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Unavoidably Delayed: A Personal Perspective of Twenty Years of Research on a Sound Localization Cue

Chapter
Part of the Springer Handbook of Auditory Research book series (SHAR, volume 50)

Abstract

Localization of sound sources depends on a variety of cues, the most important of which are the differences in sound level and arrival time at the two ears. The differences in the arrival time are only of the order of millionths of seconds, and more than 60 years ago a putative neural mechanism to decipher these tiny differences was proposed by Lloyd Jeffress. Jeffress’s model has stood the test of time, with most of its essential elements (an internal delay before comparison of the input from the two ears by a coincidence mechanism) essentially now taken as established fact. However, over the last 20 years or so there has been renewed interest in the processes by which the tiny time differences are decoded, in particular in the preprocessing of the timing information and in the mechanism that generates the internal delay. These issues are still not fully resolved, as will be clear from this short and personal perspective.

Keywords

Superior Colliculus Delay Line Inferior Colliculus Interaural Time Difference Interaural Level Difference 
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.

Notes

Acknowledgments 

I am really grateful to Trevor Shackleton and Adrian Rees for casting a critical eye over this piece of writing which, to be honest, is a little outside my usual comfort zone.

References

  1. Batra, R., Kuwada, S., & Fitzpatrick, D. C. (1997a). Sensitivity to interaural temporal disparities of low- and high-frequency neurons in the superior olivary complex. I. Heterogeneity of responses. Journal of Neurophysiology, 78, 1222–1236.PubMedGoogle Scholar
  2. Batra, R., Kuwada, S., & Fitzpatrick, D. C. (1997b). Sensitivity to interaural temporal disparities of low- and high- frequency neurons in the superior olivary complex. I. Heterogeneity of responses. Journal of Neurophysiology, 73, 1222–1236.Google Scholar
  3. Beckius, G. E., Batra, R., & Oliver, D. L. (1999). Axons from anterventral cochlear nucleus that terminate in medial superior olive of the cat: Observations related to delay lines. Journal of Neuroscience, 19, 3146–3161.PubMedGoogle Scholar
  4. Bonham, B. H., & Lewis, E. R. (1999). Localization by interaural time difference (ITD): Effects of interaural frequency mismatch. Journal of the Acoustical Society of America, 106, 281–290.PubMedCrossRefGoogle Scholar
  5. 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
  6. Burger, R. M., Fukui, I., Ohmori, H., & Rubel, E. W. (2011). Inhibition in the balance: Binaurally coupled inhibitory feedback in sound localization circuitry. Journal of Neurophysiology, 106, 4–14.PubMedCentralPubMedCrossRefGoogle Scholar
  7. Caird, D. M., Pillman, F., & Klinke, R. (1989). Processing of binaural masking level difference signals in the cat inferior colliculus. Hearing Research, 43, 1–24.PubMedCrossRefGoogle Scholar
  8. Caird, D. M., Palmer, A. R., & Rees, A. (1991). Binaural masking level difference effects in single units of the guinea pig inferior colliculus. Hearing Research, 57, 91–106.PubMedCrossRefGoogle Scholar
  9. Chase, S. M., & Young, E. D. (2005). Limited segregation of different types of sound localization information among classes of units in the inferior colliculus. Journal of Neuroscience, 25, 7575–7585.PubMedCrossRefGoogle Scholar
  10. Colburn, H. S. (1973). Theory of binaural interaction based on auditory-nerve data. I. General strategy and preliminary results on interaural discrimination. Journal of the Acoustical Society of America, 54, 1458–1470.PubMedCrossRefGoogle Scholar
  11. Goldberg, J. M., & Brown, P. B. (1969). Response of binaural neurons of dog superior olivary complex to dichotic tonal stimuli: Some physiological mechanisms of sound localization. Journal of Neurophysiology, 32, 613–636.PubMedGoogle Scholar
  12. Grothe, B. (2000). The evolution of temporal processing in the medial superior olive, an auditory brainstem structure. Progress in Neurobiology, 61, 581–610.PubMedCrossRefGoogle Scholar
  13. Hancock, K. E., & Delgutte, B. (2004). A physiologically based model of interaural time difference discrimination. Journal of Neuroscience, 24, 7110–7117.PubMedCentralPubMedCrossRefGoogle Scholar
  14. Harper, N. S., & McAlpine, D. (2004). Optimal neural population coding of an auditory spatial cue. Nature, 430, 682–686.PubMedCrossRefGoogle Scholar
  15. Jeffress, L. A. (1948). A place code theory of sound localization. Journal of Comparative and Physiological Psychology, 44, 35–39.CrossRefGoogle Scholar
  16. Jiang, D., McAlpine, D., & Palmer, A. R. (1997). Detectability index measures of binaural masking level difference across populations of inferior colliculus neurones. Journal of Neuroscience, 17, 9331–9339.PubMedGoogle Scholar
  17. Joris, P. X., & Yin, T. C. T. (2007). A matter of time: Internal delays in binaural processing. Trends in Neuroscience, 30, 70–78.CrossRefGoogle Scholar
  18. Joris, P. X., Van de Sande, B., Louage, D. H., & van der Heijden, M. (2006). Binaural and cochlear disparities. Proceedings of the National Academy of Sciences of the USA, 103, 12917–12922.Google Scholar
  19. Kapfer, C., Seidl, A. H., Schweizer, H., & Grothe, B. (2002). Experience-dependent refinement of inhibitory inputs to auditory coincidence-detector neurons. Nature Neuroscience, 5, 247–253.PubMedCrossRefGoogle Scholar
  20. Karino, S., Smith, P. H., Yin, T. C., & Joris, P. X. (2011). Axonal branching patterns as sources of delay in the mammalian auditory brainstem: A re-examination. Journal of Neuroscience, 31, 3016–3031.PubMedCentralPubMedCrossRefGoogle Scholar
  21. Knudsen, E. I., & Konishi, M. (1978). A neural map of auditory space in the owl. Science, 200, 795–797.PubMedCrossRefGoogle Scholar
  22. Kuwada, S., & Yin, T. C. (1983). 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. Journal of Neurophysiology, 50, 981–999.Google Scholar
  23. Licklider, J. C. R. (1948). The influence of interaural phase relations upon the masking of speech by white noise. Journal of the Acoustical Society of America, 20, 150–159.CrossRefGoogle Scholar
  24. McAlpine, D., Jiang, D., & Palmer, A. R. (1996a). Monaural and binaural responses of low-best frequency neurones in the inferior colliculus of the guinea pig. Hearing Research, 97, 136–152.PubMedCrossRefGoogle Scholar
  25. McAlpine, D., Jiang, D., & Palmer, A. R. (1996b). Binaural masking level differences in the inferior colliculus of the guinea pig. Journal of the Acoustical Society of America, 100, 490–503.PubMedCrossRefGoogle Scholar
  26. McAlpine, D., Jiang, D., & Palmer, A. R. (1998). Convergent input from brainstem coincidence detectors onto delay-sensitive neurones in the inferior colliculus. Journal of Neuroscience, 18, 6026–6039.PubMedGoogle Scholar
  27. McAlpine, D., Jiang, D., & Palmer, A. R. (2001). A neural code for low-frequency sound localisation in mammals. Nature Neuroscience, 4, 396–401.PubMedCrossRefGoogle Scholar
  28. Palmer, A. R., & King, A. J. (1982). The representation of auditory space in the mammalian superior colliculus. Nature, 299, 248–249.PubMedCrossRefGoogle Scholar
  29. Palmer, A. R., Rees, A., & Caird, D. (1990). Interaural delay sensitivity to tones and broad-band signals in the guinea-pig inferior colliculus. Hearing Research, 50, 71–86.PubMedCrossRefGoogle Scholar
  30. Palmer, A. R., Jiang, D., & McAlpine, D. (2000). Responses of neurones in the inferior colliculus to binaural masking level differences created by inverting the noise in one ear (NoSo vs NpSo). Journal of Neurophysiology, 84, 844–852.PubMedGoogle Scholar
  31. Palmer, A. R., Lui, L., & Shackleton, T. M. (2007). Changes in interaural time sensitivity with interaural level differences in the inferior colliculus. Hearing Research, 223, 105–113.PubMedCrossRefGoogle Scholar
  32. Rayleigh, L. (1907). Our perception of sound direction. Philosophical Magazine, 13, 214–232.CrossRefGoogle Scholar
  33. Rhode, W. S. (1971). Observations of the vibration of the basilar membrane in squirrel monkeys using the Mössbauer technique. Journal of the Acoustical Society of America, 49, 1218–1231.PubMedCrossRefGoogle Scholar
  34. Rose, J., Gross, N., Geisler, C., & Hind, J. (1966). Some neural mechanisms in the inferior colliculus of the cat which may be relevant to localization of a sound source. Journal of Neurophysiology, 2, 288–314.Google Scholar
  35. Sachs, M. B., & Young, E. D. (1979). Encoding of steady-state vowels in the auditory nerve: representation in terms of discharge rate. Journal of the Acoustical Society of America, 66, 470–479.PubMedCrossRefGoogle Scholar
  36. Schroeder, M. R. (1977). New viewpoints in binaural interactions. In E. F. Evans & J. P. Wilson (Eds.), Psychophysics and physiology of hearing (pp. 455–467.). New York: Academic Press.Google Scholar
  37. Seidl, A. H., & Grothe, B. (2003). Acoustic experience is essential for the development of normal ITD processing. Association for Research in Otolaryngology, 26, 930.Google Scholar
  38. Seidl, A. H., & Grothe, B. (2005). Development of sound localization mechanisms in the mongolian gerbil is shaped by early acoustic experience. Journal of Neurophysiology, 94, 1028–1036.PubMedCrossRefGoogle Scholar
  39. Seidl, A. H., Rubel, E. W., & Harris, D. M. (2010). Mechanisms for adjusting interaural time differences to achieve binaural coincidence detection. Journal of Neuroscience, 30, 70–80.PubMedCentralPubMedCrossRefGoogle Scholar
  40. Shackleton, T. M., McAlpine, D., & Palmer, A. R. (2000). Modelling convergent input onto interaural-delay sensitive inferior colliculus neurones. Hearing Research, 149, 199–215.PubMedCrossRefGoogle Scholar
  41. Shackleton, T. M., Skottun, B. C., Arnott, R. H., & Palmer, A. R. (2003). Interaural time difference discrimination thresholds for single neurons in the inferior colliculus of Guinea pigs. Journal of Neuroscience, 23, 716–724.PubMedGoogle Scholar
  42. Shamma, S. A. (1989). Stereausis: Binaural processing without neural delays. Journal of the Acoustical Society of America, 86, 989–1006.PubMedCrossRefGoogle Scholar
  43. Smith, P. H., Joris, P. X., & Yin, T. C. T. (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. Journal of Comparative Neurology, 331, 245–260.PubMedCrossRefGoogle Scholar
  44. Spitzer, M. W., & Semple, M. N. (1991). Interaural phase coding in auditory midbrain: Influence of dynamic stimulus features. Science, 254, 721–724.PubMedCrossRefGoogle Scholar
  45. Spitzer, M. W., & Semple, M. N. (1993). Responses of inferior colliculus neurones to time-varying interaural phase disparity: Effects of shifting the locus of virtual motion. Journal of Neurophysiology, 69, 1245–1263.PubMedGoogle Scholar
  46. Spitzer, M. W., & Semple, M. N. (1995). Neurons sensitive to interaural phase disparity in gerbil superior olive: Diverse monaural and temporal response properties. Journal of Neurophysiology, 73, 1668–1690.PubMedGoogle Scholar
  47. Tang, Z.-Q., & Lu, Y. (2012). Two GABAA responses with distinct kinetics in a sound localization circuit. Journal of Physiology, 590, 3787–3805.PubMedCentralPubMedCrossRefGoogle Scholar
  48. van Bergeijk, W. A. (1962). Variation on a theme of Bekesy: A model of binaural interaction. Journal of the Acoustical Society of America, 34, 1431–1437.CrossRefGoogle Scholar
  49. von Békésy, G. (1960). Experiments in hearing. New-York: McGraw-Hill.Google Scholar
  50. Wise, L. Z., & Irvine, D. R. (1985). Topographic organization of interaural intensity difference sensitivity in deep layers of cat superior colliculus: Implications for auditory spatial representation. Journal of Neurophysiology, 54, 185–211.PubMedGoogle Scholar
  51. Yin, T., & Kuwada, S. (1983). Binaural interaction in low-frequency neurons in inferior colliculus of the cat. III. Effects of changing frequency. Journal of Neurophysiology, 50, 1020–1042.PubMedGoogle Scholar
  52. Yin, T., Chan, J., & Irvine, D. (1986). Effects of interaural time delays of noise stimuli on low-frequency cells in the cat's inferior colliculus. I. Responses to wideband noise. Journal of Neurophysiology, 55, 280–300.PubMedGoogle Scholar
  53. Yin, T. C., & Chan, J. C. (1990). Interaural time sensitivity in medial superior olive of cat. Journal of Neurophysiology, 64, 465–488.PubMedGoogle Scholar
  54. Young, E. D., & Sachs, M. B. (1979). Representation of steady-state vowels in the temporal aspects of the discharge patterns of populations of auditory-nerve fibers. Journal of the Acoustical Society of America, 66, 1381–1403.PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2014

Authors and Affiliations

  1. 1.Medical Research Council Institute of Hearing ResearchNottinghamUK

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