Accurate Sound Localization in Reverberant Environments Is Mediated by Robust Encoding of Spatial Cues in the Auditory Midbrain

Neuron

Volumn 62, Issue 1, 2009, Pages 123-134

  Devore, Sasha ^a,b   Ihlefeld, Antje ^c   Hancock, Kenneth ^a   Shinn Cunningham, Barbara ^b,c   Delgutte, Bertrand ^a,b,d  

^a MASSACHUSETTS EYE AND EAR INFIRMARY   (United States)

^b HARVARD MIT DIVISION OF HEALTH SCIENCES AND TECHNOLOGY   (United States)

^c BOSTON UNIVERSITY   (United States)

^d MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

Author keywords

SYSNEURO

Indexed keywords

ACOUSTIC NERVE FIBER; ANIMAL TISSUE; ARTICLE; AUDITORY STIMULATION; CAT; CONTROLLED STUDY; ENVIRONMENTAL FACTOR; HUMAN; MESENCEPHALON; NONHUMAN; PRIORITY JOURNAL; SENSITIVITY ANALYSIS; SOUND DETECTION;

ACOUSTIC STIMULATION; ACTION POTENTIALS; ANIMALS; AUDITORY THRESHOLD; CATS; CUES; HUMANS; MESENCEPHALON; MODELS, BIOLOGICAL; NEURONS; PSYCHOACOUSTICS; SOUND; SOUND LOCALIZATION; SPACE PERCEPTION; USER-COMPUTER INTERFACE;

EID: 64149118604     PISSN: 08966273     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.neuron.2009.02.018     Document Type: Article

References (86)

1. Adams J.C. Ascending projections to the inferior colliculus. J. Comp. Neurol. 183 (1979) 519-538
2. Aitkin L.M., Gates G.R., and Phillips S.C. Responses of neurons in the inferior colliculus to variations in sound-source azimuth. J. Neurophysiol. 52 (1984) 1-17
3. Albeck Y., and Konishi M. Responses of neurons in the auditory pathway of the barn owl to partially correlated binaural signals. J. Neurophysiol. 74 (1995) 1689-1700
4. Allen J.B., and Berkley D.A. Image method for efficiently simulating small-room acoustics. J. Acoust. Soc. Am. 65 (1979) 943-950
5. Beranek L. Concert Halls and Opera Houses. Second Edition (2004), Springer-Verlag, New York
6. Best V., Gallun F.J., Carlile S., and Shinn-Cunningham B.G. Binaural interference and auditory grouping. J. Acoust. Soc. Am. 121 (2007) 1070-1076
7. Boehnke S.E., Hall S.E., and Marquardt T. Detection of static and dynamic changes in interaural correlation. J. Acoust. Soc. Am. 112 (2002) 1617-1626
8. Brand A., Behrand O., Marquardt T., McAlpine D., and Grothe B. Precise inhibition is essential for microsecond interaural time difference coding. Nature 417 (2002) 543-547
9. Coffey C.S., Ebert J., Charles S., Marshall A.F., Skaggs J.D., Falk S.E., Crocker W.D., Pearson J.M., and Fitzpatrick D.C. Detection of interaural correlation by neurons in the superior olivary complex, inferior colliculus and auditory cortex of the unanesthetized rabbit. Hear. Res. 221 (2006) 1-16
10. Colburn H.S. Theory of binaural interaction based on auditory-nerve data. I. General strategy and preliminary results on interaural discrimination. J. Acoust. Soc. Am. 54 (1973) 1458-1470
11. D'Angelo W.R., Sterbing S.J., Ostapoff E.-M., and Kuwada S. Effects of amplitude modulation on the coding of interaural time differences of low-frequency sounds in the inferior colliculus. II. Neural mechanisms. J. Neurophysiol. 90 (2003) 2827-2836
12. Darwin C.J. Spatial hearing and perceiving sources. In: Yost W.A. (Ed). Springer Handbook of Auditory Research: Auditory Perception of Sound Sources (2008), Springer, New York
13. Delgutte B., Joris P.X., Litovsky R.Y., and Yin T.C.T. Receptive fields and binaural interactions for virtual-space stimuli in the cat inferior colliculus. J. Neurophysiol. 81 (1999) 2833-2851
14. Devore, S., and Delgutte, B. (2008). Does spike rate adaptation mediate robust encoding of ITD in reverberation? Paper presented at Society for Neuroscience (Washington, DC).
15. Fitzpatrick D.C., Batra R., Stanford T.R., and Kuwada S. A neuronal population code for sound localization. Nature 388 (1997) 871-874
16. Fitzpatrick D.C., Kuwada S., Kim D.O., Parham K., and Batra R. Responses of neurons to click-pairs as simulated echoes: Auditory nerve to auditory cortex. J. Acoust. Soc. Am. 106 (1999) 3460-3472
17. Fitzpatrick D.C., Kuwada S., and Batra R. Neural sensitivity to interaural time differences: beyond the Jeffress model. J. Neurosci. 20 (2000) 1605-1615
18. Geisler C.D., Rhode W.S., and Hazelton D.W. Responses of inferior colliculus neurons in the cat to binaural acoustic stimuli having wide-band spectra. J. Neurophysiol. 32 (1969) 960-974
19. Giguere C., and Abel S.M. Sound localization: effects of reverberation time, speaker array, stimulus frequency, and stimulus rise/decay. J. Acoust. Soc. Am. 94 (1993) 769-776
20. Goldberg J.M., and Brown P.B. Response of binaural neurons of dog superior olivary complex to dichotic tonal stimuli: some physiological mechanisms of sound localization. J. Neurophysiol. 32 (1969) 613-636
21. Grantham D.W., and Wightman F.L. Detectability of varying interaural temporal differences. J. Acoust. Soc. Am. 63 (1978) 511-523
22. Grothe B., and Sanes D.H. Synaptic inhibition influences the temporal coding properties of medial superior olivary neurons: an in vitro study. J. Neurosci. 14 (1994) 1701-1709
23. Hancock K.E. A physiologically-based population rate code for interaural time differences predicts bandwidth-dependent lateralization. In: Verhey J. (Ed). Hearing-from Sensory Processing to Perception (2007), Springer Verlag, Berlin 389-398
24. Hancock K.E., and Delgutte B. A physiologically based model of interaural time difference discrimination. J. Neurosci. 24 (2004) 7110-7117
25. Harper N.S., and McAlpine D. Optimal neural population coding of an auditory spatial cue. Nature 430 (2004) 682-686
26. Hartmann W.M. Localization of sound in rooms. J. Acoust. Soc. Am. 74 (1983) 1380-1391
27. Hartmann W.M., Rakerd B., and Koller A. Binaural coherence in rooms. Acta Acustica United with Acustica 91 (2005) 451-462
28. Houtgast T., and Steeneken H.J.M. The modulation transfer function in room acoustics as a predictor of speech intelligibility. Acustica 28 (1973) 66-73
29. Huisman W.H.T., and Attenborough K. Reverberation and attenuation in a pine forest. J. Acoust. Soc. Am. 90 (1991) 2664-2677
30. Ingham N.J., and McAlpine D. Spike-frequency adaptation in the inferior colliculus. J. Neurophysiol. 91 (2004) 632-645
31. Jeffress L.A. A place theory of sound localization. J. Comp. Physiol. Psychol. 41 (1948) 35-39
32. Joris P.X. Interaural time sensitivity dominated by cochlea-induced envelope patterns. J. Neurosci. 23 (2003) 6345-6350
33. Joris P., and Yin T.C. A matter of time: internal delays in binaural processing. Trends Neurosci. 30 (2007) 70-78
34. Kiang N.Y.S., and Moxon E.C. Tails of tuning curves of auditory-nerve fibers. J. Acoust. Soc. Am. 55 (1974) 620-630
35. Kidd Jr. G., Arbogast T.L., Mason C.R., and Gallun F.J. The advantage of knowing where to listen. J. Acoust. Soc. Am. 118 (2005) 3804-3815
36. Kollmeier B., and Gilkey R.H. Binaural forward and backward masking: evidence for sluggishness in binaural detection. J. Acoust. Soc. Am. 87 (1990) 1709-1719
37. Krishna B.S., and Semple M.N. Auditory temporal processing: responses to sinusoidally amplitude-modulated tones in the inferior colliculus. J. Neurophysiol. 84 (2000) 255-273
38. Kuwada S., and 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. 50 (1983) 981-999
39. Kuwada S., Stanford T.R., and Batra R. Interaural phase sensitive units in the inferior colliculus of the unanesthetized rabbit. Effects of changing frequency. J. Neurophysiol. 57 (1987) 1338-1360
40. Kuwada S., Batra R., and Stanford T.R. Monaural and binaural response properties of neurons in the inferior colliculus of the rabbit: effects of sodium pentobarbital. J. Neurophysiol. 61 (1989) 269-282
41. Lane C.C., and Delgutte B. Neural correlates and mechanisms of spatial release from masking: single-unit and population responses in the inferior colliculus. J. Neurophysiol. 94 (2005) 1180-1198
42. Litovsky R.Y., and Yin T.C.T. Physiological studies of the precedence effect in the inferior colliculus of the cat. I. Correlates of psychophysics. J. Neurophysiol. 80 (1998) 1285-1301
43. Litovsky R.Y., Colburn H.S., Yost W.A., and Guzman S.J. The precedence effect. J. Acoust. Soc. Am. 106 (1999) 1633-1654
44. Longworth-Reed L., Brandewie E., and Zahorik P. Time-forward speech intelligibility in time-reversed rooms. J. Acoust. Soc. Am. 125 (2009) EL13-EL19
45. Macpherson E.A., and Middlebrooks J.C. Listener weighting of cues for lateral angle: the duplex theory of sound localization revisited. J. Acoust. Soc. Am. 111 (2002) 2219-2236
46. McAlpine D., and Palmer A.R. Blocking GABAergic inhibition increases sensitivity to sound motion cues in the inferior colliculus. J. Neurosci. 22 (2002) 1443-1453
47. McAlpine D., Jiang D., Shackleton T.M., and Palmer A.R. Convergent input from brainstem coincidence detectors onto delay-sensitive neurons in the inferior colliculus. J. Neurosci. 18 (1998) 6026-6039
48. McAlpine D., Jiang D., and Palmer A.R. A neural code for low-frequency sound localization in mammals. Nat. Neurosci. 4 (2001) 396-401
49. Nelson P.G., and Erulkar S.D. Synaptic mechanisms of excitation and inhibition in the central auditory pathway. J. Neurophysiol. 26 (1963) 908-923
50. Nelson P.C., and Carney L.H. Neural rate and timing cues for detection and discrimination of amplitude-modulated tones in the awake rabbit inferior colliculus. J. Neurophysiol. 97 (2007) 522-539
51. Nuding S.C., Chen G.D., and Sinex D.G. Monaural response properties of single neurons in the chinchilla inferior colliculus. Hear. Res. 131 (1999) 89-106
52. Oliver D.L., Beckius G.E., and Shneiderman A. Axonal projections from the lateral and medial superior olive to the inferior colliculus of the cat: a study using electron microscopic autoradiography. J. Comp. Neurol. 360 (1995) 17-32
53. Pecka M., Zahn T.P., Saunier-Rebori B., Siveke I., Felmy F., Wiegrebe L., Klug A., Pollak G.D., and Grothe B. Inhibiting the inhibition: a neuronal network for sound localization in reverberant environments. J. Neurosci. 27 (2007) 1782-1790
54. Rakerd B., and Hartmann W.M. Localization of noise in a reverberant environment. In: Collet L. (Ed). Auditory Signal Processing: Physiology, Psychophysics, and Models (2005), Springer-Verlag, Berlin 348-354
55. Rees A., and Moller A.R. Responses of neurons in the inferior colliculus of the rat to AM and FM tones. Hear. Res. 10 (1983) 301-330
56. Rees A., Sarbaz A., Malmierca M.S., and Le Beau F.E. Regularity of firing of neurons in the inferior colliculus. J. Neurophysiol. 77 (1997) 2945-2965
57. Rose J.E., Gross N.B., Geisler C.D., and Hind J.E. Some neural mechanisms in the inferior colliculus of the cat which may be relevant to localization of a sound source. J. Neurophysiol. 29 (1966) 288-314
58. Sakai H., Sato S.-i., and Ando Y. Orthogonal acoustical factors of sound fields in a forest compared with those in a concert hall. J. Acoust. Soc. Am. 104 (1998) 1491-1497
59. Scott L.L., Mathews P.J., and Golding N.L. Posthearing developmental refinement of temporal processing in principal neurons of the medial superior olive. J. Neurosci. 25 (2005) 7887-7895
60. Shackleton T.M., Meddis R., and Hewitt M.J. Across frequency integration in a model of lateralization. J. Acoust. Soc. Am. 91 (1992) 2276-2279
61. Shackleton T.M., Arnott R.H., and Palmer A.R. Sensitivity to interaural correlation of single neurons in the inferior colliculus of guinea pigs. J. Assoc. Res. Otolaryngol. 6 (2005) 244-259
62. Shinn-Cunningham B.G. Object-based auditory and visual attention. Trends Cogn. Sci. 12 (2008) 182-186
63. Shinn-Cunningham, B.G., and Kawakyu, K. (2003). Neural representation of source direction in reverberant space. Paper presented at 2003 IEEE Workshop on Applications of Signal Processing to Audio and Acoustics (New Pfaltz, NY).
64. Shinn-Cunningham, B.G., Desloge, J.G., and Kopco, N. (2001). Empirical and modeled acoustic transfer functions in a simple room: Effects of distance and direction. Paper presented at 2001 IEEE Workshop on Applications of Signal Processing to Audio and Acoustics (New Pfaltz, NY).
65. Shinn-Cunningham B.G., Kopco N., and Martin T.J. Localizing nearby sound sources in a classroom: Binaural room impulse responses. J. Acoust. Soc. Am. 117 (2005) 3100-3115
66. Shinn-Cunningham, B.G., Lin, I.F., and Streeter, T. (2005b). Trading directional accuracy for realism. Paper presented at Human-Computer Interaction International/1st International Conference on Virtual Reality.
67. Singh N.C., and Theunissen F.E. Modulation spectra of natural sounds and ethological theories of auditory processing. J. Acoust. Soc. Am. 114 (2003) 3394-3411
68. Sivaramakrishnan S., and Oliver D.L. Distinct K currents result in physiologically distinct cell types in the inferior colliculus of the rat. J. Neurosci. 21 (2001) 2861-2877
69. Smith P.H. Structural and functional differences distinguish principal from nonprincipal cells in the guinea pig MSO slice. J. Neurophysiol. 73 (1995) 1653-1667
70. Smith R.L., and Zwislocki J.J. Short-term adaptation and incremental responses of single auditory-nerve fibers. Biol. Cybern. 17 (1975) 169-182
71. Spitzer M.W., Bala A.D.S., and Takahashi T.T. A neuronal correlate of the precedence effect is associated with spatial selectivity in the barn owl's auditory midbrain. J. Neurophysiol. 92 (2004) 2051-2070
72. Stecker G.C., Harrington I.A., and Middlebrooks J.C. Location coding by opponent neural populations in the auditory cortex. PLoS Biol. 3 (2005) e78 10.1371/journal.pbio.0030078
73. Stillman R.D. Characteristic delay neurons in the inferior colliculus of the kangaroo rat. Exp. Neurol. 32 (1971) 404-412
74. Stillman R.D. Pattern responses of low-frequency inferior colliculus neurons. Exp. Neurol. 33 (1971) 432-440
75. Svirskis G., Kotak V., Sanes D.H., and Rinzel J. Sodium along with low-threshold potassium currents enhance coincidence detection of subthreshold noisy signals in MSO neurons. J. Neurophysiol. 91 (2004) 2465-2473
76. Tan M.L., and Borst J.G.G. Comparison of responses of neurons in the mouse inferior colliculus to current injections, tones of different durations, and sinusoidal amplitude-modulated tones. J. Neurophysiol. 98 (2007) 454-466
77. Ter-Mikaelian M., Sanes D.H., and Semple M.N. Transformation of temporal properties between auditory midbrain and cortex in the awake mongolian gerbil. J. Neurosci. 27 (2007) 6091-6102
78. Tollin D.J., Populin L.C., and Yin T.C.T. Neural correlates of the precedence effect in the inferior colliculus of behaving cats. J. Neurophysiol. 92 (2004) 3286-3297
79. van Bergeijk W.A. Variation on a theme of Bekesy: a model of binaural interaction. J. Acoust. Soc. Am. 34 (1962) 1431-1437
80. Wallach H., Newman E.B., and Rosenzweig M.R. The precedence effect in sound localization. J. Am. Psychol. 57 (1949) 315-336
81. Wightman F.L., and Kistler D.J. The dominant role of low-frequency interaural time differences in sound localization. J. Acoust. Soc. Am. 91 (1992) 1648-1661
82. Wu S.H., Ma C.L., Sivaramakrishnan S., and Oliver D.L. Synaptic modification in neurons of the central nucleus of the inferior colliculus. Hear. Res. 168 (2002) 43-54
83. Yin T.C.T. Physiological correlates of the precedence effect and summing localization in the inferior colliculus of the cat. J. Neurosci. 14 (1994) 5170-5186
84. Yin T.C., and Chan J.C. Interaural time sensitivity in medial superior olive of cat. J. Neurophysiol. 64 (1990) 465-488
85. Yin T.C., Chan J.C., and Irvine D.R. Effects of interaural time delays of noise stimuli on low-frequency cells in the cat's inferior colliculus. I. Responses to wideband noise. J. Neurophysiol. 55 (1986) 280-300
86. Yin T.C., Chan J.C., and Carney L.H. Effects of interaural time delays of noise stimuli on low-frequency cells in the cat's inferior colliculus. III. Evidence for crosscorrelation. J. Neurophysiol. 58 (1987) 562-583