Monaural conductive hearing loss alters the expression of the GluA3 AMPA and glycine receptor α1 subunits in bushy and fusiform cells of the cochlear nucleus

Neuroscience

Volumn 199, Issue , 2011, Pages 438-451

  Wang, H ^a   Yin, G ^a   Rogers, K ^b   Miralles, C ^b   De Blas, A L ^b   Rubio, M E ^a  

^a UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF CONNECTICUT   (United States)

Author keywords

ABRs; Biochemistry; Densitometry; Earplugging; GABA A 2 3; Immunohistochemistry

Indexed keywords

4 AMINOBUTYRIC ACID A RECEPTOR; GLUTAMATE RECEPTOR; GLUTAMATE RECEPTOR A2; GLUTAMATE RECEPTOR A3; GLYCINE RECEPTOR; GLYCINE RECEPTOR ALPHA1; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIBODY LABELING; ARTICLE; AUDITORY THRESHOLD; COCHLEAR NERVE; CONTROLLED STUDY; HEARING LOSS; IMMUNOHISTOCHEMISTRY; IMMUNOREACTIVITY; MOUSE; NERVE PROJECTION; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; STARTLE REFLEX; SYNAPSE; UPREGULATION;

ANIMALS; COCHLEAR NUCLEUS; FUNCTIONAL LATERALITY; HEARING LOSS, CONDUCTIVE; IMMUNOHISTOCHEMISTRY; NEURONS; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, AMPA; RECEPTORS, GLYCINE;

EID: 83055186498     PISSN: 03064522     EISSN: 18737544     Source Type: Journal    
DOI: 10.1016/j.neuroscience.2011.10.021     Document Type: Article

References (72)

1. Alibardi L. Ultrastructural and immunocytochemical characterization of neurons in the rat ventral cochlear nucleus projecting to the inferior colliculus. Ann Anat 1998, 180:415-426.
2. Alibardi L. Ultrastructural distribution of glycinergic and GABAergic neurons and axon terminals in the rat dorsal cochlear nucleus, with emphasis on granule cell areas. J Anat 2003, 203:31-56.
3. Argence M., Vassias I., Kerhuel L., Vidal P.P., de Waele C. Stimulation by cochlear implant in unilaterally deaf rats reverses the decrease of inhibitory transmission in the inferior colliculus. Eur J Neurosci 2008, 28:1589-1602.
4. Bauer C.A., Turner J.G., Caspary D.M., Myers K.S., Brozoski T.J. Tinnitus and inferior colliculus activity in chinchillas related to three distinct patterns of cochlear trauma. J Neurosci Res 2008, 86:2564-2578.
5. Bledsoe S.C., Koehler S., Tucci D.L., Zhou J., Le Prell C., Shore S.E. Ventral cochlear nucleus responses to contralateral sound are mediated by commissural and olivocochlear pathways. J Neurophysiol 2009, 102:886-900.
6. Brown M.C., Berglund A.M., Kiang N.Y., Ryugo D.K. Central trajectories of type II spiral ganglion neurons. J Comp Neurol 1988, 278:581-590.
7. Brozoski T.J., Bauer C.A., Caspary D.M. Elevated fusiform cell activity in the dorsal cochlear nucleus of chinchillas with psychophysical evidence of tinnitus. J Neurosci 2002, 22:2383-2390.
8. Brozoski T.J., Ciobanu L., Bauer C.A. Central neural activity in rats with tinnitus evaluated with manganese-enhanced magnetic resonance imaging (MEMRI). Hear Res 2007, 228:168-179.
9. Caicedo A., Herbert H. Topography of descending projections from the inferior colliculus to auditory brainstem nuclei in the rat. J Comp Neurol 1993, 328:377-392.
10. A receptor subunits in rat brainstem auditory pathways: cochlear nuclei, superios olivary complex and nucleus of the lateral lemniscus. Neuroscience 2001, 102:625-638.
11. Cant N.B., Benson C.G. Parallel auditory pathways: projection patterns of the different neuronal populations in the dorsal and ventral cochlear nuclei. Brain Res Bull 2003, 60:457-474.
12. Darrow K.N., Maison S.F., Liberman M.C. Cochlear efferent feedback balances interaural sensitivity. Nat Neurosci 2006, 9:1474-1476.
13. Davis G.W. Homeostatic control of neural activity: from phenomenology to molecular design. Annu Rev Neurosci 2006, 29:307-323.
14. Davis K.A., Young E.D. Granule cell activation of complex-spiking neurons in dorsal cochlear nucleus. J Neurosci 1997, 17:6798-6806.
15. Davis K.A., Young E.D. Pharmacological evidence of inhibitory and disinhibitory neuronal circuits in dorsal cochlear nucleus. J Neurophysiol 2000, 83:926-940.
16. De Blas A.L., Vitorica J., Friedrich P. Localization of the GABAA receptor in the rat brain with a monoclonal antibody to the 57,000 Mr peptide of the GABAA receptor/benzodiazepine receptor/Cl-channel complex. J Neurosci 1988, 8:602-614.
17. Derkach V.A., Oh M.C., Guire E.S., Soderling T.R. Regulatory mechanisms of AMPA receptors in synaptic plasticity. Nat Rev Neurosci 2007, 8:101-113.
18. Dong S., Mulders W.H., Rodger J., Robertson D. Changes in neuronal activity and gene expression in guinea-pig auditory brainstem after unilateral partial hearing loss. Neuroscience 2009, 159:1164-1174.
19. Doucet J.R., Ross A.T., Gillespie M.B., Ryugo D.K. Glycine immunoreactivity of multipolar neurons in the ventral cochlear nucleus which project to the dorsal cochlear nucleus. J Comp Neurol 1999, 408:515-531.
20. Douyard J., Shen L., Huganir R.L., Rubio M.E. Differential neuronal and glial expression of GluR1 AMPA receptor subunit and the scaffolding proteins SAP97 and 41N during rat cerebellar development. J Comp Neurol 2007, 502:141-256.
21. A receptors. Nat Rev Neurosci 2005, 6:215-229.
22. Gómez-Nieto R., Rubio M.E. A bushy cell network in the rant ventra cochlear nucleus. J Comp Neurol 2009, 516:241-263.
23. Haenggeli C.A., Pongstaporn T., Doucet J.R., Ryugo D.K. Projections from the spinal trigeminal nucleus to the cochlear nucleus in the rat. J Comp Neurol 2005, 484:191-205.
24. Hou Q., Zhang D., Jarzylo L., Huganir R.L., Man H.Y. Homeostatic regulation of AMPA receptor expression at single hippocampal synapses. Proc Natl Acad Sci U S A 2008, 105:775-780.
25. Huang X., Chen S., Tietz Immunocytochemical detection of regional protein changes in rat sections using computer-assisted image analysis. J Histochem Cythochem 1996, 44:981-987.
26. Hutson K.A., Durham D., Tucci D.L. Consequences of unilateral conductive hearing loss: time dependent regulation of protein synthesis in auditory brainstem nuclei. Hear Res 2007, 233:124-134.
27. Itoh K., Kamiya H., Mitani A., Yasui Y., Takada M., Mizuno N. Direct projections from the dorsal column nuclei and the spinal trigeminal nuclei to the cochlear nuclei in the cat. Brain Res 1987, 400:145-250.
28. Leblond C.P. Quantification of immunohistochemical reactions by radiography in section exposed to 125I-linked antibodies. J Histochem Cytochem 1979, 27:1516-1517.
29. Lévi S., Schweizer C., Bannai H., Pascual O., Charrier C., Triller A. Homeostatic regulation of synaptic GlyR numbers driven by lateral diffusion. Neuron 2008, 59:261-273.
30. Liberman M.C., Brown M.C. Physiology and anatomy of single olivocochlear neurons in the cat. Hear Res 1986, 24:17-36.
31. Liu S.Q., Cull-Candy S.G. Synaptic activity at calcium-permeable AMPA receptors induces a switch in receptor subtype. Nature 2000, 405:454-458.
32. Löhrke S., Friauf E. Developmental distribution of the glutamate receptor subunits KA2, GluR6/7, and delta 1/2 in the rat medial nucleus of the trapezoid body. A quantitative image analysis. Cell Tissue Res 2002, 308:19-33.
33. Lüscher B., Keller C.A. Regulation of GABAA receptor trafficking, channel activity, and functional plasticity of inhibitory synapses. Pharmacol Ther 2004, 102:195-221. [Review].
34. Malinow R., Malenka R.C. AMPA receptor trafficking and synaptic plasticity. Annu Rev Neurosci 2002, 25:103-126.
35. Matsui K., Jahr C.E., Rubio M.E. High concentration rapid transient of glutamate mediates neuron-glia communication via ectopic release. J Neurosci 2005, 25:7538-7547.
36. Middleton J.W., Kiritani T., Pedersen C., Turner J.G., Shepherd G.M., Tzounopoulos T. Mice with behavioral evidence of tinnitus exhibit dorsal cochlear nucleus hyperactivity because of decreased GABAergic inhibition. Proc Natl Acad Sci U S A 2011, 108:7601-7606.
37. Milbrandt J.C., Holder T.M., Wilson M.C., Salvi R.J., Caspary D.M. GAD levels and muscimol binding in rat inferior colliculus following acoustic trauma. Hear Res 2000, 147:251-260.
38. Miralles C.P., Li M., Mehta A.K., Khan Z.U., De Blas A.L. Immunocytochemical localization of the beta (3) subunit of the gamma-aminobutyric acid (A) receptor in the rat brain. J Comp Neurol 1999, 413:535-548.
39. Moore J.K., Osen K.K., Storm-Mathisen J., Ottersen O.P. γ-Aminobutyric acid and glycine in the baboon cochlear nuclei: an immunoctyochemical colocalization study with reference to interspecies differences in inhibitory systems. J Comp Neurol 1996, 369:497-519.
40. Newpher T.M., Ehlers M.D. Glutamate receptor dynamics in dendritic microdomains. Neuron 2008, 58:472-497.
41. O'Brien R.J., Kamboj S., Ehlers M.D., Rosen K.R., Fischbach G.C., Huganir R.L. Activity-dependent modulation of AMPA receptor accumulation. Neuron 1998, 21:1067-1078.
42. Park M., Penick E.C., Edwards J.G., Kauer J.A., Ehlers M.D. Recycing endosome supply AMPA receptors for LTP. Science 2004, 305:1972-1975.
43. Passafaro M., Piëch V., Sheng M. Subunit-specific temporal and spatial patterns of AMPA receptor exocytosis in hippocampal neurons. Nat Neurosci 2001, 4:917-926.
44. Petralia R.S., Wang Y.X., Mayat E., Wenthold R.J. Glutamate receptor subunit 2-selective antibody shows a differential distribution of calcium-impermeable AMPA receptors among populations of neurons. J Comp Neurol 1997, 385:456-476.
45. Petralia R.S., Wang Y.X., Zhao H.M., Wenthold R.J. Ionotropic and metabotropic glutamate receptors show unique postsynaptic, presynaptic, and glial localizations in the dorsal cochlear nucleus. J Comp Neurol 1996, 372:356-383.
46. Portfors C.V., Roberts P.D. Temporal and frequency characteristics of cartwheel cells in the dorsal cochlear nucleus of the awake mouse. J Neurophysiol 2007, 98:744-756.
47. Potash M., Kelly J. Development of directional responses to sounds in the rat (Rattus norvegicus). J Comp Physiol Psychol 1980, 94:864-877.
48. Potashner S.J., Suneja S.K., Benson C.G. Altered glycinergic synaptic activities in guinea pig brain stem auditory nuclei after unilateral cochlear ablation. Hear Res 2000, 147:125-136.
49. Rubio M.E. Redistribution of synaptic AMPA receptors at glutamatergic synapses in the dorsal cochlear nucleus as an early response to cochlear ablation in rats. Hear Res 2006, 216-217. 154-167.
50. Rubio M.E., Gudsnuk K.A., Smith Y., Ryugo D.K. Revealing the molecular layer of the primate dorsal cochlear nucleus. Neuroscience 2008, 154:99-113.
51. Rubio M.E., Wenthold R.J. Glutamate receptors are selectively targeted to postsynaptic sites in neurons. Neuron 1997, 18:939-950.
52. Rubio M.E., Wenthold R.J. Calnexin and the immunoglobulin binding protein (BiP) coimmunoprecipitate with AMPA receptors. J Neurochem 1999, 73:942-948.
53. Ryugo D.K., Pongstaporn T., Wright D.D., Sharp A.H. Inositol1,4,5-triphosphate receptors: immunocytochemical localization in the dorsal cochlear nucleus. J Comp Neurol 1995, 358:102-118.
54. Savtchouk I., Liu S.J. Remodeling of synaptic AMPA receptor subtype alters the probability and pattern of action potential firing. J Neurosci 2011, 31:501-511.
55. Schofield B.R., Coomes D.L. Auditory cortical projections to the cochlear nucleus in guinea pigs. Hear Res 2005, 199:89-102.
56. Shepherd J.D., Huganir R.L. The cell biology of synaptic plasticity: AMPA receptor trafficking. Annu Rev Cell Dev Biol 2007, 23:613-643.
57. Shore S.E., Helfert R.H., Bledsoe S.C., Altschuler R.A., Godfrey D.A. Descending projections to the dorsal and ventral divisions of the cochlear nucleus in guinea pig. Hear Res 1991, 52:255-268.
58. Shore S.E., Sumner C.J., Bledsoe S.C., Lu J. Effects of contralateral sound stimulation on unit activity of ventral cochlear nucleus neurons. Exp Brain Res 2003, 153:427-435.
59. Spangler K.M., Cant N.B., Henkel C.K., Farley G.R., Warr W.B. Descending projections from the superior olivary complex to the cochlear nucleus of the cat. J Comp Neurol 1987, 259:452-465.
60. Sumner C.J., Tucci D.L., Shore S.E. Responses of the ventral cochlear nucleus neurons to contralateral sound after conductive hearing loss. J Neurophysiol 2005, 94:4234-4243.
61. Tucci D.L., Cant N.B., Durham D. Conductive hearing loss results in a decrease in central auditory system activity in the young gerbil. Laryngoscope 1999, 109:1359-1371.
62. Turrigiano G.G., Nelson S.B. Homeostatic plasticity in the developing nervous system. Nat Rev Neurosci 2004, 5:97-107. [Review].
63. Vale C., Sanes D.H. The effect of bilateral deafness on excitatory and inhibitory synaptic strength in the inferior colliculus. Eur J Neurosci 2002, 16:2394-2404.
64. Wang H., Brozoski T.J., Turner J.G., Ling L., Parrish J.L., Hughes L.F., Caspary D.M. Plasticity at glycinergic synapses in dorsal cochlear nucleus of rats with behavioral evidence of tinnitus. Neuroscience 2009, 164:747-759.
65. Warren E.H., Liberman M.C. Effects of contralateral sound on auditory-nerve responses. I. Contributions of cochlear efferents. Hear Res 1989, 37:89-104.
66. Warren E.H., Liberman M.C. Effects of contralateral sound on auditory-nerve responses. II. Dependence on stimulus variables. Hear Res 1989, 37:105-121.
67. Weedman D.L., Ryugo D.K. Pyramidal cells in primary auditory cortex project to cochlear nucleus in rat. Brain Res 1996, 706:97-102.
68. Weinberg R.J., Rustioni A. A cuneocochlear pathway in the rat. Neuroscience 1987, 20:209-219.
69. Whiting B., Moiseff A., Rubio M.E. Cochlear nucleus neurons redistribute synaptic AMPA and glycine receptors in response to monaural conductive hearing loss. Neuroscience 2009, 163:1264-1276.
70. Wright D.D., Ryugo D.K. Mossy fiber projections from the cuneate nucleus to the cochlear nucleus in the rat. J Comp Neurol 1996, 365:159-172.
71. Xu H., Kotak V.C., Sanes D.H. Conductive hearing loss disrupts synaptic and spike adaptation in developing auditory cortex. J Neurosci 2007, 27:9417-9426.
72. Zhou J., Shore S. Projections from the trigeminal nuclear complex to the cochlear nuclei: a retrograde and anterograde tracing study in the guinea pig. J Neurosci Res 2004, 78:901-907.