Patterns of γ-aminobutyric acid and glycine immunoreactivities reflect structural and functional differences of the cat lateral lemniscal nuclei

Journal of Comparative Neurology

Volumn 389, Issue 2, 1997, Pages 264-276

  Saint Marie, Richard L ^a,b   Shneiderman, Amiram ^a,c   Stanforth, David A ^a  

^a HOUSE EAR INSTITUTE   (United States)

^b UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

^c Jr/Charles R ^*  (United States)

Author keywords

Auditory pathway; Inferior colliculus; Inhibitory neurotransmitter; Lateral lemniscus

Indexed keywords

4 AMINOBUTYRIC ACID; GLYCINE;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BRAIN TISSUE; CAT; IMMUNOREACTIVITY; INFERIOR COLLICULUS; NEUROANATOMY; NEUROTRANSMISSION; NONHUMAN; PRIORITY JOURNAL; STRUCTURE ACTIVITY RELATION; STRUCTURE ANALYSIS;

EID: 0030663687     PISSN: 00219967     EISSN: None     Source Type: Journal    
DOI: 10.1002/(sici)1096-9861(19971215)389:2<264::aid-cne6>3.0.co;2-%23     Document Type: Article

References (83)

1. Adams, J.C. (1979) Ascending projections to the inferior colliculus. J. Comp. Neurol. 183:519-538.
2. Adams, J.C., and E. Mugnaini (1984) Dorsal nucleus of the lateral lemniscus: A nucleus of GABAergic projection neurons. Brain Res. Bull. 13:585-590.
3. Adams J.C., and R.J. Wenthold (1987) Immunostaining of ascending auditory pathways with glycine antiserum. Assoc. Res. Otolaryngol. Abstr. 10:63.
4. Aitkin L.M. (1989) The auditory system. In A. Björklund, T. Hökfelt, and LW Swanson (eds): Handbook of Chemical Neuroanatomy, Vol. 7: Integrated Systems of the CNS, Part II. Amsterdam: Elsevier Science Publishers, pp. 165-218.
5. Aitkin, L.M., D.J. Anderson, and J.F. Brugge (1970) Tonotopic organization and discharge characteristics of single neurons in nuclei of the lateral lemniscus of the cat. J. Neurophysiol. 33:421-440.
6. 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.
7. Barker, J.L., B. Duffy, and R.N. McBurney (1986) Amino acid and peptide signals in cultured CNS neurons and clonal pituitary cells. In L.L. Iversen and E.C. Goodman (eds): Fast and Slow Chemical Signaling in the Nervous System. Oxford: Oxford University Press, pp. 16-36.
8. Batra, R., and D.C. Fitzpatrick (1997) Neurons sensitive to interaural temporal disparities in the medial part of the ventral nucleus of the lateral lemniscus. J. Neurophysiol. 78:511-515.
9. Bormann, J., O.P. Hamill, and B. Sakmann (1987) Mechanism of anion permeation through channels gated by glycine and γ-ammobutyric acid in mouse cultured spinal neurons. J. Physiol. 385:243-286.
10. Brugge, J.F., D.J. Anderson, and L.M. Aitkin (1970) Responses of neurons in the dorsal nucleus of the lateral lemniscus of cat to binaural tonal stimulation. J. Neurophysiol. 33:441-458.
11. Brunso-Bechtold, J.K., G.C. Thompson, and R.B. Masterton (1981) HRP study of the organization of auditory afferents ascending to central nucleus of inferior colliculus in cat. J. Comp. Neurol. 197:705-722.
12. Buckthought, A.D., L. Li, and J.B. Kelly (1993) Physiological properties of single neurons in the rats dorsal nucleus of the lateral lemniscus. Assoc. Res. Laryngol. 16:126.
13. Casseday, J.H., and E. Covey (1995) Mechanisms for analysis of auditory temporal patterns in the brainstem of echolocating bats. In E. Covey et al. (eds): Neural Representation of Temporal Patterns. New York: Plenum Press, pp. 25-51.
14. Covey, E. (1993a) The monaural nuclei of the lateral lemniscus: Parallel pathways from cochlear nucleus to midbrain. In M.A. Merchan, J.M. Juiz, D.A. Godfrey, and E. Mugnaini (eds): The Mammalian Cochlear Nuclei: Organization and Function. New York: Plenum Press, pp. 321-334.
15. Covey, E. (1993b) Response properties of single units in the dorsal nucleus of the lateral lemniscus and paralemniscal zone of an echolocating bat. J. Neurophysiol. 69:842-859.
16. Covey, E., and J.H. Casseday (1986) Connectional basis for frequency representation in the nuclei of the lateral lemniscus of the bat Eptesicus fuscus. J. Neurosci. 6:2926-2940.
17. Covey, E., and J.H. Casseday (1991) The monaural nuclei of the lateral lemniscus in an echolocating bat: Parallel pathways for analyzing temporal features of sound. J. Neurosci. 11:3456-3470.
18. Deisz, R.A., and H.D. Lux (1985) Gamma-aminobutyric acid-induced depression of calcium currents of chick sensory neurons. Neurosci. Lett. 56:205-240.
19. Elverland, H.H. (1978) Ascending and intrinsic projections of the superior olivary complex in the cat. Exp. Brain Res. 32:117-134.
20. Faingold, C.L., C.A. Boersma Anderson, and M.E. Randall (1993) Stimulation or blockade of the dorsal nucleus of the lateral lemniscus alters binaural and tonic inhibition in contralateral inferior colliculus neurons. Hearing Res. 69:98-106.
21. Fletcher, E.J., P.M. Beart, and D. Lodge (1990) Involvement of glycine in excitatory neurotransmission. In O.P. Ottersen and J. Storm-Mathisen (eds): Glycine Neurotransmission. Chichester: John Wiley and Sons, pp. 171-191.
22. Glendenning, K.K., J.J. Brunso-Bechtold, J.K. Thompson, and R.B. Masterton (1981) Ascending auditory projections to the nuclei of the lateral lemniscus. J. Comp. Neurol. 197:673-703.
23. Glendenning, K.K., B.N. Baker, K.A. Hutson, and R.B. Masterton (1992) Acoustic chiasm V: Inhibition and excitation in the ipsilateral and contralateral projections of LSO. J. Comp. Neurol. 319:100-122.
24. Glenn, S.L., and J.B. Kelly (1992) Kainic acid lesions of the dorsal nucleus of the lateral lemniscus: Effects on binaural evoked responses in rat auditory cortex. J. Neurosci. 12:3688-3699.
25. González-Hernández, T., B. Mantolan-Sarmiento, B. González-González, and H. Perez-González (1996) Sources of GABAergic input to the inferior colliculus of the rat. J. Comp. Neurol. 372:309-326.
26. Guinan, J.J., S.S. Guinan, and B.E. Norris (1972a) Single auditory units in the superior olivary complex. I. Responses to sounds and classifications based on physiological properties. Int. J. Neurosci. 4:101-120.
27. Guinan, J.J., B.E. Norris, and S.S. Guinan (1972b) Single auditory units in the superior olivary complex. II. Locations of unit categories and tonotopic organization. Int. J. Neurosci. 4:147-166.
28. Hamill, O.P., J. Bormann, and B. Sakmann (1983) Activation of multiple-conductance state chloride channels in spinal neurons by glycine and GABA. Nature 305:805-808.
29. Held, H. (1893) Die centrale Gehorleitung. Arch. f. Anat. u Physiol. Anat. Abtheil 17:201-248.
30. Helfert, R.H., and A. Aschoff (1997) Superior olivary complex and nuclei of the lateral lemniscus. In G. Ehret and R. Romand (eds): The Central Auditory System. New York: Oxford University Press, pp. 193-258.
31. Helfert, R.H., J.M. Bonneau, R.J. Wenthold, and R.A. Altschuler (1989) GABA and glycine immunoreactivity in the guinea pig superior olivary complex. Brain Res. 501:269-286.
32. Huffman, R.F., and E. Covey (1995) Origin of ascending projections to the nuclei of the lateral lemniscus in the big brown bat, Eptesicus fuscus. J. Comp. Neurol. 357:532-545.
33. Hunter, C., E. Chung, P. Pasik, and M.H. VanWoert (1987) Glycinergic pathways in the auditory system of the rat. Soc. Neurosci. Abstr. 13:544.
34. Hutson, K.A. (1988) Connections of the auditory midbrain: Efferent projections of the dorsal nucleus of the lateral lemniscus, the nucleus sagulum, and the origins of the GABAergic commissure of Probst [doctoral dissertation]. Florida State University, Tallahassee, FL.
35. Irvine, D.R.F. (1986) The auditory brainstem. A review of the structure and function of auditory brainstem processing mechanisms. In H. Autrum, D. Ottoson, E.R. Perl, R.F. Schmidt, H. Shimazu, and W.D. Willis (eds): Progress in Sensory Physiology 7. Berlin: Springer-Verlag, pp. 1-279.
36. Ito, M., B. vanAdel, and J.B. Kelly (1996) Sound localization after transection of the commissure of Probst in the albino rat. J. Neurophysiol. 76:3493-3502.
37. Kane, E.S., and L.M. Barone (1980) The dorsal nucleus of the lateral lemniscus in the cat: Neuronal types and their distribution. J. Comp. Neurol. 192:797-826.
38. Kelly, J.B., L. Li, and B. vanAdel (1996) Sound localization after kainic acid lesions of the dorsal nucleus of the lateral lemniscus in the albino rat. Behav. Neurosci. 110:1445-1455.
39. Kidd, S.A., and J.B. Kelly (1996) Contribution of the dorsal nucleus of the lateral lemniscus to binaural responses in the inferior colliculus of the rat: Interaural time delays. J. Neurosci. 16:7390-7397.
40. 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.
41. Kudo, M. (1981) Projections of the nuclei of the lateral lemniscus in the cat: An autoradiographic study. Brain Res. 221:57-69.
42. Li, L., and J.B. Kelly (1992) Inhibitory influence of the dorsal nucleus of the lateral lemniscus on binaural responses in the rat's inferior colliculus. J. Neurosci. 12:4530-4539.
43. Malmierca, M.S., M.A. Merchan, V.M. Bajo, and J.G. Bjaalie (1997) The ventral nucleus of the lateral lemniscus in cat is tonotopically organized. Assoc. Res. Laryngol. 20:164.
44. Markovitz, N.S., and G.D. Pollak (1993) The dorsal nucleus of the lateral lemniscus in the mustache bat: Monaural properties. Hearing Res. 71:51-63.
45. Markovitz, N.S., and G.D. Pollak (1994) Binaural processing in the dorsal nucleus of the lateral lemniscus. Hearing Res. 73:121-140.
46. Metzner, W., and S. Radtke-Schuller (1987) The nuclei of the lateral lemniscus in the rufous horseshoe bat, Rhinolophus rouxi. J. Comp. Physiol. 160:395-411.
47. 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.
48. Moore, J.K., K.K. Osen, J. Storm-Mathisen, and O.P. Ottersen (1996) γ-Aminobutyric acid and glycine in the baboon cochlear nuclei: An immunocytochemical colocalization study with reference to interspecies differences in inhibitory systems. J. Comp. Neurol. 369:497-519.
49. Mugnaini, E., and W.H. Oertel (1985) An atlas of the distribution of GABAergic neurons and terminals in the rat CNS as revealed by GAD immunohistochemistry. In A. Björklund and T. Hökfelt (eds): Handbook of Chemical Neuroanatomy, Vol. 4: GABA and Neuropeptides in the CNS, Part 1. New York: Elsevier, pp. 436-608.
50. Oliver, D.L., and A. Shneiderman (1989) An EM study of the dorsal nucleus of the lateral lemniscus: Inhibitory, commissural, synaptic connections between ascending auditory pathways. J. Neurosci. 9:967-982.
51. Oliver, D., and A. Shneiderman (1991) The anatomy of the inferior colliculus: A cellular basis for integration of monaural and binaural information. In R.A. Altschuler, R.P. Bobbin, B.M. Clopton, and D.W. Hoffman (eds): Neurobiology of Hearing: The Central Auditory System. New York: Raven Press, pp. 195-222.
52. Oliver, D.L., J.A. Winer, G.E. Beckius, and R.L. Saint Marie (1994) Morphology of GABAergic neurons in the inferior colliculus of the cat. J. Comp. Neurol. 340:27-42.
53. 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. Chichester: John Wiley and Sons, pp. 417-451.
54. Ostapoff, E.-M., C.G. Benson, and R.L. Saint Marie (1997) GABA-and glycine-immunoreactive projections from the superior olivary complex to the cochlear nucleus in guinea pig. J. Comp. Neurol. 381:500-512.
55. 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.
56. 3H]aminobutyric acid (GABA) from electrically stimulated rat cortical slices and its modulation by GABAB autoreceptors. J. Pharm. Exp. Ther. 250:648-653.
57. Ramón y Cajal, S. (1909) Histologie du Système Nerveux de l'Homme et des Vertébrés. Paris: Maloine. Translated from the French by N. Swanson and L.W. Swanson (1995) New York: Oxford University Press.
58. 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.
59. 3H]glycine from the inferior colliculus by ipsilateral projections of the superior olivary complex and nuclei of the lateral lemniscus. Brain Res. 524:244-253.
60. Saint Marie, R.L., E.-M. Ostapoff, D.K. Morest, and R.J. Wenthold (1989) Glycine-immunoreactive projection of the cat lateral superior olive: Possible role in midbrain ear dominance. J. Comp. Neurol. 279:382-396.
61. 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. Hearing Res. 51:11-28.
62. Saint Marie, R.L., L. Luo, R. Newlin, and A.F. Ryan (1995) Tonotopic representations in the auditory brainstem with acoustically induced c-fos mRNA expression. Soc. Neurosci. Abstr. 21:402.
63. Schofield, B.R., and N.B. Cant (1997) Ventral nucleus of the lateral lemniscus in guinea pigs: Cytoarchitecture and inputs from the cochlear nucleus. J. Comp. Neurol. 379:363-385.
64. Schwartz, I.R. (1992) The superior olivary complex and lateral lemniscal nuclei. In D.B. Webster, A.N. Popper, and R.R. Fay (eds): The Mammalian Auditory Pathway: Neuroanatomy. New York: Springer-Verlag, pp. 117-167.
65. Schweizer, H. (1981) The connections of the inferior colliculus and the organization of the brainstem auditory system in the greater horseshoe bat (Rhinolophus ferrumequinum). J. Comp. Neurol. 201:25-49.
66. Shneiderman, A., and D.L. Oliver (1989) EM autoradiographic study of the projections from the dorsal nucleus of the lateral lemniscus. A possible source of inhibitory inputs to the inferior colliculus. J. Comp. Neurol. 286:28-47.
67. Shneiderman, A., D.L. Oliver, and C.K. Henkel (1988) Connections of the dorsal nucleus of lateral lemniscus: An inhibitory parallel pathway in the ascending auditory system. J. Comp. Neurol. 276:188-208.
68. Shneiderman, A., M.B. Chase, J.M. Rockwood, C.G. Benson, and S.J. Potashner (1993) Evidence for a GABAergic projection from the dorsal nucleus of the lateral lemniscus to the inferior colliculus. J. Neurochem. 60:72-82.
69. Shneiderman, A., D.A. Stanforth, and R.L. Saint Marie (1996) A comparison of the crossed and uncrossed, GABA-immunoreactive projections of the cat dorsal nucleus of the lateral lemniscus. Soc. Neurosci. Abstr. 22:124.
70. Thompson, G.C., A.M. Cortez, and D.M. Lam (1985) Localization of GABA immunoreactivity in the auditory brainstem of guinea pigs. Brain Res. 339:119-122.
71. Thomson, S.M., and B.H. Gähwiler (1989) Activity-dependent disinhibition. III. Desensitization and GABAB receptor-mediated presynaptic inhibition in vitro. J. Neurophysiol. 61:524-533.
72. Vater, M., M. Kossl, and A.K.E. Horn (1992) GAD-and GABA-immunoreactivity in the ascending auditory pathway of horseshoe and mustached bats. J. Comp. Neurol. 325:183-206.
73. 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.
74. Werman, R. (1980) GABA modulates the glycine-receptor interaction in Mauthner cells allosterically. In U.Z. Littauer, Y. Dudai, I. Silman, V.I. Teichberg, and Z. Vogel (eds): Neurotransmitters and Their Receptors. New York: John Wiley, pp. 393-404.
75. Whitley, J.M., and C.K. Henkel (1984) Topographical organization of the inferior collicular projection and other connections of the ventral nucleus of the lateral lemniscus in the cat. J. Comp. Neurol. 229:257-270.
76. Willard, F.H., and D.K. Ryugo (1983) Anatomy of the central auditory system. In James F. Willott (ed): The Auditory Psychobiology of the Mouse. Springfield, IL: Charles C. Thomas, pp. 201-304.
77. Winer, J.A., D.T. Larue, and G.D. Pollak (1995) GABA and glycine in the central auditory system of the mustache bat: Structural substrates for inhibitory neuronal organization. J. Comp. Neurol. 355:317-353.
78. Wu, S.H., and J.B. Kelly (1995a) In vitro brain slice studies of the rat's dorsal nucleus of the lateral lemniscus. 1. Membrane and synaptic response properties. J. Neurophysiol. 73:780-793.
79. Wu, S.H., and J.B. Kelly (1995b) In vitro brain slice studies of the rat's dorsal nucleus of the lateral lemniscus. 2. Physiological properties of biocytin-labeled neurons. J. Neurophysiol. 73:794-809.
80. Wu, S.H., and J.B. Kelly (1996) In vitro brain slice studies of the rat's dorsal nucleus of the lateral lemniscus. 3. Synaptic pharmacology. J. Neurophysiol. 75:1271-1282.
81. Zook, J.M., and J.H. Casseday (1982a) Cytoarchitecture of auditory system in lower brainstem of the mustache bat Pteronotus parnellii. J. Comp. Neurol. 207:1-13.
82. Zook, J.M., and J.H. Casseday (1982b) Origin of ascending projections to inferior colliculus in the mustache bat, Pterontus parnellii. J. Comp. Neurol. 207:14-28.
83. Zook, J.M., and J.H. Casseday (1985) Projections from the cochlear nuclei in the mustache bat, Pteronotus parnellii. J. Comp. Neurol. 237:307-324.