The medial nucleus of the trapezoid body in rat: Spectral and temporal properties vary with anatomical location of the units

European Journal of Neuroscience

Volumn 27, Issue 10, 2008, Pages 2587-2598

  Tolnai, Sandra ^a,b,c   Hernandez, Olga ^a,b   Englitz, Bernhard ^c,d   Rübsamen, Rudolf ^c   Malmierca, Manuel S ^a,b  

^a UNIVERSITY OF SALAMANCA   (Spain)

^b UNIVERSITY OF SALAMANCA   (Spain)

^c UNIVERSITY OF LEIPZIG   (Germany)

^d MAX PLANCK INSTITUTE FOR MATHEMATICS IN THE SCIENCES   (Germany)

Author keywords

3D reconstruction; Auditory; In vivo electrophysiology; Sinusoidally amplitude modulated stimuli; Superior olivary complex; Temporal and spectral properties

Indexed keywords

AMPLITUDE MODULATION; ANIMAL EXPERIMENT; ARTICLE; AUDITORY CORTEX; AUDITORY STIMULATION; BRAIN FUNCTION; BRAIN NUCLEUS; BRAIN REGION; COCHLEAR NUCLEUS; CONTROLLED STUDY; EVOKED AUDITORY RESPONSE; MALE; MEDIAL NUCLEUS OF THE TRAPEZOID BODY; NONHUMAN; OLIVARY NUCLEUS; PRIORITY JOURNAL; RAT;

ACOUSTIC STIMULATION; ACTION POTENTIALS; ANIMALS; AUDITORY PATHWAYS; AUDITORY THRESHOLD; BRAIN MAPPING; ELECTROPHYSIOLOGY; MALE; NEURAL INHIBITION; NEURONS; OLIVARY NUCLEUS; PONS; RATS; RATS, LONG-EVANS; RATS, WISTAR; REACTION TIME; SOUND LOCALIZATION; TIME FACTORS;

EID: 44649104496     PISSN: 0953816X     EISSN: 14609568     Source Type: Journal    
DOI: 10.1111/j.1460-9568.2008.06228.x     Document Type: Article

References (76)

1. Aoki, E., Semba, R., Keino, H., Kato, K. Kashiwamata, S. (1988) Glycine-like immunoreactivity in the rat auditory pathway. Brain Res., 442, 63 71.
2. Astl, J., Popelar, J., Kvasnak, E. Syka, J. (1996) Comparison of response properties of neurons in the inferior colliculus of guinea pigs under different anesthetics. Audiology, 35, 335 345.
3. Banks, M.I. Smith, P.H. (1992) Intracellular recordings from neurobiotin-labeled cells in brain slices of the rat medial nucleus of the trapezoid body. J. Neurosci., 12, 2819 2837.
4. el Barbary, A. (1991a) Auditory nerve of the normal and jaundiced rat. I. Spontaneous discharge rate and cochlear nerve histology. Hear. Res., 54, 75 90.
5. el Barbary, A. (1991b) Auditory nerve of the normal and jaundiced rat. II. Frequency selectivity and two-tone rate suppression. Hear. Res., 54, 91 104.
6. Barnes-Davies, M. Forsythe, I.D. (1995) Pre- and postsynaptic glutamate receptors at a giant excitatory synapse in rat auditory brainstem slices. J. Physiol. (Lond.), 488, 387 406.
7. Bazwinsky, I., Bidmon, H.J., Zilles, K. Hilbig, H. (2005) Characterization of the rhesus monkey superior olivary complex by calcium binding proteins and synaptophysin. J. Anat., 207, 745 761.
8. Borst, J.G., Helmchen, F. Sakmann, B. (1995) Pre- and postsynaptic whole-cell recordings in the medial nucleus of the trapezoid body of the rat. J. Physiol. (Lond.), 489, 825 840.
9. Calford, M.B., Webster, W.R. Semple, M.M. (1983) Measurement of frequency selectivity of single neurons in the central auditory pathway. Hear. Res., 11, 395 401.
10. Chuhma, N. Ohmori, H. (1998) Postnatal development of phase-locked high-fidelity synaptic transmission in the medial nucleus of the trapezoid body of the rat. J. Neurosci., 18, 512 520.
11. Davis, K.A., Lomakin, O. Pesavento, M.J. (2007) Response properties of single units in the dorsal nucleus of the lateral lemniscus of decerebrate cats. J. Neurophysiol., 98, 1475 1488.
12. Elezgarai, I., Diez, J., Puente, N., Azkue, J.J., Benitez, R., Bilbao, A., Knopfel, T., Donate-Oliver, F. Grandes, P. (2003) Subcellular localization of the voltage-dependent potassium channel Kv3.1b in postnatal and adult rat medial nucleus of the trapezoid body. Neuroscience, 118, 889 898.
13. Forsythe, I.D. (1994) Direct patch recording from identified presynaptic terminals mediating glutamatergic EPSCs in the rat CNS, in vitro. J. Physiol., 479 (Pt. 3 381 387.
14. Frisina, R.D. (2001) Subcortical neural coding mechanisms for auditory temporal processing. Hear. Res., 158, 1 27.
15. Frisina, R.D., Smith, R.L. Chamberlain, S.C. (1990) Encoding of amplitude modulation in the gerbil cochlear nucleus: I. A hierarchy of enhancement. Hear. Res., 44, 99 122.
16. Futai, K., Okada, M., Matsuyama, K. Takahashi, T. (2001) High-fidelity transmission acquired via a developmental decrease in NMDA receptor expression at an auditory synapse. J. Neurosci., 21, 3342 3349.
17. Goldberg, J.M. Brown, P.B. (1969) Response of binaural neurons of dog superior olivary complex to dichotic tonal stimuli: some physiological mechanisms of sound localization. J. Neurophysiol., 32, 613 636.
18. Grandes, P. Streit, P. (1989) Glutamate-like immunoreactivity in calyces of Held. J. Neurocytol., 18, 685 693.
19. Guinan, J.J. Jr. Li, R.Y. (1990) Signal processing in brainstem auditory neurons which receive giant endings (calyces of Held) in the medial nucleus of the trapezoid body of the cat. Hear. Res., 49, 321 334.
20. Guinan, J.J. Jr, Guinan, S.S. Norris, B.E. (1972a) Single auditory units in the superior olivary complex I: responses to sounds and classification based on physiological properties. Int. J. Neurosci., 4, 101 120.
21. Guinan, J.J. Jr, Norris, B.E. Guinan, S.S. (1972b) Single auditory units in the superior olivary complex II: locations of unit categories and tonotopic organization. Int. J. Neurosci., 4, 147 166.
22. Harrison, J.M. Warr, W.B. (1962) A study of the cochlear nuclei and ascending auditory pathways of the medulla. J. Comp. Neurol., 119, 341 379.
23. Heffner, H.E., Heffner, R.S., Contos, C. Ott, T. (1994) Audiogram of the hooded Norway rat. Hear. Res., 73, 244 247.
24. von Hehn, C.A., Bhattacharjee, A. Kaczmarek, L.K. (2004) Loss of Kv3.1 tonotopicity and alterations in cAMP response element-binding protein signaling in central auditory neurons of hearing impaired mice. J. Neurosci., 24, 1936 1940.
25. Held, H. (1893). Die zentrale Gehorleitung. In His, W. Du Bois-Reymond, E. (Eds Archiv fur Anatomie und Physiologie. Leipzig Verlag von Veit und Comp, Leipzig, pp. 201 380.
26. Hermann, J., Pecka, M., von Gersdorff, H., Grothe, B. Klug, A. (2007) Synaptic transmission at the calyx of Held under in vivo like activity levels. J. Neurophysiol., 98, 807 820.
27. Hernandez, O., Espinosa, N., Perez-Gonzalez, D. Malmierca, M.S. (2005) The inferior colliculus of the rat: a quantitative analysis of monaural frequency response areas. Neuroscience, 132, 203 217.
28. Joris, P.X. Yin, T.C. (1992) Responses to amplitude-modulated tones in the auditory nerve of the cat. J. Acoust. Soc. Am., 91, 215 232.
29. Joris, P.X. Yin, T.C.T. (1998) Envelope coding in the lateral superior olive. III. Comparison with afferent pathways. J. Neurophysiol., 79, 253 269.
30. Joris, P.X., Schreiner, C.E. Rees, A. (2004) Neural processing of amplitude-modulated sounds. Physiol. Rev., 84, 541 577.
31. Kadner, A. Berrebi, A.S. (2008) Encoding of temporal features of auditory stimuli in the medial nucleus of the trapezoid body and superior paraolivary nucleus of the rat. Neuroscience, 151, 868 887.
32. Kadner, A., Kulesza, R.J. Jr Berrebi, A.S. (2006) Neurons in the medial nucleus of the trapezoid body and superior paraolivary nucleus of the rat may play a role in sound duration coding. J. Neurophysiol., 95, 1499 1508.
33. Kiang, N.Y., Sachs, M.B. Peake, W.T. (1967) Shapes of tuning curves for single auditory-nerve fibers. J. Acoust. Soc. Am., 42, 1341 1342.
34. Kiang, N.Y., Liberman, M.C. Levine, R.A. (1976) Auditory-nerve activity in cats exposed to ototoxic drugs and high-intensity sounds. Ann. Otol. Rhinol. Laryngol., 85, 752 768.
35. Kopp-Scheinpflug, C., Dehmel, S., Dorrscheidt, G.J. Rubsamen, R. (2002) Interaction of excitation and inhibition in anteroventral cochlear nucleus neurons that receive large endbulb synaptic endings. J. Neurosci., 22, 11004 11018.
36. Kopp-Scheinpflug, C., Fuchs, K., Lippe, W.R., Tempel, B.L. Rubsamen, R. (2003a) Decreased temporal precision of auditory signaling in Kcna1-null mice: an electrophysiological study in vivo. J. Neurosci., 23, 9199 9207.
37. Kopp-Scheinpflug, C., Lippe, W.R., Dorrscheidt, G.J. Rubsamen, R. (2003b) The medial nucleus of the trapezoid body in the gerbil is more than a relay: comparison of pre- and postsynaptic activity. J. Assoc. Res. Otolaryngol., 4, 1 23.
38. Kopp-Scheinpflug, C., Dehmel, S. Rubsamen, R. (2006) Opposite Actions of Glycine at a Mammalian Central Synapse. Midwinter Meeting of the Association for Research in Otolaryngology, Abstract no. 679, Baltimore, MD.
39. Krishna, B.S. Semple, M.N. (2000) Auditory temporal processing: responses to sinusoidally amplitude-modulated tones in the inferior colliculus. J. Neurophysiol., 84, 255 273.
40. Kulesza, R.J. Jr, Spirou, G.A. Berrebi, A.S. (2003) Physiological response properties of neurons in the superior paraolivary nucleus of the rat. J. Neurophysiol., 89, 2299 2312.
41. Kulesza, R.J. Jr, Kadner, A. Berrebi, A.S. (2007) Distinct roles for glycine and GABA in shaping the response properties of neurons in the superior paraolivary nucleus of the rat. J. Neurophysiol., 97, 1610 1620.
42. Kuwabara, N. Zook, J.M. (1991) Classification of the principal cells of the medial nucleus of the trapezoid body. J. Comp. Neurol., 314, 707 720.
43. Kuwabara, N., DiCaprio, R.A. Zook, J.M. (1991) Afferents to the medial nucleus of the trapezoid body and their collateral projections. J. Comp. Neurol., 314, 684 706.
44. Kuwada, S. Batra, R. (1999) Coding of sound envelopes by inhibitory rebound in neurons of the superior olivary complex in the unanesthetized rabbit. J. Neurosci., 19, 2273 2287.
45. LeBeau, F.E., Malmierca, M.S. Rees, A. (2001) Iontophoresis in vivo demonstrates a key role for GABA(A) and glycinergic inhibition in shaping frequency response areas in the inferior colliculus of guinea pig. J. Neurosci., 21, 7303 7312.
46. Li, W., Kaczmarek, L.K. Perney, T.M. (2001) Localization of two high-threshold potassium channel subunits in the rat central auditory system. J. Comp. Neurol., 437, 196 218.
47. Liberman, M.C. (1978) Auditory-nerve response from cats raised in a low-noise chamber. J. Acoust. Soc. Am., 63, 442 455.
48. Malmierca, M.S. (2003) The structure and physiology of the rat auditory system: an overview. Int. Rev. Neurobiol., 56, 147 211.
49. Merrill, E.G. Ainsworth, A. (1972) Glass-coated platinum-plated tungsten microelectrodes. Med. Biol. Eng., 10, 662 672.
50. Moore, M.J. Caspary, D.M. (1983) Strychnine blocks binaural inhibition in lateral superior olivary neurons. J. Neurosci., 3, 237 242.
51. Morest, D.K. (1968) The growth of synaptic endings in the mammalian brain: a study of the calyces of the trapezoid body. Z. Anat. Entwicklungsgesch., 127, 201 220.
52. Paolini, A.G., FitzGerald, J.V., Burkitt, A.N. Clark, G.M. (2001) Temporal processing from the auditory nerve to the medial nucleus of the trapezoid body in the rat. Hear. Res., 159, 101 116.
53. Pasic, T.R., Moore, D.R. Rubel, E.W. (1994) Effect of altered neuronal activity on cell size in the medial nucleus of the trapezoid body and ventral cochlear nucleus of the gerbil. J. Comp. Neurol., 348, 111 120.
54. Rees, A. Palmer, A.R. (1989) Neuronal responses to amplitude-modulated and pure-tone stimuli in the guinea pig inferior colliculus, and their modification by broadband noise. J. Acoust. Soc. Am., 85, 1978 1994.
55. Rhode, W.S. Greenberg, S. (1994) Encoding of amplitude modulation in the cochlear nucleus of the cat. J. Neurophysiol., 71, 1797 1825.
56. Sachs, M.B. Abbas, P.J. (1974) Rate versus level functions for auditory-nerve fibers in cats: tone-burst stimuli. J. Acoust. Soc. Am., 56, 1835 1847.
57. Schmiedt, R.A. (1989) Spontaneous rates, thresholds and tuning of auditory-nerve fibers in the gerbil: comparisons to cat data. Hear. Res., 42, 23 35.
58. Schneggenburger, R. Forsythe, I.D. (2006) The calyx of Held. Cell Tissue Res., 326, 311 337.
59. Smith, P.H. Rhode, W.S. (1987) Characterization of HRP-labeled globular bushy cells in the cat anteroventral cochlear nucleus. J. Comp. Neurol., 266, 360 375.
60. Smith, P.H., Joris, P.X., Carney, L.H. Yin, T.C. (1991) Projections of physiologically characterized globular bushy cell axons from the cochlear nucleus of the cat. J. Comp. Neurol., 304, 387 407.
61. Smith, P.H., Joris, P.X. Yin, T.C. (1998) Anatomy and physiology of principal cells of the medial nucleus of the trapezoid body (MNTB) of the cat. J. Neurophysiol., 79, 3127 3142.
62. Sommer, I., Lingenhohl, K. Friauf, E. (1993) Principal cells of the rat medial nucleus of the trapezoid body: an intracellular in vivo study of their physiology and morphology. Exp. Brain Res., 95, 223 239.
63. Song, P., Yang, Y., Barnes-Davies, M., Bhattacharjee, A., Hamann, M., Forsythe, I.D., Oliver, D.L. Kaczmarek, L.K. (2005) Acoustic environment determines phosphorylation state of the Kv3.1 potassium channel in auditory neurons. Nat. Neurosci., 8, 1335 1342.
64. Spangler, K.M., Warr, W.B. Henkel, C.K. (1985) The projections of principal cells of the medial nucleus of the trapezoid body in the cat. J. Comp. Neurol., 238, 249 262.
65. Spirou, G.A., Brownell, W.E. Zidanic, M. (1990) Recordings from cat trapezoid body and HRP labeling of globular bushy cell axons. J. Neurophysiol., 63, 1169 1190.
66. Sutter, M.L. (2000) Shapes and level tolerances of frequency tuning curves in primary auditory cortex: quantitative measures and population codes. J. Neurophysiol., 84, 1012 1025.
67. Sutter, M.L. Schreiner, C.E. (1991) Physiology and topography of neurons with multipeaked tuning curves in cat primary auditory cortex. J. Neurophysiol., 65, 1207 1226.
68. Taschenberger, H. von Gersdorff, H. (2000) Fine-tuning an auditory synapse for speed and fidelity: developmental changes in presynaptic waveform, EPSC kinetics, and synaptic plasticity. J. Neurosci., 20, 9162 9173.
69. Tolbert, L.P., Morest, D.K. Yurgelun-Todd, D.A. (1982) The neuronal architecture of the anteroventral cochlear nucleus of the cat in the region of the cochlear nerve root: horseradish peroxidase labelling of identified cell types. Neuroscience, 7, 3031 3052.
70. Tollin, D.J. (2003) The lateral superior olive: a functional role in sound source localization. Neuroscientist, 9, 127 143.
71. Tollin, D.J. Yin, T.C. (2005) Interaural phase and level difference sensitivity in low-frequency neurons in the lateral superior olive. J. Neurosci., 25, 10648 10657.
72. Tolnai, S., Hernandez, O., Rubsamen, R. Malmierca, M.S. (2005) The Medial Nucleus of the Trapezoid Body: An In Vivo Electrophysiological Study in Rat. Midwinter Meeting of the Association for Research in Otolaryngology, New Orleans, LA.
73. Tolnai, S., Englitz, B., Dehmel, S., Kopp-Scheinpflug, C., Jost, J. Rübsamen, R. (2006) Temporal Properties of Inhibition shaping the Response of MNTB Principal Cells. Midwinter Meeting of the Association for Research in Otolaryngology, Denver, CO.
74. Tsuchitani, C. (1997) Input from the medial nucleus of trapezoid body to an interaural level detector. Hear. Res., 105, 211 224.
75. Wenthold, R.J., Huie, D., Altschuler, R.A. Reeks, K.A. (1987) Glycine immunoreactivity localized in the cochlear nucleus and superior olivary complex. Neuroscience, 22, 897 912.
76. Yin, T.C.T. 2002. Neural mechanisms of encoding binaural localization cues in the auditory brainstem. In Oertel, D., Popper, A.N. Fay, R.R. (Eds Integrative Functions in the Mammalian Auditory Pathway. Springer-Verlag, New York, pp. 99 159.