Encoding of Interaural Timing for Binaural Hearing

The Senses: A Comprehensive Reference

Volumn 3, Issue , 2008, Pages 613-630

  Burger, R M ^a   Rubel, E W ^b  

^a LEHIGH UNIVERSITY   (United States)

^b UNIVERSITY OF WASHINGTON   (United States)

Author keywords

Binaural processing; Duplex theory; Interaural intensity disparity; Interaural phase disparity; Interaural time disparity; Jeffress model; Kv1; Kv3; Medial superior olive; Nucleus angularis; Nucleus laminaris; Nucleus magnocellularis

Indexed keywords

EID: 84882541087     PISSN: None     EISSN: None     Source Type: Book    
DOI: 10.1016/B978-012370880-9.00046-3     Document Type: Chapter

References (121)

1. Adamson C.L., Reid M.A., Mo Z.L., Bowne-English J., Davis R.L. Firing features and potassium channel content of murine spiral ganglion neurons vary with cochlear location. J. Comp. Neurol. 2002, 447:331-350.
2. Agmon-Snir H., Carr C.E., Rinzel J. The role of dendrites in auditory coincidence detection. Nature 1998, 393:268-272.
3. Bal R., Oertel D. Potassium currents in octopus cells of the mammalian cochlear nucleus. J. Neurophysiol. 2001, 86:2299-2311.
4. Banks M.I., Smith P.H. Intracellular recordings from neurobiotin-labeled cells in brain slices of the rat medial nucleus of the trapezoid body. J. Neurosci. 1992, 12:2819-2837.
5. Batra R., Fitzpatrick D.C. Neurons sensitive to interaural temporal disparities in the medial part of the ventral nucleus of the lateral lemniscus. J. Neurophysiol. 1997, 78:511-515.
6. Batra R., Kuwada S., Fitzpatrick D.C. Sensitivity to interaural temporal disparities of low- and high-frequency neurons in the superior olivary complex. II. Coincidence detection. J. Neurophysiol. 1997, 78:1237-1247.
7. Batra R., Kuwada S., Fitzpatrick D.C. Sensitivity to interaural temporal disparities of low- and high-frequency neurons in the superior olivary complex. I. Heterogeneity of responses. J. Neurophysiol. 1997, 78:1222-1236.
8. Beckius G.E., Batra R., Oliver D.L. Axons from anteroventral cochlear nucleus that terminate in medial superior olive of cat: observations related to delay lines. J. Neurosci. 1999, 19:3146-3161.
9. Ben-Ari Y., Rovira C., Gaiarsa J.L., Corradetti R., Robain O., Cherubini E. GABAergic mechanisms in the CA3 hippocampal region during early postnatal life. Prog. Brain Res. 1990, 83:313-321.
10. Brand A., Behrend O., Marquardt T., McAlpine D., Grothe B. Precise inhibition is essential for microsecond interaural time difference coding. Nature 2002, 417:543-547.
11. + conductances with complementary functions in postsynaptic integration at a central auditory synapse. J. Neurosci. 1995, 15:8011-8022.
12. Burger R.M., Cramer K.S., Pfeiffer J.D., Rubel E.W. Avian superior olivary nucleus provides divergent inhibitory input to parallel auditory pathways. J. Comp. Neurol. 2005, 481:6-18.
13. Cant N.B., Hyson R.L. Projections from the lateral nucleus of the trapezoid body to the medial superior olivary nucleus in the gerbil. Hear. Res. 1992, 58:26-34.
14. Carney L.H. Modelling the sensitivity of cells in the anteroventral cochlear nucleus to spatiotemporal discharge patterns. Philos. Trans. R. Soc. Lond. B. Biol. Sci. 1992, 336:403-406.
15. Carr C.E., Boudreau R.E. Development of the time coding pathways in the auditory brainstem of the barn owl. J. Comp. Neurol. 1996, 373:467-483.
16. Carr C.E., Code R.A. Anatomy and Physiology of the Central Auditory System of Birds and Reptiles. Comparative Hearing: Birds and Reptiles 2000, 197-248. Springer. A.N. Popper, R.R. Fay, R.J. Dooling (Eds.).
17. Carr C.E., Konishi M. A circuit for detection of interaural time differences in the brain stem of the barn owl. J. Neurosci. 1990, 10:3227-3246.
18. Carr C.E., Soares D. Evolutionary convergence and shared computational principles in the auditory system. Brain. Behav. Evol. 2002, 59:294-311.
19. Carr C.E., Fujita I., Konishi M. Distribution of GABAergic neurons and terminals in the auditory system of the barn owl. J. Comp. Neurol. 1989, 286:190-207.
20. Carr C.E., Soares D., Parameshwaran S., Perney T. Evolution and development of time coding systems. Curr. Opin. Neurobiol. 2001, 11:727-733.
21. Cherubini E., Rovira C., Gaiarsa J.L., Corradetti R., Ben Ari Y. GABA mediated excitation in immature rat CA3 hippocampal neurons. Int. J. Dev. Neurosci. 1990, 8:481-490.
22. Code R.A., Burd G.D., Rubel E.W. Development of GABA immunoreactivity in brainstem auditory nuclei of the chick: ontogeny of gradients in terminal staining. J. Comp. Neurol. 1989, 284:504-518.
23. Colburn H.S., Durlach N.I. Models of Binaural Interaction. Handbook of Perception 1978, 467-518. Academic Press. E.C. Carterette, M. Friedman (Eds.).
24. Dasika V.K., White J.A., Carney L.H., Colburn H.S. Effects of inhibitory feedback in a network model of avian brain stem. J. Neurophysiol. 2005, 94:400-414.
25. - regulation. J. Physiol. 1999, 520(Pt 1):121-137.
26. Finlayson P.G., Caspary D.M. Low-frequency neurons in the lateral superior olive exhibit phase-sensitive binaural inhibition. J. Neurophysiol. 1991, 65:598-605.
27. Funabiki K., Koyano K., Ohmori H. The role of GABAergic inputs for coincidence detection in the neurones of nucleus laminaris of the chick. J. Physiol. 1998, 508(Pt 3):851-869.
28. Gan L., Kaczmarek L.K. When, where, and how much? Expression of the Kv3.1 potassium channel in high-frequency firing neurons. J. Neurobiol. 1998, 37:69-79.
29. Glendenning K.K., Hutson K.A., Nudo R.J., Masterton R.B. Acoustic chiasm II: anatomical basis of binaurality in lateral superior olive of cat. J. Comp. Neurol. 1985, 232:261-285.
30. Goldberg J.M., Brown P.B. Response of binaural neurons of dog superior olivary complex to dichotic tonal stimuli: some physiological mechanisms of sound localization. J. Neurophysiol. 1969, 32:613-636.
31. Grigg J.J., Brew H.M., Tempel B.L. Differential expression of voltage-gated potassium channel genes in auditory nuclei of the mouse brainstem. Hear. Res. 2000, 140:77-90.
32. Grothe B. New roles for synaptic inhibition in sound localization. Nat. Rev. Neurosci. 2003, 4:540-550.
33. Grothe B., Sanes D.H. Bilateral inhibition by glycinergic afferents in the medial superior olive. J. Neurophysiol. 1993, 69:1192-1196.
34. Grothe B., Sanes D.H. Synaptic inhibition influences the temporal coding properties of medial superior olivary neurons: an in vitro study. J. Neurosci. 1994, 14:1701-1709.
35. Hackett J.T., Jackson H., Rubel E.W. Synaptic excitation of the second and third order auditory neurons in the avian brain stem. Neuroscience 1982, 7:1455-1469.
36. Hall J.L. Binaural interaction in the accessory superior-olivary nucleus of the cat. J. Acoust. Soc. Am. 1965, 37:814-823.
37. Harper N.S., McAlpine D. Optimal neural population coding of an auditory spatial cue. Nature 2004, 430:682-686.
38. Hoy R.R., Robert D. Tympanal hearing in insects. Annu. Rev. Entomol. 1996, 41:433-450.
39. Hyson R.L., Reyes A.D., Rubel E.W. A depolarizing inhibitory response to GABA in brainstem auditory neurons of the chick. Brain Res. 1995, 677:117-126.
40. Jackson H., Hackett J.T., Rubel E.W. Organization and development of brain stem auditory nuclei in the chick: ontogeny of postsynaptic responses. J. Comp. Neurol. 1982, 210:80-86.
41. Jeffress L.A. A place theory of sound localization. J. Comp. Physiol. Psychol. 1948, 41:35-39.
42. Joris P.X., Yin T.C. Envelope coding in the lateral superior olive. I. Sensitivity to interaural time differences. J. Neurophysiol. 1995, 73:1043-1062.
43. Joseph A.W., Hyson R.L. Coincidence detection by binaural neurons in the chick brain stem. J. Neurophysiol. 1993, 69:1197-1211.
44. Kakazu Y., Akaike N., Komiyama S., Nabekura J. Regulation of intracellular chloride by cotransporters in developing lateral superior olive neurons. J. Neurosci. 1999, 19:2843-2851.
45. Kandler K., Friauf E. Development of glycinergic and glutamatergic synaptic transmission in the auditory brainstem of perinatal rats. J. Neurosci. 1995, 15:6890-6904.
46. Knudsen E.I., Konishi M. Mechanisms of sound localization in the barn owl (Tyto alba). J. Comp. Physiol. A Neuroethol. Sens. Neural. Behav. Physiol. 1979, 133:13-21.
47. Koch C., Segev I. The role of single neurons in information processing. Nat. Neurosci. 2000, 3(Suppl):1171-1177.
48. Kotak V.C., Korada S., Schwartz I.R., Sanes D.H. A developmental shift from GABAergic to glycinergic transmission in the central auditory system. J. Neurosci. 1998, 18:4646-4655.
49. Kuba H., Yamada R., Fukui I., Ohmori H. Tonotopic specialization of auditory coincidence detection in nucleus laminaris of the chick. J. Neurosci. 2005, 25:1924-1934.
50. Kubke M.F., Massoglia D.P., Carr C.E. Developmental changes underlying the formation of the specialized time coding circuits in barn owls (Tyto alba). J. Neurosci. 2002, 22:7671-7679.
51. Kuwabara N., Zook J.M. Projections to the medial superior olive from the medial and lateral nuclei of the trapezoid body in rodents and bats. J. Comp. Neurol. 1992, 324:522-538.
52. Kuwada S., Yin T.C. Binaural interaction in low-frequency neurons in inferior colliculus of the cat. I. Effects of long interaural delays, intensity, and repetition rate on interaural delay function. J. Neurophysiol. 1983, 50:981-999.
53. Lachica E.A., Rubsamen R., Rubel E.W. GABAergic terminals in nucleus magnocellularis and laminaris originate from the superior olivary nucleus. J. Comp. Neurol. 1994, 348:403-418.
54. Lu T., Trussell L.O. Inhibitory transmission mediated by asynchronous transmitter release. Neuron 2000, 26:683-694.
55. Lu T., Trussell L.O. Mixed excitatory and inhibitory GABA-mediated transmission in chick cochlear nucleus. J. Physiol. 2001, 535:125-131.
56. Lu Y., Burger R.M., Rubel E.W. GABA(B) receptor activation modulates GABA(A) receptor-mediated inhibition in chicken nucleus magnocellularis neurons. J. Neurophysiol. 2005, 93:1429-1438.
57. Lu Y., Monsivais P., Tempel B.L., Rubel E.W. Activity-dependent regulation of the potassium channel subunits Kv1.1 and Kv3.1. J. Comp. Neurol. 2004, 470:93-106.
58. Macica C.M., von Hehn C.A., Wang L.Y., et al. Modulation of the kv3.1b potassium channel isoform adjusts the fidelity of the firing pattern of auditory neurons. J. Neurosci. 2003, 23:1133-1141.
59. Magnusson A.K., Kapfer C., Grothe B., Koch U. Maturation of Glycinergic Inhibition in the Gerbil Medial Superior Olive after Hearing Onset. J. Physiol. 2005, 568:497-512.
60. Maki K., Furukawa S. Acoustical cues for sound localization by the Mongolian gerbil, Meriones unguiculatus. J. Acoust. Soc. Am. 2005, 118:872-886.
61. Manis P.B., Marx S.O. Outward currents in isolated ventral cochlear nucleus neurons. J Neurosci 1991, 11:2865-2880.
62. McAlpine D., Grothe B. Sound localization and delay lines - do mammals fit the model?. Trends Neurosci 2003, 26:347-350.
63. McAlpine D., Jiang D., Palmer A.R. A neural code for low-frequency sound localization in mammals. Nat. Neurosci. 2001, 4:396-401.
64. Monsivais P., Rubel E.W. Accommodation enhances depolarizing inhibition in central neurons. J. Neurosci. 2001, 21:7823-7830.
65. Monsivais P., Yang L., Rubel E.W. GABAergic inhibition in nucleus magnocellularis: implications for phase locking in the avian auditory brainstem. J. Neurosci. 2000, 20:2954-2963.
66. Moushegian G., Rupert A.L., Langford T.L. Stimulus coding by medial superior olivary neurons. J. Neurophysiol. 1967, 30:1239-1261.
67. Moushegian G., Rupert A.L., Gidda J.S. Functional characteristics of superior olivary neurons to binaural stimuli. J. Neurophysiol. 1975, 38:1037-1048.
68. Nabekura J., Katsurabayashi S., Kakazu Y., et al. Developmental switch from GABA to glycine release in single central synaptic terminals. Nat. Neurosci. 2004, 7:17-23.
69. Oertel D. Synaptic responses and electrical properties of cells in brain slices of the mouse anteroventral cochlear nucleus. J. Neurosci. 1983, 3:2043-2053.
70. Oertel D. Encoding of timing in the brain stem auditory nuclei of vertebrates. Neuron 1997, 19:959-962.
71. Overholt E.M., Rubel E.W., Hyson R.L. A circuit for coding interaural time differences in the chick brainstem. J. Neurosci. 1992, 12:1698-1708.
72. Palmer A.R. Reassessing mechanisms of low-frequency sound localisation. Curr. Opin. Neurobiol. 2004, 14:457-460.
73. Parameshwaran S., Carr C.E., Perney T.M. Expression of the Kv3.1 potassium channel in the avian auditory brainstem. J. Neurosci. 2001, 21:485-494.
74. Parameshwaran-Iyer S., Carr C.E., Perney T.M. Localization of KCNC1 (Kv3.1) potassium channel subunits in the avian auditory nucleus magnocellularis and nucleus laminaris during development. J. Neurobiol. 2003, 55:165-178.
75. Parks T.N., Rubel E.W. Organization and development of brain stem auditory nuclei of the chicken: organization of projections from n. magnocellularis to n. laminaris. J. Comp. Neurol. 1975, 164:435-448.
76. Pena J.L., Viete S., Albeck Y., Konishi M. Tolerance to sound intensity of binaural coincidence detection in the nucleus laminaris of the owl. J. Neurosci. 1996, 16:7046-7054.
77. Perney T.M., Kaczmarek L.K. Localization of a high threshold potassium channel in the rat cochlear nucleus. J. Comp. Neurol. 1997, 386:178-202.
78. Perney T.M., Marshall J., Martin K.A., Hockfield S., Kaczmarek L.K. Expression of the mRNAs for the Kv3.1 potassium channel gene in the adult and developing rat brain. J. Neurophysiol. 1992, 68:756-766.
79. Pollak G.D., Burger R.M., Klug A. Dissecting the circuitry of the auditory system. Trends Neurosci. 2003, 26:33-39.
80. Pollak G.D., Burger R.M., Park T.J., Klug A., Bauer E.E. Roles of inhibition for transforming binaural properties in the brainstem auditory system. Hear. Res. 2002, 168:60-78.
81. Rall W. Time constants and electrotonic length of membrane cylinders and neurons. Biophys. J. 1969, 9:1483-1508.
82. Rathouz M., Trussell L. Characterization of outward currents in neurons of the avian nucleus magnocellularis. J. Neurophysiol. 1998, 80:2824-2835.
83. Rayleigh L.S. On our perception of sound direction. Philos. Mag. 1907, 13:214-232.
84. Reyes A.D., Rubel E.W., Spain W.J. Membrane properties underlying the firing of neurons in the avian cochlear nucleus. J. Neurosci. 1994, 14:5352-5364.
85. Reyes A.D., Rubel E.W., Spain W.J. In vitro analysis of optimal stimuli for phase-locking and time-delayed modulation of firing in avian nucleus laminaris neurons. J. Neurosci. 1996, 16:993-1007.
86. Robert D., Miles R.N., Hoy R.R. Directional hearing by mechanical coupling in the parasitoid fly Ormia ochracea. J. Comp. Physiol. A 1996, 179:29-44.
87. Robertson B., Owen D., Stow J., Butler C., Newland C. Novel effects of dendrotoxin homologues on subtypes of mammalian Kv1 potassium channels expressed in Xenopus oocytes. FEBS Lett. 1996, 383:26-30.
88. Rothman J.S., Young E.D., Manis P.B. Convergence of auditory nerve fibers onto bushy cells in the ventral cochlear nucleus: implications of a computational model. J. Neurophysiol. 1993, 70:2562-2583.
89. Rubel E.W., Parks T.N. Organization and development of brain stem auditory nuclei of the chicken: tonotopic organization of n. magnocellularis and n. laminaris. J. Comp. Neurol. 1975, 164:411-433.
90. + channels designed for high-frequency repetitive firing. Trends Neurosci. 2001, 24:517-526.
91. Scott L.L., Mathews P.J., Golding N.L. Posthearing developmental refinement of temporal processing in principal neurons of the medial superior olive. J. Neurosci. 2005, 25:7887-7895.
92. Seidl A.H., Grothe B. Development of sound localization mechanisms in the Mongolian Gerbil is shaped by early acoustic experience. J. Neurophysiol. 2005, 94:1028-1036.
93. Smith A.J., Owens S., Forsythe I.D. Characterisation of inhibitory and excitatory postsynaptic currents of the rat medial superior olive. J. Physiol. 2000, 529(Pt 3):681-698.
94. Smith D.J., Rubel E.W. Organization and development of brain stem auditory nuclei of the chicken: dendritic gradients in nucleus laminaris. J. Comp. Neurol. 1979, 186:213-239.
95. Smith P.H. Structural and functional differences distinguish principal from nonprincipal cells in the guinea pig MSO slice. J. Neurophysiol. 1995, 73:1653-1667.
96. Smith P.H., Joris P.X., Yin T.C. Projections of physiologically characterized spherical bushy cell axons from the cochlear nucleus of the cat: evidence for delay lines to the medial superior olive. J. Comp. Neurol. 1993, 331:245-260.
97. Smith P.H., Joris P.X., Yin T.C. Anatomy and physiology of principal cells of the medial nucleus of the trapezoid body (MNTB) of the cat. J. Neurophysiol. 1998, 79:3127-3142.
98. Song P., Yang Y., Barnes-Davies M., et al. Acoustic environment determines phosphorylation state of the Kv3.1 potassium channel in auditory neurons. Nat. Neurosci. 2005, 8:1335-1342.
99. Spirou G.A., Rowland K.C., Berrebi A.S. Ultrastructure of neurons and large synaptic terminals in the lateral nucleus of the trapezoid body of the cat. J. Comp. Neurol. 1998, 398:257-272.
100. Spitzer M.W., Semple M.N. Neurons sensitive to interaural phase disparity in gerbil superior olive: diverse monaural and temporal response properties. J. Neurophysiol. 1995, 73:1668-1690.
101. Spitzer M.W., Semple M.N. Transformation of binaural response properties in the ascending auditory pathway: influence of time-varying interaural phase disparity. J. Neurophysiol. 1998, 80:3062-3076.
102. Stotler W.A. An experimental study of the cells and connections of the superior olivary complex of the cat. J. Comp. Neurol. 1953, 98:401-431.
103. Sullivan W.E., Konishi M. Neural map of interaural phase difference in the owl's brainstem. Proc. Natl. Acad. Sci. USA 1986, 83:8400-8404.
104. Svirskis G., Dodla R., Rinzel J. Subthreshold outward currents enhance temporal integration in auditory neurons. Biol. Cybern. 2003, 89:333-340.
105. Svirskis G., Kotak V., Sanes D.H., Rinzel J. Enhancement of signal-to-noise ratio and phase locking for small inputs by a low-threshold outward current in auditory neurons. J. Neurosci. 2002, 22:11019-11025.
106. Svirskis G., Kotak V., Sanes D.H., Rinzel J. Sodium along with low-threshold potassium currents enhance coincidence detection of subthreshold noisy signals in MSO neurons. J. Neurophysiol. 2004, 91:2465-2473.
107. Thompson A.M., Schofield B.R. Afferent projections of the superior olivary complex. Microsc. Res. Tech. 2000, 51:330-354.
108. Tollin D.J. The lateral superior olive: a functional role in sound source localization. Neuroscientist 2003, 9:127-143.
109. Trussell L.O. Cellular mechanisms for preservation of timing in central auditory pathways. Curr. Opin. Neurobiol. 1997, 7:487-492.
110. Trussell L.O. Synaptic mechanisms for coding timing in auditory neurons. Annu. Rev. Physiol. 1999, 61:477-496.
111. Viete S., Pena J.L., Konishi M. Effects of interaural intensity difference on the processing of interaural time difference in the owl's nucleus laminaris. J. Neurosci. 1997, 17:1815-1824.
112. von Bartheld C.S., Code R.A., Rubel E.W. GABAergic neurons in brainstem auditory nuclei of the chick: distribution, morphology, and connectivity. J. Comp. Neurol. 1989, 287:470-483.
113. Wang L.Y., Gan L., Forsythe I.D., Kaczmarek L.K. Contribution of the Kv3.1 potassium channel to high-frequency firing in mouse auditory neurones. J. Physiol. 1998, 509(Pt 1):183-194.
114. Westerberg B.D., Schwarz D.W. Connections of the superior olive in the chicken. J. Otolaryngol. 1995, 24:20-30.
115. Wightman F.L., Kistler D.J. Sound Localization. Human Psychophysics 1993, 155-192. Springer. W.A. Yost, A.N. Popper, R.R. Fay (Eds.).
116. Yang L., Monsivais P., Rubel E.W. The superior olivary nucleus and its influence on nucleus laminaris: a source of inhibitory feedback for coincidence detection in the avian auditory brainstem. J. Neurosci. 1999, 19:2313-2325.
117. Yin T.C., Kuwada S. Binaural interaction in low-frequency neurons in inferior colliculus of the cat. III. Effects of changing frequency. J. Neurophysiol. 1983, 50:1020-1042.
118. Yin T.C., Kuwada S. Binaural interaction in low-frequency neurons in inferior colliculus of the cat. II. Effects of changing rate and direction of interaural phase. J. Neurophysiol. 1983, 50:1000-1019.
119. Yin T.C., Chan J.C. Interaural time sensitivity in medial superior olive of cat. J. Neurophysiol. 1990, 64:465-488.
120. Young S.R., Rubel E.W. Frequency-specific projections of individual neurons in chick brainstem auditory nuclei. J. Neurosci. 1983, 3:1373-1378.
121. Zhang S., Trussell L.O. Voltage clamp analysis of excitatory synaptic transmission in the avian nucleus magnocellularis. J. Physiol. 1994, 480(Pt 1):123-136.