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Evidence for Opponent Process Analysis of Sound Source Location in Humans

  • Paul M. BrileyEmail author
  • Pádraig T. Kitterick
  • A. Quentin Summerfield
Research Article

Abstract

Research with barn owls suggested that sound source location is represented topographically in the brain by an array of neurons each tuned to a narrow range of locations. However, research with small-headed mammals has offered an alternative view in which location is represented by the balance of activity in two opponent channels broadly tuned to the left and right auditory space. Both channels may be present in each auditory cortex, although the channel representing contralateral space may be dominant. Recent studies have suggested that opponent channel coding of space may also apply in humans, although these studies have used a restricted set of spatial cues or probed a restricted set of spatial locations, and there have been contradictory reports as to the relative dominance of the ipsilateral and contralateral channels in each cortex. The current study used electroencephalography (EEG) in conjunction with sound field stimulus presentation to address these issues and to inform the development of an explicit computational model of human sound source localization. Neural responses were compatible with the opponent channel account of sound source localization and with contralateral channel dominance in the left, but not the right, auditory cortex. A computational opponent channel model reproduced every important aspect of the EEG data and allowed inferences about the width of tuning in the spatial channels. Moreover, the model predicted the oft-reported decrease in spatial acuity measured psychophysically with increasing reference azimuth. Predictions of spatial acuity closely matched those measured psychophysically by previous authors.

Keywords

sound source location opponent process electroencephalography continuous stimulation paradigm computational modeling minimum audible angle 

Notes

Acknowledgments

This study was supported by a grant from Deafness Research UK to AQS and PMB. PTK was supported by a Wellcome Trust Value in People award. The authors would like to thank Dr. Katrin Krumbholz and two anonymous reviewers for their helpful comments and suggestions.

Conflict of interest

The authors declare that they have no conflicts of interest.

References

  1. Bell AJ, Sejnowski TJ (1995) An information-maximization approach to blind separation and blind deconvolution. Neural Comput 7:1129–1159PubMedCrossRefGoogle Scholar
  2. Briley PM, Breakey C, Krumbholz K (2012) Evidence for pitch chroma mapping in human auditory cortex. Cereb Cortex. doi: 10.1093/cercor/bhs242
  3. Brugge JF, Dubrovsky NA, Aitkin LM, Anderson DJ (1969) Sensitivity of single neurons in auditory cortex of cat to binaural tonal stimulation; effects of varying interaural time and intensity. J Neurophysiol 32:1005–1024PubMedGoogle Scholar
  4. Carr CE, Konishi M (1990) A circuit for detection of interaural time differences in the brain stem of the barn owl. J Neurosci 10:3227–3246PubMedGoogle Scholar
  5. Clarke S, Bellmann A, Meuli RA, Assal G, Steck AJ (2000) Auditory agnosia and auditory spatial deficits following left hemispheric lesions: evidence for distinct processing pathways. Neuropsychologia 38:797–807PubMedCrossRefGoogle Scholar
  6. Delorme A, Makeig S (2004) EEGLAB: an open source toolbox for analysis of single-trial EEG dynamics including independent component analysis. J Neurosci Methods 134:9–21PubMedCrossRefGoogle Scholar
  7. Gatehouse S, Noble W (2004) The Speech, Spatial and Qualities of Hearing Scale (SSQ). Int J Audiol 43:85–99PubMedCrossRefGoogle Scholar
  8. Getzmann S (2009) Effect of auditory motion velocity on reaction time and cortical processes. Neuropsychologia 47:2625–2633PubMedCrossRefGoogle Scholar
  9. Grantham DW (1995) Spatial hearing and related phenomena. In: Moore BCJ (ed) Hearing. Academic, San Diego, pp 297–345CrossRefGoogle Scholar
  10. Grill-Spector K, Henson R, Martin A (2006) Repetition and the brain: neural models of stimulus-specific effects. Trends Cogn Neurosci 10:14–23CrossRefGoogle Scholar
  11. Grothe B, Park TJ (1995) Time can be traded for intensity in the lower auditory system. Naturwissenschaften 82:521–523PubMedCrossRefGoogle Scholar
  12. Grothe B, Pecka M, McAlpine D (2010) Mechanisms of sound localization in mammals. Physiol Rev 90:983–1012PubMedCrossRefGoogle Scholar
  13. Hall JL (1965) Binaural interaction in the accessory superior-olivary nucleus of the cat. J Acoust Soc Am 37:814–823PubMedCrossRefGoogle Scholar
  14. Hall DA, Haggard MP, Akeroyd MA, Summerfield AQ, Palmer AR, Elliott MR, Bowtell RW (2000) Modulation and task effects in auditory processing measured using fMRI. Hum Brain Mapp 10:107–119PubMedCrossRefGoogle Scholar
  15. Hewson-Stoate N, Schönwiesner M, Krumbholz K (2006) Vowel processing evokes a large sustained response. Eur J Neurosci 24:2661–2671PubMedCrossRefGoogle Scholar
  16. Irvine DRF (1992) Physiology of the auditory brainstem. In: Popper A, Fay R (eds) The mammalian auditory pathway: neurophysiology. Springer, New York, pp 153–231CrossRefGoogle Scholar
  17. Jeffress LA (1948) A place theory of sound localization. J Comp Physiol Psychol 41:35–39PubMedCrossRefGoogle Scholar
  18. Johnson BW, Hautus MJ (2010) Processing of binaural spatial information in human auditory cortex: neuromagnetic responses to interaural timing and level differences. Neuropsychologia 48:2610–2619PubMedCrossRefGoogle Scholar
  19. Key APF, Dove GO, Maguire MJ (2005) Linking brainwaves to the brain: an ERP primer. Dev Neuropsychol 27:183–215PubMedCrossRefGoogle Scholar
  20. Kitterick PT, Lovett RES, Goman AM, Summerfield AQ (2011) The AB-York crescent of sound: an apparatus for assessing spatial-listening skills in children and adults. Cochlear Implant Int 12:164–169CrossRefGoogle Scholar
  21. Knudsen EI (1982) Auditory and visual maps of space in the optic tectum of the owl. J Neurosci 2:1177–1194PubMedGoogle Scholar
  22. Konishi M (2003) Coding of auditory space. Ann Rev Neurosci 26:31–55PubMedCrossRefGoogle Scholar
  23. Krumbholz K, Schönwiesner M, von Cramon DY, Rübsamen R, Shah NJ, Zilles K, Fink GR (2005) Representation of interaural temporal information from left and right auditory space in the human planum temporale and inferior parietal lobe. Cereb Cortex 15:317–324PubMedCrossRefGoogle Scholar
  24. Krumbholz K, Hewson-Stoate N, Schönwiesner M (2007) Cortical response to auditory motion suggests an asymmetry in the reliance on inter-hemispheric connections between the left and right auditory cortices. J Neurophysiol 97:1649–1655PubMedCrossRefGoogle Scholar
  25. Lee TW, Girolami M, Sejnowski TJ (1999) Independent component analysis using an extended Infomax algorithm for mixed subgaussian and supergaussian sources. Neural Comput 11:417–441PubMedCrossRefGoogle Scholar
  26. Litovsky RY, Macmillan NA (1994) Sound localization precision under conditions of the precedence effect: effects of azimuth and standard stimuli. J Acoust Soc Am 96:752–758PubMedCrossRefGoogle Scholar
  27. Magezi DA, Krumbholz K (2010) Evidence for opponent-channel coding of interaural time differences in human auditory cortex. J Neurophysiol 104:1997–2007PubMedCrossRefGoogle Scholar
  28. Makeig S, Jüng T-P, Bell AJ, Ghahremani D, Sejnowski TJ (1997) Blind separation of auditory event-related brain responses into independent components. Proc Natl Acad Sci U S A 94:10979–10984PubMedCrossRefGoogle Scholar
  29. Mäkelä JP, Ahonen A, Hämäläinen M, Hari R, Ilmoniemi R, Kajola M, Knuutila J, Lounasmaa OV, McEvoy L, Salmelin R, Salonen O, Sams M, Simola J, Tesche C, Vasama J-P (1993) Functional differences between auditory cortices of the two hemispheres revealed by whole-head neuromagnetic recordings. Hum Brain Mapp 1:48–56CrossRefGoogle Scholar
  30. McAlpine D (2005) Creating a sense of auditory space. J Physiol 566:21–28PubMedCrossRefGoogle Scholar
  31. McAlpine D, Grothe B (2003) Sound localization and delay lines—do mammals fit the model? Trends Neurosci 26:347–350PubMedCrossRefGoogle Scholar
  32. McAlpine D, Jiang D, Palmer AR (2001) A neural code for low-frequency sound localization in mammals. Nat Neurosci 4:396–401PubMedCrossRefGoogle Scholar
  33. Middlebrooks JC, Green DM (1991) Sound localization by human listeners. Annu Rev Psychol 42:135–159PubMedCrossRefGoogle Scholar
  34. Morey RD (2008) Confidence intervals from normalized data: a correction to Cousineau (2005). Tutor Quant Methods Psychol 4:61–64Google Scholar
  35. Morosan P, Rademacher J, Schleicher A, Amunts K, Schormann T, Zilles K (2001) Human primary auditory cortex: cytoarchitectonic subdivisions and mapping into a spatial reference system. NeuroImage 13:684–701PubMedCrossRefGoogle Scholar
  36. Näätänen R, Picton T (1987) The N1 wave of the human electric and magnetic response to sound: a review and an analysis of the component structure. Psychophysiology 24:375–425PubMedCrossRefGoogle Scholar
  37. Näätänen R, Paavilainen P, Rinne T, Alho K (2007) The mismatch negativity (MMN) in basic research of central auditory processing: a review. Clin Neurophysiol 118:2544–2590PubMedCrossRefGoogle Scholar
  38. Nunez PL, Srinivasan R (2006) Electric fields of the brain. Oxford University Press, New YorkCrossRefGoogle Scholar
  39. Pantev C, Ross B, Berg P, Elbert T, Rockstroh B (1998) Study of the human auditory cortices using a whole-head magnetometer: left vs. right hemisphere and ipsilateral vs. contralateral stimulation. Audiol Neuro Otol 3:183–190CrossRefGoogle Scholar
  40. Phillips DP, Brugge JF (1985) Progress in neurophysiology of sound localization. Annu Rev Psychol 36:245–274PubMedCrossRefGoogle Scholar
  41. Phillips DP, Hall SE (2005) Psychophysical evidence for adaptation of central auditory processors for interaural differences in time and level. Hear Res 202:188–199PubMedCrossRefGoogle Scholar
  42. Phillips DP, Irvine DRF (1981) Responses of single neurons in physiologically defined area AI of cat cerebral cortex: sensitivity to interaural intensity differences. Hear Res 4:299–307PubMedCrossRefGoogle Scholar
  43. Phillips DP, Carmichael ME, Hall SE (2006) Interaction in the perceptual processing of interaural time and level differences. Hear Res 211:96–102PubMedCrossRefGoogle Scholar
  44. Pollak GD (1988) Time is traded for intensity in the bat’s auditory system. Hear Res 36:107–124PubMedCrossRefGoogle Scholar
  45. Recanzone GH, Guard DC, Phan ML, Su T-I K (2000) Correlation between the activity of single auditory cortical neurons and sound-localization behavior in the macaque monkey. J Neurophysiol 83:2723–2739PubMedGoogle Scholar
  46. Rosenzweig MR (1951) Representations of the two ears at the auditory cortex. Am J Physiol 167:147–158PubMedGoogle Scholar
  47. Salminen NH, May PJC, Alku P, Tiitinen H (2009) A population rate code of auditory space in the human cortex. PLoS One 4:e7600PubMedCrossRefGoogle Scholar
  48. Salminen NH, Tiitinen H, Miettinen I, Alku P, May PJC (2010a) Asymmetrical representation of auditory space in human cortex. Brain Res 1306:93–99PubMedCrossRefGoogle Scholar
  49. Salminen NH, Tiitinen H, Yrttiaho S, May PJC (2010b) The neural code for interaural time difference in human auditory cortex. JASA Express Lett 127:EL60–EL65CrossRefGoogle Scholar
  50. Scheffler K, Bilecen D, Schmid N, Tschopp K, Seelig J (1998) Auditory cortical responses in hearing subjects and unilateral deaf patients as detected by functional magnetic resonance imaging. Cereb Cortex 8:156–163PubMedCrossRefGoogle Scholar
  51. Scherg M (1990) Fundamentals of dipole source potential analysis. In: Grandori F, Hoke M, Romani G (eds) Auditory evoked potentials and fields: advances in audiology. Karger, Basel, pp 40–69Google Scholar
  52. Schröger E (1996) Interaural time and level differences: integrated or separated processing? Hear Res 96:191–198PubMedCrossRefGoogle Scholar
  53. Spierer L, Bellmann-Thiran A, Maeder P, Murray MM, Clarke S (2009) Hemispheric competence for auditory spatial representation. Brain 132:1953–1966PubMedCrossRefGoogle Scholar
  54. Stecker GC, Harrington IA, Middlebrooks JC (2005) Location coding by opponent neural populations in the auditory cortex. PLOS Biol 3:e78PubMedCrossRefGoogle Scholar
  55. Sullivan WE, Konishi M (1986) Neural map of interaural phase difference in the owl’s brainstem. Proc Natl Acad Sci U S A 83:8400–8404PubMedCrossRefGoogle Scholar
  56. Teder-Sälejärvi WA, Hillyard SA (1998) The gradient of spatial auditory attention in free field: an event-related potential study. Percept Psychophys 60:1228–1242PubMedCrossRefGoogle Scholar
  57. Teder-Sälejärvi WA, Hillyard SA, Röder B, Neville HJ (1999) Spatial attention to central and peripheral auditory stimuli as indexed by event-related potentials. Cogn Brain Res 8:213–227CrossRefGoogle Scholar
  58. Tsuchitani C, Johnson DH (1991) Binaural cues and signal processing in the superior olivary complex. In: Altschuler RA, Bobbin RP, Clopton BM, Hoffman DW (eds) Neurobiology of hearing: the central auditory system. Raven, New York, pp 163–194Google Scholar
  59. Ungan P, Yagcioglu S, Goksoy C (2001) Differences between the N1 waves of the responses to interaural time and intensity disparities: scalp topography and dipole sources. Clin Neurophysiol 112:485–498PubMedCrossRefGoogle Scholar
  60. van Bergeijk WA (1962) Variation on a theme of Békésy: a model of binaural interaction. J Acoust Soc Am 34:1431–1437CrossRefGoogle Scholar
  61. von Békésy G (1930) Zur theorie des hörens. Über das richtungshören bei einer zeitdifferenz oder lautstärkenungleichheit der beiderseitigen schalleinwirkungen. Phys Z 31:824–835, 857–868Google Scholar
  62. Webster DB (1992) An overview of mammalian auditory pathways with an emphasis on humans. In: Webster DB, Popper AN, Fay RR (eds) The mammalian auditory pathway: neuroanatomy. Springer, New York, pp 1–22CrossRefGoogle Scholar
  63. Yin TC, Hirsch JA, Chan JC (1985) Responses of neurons in the cat’s superior colliculus to acoustic stimuli. II. A model of interaural intensity sensitivity. J Neurophysiol 3:746–758Google Scholar
  64. Zatorre RJ, Penhune VB (2001) Spatial localization after excision of human auditory cortex. J Neurosci 21:6321–6328PubMedGoogle Scholar

Copyright information

© Association for Research in Otolaryngology 2012

Authors and Affiliations

  • Paul M. Briley
    • 1
    Email author
  • Pádraig T. Kitterick
    • 1
  • A. Quentin Summerfield
    • 1
    • 2
  1. 1.Department of PsychologyUniversity of YorkYorkUK
  2. 2.Hull York Medical SchoolUniversity of YorkYorkUK

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