1932
0
  1. Home
  2. A-Z Publications
  3. Annual Review of Neuroscience
  4. Volume 42, 2019
  5. Article

Annual Review of Neuroscience

Volume 42, 2019

Early Binaural Hearing: The Comparison of Temporal Differences at the Two Ears

Abstract

Many mammals, including humans, are exquisitely sensitive to tiny time differences between sounds at the two ears. These interaural time differences are an important source of information for sound detection, for sound localization in space, and for environmental awareness. Two brainstem circuits are involved in the initial temporal comparisons between the ears, centered on the medial and lateral superior olive. Cells in these nuclei, as well as their afferents, display a large number of striking physiological and anatomical specializations to enable submillisecond sensitivity. As such, they provide an important model system to study temporal processing in the central nervous system. We review the progress that has been made in characterizing these primary binaural circuits as well as the variety of mechanisms that have been proposed to underlie their function.

Keyword(s): brainstem, coincidence detection, hearing, sound localization, stereo, temporal processing
Loading

Article metrics loading...

/content/journals/10.1146/annurev-neuro-080317-061925
2019-07-08
2024-04-26
Loading full text...

Full text loading...

/deliver/fulltext/neuro/42/1/annurev-neuro-080317-061925.html?itemId=/content/journals/10.1146/annurev-neuro-080317-061925&mimeType=html&fmt=ahah

Literature Cited

  1. Agmon-Snir H, Carr CE, Rinzel J 1998. The role of dendrites in auditory coincidence detection. Nature 393:268–72
     [Google Scholar]
  2. Banks MI, Smith PH. 1992. Intracellular recordings from neurobiotin-labeled cells in brain slices of the rat medial nucleus of the trapezoid body. J. Neurosci. 12:2819–37
     [Google Scholar]
  3. Batra R, Kuwada S, Fitzpatrick DC 1997. Sensitivity to interaural temporal disparities of low- and high-frequency neurons in the superior olivary complex. I. Heterogeneity of responses. J. Neurophysiol. 78:1222–36
     [Google Scholar]
  4. Beckius GE, Batra R, Oliver DL 1999. Axons from anteroventral cochlear nucleus that terminate in medial superior olive of cat: observations related to delay lines. J. Neurosci. 19:83146–61
     [Google Scholar]
  5. Benichoux V, Fontaine B, Franken TP, Karino S, Joris PX, Brette R 2015. Neural tuning matches frequency-dependent time differences between the ears. eLife 4:e06072
     [Google Scholar]
  6. Bernstein LR. 2001. Auditory processing of interaural timing information: new insights. J. Neurosci. Res. 66:61035–46
     [Google Scholar]
  7. Bernstein LR, Trahiotis C. 2018. Effects of interaural delay, center frequency, and no more than “slight” hearing loss on precision of binaural processing: empirical data and quantitative modeling. J. Acoust. Soc. Am. 144:1292
     [Google Scholar]
  8. Blodgett HC, Wilbanks WA, Jeffress LA 1956. Effect of large interaural time differences upon the judgment of sidedness. J. Acoust. Soc. Am. 28:4639–43
     [Google Scholar]
  9. Bonham BH, Lewis ER. 1999. Localization by interaural time difference (ITD): effects of interaural frequency mismatch. J. Acoust. Soc. Am. 106:281–90
     [Google Scholar]
  10. Boudreau JC, Tsuchitani C. 1968. Binaural interaction in the cat superior olive S segment. J. Neurophysiol. 31:442–54
     [Google Scholar]
  11. Brand A, Behrend O, Marquardt T, McAlpine D, Grothe B 2002. Precise inhibition is essential for microsecond interaural time difference coding. Nature 417:543–47
     [Google Scholar]
  12. Bremen P, Joris PX. 2013. Axonal recordings from medial superior olive neurons obtained from the lateral lemniscus of the chinchilla (Chinchilla laniger). J. Neurosci. 33:4417506–18
     [Google Scholar]
  13. Brette R. 2010. On the interpretation of sensitivity analyses of neural responses. J. Acoust. Soc. Am. 128:52965–72
     [Google Scholar]
  14. Brown C, May BJ. 2005. Comparative mammalian sound localization. Sound Source Localization A Popper, R Fay 124–78 New York: Springer
     [Google Scholar]
  15. Cant NB. 1984. The fine structure of the lateral superior olivary nucleus of the cat. J. Comp. Neurol. 227:63–77
     [Google Scholar]
  16. Cant NB, Casseday JH. 1986. Projections from the anteroventral cochlear nucleus to the lateral and medial superior olivary nuclei. J. Comp. Neurol. 247:4457–76
     [Google Scholar]
  17. Cant NB, Hyson RL. 1992. Projections from the lateral nucleus of the trapezoid body to the medial superior olivary nucleus in the gerbil. Hear. Res. 58:26–34
     [Google Scholar]
  18. Champoux F, Paiement P, Mercier C, Lepore F, Lassonde M, Gagné J-P 2007. Auditory processing in a patient with a unilateral lesion of the inferior colliculus. Eur. J. Neurosci. 25:1291–97
     [Google Scholar]
  19. Chung Y, Hancock KE, Delgutte B 2016. Neural coding of interaural time differences with bilateral cochlear implants in unanesthetized rabbits. J. Neurosci. 36:205520–31
     [Google Scholar]
  20. Clark GM. 1969. Vesicle shape versus type of synapse in the nerve endings of the cat medial superior olive. Brain Res 15:2548–51
     [Google Scholar]
  21. Coffey CS, Ebert CS Jr, Marshall AF, Skaggs JD, Falk SE et al. 2006. Detection of interaural correlation by neurons in the superior olivary complex, inferior colliculus and auditory cortex of the unanesthetized rabbit. Hear. Res. 221:1–21–16
     [Google Scholar]
  22. Colburn HS, Durlach NI. 1978. Models of binaural interaction. Hearing EC Carterette, MP Friedman 467–518 New York: Academic:
     [Google Scholar]
  23. Colburn HS, Han YA, Cullota CP 1990. Coincidence model of MSO responses. Hear. Res. 49:335–46
     [Google Scholar]
  24. Colburn HS, Isabelle SK. 2001. Physiologically based models of binaural detection. Physiological and Psychophysical Bases of Auditory Function DJ Breebaart 142–48 Maastricht, Neth: Shaker Publ. BV
     [Google Scholar]
  25. Cumming BG, DeAngelis GC. 2001. The physiology of stereopsis. Annu. Rev. Neurosci. 24:203–38
     [Google Scholar]
  26. Cumming BG, Parker AJ. 1997. Responses of primary visual cortical neurons to binocular disparity without depth perception. Nature 389:6648280–83
     [Google Scholar]
  27. Day ML, Koka K, Delgutte B 2012. Neural encoding of sound source location in the presence of a concurrent, spatially separated source. J. Neurophysiol. 108:92612–28
     [Google Scholar]
  28. Day ML, Semple MN. 2011. Frequency-dependent interaural delays in the medial superior olive: implications for interaural cochlear delays. J. Neurophysiol. 106:41985–99
     [Google Scholar]
  29. Devore S, Delgutte B. 2010. Effects of reverberation on the directional sensitivity of auditory neurons across the tonotopic axis: influences of interaural time and level differences. J. Neurosci. 30:237826–37
     [Google Scholar]
  30. Durlach NI. 1972. Binaural signal detection: equalization and cancellation theory. Foundations of Modern Auditory Theory, Vol. 2 JV Tobias 371–462 New York: Academic
     [Google Scholar]
  31. Durlach NI, Colburn HS. 1978. Binaural phenomena. Hearing EC Carterette, MP Friedman 365–465 New York: Academic
     [Google Scholar]
  32. Finlayson PG, Caspary DM. 1991. Low-frequency neurons in the lateral superior olive exhibit phase-sensitive binaural inhibition. J. Neurophysiol. 65:598–605
     [Google Scholar]
  33. Fitzpatrick DC, Batra R, Stanford TR, Kuwada S 1997. A neuronal population code for sound localization. Nature 388:871–74
     [Google Scholar]
  34. Ford MC, Alexandrova O, Cossell L, Stange-Marten A, Sinclair J et al. 2015. Tuning of Ranvier node and internode properties in myelinated axons to adjust action potential timing. Nat. Commun. 6:8073
     [Google Scholar]
  35. Franken TP, Bremen P, Joris PX 2014. Coincidence detection in the medial superior olive: mechanistic implications of an analysis of input spiking patterns. Front. Neural Circuits. 8:42
     [Google Scholar]
  36. Franken TP, Joris PX, Smith PH 2018. Principal cells of the brainstem's interaural sound level detector are temporal differentiators rather than integrators. eLife 7:e33854
     [Google Scholar]
  37. Franken TP, Roberts MT, Wei L, Golding NL, Joris PX 2015. In vivo coincidence detection in mammalian sound localization generates phase delays. Nat. Neurosci. 18:3444–52
     [Google Scholar]
  38. Franken TP, Smith PH, Joris PX 2016a. In vivo whole-cell recordings combined with electron microscopy reveal unexpected morphological and physiological properties in the lateral nucleus of the trapezoid body in the auditory brainstem. Front. Neural Circuits 10:69
     [Google Scholar]
  39. Franken TP, Smith PH, Joris PX 2016b. In vivo whole-cell recordings of the lateral and medial superior olive to interaural time differences of transients. Assoc. Res. Otolaryngol. Abs. 39:451
     [Google Scholar]
  40. Gabriel KG, Colburn HS. 1981. Interaural correlation discrimination: I. Bandwidth and level dependence. J. Acoust. Soc. Am. 69:1394–401
     [Google Scholar]
  41. Goldberg JM, Brown PB. 1969. Response of binaural neurons of dog superior olivary complex to dichotic tonal stimuli: some physiological mechanisms of sound localization. J. Neurophysiol. 22:613–36
     [Google Scholar]
  42. Golding NL, Oertel D. 2012. Synaptic integration in dendrites: exceptional need for speed. J. Physiol. 590:225563–69
     [Google Scholar]
  43. Gómez-Álvarez M, Saldaña E. 2016. Different tonotopic regions of the lateral superior olive receive a similar combination of afferent inputs. J. Comp. Neurol. 524:112230–50
     [Google Scholar]
  44. Goodman DFM, Benichoux V, Brette R 2013. Decoding neural responses to temporal cues for sound localization. eLife 2:e01312
     [Google Scholar]
  45. Guinan JJ, Norris BE, Guinan SS 1972. Single auditory units in the superior olivary complex. II: Locations of unit categories and tonotopic organization. Int. J. Neurosci. 4:147–66
     [Google Scholar]
  46. Hancock KE. 2007. A physiologically-based population rate code for interaural time differences (ITDs) predicts bandwidth-dependent lateralization. Hearing—From Sensory Processing to Perception B Kollmeier, G Klump, V Hohmann, U Langemann, M Mauermann et al.389–97 Berlin: Springer-Verlag
     [Google Scholar]
  47. Hancock KE, Delgutte B. 2004. A physiologically based model of interaural time difference discrimination. J. Neurosci. 24:7110–17
     [Google Scholar]
  48. Harper NS, McAlpine D. 2004. Optimal neural population coding of an auditory spatial cue. Nature 430:7000682–86
     [Google Scholar]
  49. Harrison JM, Irving R. 1966. Visual and nonvisual auditory systems in mammals. Anatomical evidence indicates two kinds of auditory pathways and suggests two kinds of hearing in mammals. Science 154:3750738–43
     [Google Scholar]
  50. Heffner RS, Heffner HE. 1992. Visual factors in sound localization in mammals. J. Comp. Neurol. 317:3219–32
     [Google Scholar]
  51. Helfert RH, Schwartz IR. 1986. Morphological evidence for the existence of multiple neuronal classes in the cat lateral superior olivary nucleus. J. Comp. Neurol. 244:533–49
     [Google Scholar]
  52. Henning GB. 1974. Detectability of interaural delay in high-frequency complex waveforms. J. Acoust. Soc. Am. 55:84–90
     [Google Scholar]
  53. Henning GB. 1980. Some observations on the lateralization of complex waveforms. J. Acoust. Soc. Am. 68:446–54
     [Google Scholar]
  54. Hirsh IJ. 1948. Binaural summation and interaural inhibition as a function of the level of masking noise. Am. J. Psychol. 61:2205–13
     [Google Scholar]
  55. Houtgast T, Steeneken HJM. 1985. A review of the MTF concept in room acoustics and its use for estimating speech intelligibility in auditoria. J. Acoust. Soc. Am. 77:31069–77
     [Google Scholar]
  56. Irvine DR, Park VN, McCormick L 2001. Mechanisms underlying the sensitivity of neurons in the lateral superior olive to interaural intensity differences. J. Neurophysiol. 86:62647–66
     [Google Scholar]
  57. Jeffress LA. 1948. A place theory of sound localization. J. Comp. Physiol. Psychol. 41:35–39
     [Google Scholar]
  58. Jenkins WM, Masterton RB. 1982. Sound localization: effects of unilateral lesions in central auditory system. J. Neurophysiol. 47:6987–1016
     [Google Scholar]
  59. Jercog PE, Svirskis G, Kotak VC, Sanes DH, Rinzel J 2010. Asymmetric excitatory synaptic dynamics underlie interaural time difference processing in the auditory system. PLOS Biol 8:6e1000406
     [Google Scholar]
  60. Johnson DH. 1980. The relationship between spike rate and synchrony in responses of auditory-nerve fibers to single tones. J. Acoust. Soc. Am. 68:1115–22
     [Google Scholar]
  61. Joris PX. 1996. Envelope coding in the lateral superior olive. II. Characteristic delays and comparison with responses in the medial superior olive. J. Neurophysiol. 76:42137–56
     [Google Scholar]
  62. Joris PX. 2003. Interaural time sensitivity dominated by cochlea-induced envelope patterns. J. Neurosci. 23:156345–50
     [Google Scholar]
  63. Joris PX. 2019. Neural binaural sensitivity at high sound speeds: single cell responses in cat midbrain to fast-changing interaural time differences of broadband sounds. J. Acoust. Soc. Am. 145:1EL45–EL51
     [Google Scholar]
  64. Joris PX, Carney LH, Smith PH, Yin TC 1994a. Enhancement of neural synchronization in the anteroventral cochlear nucleus. I. Responses to tones at the characteristic frequency. J. Neurophysiol. 71:31022–36
     [Google Scholar]
  65. Joris PX, Louage DH, Cardoen L, van der Heijden M 2006a. Correlation index: a new metric to quantify temporal coding. Hear. Res. 216–217:19–30
     [Google Scholar]
  66. Joris PX, Smith PH. 2008. The volley theory and the spherical cell puzzle. Neuroscience 154:165–76
     [Google Scholar]
  67. Joris PX, Smith PH, Yin TC 1994b. Enhancement of neural synchronization in the anteroventral cochlear nucleus. II. Responses in the tuning curve tail. J. Neurophysiol. 71:31037–51
     [Google Scholar]
  68. Joris PX, Smith PH, Yin TC 1998. Coincidence detection in the auditory system: 50 years after Jeffress. Neuron 21:61235–38
     [Google Scholar]
  69. Joris PX, Trussell LO. 2018. The calyx of Held: a hypothesis on the need for reliable timing in an intensity difference encoder. Neuron 100:534–49
     [Google Scholar]
  70. Joris PX, van de Sande B, Louage DH, van der Heijden M 2006b. Binaural and cochlear disparities. PNAS 103:3412917–22
     [Google Scholar]
  71. Joris PX, van de Sande B, Recio-Spinoso A, van der Heijden M 2006c. Auditory midbrain and nerve responses to sinusoidal variations in interaural correlation. J. Neurosci. 26:1279–89
     [Google Scholar]
  72. Joris PX, Yin TC. 1995. Envelope coding in the lateral superior olive. I. Sensitivity to interaural time differences. J. Neurophysiol. 73:31043–62
     [Google Scholar]
  73. Julesz B. 1971. Foundations of Cyclopean Perception Chicago: Univ. Chicago Press
  74. Kapfer C, Seidl AH, Schweizer H, Grothe B 2002. Experience-dependent refinement of inhibitory inputs to auditory coincidence-detector neurons. Nat. Neurosci. 5:3247–53
     [Google Scholar]
  75. Karino S, Smith PH, Yin TCT, Joris PX 2011. Axonal branching patterns as sources of delay in the mammalian auditory brainstem: a re-examination. J. Neurosci. 31:83016–31
     [Google Scholar]
  76. Klumpp RG, Eady HR. 1956. Some measurements of interaural time difference thresholds. J. Acoust. Soc. Am. 28:5859–60
     [Google Scholar]
  77. Kuwabara N, Zook JM. 1992. Projections to the medial superior olive from the medial and lateral nuclei of the trapezoid body in rodents and bats. J. Comp. Neurol. 324:4522–38
     [Google Scholar]
  78. Licklider JCR. 1948. The influence of interaural phase relations upon the masking of speech by white noise. J. Acoust. Soc. Am. 20:150–59
     [Google Scholar]
  79. Licklider JCR. 1951. A duplex theory of pitch perception. Experientia 7:4128–34
     [Google Scholar]
  80. Litovsky RY, Fligor BJ, Tramo MJ 2002. Functional role of the human inferior colliculus in binaural hearing. Hear. Res. 165:1–2177–88
     [Google Scholar]
  81. Louage DH, Joris PX, van der Heijden M 2006. Decorrelation sensitivity of auditory nerve and anteroventral cochlear nucleus fibers to broadband and narrowband noise. J. Neurosci. 26:196–108
     [Google Scholar]
  82. Masterton RB, Imig TJ. 1984. Neural mechanisms for sound localization. Annu. Rev. Physiol. 46:275–87
     [Google Scholar]
  83. Masterton RB, Thompson GC, Bechtold JK, RoBards MJ 1975. Neuroanatomical basis of binaural phase-difference analysis for sound localization: a comparative study. J. Comp. Physiol. Psychol. 89:5379–86
     [Google Scholar]
  84. Mc Laughlin M, Verschooten E, Joris PX 2010. Oscillatory dipoles as a source of phase shifts in field potentials in the mammalian auditory brainstem. J. Neurosci. 30:4013472–87
     [Google Scholar]
  85. McAlpine D, Jiang D, Palmer A 1996. Interaural delay sensitivity and the classification of low best-frequency binaural responses in the inferior colliculus of the guinea pig. Hear. Res. 97:136–52
     [Google Scholar]
  86. McAlpine D, Jiang D, Palmer A 2001. A neural code for low-frequency sound localization in mammals. Nat. Neurosci. 4:396–401
     [Google Scholar]
  87. McCulloch WS, Pitts W. 1943. A logical calculus of the ideas immanent in nervous activity. Bull. Math. Biophys. 5:4115–33
     [Google Scholar]
  88. McFadden D, Pasanen EG. 1976. Lateralization at high frequencies based on interaural time differences. J. Acoust. Soc. Am. 59:634–39
     [Google Scholar]
  89. Middlebrooks JC, Green DM. 1991. Sound localization by human listeners. Annu. Rev. Psychol. 42:135–59
     [Google Scholar]
  90. Mills AW. 1958. On the minimum audible angle. J. Acoust. Soc. Am. 30:4237–46
     [Google Scholar]
  91. Moore JK, Moore RY. 1971. A comparative study of the superior olivary complex in the primate brain. Folia Primatol 16:135–51
     [Google Scholar]
  92. Myoga MH, Lehnert S, Leibold C, Felmy F, Grothe B 2014. Glycinergic inhibition tunes coincidence detection in the auditory brainstem. Nat. Commun. 5:3790
     [Google Scholar]
  93. Nuetzel JM, Hafter ER. 1981. Discrimination of interaural delays in complex waveforms: spectral effects. J. Acoust. Soc. Am. 69:1112–18
     [Google Scholar]
  94. Pecka M, Brand A, Behrend O, Grothe B 2008. Interaural time difference processing in the mammalian medial superior olive: the role of glycinergic inhibition. J. Neurosci. 28:276914–25
     [Google Scholar]
  95. Plauška A, Borst JG, van der Heijden M 2016. Predicting binaural responses from monaural responses in the gerbil medial superior olive. J. Neurophysiol. 115:62950–63
     [Google Scholar]
  96. Plauška A, van der Heijden M, Borst JGG 2017. A test of the stereausis hypothesis for sound localization in mammals. J. Neurosci. 37:307278–89
     [Google Scholar]
  97. Ramón y Cajal S. 1909. Histologie du Système Nerveux de l'Homme & des Vertébrés Paris: Maloine
  98. Rautenberg PL, Grothe B, Felmy F 2009. Quantification of the three-dimensional morphology of coincidence detector neurons in the medial superior olive of gerbils during late postnatal development. J. Comp. Neurol. 517:3385–96
     [Google Scholar]
  99. Rayleigh L. 1907. XII. On our perception of sound direction. Philos. Mag. 13:214–32
     [Google Scholar]
  100. Roberts MT, Seeman SC, Golding NL 2014. The relative contributions of MNTB and LNTB neurons to inhibition in the medial superior olive assessed through single and paired recordings. Front. Neural Circuits 8:49
     [Google Scholar]
  101. Rose JE, Brugge JF, Anderson DJ, Hind JE 1967. Phase-locked response to low-frequency tones in single auditory nerve fibers of the squirrel monkey. J. Neurophysiol. 30:769–93
     [Google Scholar]
  102. Rose JE, Gross NB, Geisler CD, Hind JE 1966. 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
     [Google Scholar]
  103. Roth GL, Kochhar RK, Hind JE 1980. Interaural time differences: implications regarding the neurophysiology of sound localization. J. Acoust. Soc. Am. 68:1643–51
     [Google Scholar]
  104. Sayles M, Smith PH, Joris PX 2016. Inter-aural time sensitivity of superior-olivary-complex neurons is shaped by systematic cochlear disparities. Assoc. Res. Otolaryngol. Abs. 39:273
     [Google Scholar]
  105. Schroeder MR. 1977. New viewpoints in binaural interactions. Psychophysics and Physiology of Hearing EF Evans, JP Wilson 455–67 New York: Academic
     [Google Scholar]
  106. Scott BH, Malone BJ, Semple MN 2007. Effect of behavioral context on representation of a spatial cue in core auditory cortex of awake macaques. J. Neurosci. 27:246489–99
     [Google Scholar]
  107. Scott LL, Hage TA, Golding NL 2007. Weak action potential backpropagation is associated with high-frequency axonal firing capability in principal neurons of the gerbil medial superior olive. J. Physiol. 583:Pt. 2647–61
     [Google Scholar]
  108. Seidl AH, Rubel EW, Harris DM 2010. Mechanisms for adjusting interaural time differences to achieve binaural coincidence detection. J. Neurosci. 30:170–80
     [Google Scholar]
  109. Shackleton TM, Arnott RH, Palmer AR 2005. Sensitivity to interaural correlation of single neurons in the inferior colliculus of guinea pigs. J. Assoc. Res. Otolaryngol. 6:3244–59
     [Google Scholar]
  110. Shamma SA, Shen NM, Gopalaswamy P 1989. Stereausis: binaural processing without neural delays. J. Acoust. Soc. Am. 86:3989–1006
     [Google Scholar]
  111. Shneiderman A, Henkel CK. 1985. Evidence of collateral axonal projections to the superior olivary complex. Hear. Res. 19:199–205
     [Google Scholar]
  112. Smith PH. 1995. Structural and functional differences distinguish principal from nonprincipal cells in the guinea pig MSO slice. J. Neurophysiol. 73:1653–67
     [Google Scholar]
  113. Smith PH, Joris PX, Carney LH, Yin TC 1991. Projections of physiologically characterized globular bushy cell axons from the cochlear nucleus of the cat. J. Comp. Neurol. 304:3387–407
     [Google Scholar]
  114. Smith PH, Joris PX, Yin TC 1993. 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. 331:2245–60
     [Google Scholar]
  115. Smith PH, Joris PX, Yin TC 1998. Anatomy and physiology of principal cells of the medial nucleus of the trapezoid body (MNTB) of the cat. J. Neurophysiol. 79:63127–42
     [Google Scholar]
  116. Spangler KM, Warr WB, Henkel CK 1985. The projections of principal cells of the medial nucleus of the trapezoid body in the cat. J. Comp. Neurol. 238:249–62
     [Google Scholar]
  117. Spirou GA, Berrebi AS. 1996. Organization of ventrolateral periolivary cells of the cat superior olive as revealed by PEP-19 immunocytochemistry and Nissl stain. J. Comp. Neurol. 368:1100–20
     [Google Scholar]
  118. Spirou GA, Berrebi AS. 1997. Glycine immunoreactivity in the lateral nucleus of the trapezoid body of the cat. J. Comp. Neurol. 383:4473–88
     [Google Scholar]
  119. Spirou GA, Brownell WE, Zidanic M 1990. Recordings from cat trapezoid body and HRP labeling of globular bushy cell axons. J. Neurophysiol. 63:1169–90
     [Google Scholar]
  120. Stern RM, Zeiberg AS, Trahiotis C 1988. Lateralization of complex binaural stimuli: a weighted-image model. J. Acoust. Soc. Am. 84:156–65
     [Google Scholar]
  121. Stotler WA. 1953. An experimental study of the cells and connections of the superior olivary complex of the cat. J. Comp. Neurol. 98:401–32
     [Google Scholar]
  122. Tollin DJ. 2003. The lateral superior olive: a functional role in sound source localization. Neuroscientist 9:2127–43
     [Google Scholar]
  123. Tollin DJ, Yin TC. 2002. The coding of spatial location by single units in the lateral superior olive of the cat. II. The determinants of spatial receptive fields in azimuth. J. Neurosci. 22:41468–79
     [Google Scholar]
  124. Tollin DJ, Yin TC. 2005. Interaural phase and level difference sensitivity in low-frequency neurons in the lateral superior olive. J. Neurosci. 25:4610648–57
     [Google Scholar]
  125. Tolnai S, Beutelmann R, Klump GM 2018. Interaction of interaural cues and their contribution to the lateralisation of Mongolian gerbils (Meriones unguiculatus). J. Comp. Physiol. A 204:5435–48
     [Google Scholar]
  126. Tsuchitani C, Boudreau JC. 1966. Single unit analysis of cat superior olive S segment with tonal stimuli. J. Neurophysiol. 29:4684–97
     [Google Scholar]
  127. van de Par S, Trahiotis C, Bernstein LR 2001. A consideration of the normalization that is typically included in correlation-based models of binaural detection. J. Acoust. Soc. Am. 109:830–33
     [Google Scholar]
  128. van der Heijden M. 2018. A synaptic theory of internal delays. J. Acoust. Soc. Am. 144:2967–70
     [Google Scholar]
  129. van der Heijden M, Joris PX 2010. Interaural correlation fails to account for detection in a classic binaural task: dynamic ITDs dominate NoSπ detection. J. Assoc. Res. Otolaryngol. 11:1113–31
     [Google Scholar]
  130. van der Heijden M, Lorteije JAM, Plauška A, Roberts MT, Golding NL, Borst JGG 2013. Directional hearing by linear summation of binaural inputs at the medial superior olive. Neuron 78:5936–48
     [Google Scholar]
  131. van der Heijden M, Louage DH, Joris PX 2011. Responses of auditory nerve and anteroventral cochlear nucleus fibers to broadband and narrowband noise: implications for the sensitivity to interaural delays. J. Assoc. Res. Otolaryngol. 12:4485–502
     [Google Scholar]
  132. van der Heijden M, Trahiotis C 1999. Masking with interaurally delayed stimuli: the use of “internal” delays in binaural detection. J. Acoust. Soc. Am. 105:388–99
     [Google Scholar]
  133. Wakeford OS, Robinson DE. 1974. Lateralization of tonal stimuli by the cat. J. Acoust. Soc. Am. 55:3649–52
     [Google Scholar]
  134. Wallach H, Newman EB, Rosenzweig MR 1949. The precedence effect in sound localization. Am. J. Psychol. 62:3315–36
     [Google Scholar]
  135. Weiss TF, Rose C. 1988. A comparison of synchronization filters in different auditory receptor organs. Hear. Res. 33:175–80
     [Google Scholar]
  136. Yin TC, Chan JC, Carney LH 1987. Effects of interaural time delays of noise stimuli on low-frequency cells in the cat's inferior colliculus. III. Evidence for cross-correlation. J. Neurophysiol. 58:3562–83
     [Google Scholar]
  137. Yin TC, Chan JK. 1990. Interaural time sensitivity in medial superior olive of cat. J. Neurophysiol. 64:465–88
     [Google Scholar]
  138. Yin TC, Chan JK, Irvine DR 1986. 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. 55:280–300
     [Google Scholar]
  139. Yin TC, Kuwada S. 1983. Binaural interaction in low-frequency neurons in inferior colliculus of the cat. III. Effects of changing frequency. J. Neurophysiol. 50:1020–42
     [Google Scholar]
  140. Young ED, Oertel D. 2004. Cochlear nucleus. The Synaptic Organization of the Brain GM Shepherd 125–63 Oxford, UK: Oxford Univ. Press
     [Google Scholar]
  141. Zhou Y, Carney LH, Colburn HS 2005. A model for interaural time difference sensitivity in the medial superior olive: interaction of excitatory and inhibitory synaptic inputs, channel dynamics, and cellular morphology. J. Neurosci. 25:123046–58
     [Google Scholar]
/content/journals/10.1146/annurev-neuro-080317-061925
Loading
Early Binaural Hearing: The Comparison of Temporal Differences at the Two Ears
Annual Review of Neuroscience 42, 433 (2019); https://doi.org/10.1146/annurev-neuro-080317-061925
/content/journals/10.1146/annurev-neuro-080317-061925
/content/journals/10.1146/annurev-neuro-080317-061925
Loading

Data & Media loading...

  • Article Type: Review Article

Most Cited Most Cited RSS feed

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error