γ-Aminobutyric acid and glycine in the baboon cochlear nuclei: An immunocytochemical colocalization study with reference to interspecies differences in inhibitory systems

Journal of Comparative Neurology

Volumn 369, Issue 4, 1996, Pages 497-519

  Moore, Jean K ^a   Osen, Kirsten K ^b   Storm Mathisen, Jon ^b   Ottersen, Ole Fetter ^b  

^a HOUSE EAR INSTITUTE   (United States)

^b UNIVERSITY OF OSLO   (Norway)

Author keywords

amino acids; auditory pathways; neurotransmitters; phylogeny; primates

Indexed keywords

4 AMINOBUTYRIC ACID; GLYCINE;

ANIMAL TISSUE; ARTICLE; BABOON; COCHLEAR NUCLEUS; FEMALE; IMMUNOCYTOCHEMISTRY; MALE; NERVE PROJECTION; NONHUMAN; OPTICAL DENSITY; PRIORITY JOURNAL;

EID: 0029999784     PISSN: 00219967     EISSN: None     Source Type: Journal    
DOI: 10.1002/(sici)1096-9861(19960610)369:4<497::aid-cne2>3.0.co;2-%23     Document Type: Article

References (96)

1. Adams, J.C. (1986) Neuronal morphology in the human cochlear nucleus. Arch. Otol. Head Neck Surg. 112:1253-1261.
2. Adams, J.C., and E. Mugnaini (1987) Patterns of glutamate decarboxylase immunostaining in the feline cochlear nuclear complex studied with silver enhancement and electron microscopy. J. Comp. Neurol. 262:375-401.
3. Altschuler, R.A., H. Betz, M.H. Parakkal, K.A. Reeks, and R.J. Wenthold (1986) Identification of glycinergic synapses in the cochlear nucleus through immunocytochemical localization of the postsynaptic receptor. Brain Res. 369:316-320.
4. Aoki, E., R. Semba, H. Keino, K. Kato, and S. Kashiwamata (1988) Glycine-like immunoreactivity in the rat auditory pathway. Brain Res. 442:63-71.
5. 3H]lglycine from the cochlear nucleus to the superior olive in the guinea pig. J. Comp. Neurol. 296:415-426.
6. Bergman, M., C. Staatz-Benson, and S.J. Potashner (1989) Amino-acid uptake and release in the guinea pig cochlear nucleus after inferior colliculus ablation. Hearing Res. 42:283-292.
7. Berrebi, A.S., and E. Mugnaini (1991) Distribution and targets of the cartwheel cell axon in the dorsal cochlear nucleus of the guinea pig. Anat. Embryol. 183:427-454.
8. Cant, N.B. (1993) The synaptic organization of the ventral cochlear nucleus of the cat: The peripheral cap of small cells. In M.A. Merchan (ed): The Mammalian Cochlear Nuclei: Organization and Function. New York: Plenum Press, pp. 91-105.
9. Cant, N.B., and K.C. Gaston (1982) Pathways connecting the right and left cochlear nuclei. J. Comp. Neurol. 212:313-326.
10. Caspary, D.M., D.C. Havey, and C.L. Faingold (1979) Effects of microiontophoretically applied glycine and GABA on neuronal response patterns in the cochlear nuclei. Brain Res. 172:179-185.
11. Caspary, D.M., L.P. Rybak, and C.L. Faingold (1984) Baclofen reduces toneevoked activity of cochlear nucleus neurons. Hearing Res. 13:113-122.
12. Caspary, D.M., K.E. Pazara, M. Koessl, and C.L. Faingold (1987) Strichnine alters the fusiform cell output from the dorsal cochlear nucleus. Brain Res. 417:273-282.
13. Dale, N., O.P. Ottersen, A. Roberts, and J. Storm-Mathisen (1986) Inhibitory neurones of a motor pattern generator in Xenopus revealed by antibodies to glycine. Nature 324:255-257.
14. Evans, E.F., and P.G. Nelson (1973) The responses of single neruones in the cochlear nucleus of the cat as a function of their location and the anesthetic state. Exp. Brain Res. 17:402-427.
15. Evans, E.F., and W. Zhao (1993) Neuropharmacological and neurophysiological dissection of inhibition in the mammalian dorsal cochlear nucleus. In M.A. Merchan (ed): The Mammalian Cochlear Nuclei: Organization and Function. New York: Plenum Press, pp. 253-266.
16. Feng, A.S., and M. Vater (1985) Functional organization of the cochlear nucleus of rufous horseshoe bats (Rhinolophus rouxi): Frequencies and internal connections are arranged in slabs. J. Comp. Neurol. 235:529-553.
17. Fisher, S.K., and W.E. Davies (1976) GABA and its related enzymes in the lower auditory system of the guinea pig. J. Neurochem. 27:1145-1155.
18. Frostholm, A., and A. Rotter (1986) Autoradiographic localization of receptors in the cochlear nucleus of the mouse. Brain Res. Bull. 16:189-203.
19. Fuse, G. (1913) Das ganglion ventrale and das Tuberculum acusticum bei einigen Saugern und beim Menschen. Arbeit. Hirnanat. Inst. Zurich 2:1-210.
20. Glendenning, K.K., and B.N. Baker (1988) Neuroanatomical distribution of receptors for three potential inhibitory neurotransmitters in the brainstem auditory nuclei of the cat. J. Comp. Neurol. 275:288-308.
21. Godfrey, D.A., J.A. Carter, S.J. Berger, O.H. Lowry, and P.M. Matschinsky (1977) Quantitative histochemical mapping of candidate transmitter amino acids in cat cochlear nucleus. J. Histochem. Cytochem. 15:417-421.
22. Godfrey, D.A., J.A. Carter, O.H. Lowry, and F.M. Matchinsky (1978) Distribution of gamma-aminobutyric acid, glycine, glutamate and aspartate in the cochlear nucleus of the rat. J. Histochem. Cytochem. 26:118-126.
23. Godfrey, D.A., J.A. Parli, J.D. Dunn, and C.D. Ross (1988) Neurotransmitter microchemistry of the cochlear nucleus and superior olivary complex. In J. Syka and R.B. Masterton (eds): Auditory Pathway: Structure and Function. New York: Plenum Press, pp. 107-121.
24. Goldberg, J.M., and W.E. Brownell (1973) Discharge characteristics of neurons in anteroventral and dorsal cochlear nucleus of cat. Brain Res. 64:35-54.
25. Hackney, C.M., K.K. Osen, and J. Kolston (1990) Anatomy of the cochlear nuclear complex of guinea pig. Anat. Embryol. 182:123-149.
26. Hackney, C.M., K.K. Osen, O.P. Ottersen, J. Storm-Mathisen, and G. Manjaly (1995) Immunocytochemical evidence that glutamate is a neurotransmitter in the cochlear nerve: A quantitative study in the guinea-pig anteroventral cochlear nucleus. Eur. J. Neurosci. 8:79-91.
27. Johnson, J.I., J.A. Kirsch, R.L. Reep, and R.C. Switzer III (1994) Phylogeny through brain traits: More characters for the analysis of mammalian evolution. Brain Behav. Evol. 43:319-347.
28. A/benzodiazepine receptor in the guinea pig cochlear nucleus: Evidence for receptor localization heterogeneity. Brain Res. 504:173-179.
29. Kakehata, S., T. Nakagawa, T. Takasaka, and N. Akaike (1992) Glycine response in isolated dorsal cochlear nucleus of C57BL/6J mouse. Brain Res. 574:21-25.
30. Kolston, J., K.K. Osen, C.M. Hackney, O.P. Ottersen, and J. Storm-Mathisen (1992) An atlas of glycine- and GABA-like immunoreactivity and colocalization in the cochlear nuclear complex of the guinea pig. Anat. Embryol. 186:443-465.
31. Lorente de Nó, R. (1933) Anatomy of the eighth nerve: III. General plan of structure of the primary cochlear nuclei. Laryngoscope 43:3227-350.
32. Lorente de Nó, R. (1981) The Primary Acoustic Nuclei. New York: Raven Press.
33. Mast, T.E. (1970) Binaural interaction and contralateral inhibition in dorsal cochlear nucleus of the chinchilla. J. Neurophysiol. 33:108-115.
34. Moore, J.K. (1980) The primate cochlear nuclei: Loss of lamination as a phylogenetic process. J. Comp. Neurol. 193.609-629.
35. Moore, J.K. (1986) Cochlear nuclei: Relationship to the auditory nerve. In R.A. Altschuler, D.W. Huffman, and R.P. Bobbin (eds): Neurobiology of Hearing: The Cochlea. New York: Raven Press, pp. 283-301.
36. Moore, J.K., and R.Y. Moore (1971) A comparative study of the superior olivary complex in the primate brain. Folia Primat. 16:35-51.
37. Moore, J.K., and R.Y. Moore (1987) Glutamic acid decarboxylase-like immunoreactivity in brainstem auditory nuclei of the rat. J. Comp. Neurol. 260:157-174.
38. Moore, J.K., and K.K. Osen (1979) The cochlear nuclei in man. Am. J. Anat. 154:393-418.
39. Moore, J.K., and K.K. Osen (1990) Colocalization of GABA-like and glycinelike immunoreactivity in the cochlea nuclei of the baboon (Papio anubis). Assoc. Res. Otolaryngol. Abstr., p. 716.
40. Moskowitz, N. (1969) Comparative aspects of some features of the central auditory system of primates. Ann. NY Acad. Sci. 167:357-369.
41. Moskowitz, N., and J.-C.Liu (1972) Central projections of the spiral ganglion of the squirrel monkey. J. Comp. Neurol 144:335-344.
42. Mugnaini, E. (1985) GABA neurons in the superficial layers of the rat dorsal cochlear nucleus: Light and electron microscopic immunocytochemistry. J. Comp. Neurol. 235:61-81.
43. Mugnaini, E., and J.I. Morgan (1987) The neuropeptide cerebellin is a marker for two similar neuronal circuits in rat brain. Proc. Natl. Acad. Sci. USA 84:8692-8696.
44. Mugnaini, E., W.B. Warr, and K.K. Osen (1980a) Distribution and light microscopic features of granule cells in the cochlear nuclei of cat, rat and mouse. J. Comp. Neurol. 191:581-606.
45. Mugnaini, E., K.K. Osen, A.-L. Dahl, V.L. Friedrich Jr., and G. Korte (1980b) Fine structure of granule cells and related interneurons (termed Golgi cells) in the cochlear nuclear complex of cat, rat and mouse. J. Neurocytol. 9:537-570.
46. Mugnaini, E. A.S. Berrebi, A.-L. Dahl, V. Friedrich Jr., and G. Korte (1987) The polypeptide PEP-19 is a marker for Purkinje neurons in cerebellar cortex and cartwheel neurons in the dorsal cochlear nucleus Arch. Ital. Biol. 126:41-067.
47. Oertel, D., and S.H. Wu (1989) Morphology and physiology of cells in slice preparations of the dorsal cochlear nucleus of mice. J. Comp. Neurol. 283:228-247.
48. Oertel, D., S.H. Wu, M.W. Garb, and C. Dizack (1990) Morphology and physiology of cells in slice preparations of the posteroventral cochlear nucleus of mice. J. Comp. Neurol. 295:136-154.
49. Osen, K.K. (1969) Cytoarchitecture of the cochlear nuclei in the cat. J. Comp. Neurol. 136:453-484.
50. Osen, K.K. (1970) Course and termination of the primary afferents in the cochlear nuclei of the cat: An experimental anatomical study. Arch. Ital. Biol. 108:21-51.
51. Osen, K.K. (1983) Orientation of dendritic arbors studied in Golgi sections of the cat dorsal cochlear nucleus. In W.R. Webster and L.M. Aitkin (eds.): Mechanisms of Hearing. Clayton, Victoria: Monash University Press, pp. 83-89.
52. Osen, K.K., and J. Jansen (1965) The cochlear nuclei in the common porpoise, Phocaena phocaena. J. Comp. Neurol. 125:223-257.
53. Osen, K.K., E. Mugnaini, A.-L. Dahl, and A.H. Christiansen (1984) Histochemical localization of acetylcholinesterase in the cochlear and superior olivary nuclei. A reappraisal with emphasis on the cochlear granule cell system. Arch. Ital. Biol. 122:169-212.
54. Osen, K.K., O.P. Ottersen, and J. Storm-Mathisen (1990) Colocalization of glycine-like and GABA-like immunoreactivities: A semiquantitative study of individual neurons in the dorsal cochlear nucleus of cat. In O.P. Ottersen and J. Storm-Mathisen (eds): Glycine Neurotransmission. London: Wiley, pp. 417-451.
55. Osen K.K., J. Storm-Mathisen, O.P. Ottersen, and B. Dihle (1995) Glutamate is concentrated in and released from parallel fiber terminals in the dorsal cochlear nucleus: A quantitative immunocytochemical analysis in guinea pig. J. Comp. Neurol. 357:482-500.
56. 3H]GABA from the cochlear nucleus to the superior olive in the guinea pig. J. Chem. Neuroanat, 3:285-295.
57. Ottersen, O.P. (1987) Postembedding light and electron microscopic immunohistochemistry of amino acids: Description of a new model system allowing identical conditions for specificity testing and tissue processing. Exp. Brain Res. 69:167-174.
58. Ottersen, O.P., and J. Storm-Mathisen (1984) Glutamate- and GABA-containing neurons in the mouse and rat brain, as demonstrated with a new immunocytochemical technique. J. Comp. Neurol. 229:374-392.
59. Ottersen, O.P., O.P. Hjelle, K.K. Osen, and J.H. Laake (1995) Amino Acid Transmitters. In G. Paxinos (ed): The Rat Nervous System, Second Edition. New York: Academic Press, Inc., pp. 1017-1037.
60. Peyret, D., M. Geffard, and J.-M. Aran (1986) GABA immunoreactivity in the primary nuclei of the auditory central nervous system. Hearing Res. 23:115-121.
61. Peyret, D., G. Campistron, M. Geffard, and J.-H. Aran (1987) Glycine immunoreactivity in the brainstem auditory and vestibular nuclei of the guinea pig. Acta Otolaryngol. (Stockholm) 104:71-76.
62. Potashner, S.J., N. Lindberg, and D.K. Morest (1985) Uptake and release of γ-aminobutyric acid in the guinea pig cochlear nucleus after axotomy of cochlear and centrifugal fibers. J. Neurochem. 45:1558-1866.
63. Roberts, R.C., and C.E. Ribak (1987) GABAergic neurons and axon terminals in the brainstem auditory nuclei of the gerbil. J. Comp. Neurol. 258:267-280.
64. Saint Marie, R.L., D.K. Morest, and C.J. Brandon (1989) The form and distribution of GABAergie synapses on the principal cell types of the ventral cochlear nucleus of the cat. Hearing Res. 42:97-112.
65. Saint Marie, R.L., C.G. Benson, E.-M. Ostapoff, and D.K. Morest (1991) Glycine immunoreactive projections from the dorsal to the anteroventral cochlear nucleus. Brain Res. 51-370-379.
66. Saint Marie, R.L., E.-M. Ostapoff, C.G. Benson, D.K. Morest, and S.J. Potashner (1993) noncochlear projections to the ventral cochlear nucleus: Are they mainly inhibitory? In M.A. Merchan (ed): The Mammalian Cochlear Nuclei: Organization and Function. New York: Plenum Press, pp. 121-131.
67. Sanes, D.H., W.A. Geary, G.F. Wooten, and E.W. Rubel (1987) Quantitative distribution of the glycine receptor in the auditory brainstem of the gerbil. J. Neurosci. 7:3793-3802.
68. Smith, P.H., and W.S. Rhode (1989) Structural and functional properties distinguish two types of multipolar cells in the ventral cochlear nucleus. J. Comp. Neural. 282:595-616.
69. Snyder, R.L., and P.A. Leake (1988) Intrinsic connections within and between cochlear nucleus subdivisions in cat. J. Comp. Neurol. 278:208-225.
70. Somogyi, P., A.J. Hodgson, A.D. Smith, M.G. Nunzi, A. Gorio, and J.-Y. Wu (1984) Different populations of GABAergic neurons in the visual cortex and hippocampus of cat contain somatostatin- or cholecystokinin-immunoreactive material. J. Neurosci. 4:2590-2603.
71. Staatz-Benson, C., and S.J. Potashner (1988) Uptake and release of glycine in the guinea pig cochlear nucleus after axotomy of afferent or centrifugal fibers. J. Neurochem. 51:370-379.
72. Storm-Mathisen, J., A.K. Leknes, A.T. Bore, J.L. Vaaland, P. Edminson, F.-M.S. Haug, and O.P. Ottersen (1983) First visualization of glutamate and GABA in neurones by immunocytochemistry. Nature 301:517-520.
73. Strominger, N.L. (1973) The origins, course and distribution of the dorsal and intermediate acoustic striae in the rhesus monkey. J. Comp. Neurol. 147:209-234.
74. Strominger, N.L., L.R. Nelson, and W.J. Doherty (1977) Second order pathways in the chimpanzee. J. Comp. Neurol. 172:349-366.
75. Sutherland, E.P. (1991) A role of the dorsal cochlear nucleus in the localization of elevated sound sources. Assoc. Res. Otolaryngol. Abstr., p. 33.
76. Thompson, G.C., A.M. Cortez, and D.M.-K. Lam (1985) Localization of GABA immunoreactivity in the auditory brainstem of guinea pigs. Brain Res. 339:119-122.
77. Vater, M., M. Koessl, and A.K. Horn (1992) GAD- and GABA-immunoreactivity in the ascending auditory pathway of horseshoe and mustached bats. J. Comp. Neurol. 325:183-206.
78. Voigt, H.F., and E.D. Young (1980) Evidence of inhibitory interactions between neurons in dorsal cochlear nucleus. J. Neurophysiol. 44:76-96.
79. Voigt, H.F., and E.D. Young (1990) Cross-correlation analysis of inhibitory interactions in dorsal cochlear nucleus. J. Neurophysiol. 64:1590-1610.
80. Walsh, E.J., J. McGee, and J.L. Fitzkerly (1990) GABA actions within the caudal cochlear nucleus of developing kittens. J. Neurophysiol. 64:961-977.
81. Wenthold, R. J. (1987) Evidence for a glycinergic pathway connecting the two cochlear nuclei: An immunocytochemical and retrograde transport study. Brain Res. 415:183-187.
82. Wenthold, R.J., J.M. Zempel, M.H. Parakkal, K.A. Reeks, and R.A. Altschuler (1986) Immunocytochemical localization of GABA in the cochlear nucleus of guinea pig. Brain Res. 380:7-18.
83. Wenthold, R.J., D. Huie, R.A. Altschuler, and K.A. Reeks (1987) Glycine immunoreactivity localized in the cochlear nucleus and superior olivary complex. Neuroscience 22:897-912.
84. Wenthold, R.J., M.H. Parakkal, M.D. Oberdorfer, and R.A. Altschuler (1988) Glycine receptor immunoreactivity in the ventral cochlear nucleus of the guinea pig. J. Comp. Neurol. 276:423-435.
85. Wickesberg, R.E., and D. Oertel (1988) Tonotopic projection from the dorsal to the anteroventral cochlear nucleus of mice. J. Comp. Neurol. 265:389-399.
86. Wickesberg, R.E., D. Whitlon, and D. Oertel (1991) Tuberculoventral neurons project to the multipolar cell area but not to the octopus cell area of the posteroventral cochlear nucleus. J. Comp. Neurol. 313:457-486.
87. Wouterlood, F.G., and E. Mugnaini (1984) Cartwheel neurons of the dorsal cochlear nucleus: A Golgi-electron microscopic study in rat. J. Comp. Neurol. 227:136-157.
88. Wouterlood, F.G., E. Mugnaini, K.K. Osen, and A.-L. Dahl (1984) Stellate neurons in the rat dorsal cochlear nucleus studied with combined Golgi impregnation and electron microscopy: Synaptic connections and mutual coupling by gap junctions. J. Neurocytol. 13:639-664.
89. Wu, S.H., and D. Oertel (1986) Inhibitory circuitry in the ventral cochlear nucleus is probably mediated by glycine. J. Neurosci. 6:2691-2706.
90. Young, E.D., and W.E. Brownell (1976) Responses to tones and noise of single cells in dorsal cochlear nucleus of unanesthetized cats. Neurophysiology 39:282-300.
91. Young, E.D., and H.F. Voigt (1982) Response properties of type II and type III units in dorsal cochlear nucleus. Hearing Res. 6.153-169.
92. Zhang, S., and D. Oertel (1993) Tuberculoventral cells of the dorsal cochlear nucleus of mice: Intracellular recordings in slices. J. Neurophysiol. 69:1409-1421.
93. Zhao, W. (1995) The inhibitory mechanisms of sound processing in the dorsal cochlear nucleus of the guinea pig. University of Keele, doctoral dissertation.
94. Zhao, W., and E.F. Evans (1990) Pharmacological microiontophoretic investigation of receptive-field and temporal properties of units in the cochlear nucleus. Br. J. Audiol. 24:193.
95. Zhao, W., and E.F. Evans (1991) Dorsal cochlear nucleus units: Neuropharmacological effects on dynamic range and off-inhibition. Br. J. Audiol. 25:53-54.
96. Zhao, W., and E.F. Evans (1992) Bandwidths of excitatory and inhibitory receptive fields in the dorsal cochlear nucleus. Br. J. Audiol. 26:179-180.