2001) Stimulation of Na-K-2Cl cotransporter in neurons by activation of non-NMDA ionotropic receptor and group-I mGluRs. J. Neurophysiol., 85, 2563-2575.
71. Shepherd, R.K., Baxi, J.H. & Hardie, N.A. (1999) Response of inferior colliculus neurons to electrical stimulation of the auditory nerve in neonatally deafened cats. J. Neurophysiol., 82, 1363-1383.
72. Sherman, S.M. & Spear, P.D. (1982) Organization of visual pathways in normal and visually deprived cats. Physiol. Rev., 62, 738-855.
73. Smith, P.H. (1992) Anatomy and physiology of multipolar-cells in the rat inferior collicular cortex using the in vitro brain slice techniques. J. Neurosci., 12, 3700-3715.
74. Smith, Z.D.J., Gray, L. & Rubel, E.W. (1983) Afferent influences on brainstem auditory nuclei of the chicken: N. laminaris dendritic length following monaural conductive hearing loss. J. Comp. Neurol., 220, 199- 205.
75. Steward, O. & Rubel, E.W. (1985) Afferent influences on brain stem auditory nuclei of the chicken: Cessation of amino acid incorporation as an antecedent to age-dependent transneuronal degeneration. J. Comp. Neurol., 231, 385-395.
76. Sun, D. & Murali, S.G. (1998) Stimulation of Na+-K+-2Cl- cotransporter in neuronal cells by excitatory neurotransmitter glutamate. Am. J. Physiol., 275, C772-C779.
77. Suneja, S.K., Potashner, S.J. & Benson, C.G. (1998) Plastic changes in glycine and GABA release and uptake in adult brain stem auditory nuclei after unilateral middle ear ossicle removal and cochlear ablation. Exp. Neurol., 151, 273-288.
78. Suneja, S.K., Potashner, S.J. & Benson, C.G. (2000) AMPA receptor binding in adult guinea pig brain stem auditory nuclei after unilateral cochlear ablation. Exp. Neurol., 165, 355-369.
79. Thomson, A.M., Deuchars, J. & West, D.C. (1993) Large, deep layer pyramid-pyramid single axon EPSPs in slices of rat motor cortex display paired pulse and frequency-dependent depression, mediated presynaptically and self-facilitation, mediated postsynaptically. J. Neurophysiol., 70, 2354-2369.
80. Tierney, T.S., Russell, F.A. & Moore, D.R. (1997) Susceptibility of developing cochlear nucleus neurons to deafferentation-induced death abruptly ends just before the onset of hearing. J. Comp. Neurol., 378, 295-306.
81. Turrigiano, G.G., Leslie, K.R., Desai, N.S., Rutherford, L.C. & Nelson, S.B. (1998) Activity-dependent scaling of quantal amplitude in neocortical neurons. Nature, 391, 892-896.
82. Vale, C. & Sanes, D.H. (2000) Afferent regulation of inhibitory synaptic transmission in the developing auditory midbrain. J. Neurosci., 20, 1912- 1921.
83. Wagner, T. (1996) Lemniscal input to identified neurons of the central nucleus of mouse inferior colliculus: An intracellular brain slice study. Eur. J. Neurosci., 8, 1231-1239.
84. Webster, D.B. & Webster, M. (1979) Effects of neonatal conductive hearing loss on brain stem auditory nuclei. Ann. Otol. Rhinol. Laryngol., 88, 684-688.
85. Wiesel, T.N. & Hubel, D.H. (1963a) Single-cell responses in striate cortex of kittens deprived of vision in one eye. J. Neurophysiol., 26, 1003-1017.
86. Wiesel, T.N. & Hubel, D.H. (1963b) Effects of visual deprivation on morphology and physiology of cells in the cat's lateral geniculate body. J. Neurophysiol., 26, 978-993.
87. Williams, J.R., Sharp, J.W., Kumari, V.G., Wilson, M. & Payne, J.A. (1999) The neuron-specific K-Cl cotransporter, KCC2. Antibody development and initial characterization of the protein. J. Biol. Chem., 274, 12656-12664.
88. Willott, J.F., Milbrandt, J.C., Bross, L.S. & Caspary, D.M. (1997) Glycine immunoreactivity and receptor binding in the cochlear nucleus of C57BL/6J and CBA/CaJ mice: Effects of cochlear impairment and aging. J. Comp. Neurol., 385, 405-414.
89. Woolf, N.K. & Ryan, A.F. (1985) Ontogeny of neural discharge patterns in the ventral cochlear nucleus of the Mongolian gerbil. Dev. Brain Res., 17, 131-147.
90. Wu, S.H. & Kelly, J.B. (1996) In vitro brain slice studies of the rat's dorsal nucleus of the lateral lemniscus. III. Synaptic pharmacology. J. Neurophysiol., 75, 1271-1282.
91. Xue, J. & Cooper, G.F. (2001) The modification of NMDA receptors by visual experience in the rat retina is age dependent. Mol. Brain. Res., 91, 196-203.