The inferior colliculus of the rat: Quantitative immunocytochemical study of GABA and glycine

Neuroscience

Volumn 136, Issue 3, 2005, Pages 907-925

  Merchan M ^a,b   Aguilar, L A ^a,b,c   Lopez Poveda, E A ^b   Malmierca, M S ^a,b  

^a UNIVERSITY OF SALAMANCA   (Spain)

^b UNIVERSITY OF SALAMANCA   (Spain)

^c UNIVERSIDAD PERUANA CAYETANO HEREDIA   (Peru)

Author keywords

Amino acids; Auditory pathway; Axosomatic endings; Inferior colliculus; Inhibitory neurotransmitters; Optical densitometry

Indexed keywords

4 AMINOBUTYRIC ACID; CYCLINE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; DATA ANALYSIS; DENSITOMETRY; FEMALE; IMMUNOCYTOCHEMISTRY; IMMUNOHISTOCHEMISTRY; IMMUNOREACTIVITY; INFERIOR COLLICULUS; MALE; NONHUMAN; PRIORITY JOURNAL; QUANTITATIVE ANALYSIS; RAT; TOPOGRAPHY;

ANIMALS; BRAIN MAPPING; CELL COUNT; FEMALE; GAMMA-AMINOBUTYRIC ACID; GLYCINE; IMMUNOHISTOCHEMISTRY; INFERIOR COLLICULUS; MALE; MICROSCOPY, ELECTRON, SCANNING; MODELS, ANATOMIC; NEURONS; RATS; RATS, WISTAR;

EID: 28844483712     PISSN: 03064522     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.neuroscience.2004.12.030     Document Type: Article

References (109)

1. J.C. Adams Ascending projections to the inferior colliculus J Comp Neurol 183 1979 519 538
2. J.C. Adams Multipolar cells in the ventral cochlear nucleus project to the dorsal cochlear nucleus and the inferior colliculus Neurosci Lett 37 1983 205 208
3. L.M. Aitkin, S.C. Phillips Is the inferior colliculus an obligatory relay in the cat auditory system? Neurosci Lett 44 1984 259 264
4. L.M. Aitkin, S.C. Phillips The interconnections of the inferior colliculi through their commissure J Comp Neurol 228 1984 210 216
5. P. Arcelli, C. Frassoni, M.C. Regondi, S. De Biasi, R. Spreafico GABAergic neurons in mammalian thalamus a marker of thalamic complexity? Brain Res Bull 42 1997 27 37
6. V.M. Bajo, M.A. Merchán, D.E. López, E.M. Roullier Neuronal morphology and efferent projections of the dorsal nucleus of the lateral lemniscus of the cat J Comp Neurol 334 1993 241 262
7. E.L. Bartlett, J.M. Stark, R.W. Guillery, P.H. Smith Comparison of the fine structure of cortical and collicular terminals in the rat medial geniculate body Neuroscience 100 2000 811 828
8. C.A. Bauer, T.J. Brozoski, T.M. Holder, D.M. Caspary Effects of chronic salicylate on GABAergic activity in rat inferior colliculus Hear Res 147 2000 175 182
9. B.D. Beyerl Afferent projections to the central nucleus of the inferior colliculus in the rat Brain Res 145 1978 209 223
10. P. Brodal, G. Mihailoff, B. Border, O.P. Ottersen, J. Storm-Mathisen GABA-containing neurons in the pontine nuclei of rat cat and monkey an immunocytochemical study Neuroscience 25 1988 27 45
11. J.K. Brunsø-Bechtold, G.C. Thompson, R.B. Masterton HRP study of the organization of auditory afferents ascending to central nucleus of inferior colliculus in cat J Comp Neurol 197 1981 705 722
12. D.M. Caspary, T.M. Holder, L.F. Hughes, J.C. Milbrandt, R.M. McKernan, D.K. Naritoku Age-related changes in GABAA receptor subunit composition and function in rat auditory system Neuroscience 93 1999 307 312
13. J.H. Casseday, T. Fremouw, E. Covey The inferior colliculus, a hub in the midbrain D. Oertel R.R. Fay A.N. Popper Integrative functions in the mammalian auditory pathway 2002 Springer-Verlag New York 238 318
14. J.R. Coleman, W.J. Clerici Sources of projections to subdivisions of the inferior colliculus in the rat J Comp Neurol 262 1987 215 226
15. D.L. Coomes, M.E. Bickford, B.R. Schofield GABAergic circuitry in the dorsal division of the cat medial geniculate nucleus J Comp Neurol 453 2002 45 56
16. C.L. Faingold Neuronal networks in the genetically epilepsy-prone rat Adv Neurol 79 1999 311 321
17. C.L. Faingold Role of GABA abnormalities in the inferior colliculus pathophysiology audiogenic seizures Hear Res 168 2002 223 237
18. C.L. Faingold, C.A. Boersma-Anderson, D.M. Caspary Involvement of GABA in acoustically-evoked inhibition in inferior colliculus neurons Hearing Res 52 1991 201 216
19. C.L. Faingold, G. Gehlbach, D.M. Caspary On the role of GABA as an inhibitory neurotransmitter in inferior colliculus neurons iontophoretic studies Brain Res 500 1989 302 312
20. H. Faye-Lund, K.K. Osen Anatomy of the inferior colliculus in rat Anat Embryol 171 1985 1 20
21. T. Fremouw, A. Kleiser, A. Heilman, J.H. Casseday, E. Covey Intrinsic and commissural GABAergic connections in the inferior colliculus of the big brown bat Neurosci Abstr 25 1999 1417
22. K.K. Glendenning, B.N. Baker Neuroanatomical distribution of receptors for three potential inhibitory neurotransmitters in the brainstem auditory nuclei of the cat J Comp Neurol 275 1988 288 308
23. T. González-Hernández, B. Mantolan, B. González, H. Pérez Sources of GABAergic input to the inferior colliculus of the rat J Comp Neurol 372 1996 309 326
24. S.R. Hage, G. Ehret Mapping responses to frequency sweeps and tones in the inferior colliculus of house mice Eur J Neurosci 18 2003 2301 2312
25. D.R.F. Irvine Physiology of the auditory brainstem A.N. Popper R.R. Fay Springer handbook of auditory pathway neurophysiology 1992 Springer-Verlag New York 153 231
26. J.B. Kelly, S.L. Glenn, C.J. Beaver Sound frequency and binaural response properties of single neurons in rat inferior colliculus Hear Res 56 1991 273 280
27. J.B. Kelly, A.L. Liscum, B. van Abel, M. Ito Projections from the superior olive and lateral lemniscus to tonotopic regions of the rat's inferior colliculus Hear Res 116 1998 43 54
28. J. Kolston, K.K. Osen, C.M. Hackney, O.P. Ottersen, J. Storm-Mathisen An atlas of glycine- and GABA-like immunoreactivity and colocalization in the cochlear nuclear complex of the guinea pig Anat Embryol 186 1992 443 465
29. R.J. Kulesza Jr, A.S. Berrebi Superior paraolivary nucleus of the rat is a GABAergic nucleus J Assoc Res Otolaryngol 1 2000 255 269
30. S. Kuwada, R. Batra, T.C.T. Yin, D.L. Oliver, L.B. Haberly, T.R. Stanford Intracellular recordings in response to monaural and binaural stimulation of neurons in the inferior colliculus of the cat J Neurosci 17 1997 7565 7581
31. G. Langner, M. Albert, T. Briede Temporal and spatial coding of periodicity information in the inferior colliculus of awake chinchilla, Chinchilla laniger Hear Res 168 2002 110 130
32. F.E.N. LeBeau, M.S. Malmierca, A. Rees The role of inhibition in determining neuronal responses properties in the inferior colliculus G.A. Manley G. Klump C.H. Koppl H. Fastls O. Oekinghaus Advances in hearing research 1995 World Scientific Press Singapore 250 257
33. A and glycinergic inhibition in shaping frequency response areas in the inferior colliculus of guinea pig J Neurosci 21 2001 7303 7312
34. F.E.N. LeBeau, A. Rees, M.S. Malmierca The contribution of GABA and Glycine mediated inhibition to the monaural temporal response properties of neurons in the inferior colliculus J Neurophysiol 75 1996 902 919
35. J. Lerma, A.V. Paternain, A. Rodriguez-Moreno, J.C. Lopez-Garcia Molecular physiology of kainate receptors Physiol Rev 81 2001 971 998
36. L. Li, J.B. Kelly Inhibitory influence of the dorsal nucleus of the lateral lemniscus on binaural responses in the rat's inferior colliculus J Neurosci 12 1992 4530 4539
37. C.L. Ma, J.B. Kelly, S.H. Wu AMPA and NMDA receptors mediate synaptic excitation in the rat's inferior colliculus Hear Res 168 2002 25 34
38. M.S. Malmierca Computer-assisted 3-D reconstructions of Golgi-impregnated cells in the rat inferior colliculus Doctoral Thesis University of Oslo and Salamanca 1991
39. M.S. Malmierca The structure and physiology of the rat auditory system an overview Int Rev Neurobiol 58 2003 147 211
40. M.S. Malmierca, T.W. Blackstad, K.K. Osen, T. Karagulle, R.L. Molowny The central nucleus of the inferior colliculus in rat a Golgi and computer reconstruction study of neuronal and laminar structure J Comp Neurol 333 1993 1 27
41. M.S. Malmierca, O. Hernández, A. Falconi, E.A. López-Póveda, M.A. Merchán, A. Rees The commissure of the inferior colliculus shapes frequency response areas in rat an in vivo study using reversible blockade with microinjection of kynurenic acid Exp Brain Res 153 2003 522 529
42. M.S. Malmierca, T.B. Leergaard, V.M. Bajo, J.G. Bjaalie Anatomic evidence of a 3-D mosaic pattern of tonotopic organization in the ventral complex of the lateral lemniscus in cat J Neurosci 19 1998 10603 10618
43. M.S. Malmierca, M. Merchán The auditory system G. Paxinos The rat nervous system 2004 Academic Press San Diego 997 1082
44. M.S. Malmierca, M. Merchán, C.K. Henkel, D.L. Oliver Direct projections from the dorsal cochlear nucleus to the auditory thalamus in rat J Neurosci 22 2002 10891 10897
45. M.S. Malmierca, M.A. Merchán, D.L. Oliver Convergence of dorsal and ventral cochlear nuclei input onto frequency-band laminae of the inferior colliculus a double tracer study in rat and cat ARO Abstr 22 1999 221
46. M.S. Malmierca, D.L. Oliver, M.A. Merchán Convergence laminar projections from dorsal DCN and ventral cochlear nucleus VCN to inferior colliculus IC of rat and cat SFN Abstr 25 1999 1418
47. M.S. Malmierca, A. Rees, F.E.N. LeBeau Ascending projections to the medial geniculate body from physiologically identified loci in the inferior colliculus J. Syka Acoustic signal processing in the central auditory system 1997 Plenum Press New York 295 302
48. M.S. Malmierca, A. Rees, F.E.N. LeBeau, J.G. Bjaalie Laminar organization of frequency-defined local axons within and between the inferior colliculi of the guinea pig J Comp Neurol 357 1995 124 144
49. M.S. Malmierca, K.L. Seip, K.K. Osen Morphological classification and identification of neurons in the inferior colliculus a multivariate analysis Anat Embryol 191 1995 343 350
50. R. Marianowski, Liao W.H. Van Den, T. Abbeele, P. Fillit, P. Herman, B. Frachet, P.T. Huy Expression of NMDA AMPA and GABA(A) receptor subunit mRNAs in the rat auditory brainstem: I. Influence of early auditory deprivation Hear Res 150 2000 1 11
51. M.A. Merchán, P. Berbel Anatomy of the ventral nucleus of the lateral lemniscus in rats a nucleus with a concentric laminar organization J Comp Neurol 372 1996 245 263
52. M.A. Merchán, E. Saldaña, I. Plaza Dorsal nucleus of the lateral lemniscus in the rat concentric organization and tonotopic projection to the inferior colliculus J Comp Neurol 342 1994 259 278
53. J.K. Moore, K.K. Osen, J. Størm-Mathisen, O.P. Ottersen gamma-Aminobutyric acid and glycine in the baboon cochlear nuclei an immunocytochemical colocalization study with reference to interspecies differences in inhibitory systems J Comp Neurol 369 1996 497 519
54. D.K. Morest The laminar structure of the inferior colliculus of the cat Anat Rec 148 1964 314
55. W.H.A.M. Mulders, D. Robertson Effects on cochlear responses of activation of descending pathways from the inferior colliculus Hear Res 149 2000 11 23
56. P.G. Nelson, S.D. Erulkar Synaptic mechanisms of excitation and inhibition in the central auditory pathway J Neurophysiol 26 1963 908 923
57. D.L. Oliver Dorsal cochlear nucleus projections to the inferior colliculus in the cat a light and electron microscopic study J Comp Neurol 224 1984 155 172
58. D.L. Oliver Neurons types in the central nucleus of the inferior colliculus that project to the medial geniculate body Neuroscience 11 1984 409 424
59. D.L. Oliver Projections to the inferior colliculus from the anteroventral cochlear nucleus in the cat possible substrates for binaural interaction J Comp Neurol 264 1987 24 46
60. D.L. Oliver Ascending efferent projections of the superior olivary complex Microsc Res Tech 51 2000 355 363
61. D.L. Oliver, G.E. Beckius, D.C. Bishop, S. Kuwada Simultaneous anterograde labeling of axonal layers from lateral superior olive and dorsal cochlear nucleus in the inferior colliculus of cat J Comp Neurol 382 1997 215 229
62. D.L. Oliver, G.E. Beckius, A. Shneiderman Axonal projections from the lateral and medial superior olive to the inferior colliculus of the cat a study using electron microscopic autoradiography J Comp Neurol 360 1995 17 32
63. D.L. Oliver, M. Huerta Inferior and superior colliculi D.B. Webster A.N. Popper R.R. Fay The mammalian auditory pathway neuroanatomy 1992 Springer-Verlag Berlin 168 221
64. D.L. Oliver, S. Kuwada, T.C.T. Yin, L.B. Haberly, C.K. Henkel Dendritic and axonal morphology of HRP-injected neurons in the inferior colliculus of the cat J Comp Neurol 303 1991 75 100
65. D.L. Oliver, D.K. Morest The central nucleus of the inferior colliculus in the cat J Comp Neurol 222 1984 237 264
66. D.L. Oliver, E.M. Ostapoff, G.E. Beckius Direct innervation of identified tectothalamic neurons in the inferior colliculus by axons from the cochlear nucleus Neuroscience 93 1999 643 658
67. D.L. Oliver, A. Shneiderman The anatomy of the inferior colliculus a cellular basis for integration of monaural and binaural information R.A. Altschuler R.P. Bobbin B.M. Clopton D.W. Hoffmann Neurobiology of hearing 1991 Raven Press New York 195 222
68. D.L. Oliver, J.A. Winer, G.E. Beckius, R.L. Saint Marie Morphology of GABAergic neurons in the inferior colliculus of the cat J Comp Neurol 340 1994 27 42
69. G. Ornung, O. Shupliakov, H. Linda, O.P. Ottersen, J. Storm-Mathisen, B. Ulfhake, S. Cullheim Qualitative and quantitative analysis of glycine and GABA-immunoreactive nerve terminals on motoneuron cell bodies in the cat spinal cord a postembedding electron microscopic study J Comp Neurol 365 1996 413 426
70. K.K. Osen, O.P. Ottersen, J. Størm-Mathisen Colocalization of glycine-like and GABA-like immunoreactivities a semiquantitative study of individual neurons in the dorsal cochlear nucleus of cat O.P. Ottersen J. Størm-Mathissen Glycine neurotransmission 1990 Wiley Chichester 417 451
71. O.P. Ottersen Postembedding light- and electron microscopic immunocytochemistry of amino acids description of a new model system allowing identical conditions for specificity testing and tissue processing Exp Brain Res 69 1987 167 174
72. O.P. Ottersen, O.P. Hjelle, K.K. Osen, J.H. Laake Amino acid transmitters G. Paxinos The rat nervous system 2nd ed 1995 Academic Press San Diego 1017 1037
73. O.P. Ottersen, J. Storm-Mathisen Glutamate- and GABA-containing neurons in the mouse and rat brain as demonstrated with a new immunocytochemical technique J Comp Neurol 229 1984 374 392
74. D. Peruzzi, E. Bartlett, P.H. Smith, D.L. Oliver A monosynaptic GABAergic input from the inferior colliculus to the medial geniculate body in rat J Neurosci 17 1997 3766 3777
75. A. Rees, A. Sarbaz, M.S. Malmierca, F.E.N. LeBeau Regularity of firing of neurons in the inferior colliculus of the guinea-pig J Neurophysiol 77 1997 2945 2965
76. I. Reichenberger, H. Straka, O.P. Ottersen, P. Streit, N.M. Gerrits, N. Dieringer Distribution of GABA glycine and glutamate immunoreactivities in the vestibular nuclear complex of the frog J Comp Neurol 377 1997 149 164
77. R. Riquelme, E. Saldaña, K.K. Osen, O.P. Ottersen, M.A. Merchán Colocalization of GABA and glycine in the ventral nucleus of the lateral lemniscus in rat an in situ hybridization and semiquantitative immunocytochemical study J Comp Neurol 432 2001 409 424
78. R.C. Roberts, C.E. Ribak An electron microscopic study of GABAergic neurons and terminals in the central nucleus of the inferior colliculus of the rat J Neurocytol 16 1987 333 345
79. R.C. Roberts, C.E. Ribak, L.M. Kitzes, W.H. Oertel Regional distribution of GABAergic neurons and axon terminals in the brainstem auditory nuclei of the gerbil Anat Rec 211 1985 161A
80. J.E. Rose, D.O. Greenwood, J.M. Golderberg, J.E. Hind Some discharge characteristic of single neurons in the inferior colliculus of the cat: I. Tonopic organization relation of spike-counts to tone intensity and firing patterns of single elements J Neurophysiol 26 1963 294 320
81. A.F. Ryan, Z. Furlow, N.K. Wool, E.M. Keithley The spatial representation of frequency in the rat dorsal cochlear nucleus and inferior colliculus Hear Res 36 1988 181 189
82. D.K. Ryugo, F.H. Willard, D.M. Fekete Differential afferent projections to the inferior colliculus from the cochlear nucleus in the albino mouse Brain Res 210 1981 342 349
83. 3H] glycine from the inferior colliculus by ipsilateral projections of the superior olivary complex and nuclei of the lateral lemniscus Brain Res 524 1990 244 253
84. R.L. Saint Marie, E.M. Ostapoff, D.K. Morest, R.J. Wenthold Glycine-immunoreactive projection of the cat lateral superior olive possible role in midbrain ear dominance J Comp Neurol 279 1989 382 396
85. R.L. Saint Marie, D.A. Stanforth, E.M. Jubelier Substrate for rapid feedforward inhibition of the auditory forebrain Brain Res 765 1997 173 176
86. D.H. Sanes, W.A. Geary, G.F. Wooten, E.W. Rubel Quantitative distribution of the glycine receptor in the auditory brain stem of the gerbil J Neurosci 711 1987 3793 3802
87. C.E. Schreiner, G. Langner Coding of temporal patterns in the central auditory nervous system G.M. Edelman W.E. Gall W.M. Cowan Auditory function 1988 Wiley New York 337 340
88. S. Shiraishi, Y. Shiraishi, D.L. Oliver, R.A. Altschuler Expression of GABA(A) receptor subunits in the rat central nucleus of the inferior colliculus Brain Res Mol Brain Res 96 2001 122 132
89. A. Shneiderman, C.K. Henkel Banding of lateral superior olivary nucleus afferents in the inferior colliculus a possible substrate for sensory integration J Comp Neurol 266 1987 519 534
90. A. Shneiderman, D.L. Oliver, C.K. Henkel Connections of the dorsal nucleus of the lateral lemniscus an inhibitory parallel pathway in the ascending auditory system? J Comp Neurol 276 1988 188 208
91. A. Shneiderman, M.B. Chase, J.M. Rockwood, C.G. Benson, S.J. Potashner Evidence for a GABAergic projection from the dorsal nucleus of the lateral lemniscus to the inferior colliculus J Neurochem 60 1998 72 82
92. P. Somogyi, A.J. Hodgson, A.D. Smith, M.G. Nunzi, A. Gorio, J.Y. Wu Different populations of GABAergic neurons in the visual cortex and hippocampus of cat contain somatostatin- or cholecystokinin-immunoreactive material J Neurosci 4 1984 2590 2603
93. P. Somogyi, K. Halasy, J. Somogyi, J. Storm-Mathisen, O.P. Ottersen Quantification of immunogold labeling reveals enrichment of glutamate in mossy and parallel fibre terminals in cat cerebellum Neuroscience 19 1986 1045 1050
94. G.A. Spirou, A.S. Berrebi Glycine immunoreactivity in the lateral nucleus of the trapezoid body of the cat J Comp Neurol 383 1997 473 488
95. S.K. Suneja, C.G. Benson, S.J. Potashner Glycine receptors in adult guinea pig brain stem auditory nuclei regulation after unilateral cochlear ablation Exp Neurol 154 1998 473 488
96. G.C. Thompson, A.M. Cortez, Man-Kit, D. Lam Localization of GABA immunoreactivity in the auditory brainstem of guinea pigs Brain Res 339 1985 119 122
97. M. Vater, M. Kossl, A.K. Horn GAD- and GABA-immunoreactivity in the ascending auditory pathway of horseshoe and mustached bats J Comp Neurol 325 1992 183 206
98. D.E. Vetter, E. Mugnaini Immunocytochemical localization of GABAergic elements in the rat inferior colliculus Society for Neuroscience Abstr 10 1984 1148
99. D.E. Vetter, E. Mugnaini Discrete bilateral GABAergic neuron pools at the commissures of superior and inferior colliculi in the rat Society for Neuroscience Abstr 11 1985 246
100. G. von Bèkèsy Experiments in hearing 1960 McGraw-Hill New York
101. F. Walberg, O.P. Ottersen Demonstration of GABA immunoreactive cells in the inferior olive of baboons (Papio papio and Papio anubis) Neurosci Lett 101 1989 149 155
102. F. Walberg, O.P. Ottersen Neuroactive amino acids in the area postrema an immunocytochemical investigation in rat with some observations in cat and monkey (Macaca fascicularis) Anat Embryol (Berl) 185 1992 529 545
103. R.J. Wenthold, D. Huie, R.A. Altschuler, K.A. Reeks Glycine immunoreactivity localized in the cochlear nucleus and superior olivary complex Neuroscience 22 1987 897 912
104. J.A. Winer, D.T. Larue Anatomy of glutamic acid decarboxylase immunoreactive neurons and axons in the rat medial geniculate body J Comp Neurol 278 1988 47 68
105. J.A. Winer, D.T. Larue, G.D. Pollak GABA and glycine in the central auditory system of the mustache bat structural substrates for inhibitory neural organization J Comp Neurol 352 1995 1 37
106. J.A. Winer, R.L. Saint Marie, D.T. Laure, D.L. Oliver Gabaergic feedforward projections from the inferior colliculus to the medial geniculate body Proc Natl Acad Sci USA 93 1996 80005 80010
107. Y. Yang, A.M. Surette, D. Bishop, D.L. Oliver Properties of local circuits in the central nucleus of the IC (CIC) SFN Abstr 26 2000 674
108. H. Zhang, J.B. Kelly AMPA and NMDA receptors regulate responses of neurons in the rat's inferior colliculus J Neurophysiol 86 2001 871 880
109. H. Zhang, J.B. Kelly Glutamatergic and GABAergic regulation of neural responses in inferior colliculus to amplitude-modulated sounds J Neurophysiol 90 2003 477 490