Inhibition in the balance: Binaurally coupled inhibitory feedback in sound localization circuitry

Journal of Neurophysiology

Volumn 106, Issue 1, 2011, Pages 4-14

  Michael Burger, R ^a   Fukui, Iwao ^b   Ohmori, Harunori ^b   Rubel, Edwin W ^c  

^a LEHIGH UNIVERSITY   (United States)

^b KYOTO UNIVERSITY   (Japan)

^c UNIVERSITY OF WASHINGTON SCHOOL OF MEDICINE   (United States)

Author keywords

aminobutyric acid; Coincidence detection; Efferent; Interaural time disparity; Phase locking

Indexed keywords

ASSOCIATION; AUDITORY SYSTEM; BINAURAL HEARING; BODY EQUILIBRIUM; BRAIN NERVE CELL; BRAIN STEM; COCHLEAR NUCLEUS; HUMAN; INTERAURAL TIME DISCRIMINATION; NEGATIVE FEEDBACK; NEUROFEEDBACK; NEUROMODULATION; NONHUMAN; PRIORITY JOURNAL; REVIEW; SOUND DETECTION; SYNAPSE; TASK PERFORMANCE; TIME;

ANIMALS; AUDITORY PATHWAYS; BIRDS; BRAIN STEM; FEEDBACK, PHYSIOLOGICAL; HUMANS; NEURONS; SOUND LOCALIZATION;

EID: 79959922088     PISSN: 00223077     EISSN: 15221598     Source Type: Journal    
DOI: 10.1152/jn.00205.2011     Document Type: Review

References (88)

1. Adams JC. Cytology of periolivary cells and the organization of their projections in the cat. J Comp Neurol 215: 275-289, 1983.
2. Agmon-Snir H, Carr CE, Rinzel J. The role of dendrites in auditory coincidence detection. Nature 393: 268-272, 1998.
3. Blauert J. Spatial Hearing: the Psychophysics of Human Sound Localization. Cambridge, MA: MIT Press, 1983.
4. Brand A, Behrend O, Marquardt T, McAlpine D, Grothe B. Precise inhibition is essential for microsecond interaural time difference coding. Nature 417: 543-547, 2002.
5. Brenowitz S, Trussell LO. Maturation of synaptic transmission at end-bulb synapses of the cochlear nucleus. J Neurosci 21: 9487-9498, 2001.
6. Burger RM, Rubel EW. Encoding of interaural timing for sound localization. In: The Senses: a Comprehensive Reference, edited by Dallos P, Oertel D. Oxford: Academic, 2008, chapt. 3.35, p. 613.
7. Burger RM, Cramer KS, Pfeiffer JD, Rubel EW. Avian superior olivary nucleus provides divergent inhibitory input to parallel auditory pathways. J Comp Neurol 481: 6-18, 2005a.
8. Burger RM, Pfeiffer JD, Westrum LE, Bernard A, Rubel EW. Expression of GABAB receptor in the avian auditory brainstem: ontogeny, afferent deprivation, and ultrastructure. J Comp Neurol 489: 11-22, 2005b.
9. Calford MB, Piddington RW. Avian interaural canal enhances interaural delay. J Comp Physiol A 162: 503-510, 1988.
10. Carr CE, Fujita I, Konishi M. Distribution of GABAergic neurons and terminals in the auditory system of the barn owl. J Comp Neurol 286: 190-207, 1989.
11. Carr CE, Konishi M. A circuit for detection of interaural time differences in the brain stem of the barn owl. J Neurosci 10: 3227-3246, 1990.
12. Carr CE, Konishi M. Axonal delay lines for time measurement in the owl's brainstem. Proc Natl Acad Sci USA 85: 8311-8315, 1988.
13. Caspary DM, Backoff PM, Finlayson PG, Palombi PS. Inhibitory inputs modulate discharge rate within frequency receptive fields of anteroventral cochlear nucleus neurons. J Neurophysiol 72: 2124-2133, 1994.
14. Code RA, Burd GD, Rubel EW. Development of GABA immunoreactivity in brainstem auditory nuclei of the chick: ontogeny of gradients in terminal staining. J Comp Neurol 284: 504-518, 1989.
15. Code RA, Rubel EW. Glycine-immunoreactivity in the auditory brain stem of the chick. Hear Res 40: 167-172, 1989.
16. Colburn HS, Durlach NI. Models of binaural interaction. In: Handbook of Perception, edited by Carterette EC, Friedman M. New York: Academic, 1978, p. 467-518.
17. Coleman WL, Fischl MA, Weimann SR, Burger RM. GABAergic and glycinergic inhibition modulate monaural auditory response properties in the avian superior olivary nucleus. J Neurophysiol; doi: 10.1152/jn.01088.2010.
18. Conlee JW, Parks TN. Origin of ascending auditory projections to the nucleus mesencephalicus lateralis pars dorsalis in the chicken. Brain Res 367: 96-113, 1986.
19. Cook DL, Schwindt PC, Grande LA, Spain WJ. Synaptic depression in the localization of sound. Nature 421: 66-70, 2003.
20. Darrow KN, Maison SF, Liberman MC. Cochlear efferent feedback balances interaural sensitivity. Nat Neurosci 9: 1474-1476, 2006.
21. Dasika VK, White JA, Carney LH, Colburn HS. Effects of inhibitory feedback in a network model of avian brain stem. J Neurophysiol 94: 400-414, 2005.
22. Fukui I, Burger RM, Ohmori H, Rubel EW. GABAergic inhibition sharpens the frequency tuning and enhances phase locking in chicken nucleus magnocellularis neurons. J Neurosci 30: 12075-12083, 2010.
23. Fukui I, Ohmori H. Tonotopic gradients of membrane and synaptic properties for neurons of the chicken nucleus magnocellularis. J Neurosci 24: 7514-7523, 2004.
24. Fukui I, Ohmori H. Developmental changes in membrane excitability and morphology of neurons in the nucleus angularis of the chicken. J Physiol 548: 219-232, 2003.
25. Fukui I, Sato T, Ohmori H. Improvement of phase information at low sound frequency in nucleus magnocellularis of the chicken. J Neurophysiol 96: 633-641, 2006.
26. 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 508: 851-869, 1998.
27. Goldberg JM, Brown PB. Response of binaural neurons of dog superior olivary complex to dichotic tonal stimuli: some physiological mechanisms of sound localization. J Neurophysiol 32: 613-636, 1969.
28. Grothe B. New roles for synaptic inhibition in sound localization. Nat Rev Neurosci 4: 540-550, 2003.
29. Grothe B, Pecka M, McAlpine D. Mechanisms of sound localization in mammals. Physiol Rev 90: 983-1012, 2010.
30. Hackett JT, Jackson H, Rubel EW. Synaptic excitation of the second and third order auditory neurons in the avian brain stem. Neuroscience 7: 1455-1469, 1982.
31. Howard MA, Burger RM, Rubel EW. A developmental switch to GABAergic inhibition dependent on increases in Kv1-type K_ currents. J Neurosci 27: 2112-2123, 2007.
32. Howard MA, Rubel EW. Dynamic spike thresholds during synaptic integration preserve and enhance temporal response properties in the avian cochlear nucleus. J Neurosci 30: 12063-12074, 2010.
33. Hyson RL, Overholt EM, Lippe WR. Cochlear microphonic measurements of interaural time differences in the chick. Hear Res 81: 109-118, 1994.
34. Hyson RL, Reyes AD, Rubel EW. A depolarizing inhibitory response to GABA in brainstem auditory neurons of the chick. Brain Res 677: 117-126, 1995.
35. Jackson H, Hackett JT, Rubel EW. Organization and development of brain stem auditory nuclei in the chick: ontogeny of postsynaptic responses. J Comp Neurol 210: 80-86, 1982.
36. Jeffress LA. A place theory of sound localization. J Comp Physiol Psychol 41: 35-39, 1948.
37. Jhaveri S, Morest DK. Neuronal architecture in nucleus magnocellularis of the chicken auditory system with observations on nucleus laminaris: a light and electron microscope study. Neuroscience 7: 809-836, 1982.
38. Joris P, Yin TCT. A matter of time: internal delays in binaural processing. Trends Neurosci 30: 70-78, 2007.
39. Joseph AW, Hyson RL. Coincidence detection by binaural neurons in the chick brain stem. J Neurophysiol 69: 1197-1211, 1993.
40. Konishi M. Coding of auditory space. Annu Rev Neurosci 26: 31-55, 2003.
41. Köppl C. Phase locking to high frequencies in the auditory nerve and cochlear nucleus magnocellularis of the barn owl, Tyto alba. J Neurosci 17: 3312-3321, 1997.
42. Köppl C, Carr CE. Maps of interaural time difference in the chicken's brainstem nucleus laminaris. Biol Cybern 98: 541-559, 2008.
43. Köppl C, Carr CE. Computational diversity in the cochlear nucleus angularis of the barn owl. J Neurophysiol 89: 2313-2329, 2003.
44. Kuba H, Koyano K, Ohmori H. Synaptic depression improves coincidence detection in the nucleus laminaris in brainstem slices of the chick embryo. Eur J Neurosci 15: 984-990, 2002.
45. Kuba H, Yamada R, Ohmori H. Evaluation of the limiting acuity of coincidence detection in nucleus laminaris of the chicken. J Physiol 552: 611-620, 2003.
46. Kuba H, Ohmori H. Roles of axonal sodium channels in precise auditory time coding at nucleus magnocellularis of the chick. J Physiol 587: 87-100, 2009.
47. Kuba H, Yamada R, Fukui I, Ohmori H. Tonotopic specialization of auditory coincidence detection in nucleus laminaris of the chick. J Neurosci 25: 1924-1934, 2005.
48. Kuo SP, Bradley LA, Trussell LO. Heterogeneous kinetics and pharmacology of synaptic inhibition in the chick auditory brainstem. J Neurosci 29: 9625-9634, 2009.
49. Lachica EA, Rubsamen R, Rubel EW. GABAergic terminals in nucleus magnocellularis and laminaris originate from the superior olivary nucleus. J Comp Neurol 348: 403-418, 1994.
50. Lu T, Trussell LO. Mixed excitatory and inhibitory GABA-mediated transmission in chick cochlear nucleus. J Physiol 535: 125-131, 2001.
51. Lu T, Trussell LO. Inhibitory transmission mediated by asynchronous transmitter release. Neuron 26: 683-694, 2000.
52. Lu Y, Burger RM, Rubel EW. GABAB receptor activation modulates GABAA receptor-mediated inhibition in chicken nucleus magnocellularis neurons. J Neurophysiol 93: 1429-1438, 2005.
53. McAlpine Grothe D, B. Sound localization and delay lines-do mammals fit the model? Trends Neurosci 26: 347-350, 2003.
54. Monsivais P, Rubel EW. Accommodation enhances depolarizing inhibition in central neurons. J Neurosci 21: 7823-7830, 2001.
55. Monsivais P, Yang L, Rubel EW. GABAergic inhibition in nucleus magnocellularis: implications for phase locking in the avian auditory brainstem. J Neurosci 20: 2954-2963, 2000.
56. Nishino E, Yamada R, Kuba H, Hioki H, Furuta T, Kaneko T, Ohmori H. Sound-intensity-dependent compensation for the small interaural time difference cue for sound source localization. J Neurosci 28: 7153-7164, 2008.
57. Oertel D. Encoding of timing in the brain stem auditory nuclei of vertebrates. Neuron 19: 959-962, 1997.
58. Ostapoff EM, Benson CG, Saint Marie RL. GABA- and glycine-immunoreactive projections from the superior olivary complex to the cochlear nucleus in guinea pig. J Comp Neurol 381: 500-512, 1997.
59. Overholt EM, Rubel EW, Hyson RL. A circuit for coding interaural time differences in the chick brainstem. J Neurosci 12: 1698-1708, 1992.
60. Parks TN, Rubel EW. Organization and development of the brain stem auditory nuclei of the chicken: primary afferent projections. J Comp Neurol 180: 439-448, 1978.
61. Parks TN, Rubel EW. Organization and development of brain stem auditory nuclei of the chicken: organization of projections from n. magnocellularis to n. laminaris. J Comp Neurol 164: 435-448, 1975.
62. Pecka M, Brand A, Behrend O, Grothe B. Interaural time difference processing in the mammalian medial superior olive: the role of glycinergic inhibition. J Neurosci 28: 6914-6925, 2008.
63. Pena JL, Viete S, Albeck Y, Konishi M. Tolerance to sound intensity of binaural coincidence detection in the nucleus laminaris of the owl. J Neurosci 16: 7046-7054, 1996.
64. Rayleigh L (Strutt JW). On our perception of sound direction. Philos Mag 13: 214-232, 1907.
65. Reyes AD, Rubel EW, Spain WJ. In vitro analysis of optimal stimuli for phase-locking and time-delayed modulation of firing in avian nucleus laminaris neurons. J Neurosci 16: 993-1007, 1996.
66. Reyes AD, Rubel EW, Spain WJ. Membrane properties underlying the firing of neurons in the avian cochlear nucleus. J Neurosci 14: 5352-5364, 1994.
67. Rose JE, Gross NB, Geisler CD, Hind JE. Some neural mechanisms in the inferior colliculus of the cat which may be relevant to localization of a sound source. J Neurophysiol 29: 288-314, 1966.
68. Rosowski JJ, Saunders JC. Sound-transmission through the avian inter-aural pathways. J Comp Physiol 136: 183, 1980.
69. Rubel EW, Parks TN. Organization and development of brain stem auditory nuclei of the chicken: tonotopic organization of n. magnocellularis and n. laminaris. J Comp Neurol 164: 411-433, 1975.
70. Sachs MB, Sinnott JM. Responses to tones of single cells in nucleus magnocellularis and nucleus angularis of the redwing blackbird (Agelaius phoeniceus). J Comp Physiol A 126: 347, 1978.
71. Schnupp JWH, Carr CE. On hearing with more than one ear: lessons from evolution. Nat Neurosci 12: 692-697, 2009.
72. Schofield BR. Projections to the cochlear nuclei from principal cells in the medial nucleus of the trapezoid body in guinea pigs. J Comp Neurol 344: 83-100, 1994.
73. Seidl AH, Rubel EW, Harris DM. Mechanisms for adjusting interaural time differences to achieve binaural coincidence detection. J Neurosci 30: 70-80, 2010.
74. Soares D, Chitwood RA, Hyson RL, Carr CE. Intrinsic neuronal properties of the chick nucleus angularis. J Neurophysiol 88: 152-162, 2002.
75. Spangler KM, Cant NB, Henkel CK, Farley GR, Warr WB. Descending projections from the superior olivary complex to the cochlear nucleus of the cat. J Comp Neurol 259: 452-65, 1987.
76. Stillman RD. Characteristic delay neurons in the inferior colliculus of the kangaroo rat. Exp Neurol 32: 402-412, 1971.
77. Sullivan WE, Konishi M. Neural map of interaural phase difference in the owl's brainstem. Proc Natl Acad Sci USA 83: 8400-8404, 1986.
78. Thompson AM, Schofield BR. Afferent projections of the superior olivary complex. Microsc Res Tech 51: 330-354, 2000.
79. Trussell LO. Cellular mechanisms for preservation of timing in central auditory pathways. Curr Opin Neurobiol 7: 487-492, 1997.
80. von Bartheld CS, Code RA, Rubel EW. GABAergic neurons in brainstem auditory nuclei of the chick: distribution, morphology, and connectivity. J Comp Neurol 287: 470-483, 1989.
81. Wagner H, Brill S, Kempter R, Carr CE. Microsecond precision of phase delay in the auditory system of the barn owl. J Neurophysiol 94: 1655-1658, 2005.
82. Warchol ME, Dallos P. Neural coding in the chick cochlear nucleus. J Comp Physiol A 166: 721-734, 1990.
83. Warr WB, Beck JE. Multiple projections from the ventral nucleus of the trapezoid body in the rat. Hear Res 93: 83-101, 1996.
84. Yang L, Monsivais P, Rubel EW. 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 19: 2313-2325, 1999.
85. Yin TC, Chan JC. Interaural time sensitivity in the medial superior olive of cat. J Neurophysiol 64: 465-488, 1990.
86. Yin TC, Kuwada S. Binaural interaction in low-frequency neurons in the inferior colliculus of the cat. III. Effects of changing frequency. J Neurophysiol 50: 1020-1042, 1983.
87. Young SR, Rubel EW. Frequency-specific projections of individual neurons in chick brainstem auditory nuclei. J Neurosci 3: 1373-1378, 1983.
88. Zhang S, Trussell LO. A characterization of excitatory postsynaptic potentials in the avian nucleus magnocellularis. J Neurophysiol 72: 705-718, 1994.