Hearing loss alters the subcellular distribution of presynaptic GAD and postsynaptic GABAA receptors in the auditory cortex

Cerebral Cortex

Volumn 18, Issue 12, 2008, Pages 2855-2867

  Sarro, Emma C ^a   Kotak, Vibhakar C ^a   Sanes, Dan H ^a   Aoki, Chiye ^a  

^a NEW YORK UNIVERSITY   (United States)

Author keywords

2 3 subunits; Deafness; Development; Electron microscopy; Immunocytochemistry

Indexed keywords

4 AMINOBUTYRIC ACID; 4 AMINOBUTYRIC ACID A RECEPTOR; 4 AMINOBUTYRIC ACID A RECEPTOR BETA2; 4 AMINOBUTYRIC ACID A RECEPTOR BETA3; GLUTAMATE DECARBOXYLASE; POSTSYNAPTIC RECEPTOR; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; AUDITORY CORTEX; CELL MEMBRANE; CELLULAR DISTRIBUTION; CONTROLLED STUDY; ELECTRON MICROSCOPY; GERBIL; HEARING LOSS; IMMUNOCYTOCHEMISTRY; IMMUNOREACTIVITY; INTERNEURON; NERVE CELL EXCITABILITY; NERVE ENDING; NONHUMAN; PERCEPTION DEAFNESS; PERIKARYON; POSTSYNAPTIC MEMBRANE; PRESYNAPTIC MEMBRANE; PRIORITY JOURNAL; PYRAMIDAL NERVE CELL; UPREGULATION;

ANIMALS; AUDITORY CORTEX; AXONS; DENDRITES; GERBILLINAE; GLUTAMATE DECARBOXYLASE; HEARING LOSS, SENSORINEURAL; NEURONS; RECEPTORS, GABA-A; REFERENCE VALUES; SYNAPSES; THALAMUS;

EID: 56449091441     PISSN: 10473211     EISSN: 14602199     Source Type: Journal    
DOI: 10.1093/cercor/bhn044     Document Type: Article

References (94)

1. Abbott SD, Hughes LF, Bauer CA, Salvi R, Caspary DM. 1999. Detection of Glutamate Decarboxylase isoforms in rat inferior colliculus following acoustic exposure. Neuroscience. 93:1375-1381.
2. Amin J, Weiss DS. 1993. GABAA receptor needs two homologous domains of the beta-subunit for activation by GABA but not by pentobarbital. Nature. 366:565-569.
3. Aoki C, Mahodomrongkul V, Fujisawa S, Habersat R, Shirao T. 2007. Chemical and morphological alterations of spines within the hippocampus and entorhinal cortex precedes the onset of Alzheimer's disease pathology in double knock-in mice. J Comp Neurol. 505:352-462.
4. Aoki C, Rodrigues S, Kurose H. 2000. Use of electron microscopy in the detection of adrenergic receptors. Methods Mol Biol. 126:535-63.
5. Barnes EM, Jr. 1996. Use-dependent regulation of GABAA receptors. Int Rev Neurobiol. 39:53-76.
6. Baumann SW, Baur R, Sigel E. 2002. Forced subunit assembly in α1β2γ2 GABAA receptors. J Biochem Chem. 277:46020-46025.
7. A receptors. J Neurosci. 23:11158-11166.
8. Bear MF, Schmechel DE, Ebner FF. 1985. Glutamic acid decarboxylase in the striate cortex of normal and monocularly deprived kittens. J Neurosci. 5:1262-1276.
9. A receptor agonists modulate K+ currents in adult hippocampal glial cells in situ. Glia. 26:129-138.
10. Benson DL, Isackson PJ, Hendry SH, Jones EG. 1989. Expression of glutamic acid decarboxylase mRNA in normal and monocularly deprived cat visual cortex. Brain Res Mol Brain Res. 5:279-287.
11. Bragina L, Melone M, Fattorini G, Conti F. 2007. Clozapine upregulates the expression of the vesicular GABA transporter (VGAT) in rat frontal cortex. Mol Psychol. 12:612-619.
12. A receptors in single thalamic neurons and GABAA subunit expression. J Neurophysiol. 86:2312-2322.
13. Browning MD, Bureau M, Dudek EM, Olsen RW. 1990. Protein kinase C and cAMP-dependent protein kinase phosphorylate the β subunit of the purified γ-aminobutyric acid A receptor. Proc Natl Acad Sci USA. 87:1315-1318.
14. A receptor protein in mature brain. J Neurochem. 65:2006-2015.
15. A receptors. Brain Res. 603:234-242.
16. A receptor subunit composition and function in rat auditory system. Neuroscience. 93:307-312.
17. Caspary DM, Milbrandt JC, Helfert RH. 1995. Central auditory aging: GABA changes in the inferior colliculus. Exp Gerontol. 3-4:349-360.
18. Caspary DM, Raze A, Lawhorn Armour BA, Pippin J, Americ SP. 1990. Immunocytochemical and neurochemical evidence for age-related loss of GABA in the inferior colliculus: implications for neural presbycusis. J Neurosci. 10:2363-2372.
19. Charara A, Pare JF, Levey AI, Smith Y. 2005. Synaptic and extrasynaptic GABA-A and GABA-B receptors in the globus pallidus: an electron microscopic immunogold analysis in monkeys. Neuroscience. 131:917-933.
20. Connolly CN, Wooltorton JR, Smart TG, Moss SJ. 1996. Subcellular localization of gamma-aminobutyric acid type A receptors is determined by receptor beta subunits. Proc Natl Acad Sci USA. 93:9899-9904.
21. Davis GW, DiAntonio A, Petersen SA, Goodman CS. 1998. Postsynaptic PKA controls quantal size and reveals a retrograde signal that regulates presynaptic transmitter release in Drosophila. Neuron. 20:305-315.
22. Ducic I, Caruncho HJ, Zhu WJ, Vicini S, Costa E. 1995. γ-Aminobutyric acid gating of Cl- channels in recombinant GABAA receptors. J Pharmacol Exp Ther. 272:438-445.
23. A/benzodiazepine receptor. J Cell Biol. 110:2043-2048.
24. Feldblum S, Ackermann RF, Tobin AJ. 1990. Long-term increase of glutamate decarboxylase mRNA in a rat model of temporal lobe epilepsy. Neuron. 5:361-371.
25. Feldman ML. 1984. Morphology of the neocortical pyramidal neuron. In: Peters A, Jones EG, editors. Cerebral cortex, cellularcomponents of the cerebral cortex. Vol. 1. New York: Plenum Press. p. 123-200.
26. Frank CA, Kennedy MJ, Goold CP, Marek KW, Davis GW. 2006. Mechanisms underlying the rapid induction and sustained expression of synaptic homeostasis. Neuron. 52:663-677.
27. A receptors). Biochem Soc Trans. 31:889-892.
28. A receptor binding in the barrel cortex of developing and adult rats. J Comp Neurol. 395:209-216.
29. Fueta Y, Vasilets LA, Takeda K, Kawamura M, Schwartz W. 2003. Down-regulation of GABA-transporter function by hippocampal translation product: its possible role in epilepsy. Neuroscience. 118:371-378.
30. A receptor subunits in the substantia nigra of the rat: effects of quinolinic acid lesions of the striatum. Eur J Neurosci. 15:1961-1975.
31. Golan H, Grossman Y. 1996. Block of glutamate decarboxylase decreases GABAergic inhibition at the crayfish synapses: possible role of presynaptic metabotropic mechanisms. J Neurophysiol. 75:2089-2098.
32. Häring P, Stähli C, Schoch P, Takács B, Staehelin T, Möhler H. 1985. Monoclonal antibodies reveal structural homogeneity of γ-aminobutyric acid/benzodiazepine receptors in different brain areas. Proc Natl Acad Sci USA. 82:4837-4841.
33. Hendry SH, Jones EG. 1988. Activity-dependent regulation of GABA expression in the visual cortex of adult monkeys. Neuron. 1:701-712.
34. Hirao T, Morimoto K, Yamamoto Y, Watanabe T, Sato H, Sato K, Sato S, Yamada N, Tanaka K, Suwaki H. 1998. Time-dependent and regional expression of GABA transporter mRNAs following amygdala-kindled seizures in rats. Mol. Brain Res. 54:49-55.
35. Holt AG, Asako M, Lomax CA, MacDonald JW, Tong L, Lomax ML, Altschuler RA. 2005. Deafness-related plasticity in the inferior colliculus: gene expression profiling following removal of peripheral activity. J Neurochem. 93:1069-1086.
36. Hua YH, Hu JH, Zhao WJ, Fei J, Yu Y, Zhou XG, Mei ZT, Guo LH. 2001. Overexpression of c-aminobutyric acid transporter subtype I leads to susceptibility to kainic acid-induced seizure in transgenic mice. Cell Res. 11:61-67.
37. Huntsman MM, Isackson PJ, Jones EG. 1994. Lamina-specific expression and activity-dependent regulation of seven GABA, receptor subunit mRNAs in monkey visual cortex. J Neurosci. 14:2236-2259.
38. A receptor heterogeneity between the hypothalamus and cortex. J Chem Neuroanat. 7:243-252.
39. A receptors. J Neurosci. 25:10469-10478.
40. Jiao Y, Zhang C, Yanagawa Y, Sun QQ. 2006. Major effects of sensory experiences on the neocortical inhibitory circuits. J Neurosci. 26:8691-8701.
41. Kang TC, An SJ, Park SK, Hwang IK, Bae JC, Won MH. 2003. Changed vesicular GABA transporter immunoreactivity in the gerbil hippocampus following spontaneous seizure and vigabatrin administration. Neurosci Lett. 335:201-211.
42. A receptors clustered at neocortical synapses. J Neurosci. 22:1328-1337.
43. Kitzes LM. 1984. Some physiological consequences of neonatal cochlear destruction in the inferior colliculus of the gerbil, Meriones unguiculatus. Brain Res. 306:171-178.
44. Kitzes LM, Semple MN. 1985. Single-Unit Responses in the Inferior colliculus: effects of neonatal unilateral cochlear ablation. J Neurophys. 53:1483-1500.
45. Korada S, Schwartz IR. 1999. Development of GABA, glycine and their receptors in the auditory brainstem of gerbil: a light and electron microscopic study. J Comp Neurol. 409:664-681.
46. Kotak VC, Fujusawa S, Lee FA, Karthikeyan O, Aoki C, Sanes DH. 2005. Hearing loss raises excitability in the auditory cortex. J Neurosci. 25:3908-3918
47. Kotak VC, Sanes DHS. 1996. Developmental influence of glycinergic transmission: regulation of NMDA receptor-mediated EPSPs. J Neurosci. 16:1836-1843.
48. Kotak VC, Takesian AE, Sanes DH. Forthcoming. Hearing loss prevents the maturation of GABAergic transmission in the auditory cortex. Cerebral Cortex.
49. MacDonald RL, Olsen RW. 1994. GABAA receptor channels. Annu Rev Neurosci. 17:569-602.
50. Maffei A, Nelson SB, Turrigiano GG. 2004. Selective reconfiguration of layer 4 visual cortical circuitry by visual deprivation. Nat Neurosci. 7:1353-1359.
51. McAlpine D, Martin RL, Mossop JE, Moore DR. 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.
52. Maqueda J, Ramirez M, Lamas M, Gutierrez R. 2003. Glutamic acid decarboxylase (GAD)67, but not GAD65, is constitutively expressed during development and transiently overexpressed by activity in the granule cells of the rat. Neurosci Lett. 353:69-71.
53. Martin DL, Rimvall R. 1993. Regulation of y-aminobutyric acid synthesis in the brain. J Neurochem. 60:395-407.
54. Maxwell DJ, Christie WM, Short AD, Brown AG. 1990. Direct observations of synapses between GABA-immunocreactive boutons and muscle afferent terminals in lamina VI of the cat's spinal cord. Brain Res. 530:215-222.
55. Meier J, Grantyn R. 2004. A gephyrin-related mechanism restraining glycine receptor anchoring at GABAergic synapses. J Neurosci. 24:1398-1405.
56. Micheva KD, Beaulieu C. 1995. Neonatal sensory deprivation induces selective changes in the quantitative distribution of GABA-immunoreactive neurons in the rat barrel field cortex. J Comp Neurol. 361:574-584.
57. A-receptor subtypes really occur in the brain? Trends Neurosci. 19:139-143.
58. Milbrandt JC, Holder TM, Wilson MC, Salvi RJ, Caspary DM. 2000. GAD levels and muscimol binding in rat inferior colliculus following acoustic trauma. Hear Res. 147:251-260.
59. Möhler H. 2006. GABAA receptor diversity and pharmacology. Cell Tissue Res. 326:505-516.
60. Mouton PR. 2002. Principles and Practices of Unbiased Stereology: An Introduction for Bioscientists. Baltimore, MD: Johns Hopkins University Press. p. 1-236.
61. Mower GD, Rustad R, White WF. 1988. Quantitative comparisons of gamma-aminobutyric acid neurons and receptors in the visual cortex of normal and dark-reared cats. J Comp Neurol. 272:293-302.
62. Mower GD, White WF, Rustad R. 1986. [3H]muscimol binding of GABA receptors in the visual cortex of normal and monocularly. Brain Res. 380:253-260.
63. Mossop JR, Wilson MJ, Caspary DM, Moore DR. 2000. Down-regulation of inhibition following unilateral deafening. Hear Res. 147:183-187.
64. Mower GD, Guo Y. 2001. Comparison of the expression of two forms of glutamic acid decarboxylase (GAD67 and GAD65) in the visual cortex of normal and dark-reared cats. Dev Brain Res. 126:65-74.
65. Mugnaini E, Oertel WH. 1985. An atlas of the distribution of GABAergic neurons and terminals in the rat CNS as revealed by GAD immunohistochemistry. In: Bjö rklund A, Hökfelt T, editors. GABA and neuropeptides in the CNS. Vol. 4. New York: Elsevier. p. 436-595.
66. Muzio L, DiBenedetto B, Stoykova A, Boncinelli E, Gruss P, Mallamaci A. 2002. Conversion of cerebral cortex into basal ganglia in Emx2(-/-) Pax6(Sey/Sey) double mutant mice. Nat Neurosci. 5:737-745.
67. A receptor number underlie variation in GABA mini amplitude. Neuron. 19:697-709.
68. A receptors underlies potentiation at hippocampal inhibitory synapses. Nature. 395:172-177.
69. Orozco-Suarez S, Brunson KL, Feria-Velasco A, Ribak CE. 2000. Increased expression of gamma-aminobutyric acid transporter-1 in the forebrain of infant rats with corticotropin-releasing hormone-induced seizures but not in those with hyperthermia-induced seizures. Epilepsy Res. 42:141-157.
70. Peters A, Saint Marie RL. 1984. Smooth and sparsely spinous non-pyramidal cells forming local axonal plexuses. In: Peters A, Jones EG, editors. Cerebral cortex, cellular components of the cerebral cortex. Vol. 1. New York: Plenum Press. p. 419-446.
71. Petersen SA, Fetter RD, Noordermeer JN, Goodman CS, DiAntonio A. 1997. Genetic analysis of glutamate receptors in drosophila reveals a retrograde signal regulating presynaptic transmitter release. Neuron. 19:1237-1248.
72. Rajan R. 1998. Receptor organ damage causes loss of cortical surround inhibition without topographic map plasticity. Nat Neurosci. 1:138-143.
73. Ramirez M, Gutierrez R. 2001. Activity-dependent expression of GAD67 in the granule cells of the rat hippocampus. Brain Res. 917:139-46.
74. Richards JG, Schoch P, Häring P, Takács B, Möhler H. 1987. Resolving GABAA/benzodiazepine receptors: cellular and subcellular localization in the CNS with monoclonal antibodies. J Neurosci. 7:1866-1886.
75. Rimvall K, Martin DL. 1994. The level of GAD67 protein is highly sensitive to small increases in intraneuronal gamma-aminobutyric acid levels. J Neurochem. 62:1375-1381.
76. Rutledge LT. 1978. The effects of denervation and stimulation upon synaptic ultrastructure. J Comp Neurol. 178:117-128.
77. Salvi RJ, Wange J, Ding D. 2000. Auditory plasticity and hyperactivity following cochlear damage. Hear Res. 147:261-274.
78. Sanes DH, 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.
79. Shepherd GM, Pologruto TA, Svoboda K. 2003. Circuit analysis of experience-dependent plasticity in the developing rat barrel cortex. Neuron. 2003(38):277-289.
80. Silver MA, Stryker MP. 2000. Distributions of synaptic vesicle proteins and GAD65 in deprived and nondeprived ocular dominance columns in Layer IV of kitten primary visual cortex are unaffected by monocular deprivation. J Comp Neurol. 422:652-664.
81. Studler B, Sidler C, Fritschy JM. 2005. Differential regulation of GABAA receptor and gephyrin postsynaptic clustering in immature hippocampal neuronal cultures. J Comp Neurol. 484:344-355.
82. Tehrani MH, Barnes EM, Jr. 1991. Agonist-dependent internalization of gamma-aminobutyric acid A/benzodiazepine receptors in chick cortical neurons. J Neurochem. 57:1307-1312.
83. Tierney TS, Moore DR. 1997. Naturally occurring neuron death during postnatal development of the gerbil ventral cochlear nucleus begins at the onset of hearing. J Comp Neurol. 387:421-429.
84. Tongjaroenbungam W, Jongkamonwiwat N, Cunningham J, Phansuwan-Pujito P, Dodson HC, Forge A, Govitrapong P, Casalotti SO. 2004. Opioid modulation of GABA release in the rat inferior colliculus. BMC Neurosci. 5:31.
85. Trachtenberg JT, Stryker MP. 2001. Rapid anatomical plasticity of horizontal connections in the developing visual cortex. J Neurosci. 21:3476-3482.
86. Turecek R, Trussell LO. 2002. Presynaptic glycine receptors enhance transmitter release at a mammalian central synapse. Nature. 411:587-590.
87. Turrigiano G. 2007. Homeostatic signaling: the positive side of negative feedback. Curr Opin Neurobiol. 17:318-324.
88. Vale C, Sanes DH. 2002. The effect of bilateral deafness on excitatory and inhibitory synaptic strength in the inferior colliculus. Eur J Neurosci. 16:2394-2404.
89. Vale C, Schoorlemmer J, Sanes DH. 2003. Deafness disrupts chloride transporter function and inhibitory synaptic transmission. J Neurosci. 23:7516-7524.
90. Vale C, Juiz JM, Moore DR, Sanes DH. 2004. Unilateral cochlear ablation produces greater loss of inhibition in the contralateral inferior colliculus. Eur J Neurosci. 20:2133-2140.
91. A receptors depend on subunit composition. Neuron. 4:919-928.
92. Wafford KA, Bain CJ, Quirk K, McKernan RM, Wingrove PB, Whiting PJ, Kemp JA. 1994. A novel allosteric modulatory site on the GABAA receptor beta subunit. Neuron. 12:775-782.
93. Wierenga CJ, Walsh MF, Turrigiano GG. 2006. Temporal regulation of the expression locus of homeostatic plasticity. J Neurophysiol. 96:2127-2133.
94. Wisden W, Laurie DJ, Monyer H, Seeburg PH. 1992. The distribution of 13 GABA, receptor subunit mRNAs in the rat brain. I. Telencephalon, diencephalon, mesencephalon. J Neurosci. 12:1040-1062.