Physiological properties of neurons in the ventral nucleus of the lateral lemniscus of the rat: Intrinsic membrane properties and synaptic responses

Journal of Neurophysiology

Volumn 81, Issue 6, 1999, Pages 2862-2874

  Wu, Shu Hui ^a  

^a CARLETON UNIVERSITY   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL TISSUE; ARTICLE; AUDITORY STIMULATION; BRAIN DEPTH STIMULATION; BRAIN NUCLEUS; DEPOLARIZATION; HYPERPOLARIZATION; MEDIAL LEMNISCUS; MEMBRANE STEADY POTENTIAL; NERVE CELL; NERVE POTENTIAL; NEWBORN; NONHUMAN; PRIORITY JOURNAL; RAT; SYNAPTIC MEMBRANE; SYNAPTIC POTENTIAL;

EID: 0005386543     PISSN: 00223077     EISSN: None     Source Type: Journal    
DOI: 10.1152/jn.1999.81.6.2862     Document Type: Article

References (90)

1. ADAMS, J. C. Ascending projections to the inferior colliculus. J. Comp. Neurol. 183: 519-538, 1979.
2. ADAMS, J. C. Multipolar cells in the ventral cochlear nucleus project to the dorsal cochlear nucleus and the inferior colliculus. Neurosci. Lett. 37: 205-208, 1983.
3. ADAMS, J. C. Projections from octopus cells of the posteroventral cochlear nucleus to the ventral nucleus of the lateral lemniscus in cat and human. Auditory Neurosci. 3: 335-350, 1997.
4. ADAMS, J. C. AND MUGNAINI, E. Immunocytochemical evidence for inhibitory and disinhibitory circuits in the superior olive. Hear. Res. 49: 281-298, 1990.
5. ADAMS, J. C. AND WARR, W. B. Origins of axons in the cat's acoustic striae determined by injection of horseradish peroxidase into severed tracts. J. Comp. Neurol. 182: 519-538, 1976.
6. AITKIN, L. M., ANDERSON, D. J., AND BRUGGE, J. F. Tonotopic organization and discharge characteristics of single neurons in nuclei of the lateral lemniscus of the cat. J. Neurophysiol. 33: 421-440, 1970.
7. BANKS, M. I. AND SMITH, P. H. Intracellular recordings from neurobiotin-labeled cells in brain slices of the rat medial nucleus of the trapezoid body. J. Neurosci. 12: 2819-2837, 1992.
8. BATRA, R. AND FITZPATRICK, D. C. Neurons sensitive to interaural temporal disparities in the medial part of the ventral nucleus of the lateral lemniscus. J. Neurophysiol. 78: 511-515, 1997.
9. + conductances with complementary functions in postsynaptic integration at a central auditory synapse. J. Neurosci. 15: 8011-8022, 1995.
10. BROWNER, R. H. AND WEBSTER, D. B. Projections of the trapezoid body and the superior olivary complex of the kangaroo rat (Dipodomys merriami). Brain Behav. Evol. 11: 322-354, 1975.
11. BRUNSO-BECHTOLD, J. K., THOMPSON, G. C., AND MASTERTON, R. B. HRP study of the organization of auditory afferents ascending to the central nucleus of inferior colliculus in cat. J. Comp. Neurol. 197: 705-722, 1981.
12. CASSEDAY, J. H. AND COVEY, E. Mechanisms for analysis of auditory temporal patterns in the brainstem of echolocating bats. In: Neural Representation of Temporal Patterns. New York: Plenum, 1995, p. 25-51.
13. COLEMAN, J. R. AND CLERICI, W. J. Sources of projections to subdivisions of the inferior colliculus in the rat. J. Comp. Neurol. 262: 215-226, 1987.
14. COVEY, E. The monaural nuclei of the lateral lemniscus: parallel pathways from cochlear nucleus to midbrain. In: The Mammalian Cochlear Nuclei: Organization and Function. New York: Plenum, 1993, p. 321-334.
15. COVEY, E. AND CASSEDAY, J. H. Connectional basis for frequency representation in the nuclei of the lateral lemniscus of the bat Eptesicus fuscus. J. Neurosci. 6: 2926-2940, 1986.
16. COVEY, E. AND CASSEDAY, J. H. The monaural nuclei of the lateral lemniscus in an echolocating bat: parallel pathway for analyzing temporal features of sound. J. Neurosci. 11: 3455-3470, 1991.
17. DRUGA, R. AND SYKA, J. Ascending and descending projections to the inferior colliculus in the rat. Physiol. Bohemoslov. 33: 31-42, 1984.
18. ELVERLAND, H. Ascending and intrinsic projections of the superior olivary complex in the cat. Exp. Brain Res. 32: 117-134, 1978.
19. FORSYTHE, I. D. AND BARNES-DAVIES, M. The binaural auditory pathway: membrane currents limiting multiple action potential generation in the rat medial nucleus of the trapezoid body. Proc. R. Soc. Lond. B Biol. Sci. 251: 143-150, 1993.
20. FRIAUF, E. AND OSTWALD, J. Divergent projections of physiologically characterized rat ventral cochlear nucleus neurons as shown by intra-axonal injection of horseradish peroxidase. Exp. Brain Res. 73: 263-284, 1988.
21. FRISINA, R. D., WALTON, J. P., LYNCH-ARMOUR, M. A., AND BYRD, J. D. Inputs to a physiologically characterized region of the inferior colliculus of the young adult CBA mouse. Hear. Res. 115: 61-81, 1998.
22. GLENDENNING, K. K., BRUNSO-BECHTOLD, J. K., THOMPSON, G. C., AND MASTERTON, R. B. Ascending auditory afferents to the nuclei of the lateral lemniscus. J. Comp. Neurol. 232: 673-703, 1981.
23. GOLDING, N. L., ROBERTSON, D., AND OERTEL, D. Recordings from slices indicate that octopus cells of the cochlear nucleus detect coincident firing of auditory nerve fibers with temporal precision. J. Neurosci. 15: 3138-3153, 1995.
24. GONZÁLEZ-HERNÁNDEZ, T., MANTOLÁN-SARMIENTO, B., GONZÁLEZ-GONZÁLEZ, B., AND PÉREZ-GONZÁLEZ, H. Sources of GABAergic inputs to the inferior colliculus of the rat. J. Comp. Neurol. 372: 309-326, 1996.
25. GUINAN, J. J., JR., GUINAN, S. S., AND NORRIS, B. E. Single auditory units in the superior olivary complex. I. Responses to sound and classifications based on physiological properties. Intern. J. Neurosci. 4: 101-120, 1972a.
26. GUINAN, J. J., JR., NORRIS, B. E., AND GUINAN, S. S. Single auditory units in the superior olivary complex. II. Locations of unit categories and tonotopic organization. Intern. J. Neurosci. 4: 147-166, 1972b.
27. HELFERT, R. H. AND ASCHOFF, A. Superior olivary complex and nuclei of the lateral lemniscus. In: The Central Auditory System. New York: Oxford, 1997, p. 193-258.
28. HELFERT, R. H., BONNEAU, J. M., WENTHOLD, R. J., AND ALTSCHULER, R. A. GABA and glycine immunoreactivity in the guinea pig superior olivary complex. Brain Res. 6: 269-286, 1989.
29. HELFERT, R. H., SNEAD, C. R., AND ALTSCHULER, R. A. The ascending auditory pathways. In: Neurobiology of Hearing: The Central Auditory System. New York: Raven, 1991, p. 1-25.
30. HUFFMAN, R. F. AND COVEY, E. Origin of ascending projections to the nuclei of the lateral lemniscus in the big brown bat, Eptesicus fuscus. J. Comp. Neurol. 357: 532-545, 1995.
31. IWAHORI, N. A Golgi study on the dorsal nucleus of the lateral lemniscus in the mouse. Neurosci. Res. 3: 196-212, 1986.
32. KUDO, M. Projections of the nuclei of the lateral lemniscus in the cat: an autoradiographic study. Brain Res. 221: 57-69, 1981.
33. KUDO, M., NAKAMURA, Y., TOKUNO, H., AND KITAO, Y. Auditory brainstem in the mole (Mogera): nuclear configurations and the projections to the inferior colliculus. J. Comp. Neurol. 298: 400-412, 1990.
34. LENN, N. J. AND REESE, T. S. The fine structure of nerve endings in the nucleus of the trapezoid body and the ventral cochlear nucleus. Am. J. Anat. 118: 375-390, 1966.
35. LORENTE DE NÓ, R. Some unresolved problems concerning the cochlear nerve. Ann. Otol. Rhinol. Laryngol. 85: 1-28, 1976.
36. LORENTE DE NÓ, R. The Primary Acoustic Nuclei. New York: Raven, 1981.
37. MAJOROSSY, K. AND KISS, A. Convergence of topographic projections to the inferior colliculus from the auditory subcollicular nuclei. Acta Biol. Hung. 45: 347-359, 1994.
38. MANIS, P. B. Membrane properties and discharge characteristics of guinea pig dorsal cochlear nucleus neurons studied in vitro. J. Neurosci. 10: 2338-2351, 1990.
39. MANIS, P. B. AND MARX, S. O. Outward currents in isolated ventral cochlear nucleus neurons. J. Neurosci. 11: 2865-2880, 1991.
40. METZNER, W. AND RADTKE-SCHULLER, S. The nuclei of the lateral lemniscus in the rufous horseshoe bat, Rhinolophus rouxi. J. Comp. Physiol. 160: 395-411, 1987.
41. MOORE, D. Auditory brainstem of the ferret: sources of projections to the inferior colliculus. J. Comp. Neurol. 269: 342-354, 1988.
42. MOORE, M. J. AND CASPARY, D. M. Strychnine blocks binaural inhibition in lateral superior olivary neurons. J. Neurosci. 3: 237-242, 1983.
43. MOORE, J. K. AND MOORE, R. Y. Glutamic acid decarboxylase-like immunoreactivity in brainstem auditory nuclei of the rat. J. Comp. Neurol. 260: 157-174, 1987.
44. MOREST, D. K. The collateral system of the medial nucleus of the trapezoid body of the cat, its neuronal architecture and relation to the olivo-cochlear bundle. Brain Res. 9: 288-311, 1968a.
45. MOREST, D. K. The growth of synaptic endings in the mammalian brain: a study of the calyces of the trapezoid body. Z. Anat. Entwicklungsgesch. 127: 201-220, 1968b.
46. NORDEEN, K. W., KILLACKEY, J. P., AND KITZES, L. M. Ascending auditory projections to the inferior colliculus in the adult gerbil, Meriones unguiculatus. J. Comp. Neurol. 214: 131-143, 1983.
47. OERTEL, D. Synaptic responses and electrical properties of cells in brain slices of the mouse anteroventral cochlear nucleus. J. Neurosci. 3: 2043-2053, 1983.
48. OERTEL, D. The role of intrinsic neuronal properties in the encoding of auditory information in the cochlear nuclei. Curr. Opin. Neurobiol. 1: 221-228, 1991.
49. OERTEL, D. Encoding of timing in the brain stem auditory nuclei of vertebrates. Neuron 19: 959-962, 1997.
50. OLIVER, D. L. Projections to the inferior colliculus from the anteroventral cochlear nucleus in the cat: possible substrates for binaural interaction. J. Comp. Neurol. 264: 24-46, 1987.
51. PFEIFFER, R. R. Classification of response patterns of spike discharges for units in the cochlear nucleus: tone-burst stimulation. Exp. Brain Res. 1: 220-235, 1966.
52. RHODE, W. S., OERTEL, D., AND SMITH, P. H. Physiological response properties of cells labeled intracellularly with horseradish peroxidase in cat ventral cochlear nucleus. J. Comp. Neurol. 213: 448-463, 1983.
53. RHODE, W. S. AND SMITH, P. H. Physiological studies of neurons in the dorsal cochlear nucleus of the cat. J. Neurophysiol. 56: 287-307, 1986.
54. ROBERTS, R. C. AND RIBAK, C. E. GABAergic neurons and axon terminals in the brainstem auditory nuclei of the gerbil. J. Comp. Neurol. 258: 267-280, 1987.
55. ROSS, L. S., POLLAK, G. D., AND ZOOK, J. M. Origin of ascending projections to an isofrequency region of the mustache bat's inferior colliculus. J. Comp. Neurol. 270: 488-505, 1988.
56. RYUGO, D. K. AND SENTO, S. Synaptic connections of the auditory nerve in cats: relationship between endbulbs of Held and spherical bushy cells. J. Comp. Neurol. 305: 35-48, 1991.
57. 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, 1990.
58. SAINT MARIE, R. L., SHNEIDERMAN, A., AND STANFORTH, D. A. Patterns of γ-aminobutyric acid and glycine immunoreactivities reflect structural and functional differences of the cat lateral lemniscal nuclei. J. Comp. Neurol. 389: 264-276, 1997.
59. SCHOFIELD, B. R. AND CANT, N. B. Ventral nucleus of the lateral lemniscus in guinea pigs: cytoarchitecture and inputs from the cochlear nucleus. J. Comp. Neurol. 379: 363-385, 1997.
60. SCHWARTZ, A. M. AND GULLEY, R. L. Non-primary afferents to the principal cells of the rostral anteroventral cochlear nucleus of the guinea pig. Am. J. Anat. 153: 489-508, 1978.
61. SCHWARTZ, I. R. The superior olivary complex and lateral lemniscal nuclei. In: The Mammalian Auditory Pathway: Neuroanatomy. New York: Springer-Verlag, 1992, p. 117-167.
62. SCHWEIZER, H. 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, 1981.
63. SMITH, P. H. Structural and functional differences distinguish principal from nonprincipal cells in the guinea pig MSO slice. J. Neurophysiol. 73: 1653-1667, 1995.
64. SMITH, P. H., JORIS, P. X., AND YIN, T.C.T. Anatomy and physiology of principal cells of the medial nucleus of the trapezoid body (MNTB) of the cat. J. Neurophysiol. 79: 3127-3142, 1998.
65. SPANGLER, K. M., WARR, W. B., AND HENKEL, C. K. The projections of principal cells of the medial nucleus of the trapezoid body in the cat. J. Comp. Neurol. 238: 249-262, 1985.
66. STRUTZ, J. The origin of the afferent innervation to the inferior colliculus in guinea pig. Arch. Otorhinolaryngol. 228: 285-294, 1980.
67. SUNEJA, S. K., BENSON, C. G., GROSS, J., AND POTASHNER, S. J. Uptake and release of D-aspartate, GABA, and glycine in guinea pig brainstem auditory nuclei. J. Neurochem. 64: 147-160, 1995a.
68. SUNEJA, S. K., BENSON, C. G., GROSS, J., AND POTASHNER, S. J. Evidence for glutamatergic projections from the cochlear nucleus to the superior olive and the ventral nucleus of the lateral lemniscus. J. Neurochem. 64: 161-171, 1995b.
69. THOMPSON, A. M. Heterogeneous projections of the cat posteroventral cochlear nucleus. J. Comp. Neurol. 390: 439-453, 1998.
70. VATER, M., COVEY, E., AND CASSEDAY, J. H. The columnar region of the ventral nucleus of the lateral lemniscus in the big brown bat (Eptesicus juscus): synaptic arrangements and structural correlates of feedforward inhibitory function. Cell Tissue Res. 289: 223-233, 1997.
71. VATER, M. AND FENG, A. S. Functional organization of ascending and descending connections of the cochlear nucleus of horseshoe bats. J. Comp. Neurol. 292: 373-395, 1990.
72. VATER, M., KÖSSL, M., AND HORN, A.K.E. GAD- and GABA-immunoreactivity in the ascending auditory pathway of horseshoe and mustache bats. J. Comp. Neurol. 325: 183-206, 1992.
73. WARR, W. B. Fiber degeneration following lesions in the multipolar and globular cell areas in the ventral cochlear nucleus of the cat. Brain Res. 40: 247-270, 1972.
74. WARR, W. B. Parallel ascending pathways from the cochlear nucleus: Neuroanatomical evidence of functional specialization. In: Contributions to Sensory Physiology. New York: Academic, 1982, vol. 7, p. 1-38.
75. WARR, W. B. AND BECK, J. E. Multiple projections from the ventral nucleus of the trapezoid body in the rat. Hear. Res. 93: 83-101, 1996.
76. WHITLEY, J. M. AND HENKEL, C. K. Topographical organization of the inferior colliculus projection and other connections of the ventral nucleus of the lateral lemniscus in the cat. J. Comp. Neurol. 229: 257-270, 1984.
77. WILLARD, F. H. AND MARTIN, G. F. The auditory brainstem nuclei and some of their projections to the inferior colliculus in the North American opossum. Neuroscience 10: 1203-1232, 1983.
78. WILLARD, F. H. AND RYUGO, D. K. Anatomy of the central auditory system. In: The Auditory Psychobiology of the Mouse. Springfield, IL: Charles Thomas, 1983, p. 201-304.
79. WINER, J. A., LARUE, D. T., AND POLLAK, G. D. GABA and glycine in the central auditory system of the mustache bat: structural substrates for inhibitory neuronal organization. J. Comp. Neurol. 355: 317-353, 1995.
80. WU, S. H. Intrinsic membrane properties and firing characteristics of neurons in the ventral nucleus of the lateral lemniscus studied in rat brain slice. Soc. Neurosci. Abstr. 22: 647, 1996.
81. WU, S. H. Excitatory and inhibitory synaptic responses in the rat's ventral nucleus of the lateral lemniscus studied in brain slices. Soc. Neurosci. Abstr. 23: 1549, 1997.
82. WU, S. H. AND FU, X. W. Glutamate receptors underlying excitatory synaptic transmission in the rat's lateral superior olive studied in vitro. Hear. Res. 122: 47-59, 1998.
83. WU, S. H. AND KELLY, J. B. Physiological properties of neurons in the mouse superior olive: membrane characteristics and postsynaptic responses studied in vitro. J. Neurophysiol. 65: 230-246, 1991.
84. WU, S. H. AND KELLY, J. B. In vitro brain slice studies of the rat's dorsal nucleus of the lateral lemniscus. II. Physiological properties of biocytin-labeled neurons. J. Neurophysiol. 73: 794-809, 1995.
85. WU, S. H. AND OERTEL, D. Intracellular injection with horseradish peroxidase of physiologically characterized stellate and bushy cells in slices of mouse anteroventral cochlear nucleus. J. Neurosci. 4: 1577-1588, 1984.
86. ZHANG, D. X., LI, L., KELLY, J. B., AND WU, S. H. GABAergic projections from the lateral lemniscus to the inferior colliculus of the rat. Hear. Res. 117: 1-12, 1998.
87. ZHAO, M. AND WU, S. H. Intracellular labeling of cells in brain slice preparation of the rat's ventral nucleus of the lateral lemniscus. Assoc. Res. Otolaryngol. Abstr. 21: 93, 1998.
88. ZOOK, J. M. AND CASSEDAY, J. H. Cytoarchitecture of auditory system in lower brainstem of the mustache bat, Pteronotus parnellii. J. Comp. Neurol. 207: 1-13, 1982.
89. ZOOK, J. M. AND CASSEDAY, J. H. Projections from the cochlear nuclei in the mustache bat, Pteronotus parnellii, J. Comp. Neurol. 237: 307-324, 1985.
90. ZOOK, J. M. AND CASSEDAY, J. H. Convergence of ascending pathways at the inferior colliculus of the mustache bat, Pteronotus parnelli. J. Comp. Neurol. 261: 347-361, 1987.