Models of the Superior Olivary Complex

  • T. R. Jennings
  • H. S. Colburn
Part of the Springer Handbook of Auditory Research book series (SHAR, volume 35)


Sounds in the real world originate from specific sources, either alone or in combination, so that a natural description of a sound includes its location and other spatial properties. The extraction of these spatial properties by the mammalian auditory system involves early extraction of interaural difference information in the superior olivary complex (SOC), and the modeling of this processing by the neurons in the SOC is the topic of this chapter. This chapter’s focus on the SOC and on interaural difference information means that the monaural localization cues, notably the direction-dependent spectral filtering of the source waveform, are not addressed here, even though these cues also carry information about source location, especially its elevation. The spectral cues for location are discussed in  Chapter 5, describing models of the inferior colliculus (IC) in relation to psychophysical abilities.


Interaural Time Difference Interaural Level Difference Lateral Superior Olive Superior Olivary Complex Medial Superior Olive 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Abbreviations and Acronyms




Anteroventral cochlear nucleus


Best delay


Best phase


Characteristic delay


Cochlear nucleus


Characteristic phase








Excitatory postsynaptic potential


Inferior colliculus




Interaural level difference


Interaural phase difference


Interspike interval


Interaural time difference


Just noticeable difference


Leaky integrate-and-fire


Lateral nucleus of the trapezoid body


Lateral superior olive


Medial nucleus of the trapezoid body


Medial superior olive


Nucleus angularis


Nucleus laminaris


Nucleus magnocellularis


Poststimulus time histogram


Superior olivary complex


Superior olivary nucleus


Ventral nucleus of the lateral lemniscus pars posterior


  1. Adams JC, Mugnaini E (1990) Immunocytochemical evidence for inhibitory and disinhibitory circuits in the superior olive. Hear Res 49:281–298.PubMedCrossRefGoogle Scholar
  2. Armin HS, Edwin WR, David MH Mechanisms for adjusting interaural time differences to achieve binaural coincidence detection (in press).Google Scholar
  3. Ashida G, Abe K, Funabiki K, Konishi M (2007) Passive soma facilitates submillisecond coincidence detection in the owl’s auditory system. J Neurophysiol 97:2267–2282.PubMedCrossRefGoogle Scholar
  4. Barnes-Davies M, Barker MC, Osmani Forsythe ID (2004) Kv1 currents mediate a gradient of principal neuron excitability across the tonotopic axis in the rat lateral superior olive. Eur J Neurosci 19:325–333.PubMedCrossRefGoogle Scholar
  5. Blum JJ, Reed MC (1991) Further studies of a model for azimuthal encoding: lateral superior olive neuron response curves and developmental processes. J Acoust Soc Am 90:1968–1978.PubMedCrossRefGoogle Scholar
  6. Boudreau JC, Tsuchitani C (1968) Binaural interaction in the cat superior olive s segment. J Neurophysiol 31:442–454.PubMedGoogle Scholar
  7. Brand A, Behrend O, Marquardt T, McAlpine D, Grothe B (2002) Precise inhibition is essential for microsecond interaural time difference coding. Nature 417:543–547.PubMedCrossRefGoogle Scholar
  8. Breebaart J, van de Par S, Kohlrausch A (2001a) Binaural processing model based on contralateral inhibition. I. Model structure. J Acoust Soc Am 110:1074–1088.PubMedCrossRefGoogle Scholar
  9. Breebaart J, van de Par S, Kohlrausch A (2001b) Binaural processing model based on contralateral inhibition. II. Dependence on spectral parameters. J Acoust Soc Am 110:1089–1104.PubMedCrossRefGoogle Scholar
  10. Breebaart J, van de Par S, Kohlrausch A (2001c) Binaural processing model based on contralateral inhibition. III. Dependence on temporal parameters. J Acoust Soc Am 110:1105–1117.PubMedCrossRefGoogle Scholar
  11. Brew H (1998) Modeling of interaural time difference detection by neurons of mammalian superior olivary nucleus. Assoc Res Otolaryngol 25:680.Google Scholar
  12. Brughera AR, Stutman ER, Carney LH, Colburn HS (1996) A model with excitation and ­inhibition for cells in the medial superior olive. Audit Neurosci 2:219–233.Google Scholar
  13. 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.PubMedCrossRefGoogle Scholar
  14. Carr CE, Konishi M (1988) Axonal delay lines for time measurement in the owl’s brainstem. Proc Natl Acad Sci U S A 85:8311–8315.PubMedCrossRefGoogle Scholar
  15. Carr CE, Konishi M (1990) A circuit for detection of interaural time differences in the brain stem of the barn owl. J Neurosci 10:3227–3246.PubMedGoogle Scholar
  16. Chirila FV, Rowland KC, Thompson JM, Spirou GA (2007) Development of gerbil medial ­superior olive: integration of temporally delayed excitation and inhibition at physiological ­temperature. J Physiol 584:167–190.PubMedCrossRefGoogle Scholar
  17. Clack JA (1997) The evolution of tetrapod ears and the fossil record. Brain Behav Evol 50:198–212.PubMedCrossRefGoogle Scholar
  18. Colburn HS (1973) Theory of binaural interaction based on auditory-nerve data. I. General strategy and preliminary results on interaural discrimination. J Acoust Soc Am 6:1458–1470.CrossRefGoogle Scholar
  19. Colburn HS (1977) Theory of binaural interaction based on auditory-nerve data. II. Detection of tones in noise. J Acoust Soc Am 54:525–533.CrossRefGoogle Scholar
  20. Colburn HS (1996) Computational models of binaural processing. In: Hawkins HL, McMullen TA, Popper AN, Fay RR (eds), Auditory Computation. New York: Springer, pp. 332–400.CrossRefGoogle Scholar
  21. Colburn HS, Durlach NI (1978) Models of binaural interaction. In: Carterette EC, Freidman M (eds), Handbook of Perception, Vol. IV. New York: Academic, pp. 467–518.Google Scholar
  22. Colburn HS, Latimer JS (1978) Theory of binaural interaction based on auditory-nerve data. III. Joint dependence on interaural time and amplitude differences in discrimination and detections. J Acoust Soc Am 64:95–106.PubMedCrossRefGoogle Scholar
  23. Colburn HS, Moss PJ (1981) Binaural interaction models and mechanisms. In: Syka J, Aitkin L (eds), Neuronal Mechanisms of Hearing. New York: Plenum, pp. 283–288.CrossRefGoogle Scholar
  24. Colburn HS, Han YA, Culotta CP (1990) Coincidence model of MSO responses. Hear Res 49:335–346.PubMedCrossRefGoogle Scholar
  25. Dasika VK, White JA, Carney LH, Colburn HS (2005) Effects of inhibitory feedback in a network model of avian brain stem. J Neurophysiol 94:400–414.PubMedCrossRefGoogle Scholar
  26. Dasika VK, White JA, Colburn HS (2007) Simple models show the general advantages of ­dendrites in coincidence detection. J Neurophysiol 97:3449.PubMedCrossRefGoogle Scholar
  27. Dayan P, Abbott LF (2001) Theoretical Neuroscience. Cambridge, MA: MIT Press, pp. 162–166.Google Scholar
  28. Diranieh YM (1992) Computer-based neural models of single lateral superior olivary neurons. M.S. Thesis, Boston University, Boston, MA.Google Scholar
  29. Donoghue PC, Benton MJ (2007) Rocks and clocks: calibrating the tree of life using fossils and molecules. Trends Ecol Evol 22:424–431.PubMedCrossRefGoogle Scholar
  30. Durlach NI (1963) Equalization and cancellation theory of binaural masking-level differences. J Acoust Soc Am 35:1206–1218.CrossRefGoogle Scholar
  31. Durlach NI (1972) Binaural signal detection: equalization and cancellation theory. In: Tobias J (ed), Foundations of Modern Auditory Theory. New York: Academic, pp. 371–462.Google Scholar
  32. Galambos R, Davis H (1943) The response of single auditory-nerve fibers to acoustic stimulation. J Neurophysiol 6:39–57.Google Scholar
  33. Glendenning KK, Hutson KA, Nudo RJ, Masterton RB (1985) Acoustic chiasm II: Anatomical basis of binaurality in lateral superior olive of cat. J Comp Neurol 232:261–285.PubMedCrossRefGoogle Scholar
  34. 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 32:613–636.PubMedGoogle Scholar
  35. Grau-Serrat V, Carr CE, Simon JZ (2003) Modeling coincidence detection in nucleus laminaris. Biol Cybern 89:388–396.PubMedCrossRefGoogle Scholar
  36. Grothe B, Sanes DH (1993) Bilateral inhibition by glycinergic afferents in the medial superior olive. J Neurophysiol 69:1192–1196.PubMedGoogle Scholar
  37. Guinan JJ, Guinan SS, Norriss BE (1972a) Single auditory units in the superior olivary complex I: responses to sounds and classifications based on physiological properties. Int J Neurosci 4:101–120.CrossRefGoogle Scholar
  38. Guinan JJ, Norriss BE, Guinan SS (1972b) Single auditory units in the superior olivary complex II: locations of unit categories and tonotopic organization. Int J Neurosci 4:147–166.CrossRefGoogle Scholar
  39. Hall JL (1965) Binaural interaction in the accessory superior-olivary nucleus of the cat. J Acoust Soc Am 37:814–823.PubMedCrossRefGoogle Scholar
  40. Han Y, Colburn HS (1993) Point-neuron model for binaural interaction in MSO. Hear Res 68:115–130.PubMedCrossRefGoogle Scholar
  41. Harper NS, McAlpine D (2004) Optimal neural population coding of an auditory spatial cue. Nature 430:682–686.PubMedCrossRefGoogle Scholar
  42. Hodgkin AL, Huxley AF (1952) Propagation of electrical signals along giant nerve fibers. Proc R Soc Lond B Biol Sci 140:177–183.PubMedCrossRefGoogle Scholar
  43. Jeffress LA (1948) A place theory of sound localization. J Comp Physiol Psychol 41:35–39.PubMedCrossRefGoogle Scholar
  44. Jeffress LA (1958) Medial geniculate body – a disavowal. J Acoust Soc Am 30:802–803.Google Scholar
  45. Johnson DH, Tsuchitani C, Linebarger DA, Johnson MJ (1986) Application of a point process model to responses of cat lateral superior olive units to ipsilateral tones. Hear Res 21:135–159.PubMedCrossRefGoogle Scholar
  46. Kandler K, Gillespie D (2005) Developmental refinement of inhibitory sound-localization ­circuits. Trends Neurosci 28:290–296.PubMedCrossRefGoogle Scholar
  47. Koppl C, Carr CE (2008) Maps of interaural time difference in the chicken’s brainstem nucleus laminaris. Biol Cybern 98:541–559.PubMedCrossRefGoogle Scholar
  48. Kulesza RJ (2008) Cytoarchitecture of the human superior olivary complex: nuclei of the trapezoid body and posterior tier. Hear Res 241:52–63.PubMedCrossRefGoogle Scholar
  49. Kuroki S, Kaga K (2006) Better time-intensity trade revealed by bilateral giant magnetostrictive bone conduction. Neuroreport 17:27.PubMedCrossRefGoogle Scholar
  50. Lindemann W (1986a) Extension of a binaural cross-correlation model by contralateral inhibition. I. Simulation of lateralization for stationary signals. J Acoust Soc Am 80:1608–1622.PubMedCrossRefGoogle Scholar
  51. Lindemann W (1986b) Extension of a binaural cross-correlation model by contralateral inhibition. II. The law of the first wave front. J Acoust Soc Am 80:1623–1630.PubMedCrossRefGoogle Scholar
  52. Marsálek P, Lansky P (2005) Proposed mechanisms for coincidence detection in the auditory brainstem. Biol Cybern 92:445–451.PubMedCrossRefGoogle Scholar
  53. McAlpine D, Jiang D, Palmer AR (2001) A neural code for low-frequency sound localization in mammals. Nat Neurosci 4:396–401.PubMedCrossRefGoogle Scholar
  54. Mills AW (1960) Lateralization of high-frequency tones. J Acoust Soc Am 32:132–134.CrossRefGoogle Scholar
  55. Moiseff A, Konishi M (1983) Binaural characteristics of units in the owl’s brainstem auditory pathway: precursors of restricted spatial receptive fields. J Neurosci 3:2553–2562.PubMedGoogle Scholar
  56. 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 28:6914–6925.PubMedCrossRefGoogle Scholar
  57. Reed MC, Blum JJ (1990) A model for the computation and encoding of azimuthal information by the lateral superior olive. J Acoust Soc Am 88:1442–1453.PubMedCrossRefGoogle Scholar
  58. Richter EA, Norris BE, Fullerton BC, Levine RA, Kiang NY (1983) Is there a medial nucleus of the trapezoid body in humans? Am J Anat 168:157–166.PubMedCrossRefGoogle Scholar
  59. Rieke F, Warland D, van Steveninck R, Bialek W (1997) Spikes: Exploring the Neural Code. Cambridge, MA: MIT Press.Google Scholar
  60. Rothman JS, Young ED, Manis PB (1993) Convergence of auditory nerve fibers onto bushy cells in the ventral cochlear nucleus: implications of a computational model. J Neurophysiol 70:2562–2583.PubMedGoogle Scholar
  61. Sayers BM, Cherry EC (1957) Mechanism of binaural fusion in the hearing of speech. J Acoust Soc Am 29:973–987.CrossRefGoogle Scholar
  62. Schwartz IR (1992) The superior olivary complex and lateral lemniscal nuclei. In: Webster DB, Popper AN, Fay RR (eds), The Mammalian Auditory Pathway: Neuroanatomy. New York: Springer, pp. 117–167.CrossRefGoogle Scholar
  63. Shackleton TM, Skottun BC, Arnott RH, Palmer AR (2003) Interaural time difference discrimination thresholds for single neurons in the inferior colliculus of guinea pigs. J Neurosci 23:716–724.PubMedGoogle Scholar
  64. Simon JZ, Carr CE, Shamma SA (1999) A dendritic model of coincidence detection in the avian brainstem. Neurocomputing 26–27:263–269.CrossRefGoogle Scholar
  65. Smith AJ, Owens S, Forsythe ID (2000) Characterisation of inhibitory and excitatory postsynaptic currents of the rat medial superior olive. J Physiol 529:681–698.PubMedCrossRefGoogle Scholar
  66. Smith PH (1995) Structural and functional differences distinguish principal from nonprincipal cells in the guinea pig MSO slice. J Neurophysiol 73:1653–1667.PubMedGoogle Scholar
  67. Solodovnikov A, Reed MC (2001) Robustness of a neural network model for differencing. J Comput Neurosci 11:165–173.PubMedCrossRefGoogle Scholar
  68. Stern R, Colburn H (1978) Theory of binaural interaction based on auditory-nerve data. IV. A model for subjective lateral position. J Acoust Soc Am 64:127–140.PubMedCrossRefGoogle Scholar
  69. Strata P, Harvey R (1999) Dale’s principle. Brain Res Bull 50:349–350.PubMedCrossRefGoogle Scholar
  70. Strutt JW (1907) On our perception of sound direction. Philos Mag 13:214–232.CrossRefGoogle Scholar
  71. Svirskis G, Dodla R, Rinzel J (2003) Subthreshold outward currents enhance temporal integration in auditory neurons. Biol Cybern 89:333–340.PubMedCrossRefGoogle Scholar
  72. Tollin DJ, Yin TCT (2005) Interaural phase and level difference sensitivity in low-frequency ­neurons in the lateral superior olive. J Neurosci 25:10648–10657.PubMedCrossRefGoogle Scholar
  73. Tsuchitani C (1977) Functional organization of lateral cell groups of cat superior olivary complex. J Neurophysiol 40:296–318.PubMedGoogle Scholar
  74. Tsuchitani C (1988) The inhibition of cat lateral superior olive unit excitatory responses to binaural tone bursts. I. The transient chopper response. J Neurophysiol 59:164–183.PubMedGoogle Scholar
  75. Tsuchitani C, Johnson DH (1985) The effects of ipsilateral tone burst stimulus level on the ­discharge patterns of cat lateral superior olivary units. J Acoust Soc Am 77:1484–1496.PubMedCrossRefGoogle Scholar
  76. van Bergeijk WA (1962) Variation on a theme of Békésy: a model of binaural interaction. J Acoust Soc Am 34:1431–1437.CrossRefGoogle Scholar
  77. von Békésy G (1930) Zur theorie des hörens; über das richtungshören bei einer zeitdifferenz oder lautstärkenungleichheit der beiderseitigen schalleinwirkungen. Physik Zeits 31:824–835.Google Scholar
  78. Yang L, Monsivais P, Rubel EW (1999) 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.PubMedGoogle Scholar
  79. Yue L, Johnson DH (1997) Optimal binaural processing based on point process models of preprocessed cues. J Acoust Soc Am 101:982–992.CrossRefGoogle Scholar
  80. Zacksenhouse M, Johnson DH, Tsuchitani C (1992) Excitatory/inhibitory interaction in the LSO revealed by point process modeling. Hear Res 62:105–123.PubMedCrossRefGoogle Scholar
  81. Zacksenhouse M, Johnson DH, Tsuchitani C (1993) Excitation effects on LSO unit sustained responses: point process characterization. Hear Res 68:202–216.PubMedCrossRefGoogle Scholar
  82. Zacksenhouse M, Johnson DH, Williams J, Tsuchitani C (1998) Single-neuron modeling of LSO unit responses. J Neurophysiol 79:3098–3110.PubMedGoogle Scholar
  83. Zhou Y, Colburn HS (2009) Effects of membrane afterhyperpolarization on interval statistics and interaural level difference coding in the lateral superior olive. J Neurophysiol (in review).Google Scholar
  84. 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 25:3046–3058.PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag US 2010

Authors and Affiliations

  1. 1.Department of Biomedical EngineeringBoston UniversityBostonUSA

Personalised recommendations