fMRI of the Central Auditory System

  • Deborah Ann HallEmail author
  • Aspasia Eleni Paltoglou
Part of the Neuromethods book series (NM, volume 119)


Over the years, blood oxygen level-dependent (BOLD) fMRI has made important contributions to the understanding of central auditory processing in humans. Although there are significant technical challenges to overcome in the case of auditory fMRI, the unique methodological advantage of fMRI as an indicator of population neural activity lies in its spatial precision. It can be used to examine the neural basis of auditory representation at a number of spatial scales, from the micro-anatomical scale of population assemblies to the macro-anatomical scale of cortico-cortical circuits. The spatial resolution of fMRI is maximized in the case of mapping individual brain activity, and here it has been possible to demonstrate known organizational features of the auditory system that have hitherto been possible only using invasive electrophysiological recording methods. Frequency coding in the primary auditory cortex is one such example that we shall discuss in this chapter. Of course, noninvasive procedures for neuroscience are the ultimate aim and as the field moves towards this goal by recording in awake, behaving animals so human neuroimaging techniques will be increasingly relied upon to provide an interpretive link between animal neurophysiology at the multi-unit level and the operation of larger neuronal assemblies, as well as the mechanisms of auditory perception itself. For example, the neural effects of intentional behavior on stimulus-driven coding have been explored both in animals, using electrophysiological techniques, and in humans, using fMRI. While the feature-specific effects of selective attention are well established in the visual cortex, the effect of auditory attention in the auditory cortex has generally been examined at a very coarse spatial scale. Ongoing research in our laboratory has started to address this question and here we present preliminary evidence for frequency-specific effects of attentional enhancement in the human auditory cortex. We end with a brief discussion of several future directions for auditory fMRI research.

Key words

Technical challenges Frequency coding Selective attention Perceptual representation Task specificity 


  1. 1.
    Palmer AR, Bullock DC, Chambers JD (1998) A high-output, high-quality sound system for use in auditory fMRI. Neuroimage 7:S357Google Scholar
  2. 2.
    Chou CK, McDougall JA, Chan KW (1995) Absence of radiofrequency heating from auditory implants during magnetic-resonance imaging. Bioelectromagnetics 16(5):307–316PubMedCrossRefGoogle Scholar
  3. 3.
    Heller JW, Brackmann DE, Tucci DL, Nyenhuis JA, Chou CK (1996) Evaluation of MRI compatibility of the modified nucleus multichannel auditory brainstem and cochlear implants. Am J Otol 17(5):724–729PubMedGoogle Scholar
  4. 4.
    Shellock FG, Morisoli S, Kanal E (1993) MR procedures and biomedical implants, materials, and devices—1993 update. Radiology 189(2):587–599PubMedCrossRefGoogle Scholar
  5. 5.
    Weber BP, Neuburger J, Battmer RD, Lenarz T (1997) Magnetless cochlear implant: relevance of adult experience for children. Am J Otol 18(6):S50–S51PubMedGoogle Scholar
  6. 6.
    Wild DC, Head K, Hall DA (2006) Safe magnetic resonance scanning of patients with metallic middle ear implants. Clin Otolaryngol 31(6):508–510PubMedCrossRefGoogle Scholar
  7. 7.
    Giraud AL, Truy E, Frackowiak R (2001) Imaging plasticity in cochlear implant patients. Audiol Neurootol 6(6):381–393PubMedCrossRefGoogle Scholar
  8. 8.
    Moelker A, Wielopolski PA, Pattynama PM (2003) Relationship between magnetic field strength and magnetic-resonance-related acoustic noise levels. MAGMA 16:52–55PubMedCrossRefGoogle Scholar
  9. 9.
    Foster JR, Hall DA, Summerfield AQ, Palmer AR, Bowtell RW (2000) Sound-level measurements and calculations of safe noise dosage during fMRI at 3T. J Magn Reson Imaging 12:157–163PubMedCrossRefGoogle Scholar
  10. 10.
    Ravicz ME, Melcher JR (2001) Isolating the auditory system from acoustic noise during functional magnetic resonance imaging: examination of noise conduction through the ear canal, head, and body. J Acoust Soc Am 109(1):216–231PubMedPubMedCentralCrossRefGoogle Scholar
  11. 11.
    Price DL, De Wilde JP, Papadaki AM, Curran JS, Kitney RI (2001) Investigation of acoustic noise on 15 MRI scanners from 0.2 T to 3 T. J Magn Reson Imaging 13(2):288–293PubMedCrossRefGoogle Scholar
  12. 12.
    Hedeen RA, Edelstein WA (1997) Characterization and prediction of gradient acoustic noise in MR imagers. Magn Reson Med 37(1):7–10PubMedCrossRefGoogle Scholar
  13. 13.
    Hennel F, Girard F, Loenneker T (1999) “Silent” MRI with soft gradient pulses. Magn Reson Med 42:6–10PubMedCrossRefGoogle Scholar
  14. 14.
    Brechmann A, Baumgart F, Scheich H (2002) Sound-level-dependent representation of frequency modulations in human auditory cortex: a low-noise fMRI study. J Neurophysiol 87:423–433PubMedGoogle Scholar
  15. 15.
    Sumby WH, Pollack I (1954) Visual contribution to speech intelligibility in noise. J Acoust Soc Am 26(2):212–215CrossRefGoogle Scholar
  16. 16.
    Assmann P, Summerfield Q (2004) Perception of speech under adverse conditions. In: Greenberg S, Ainsworth WA, Popper AN, Fay RR (eds) Speech processing in the auditory system. Springer, New York, pp 231–308CrossRefGoogle Scholar
  17. 17.
    Healy EW, Moser DC, Morrow-Odom KL, Hall DA, Fridriksson J (2007) Speech perception in MRI scanner noise by persons with aphasia. J Speech Lang Hear Res 50:323–334PubMedCrossRefGoogle Scholar
  18. 18.
    Harms MP, Melcher JR (2002) Sound repetition rate in the human auditory pathway: representations in the waveshape and amplitude of fMRI activation. J Neurophysiol 88:1433–1450PubMedGoogle Scholar
  19. 19.
    Chambers JD, Akeroyd MA, Summerfield AQ, Palmer AR (2001) Active control of the volume acquisition noise in functional magnetic resonance imaging: method and psychoacoustical evaluation. J Acoust Soc Am 110(6):3041–3054PubMedCrossRefGoogle Scholar
  20. 20.
    Hall DA, Chambers J, Foster J, Akeroyd MA, Coxon R, Palmer AR (2009) Acoustic, psychophysical, and neuroimaging measurements of the effectiveness of active cancellation during auditory functional magnetic resonance imaging. J Acoust Soc Am 125(1):347–359PubMedCrossRefGoogle Scholar
  21. 21.
    Hall DA, Haggard MP, Akeroyd MA, Palmer AR, Summerfield AQ, Elliott MR, Gurney EM, Bowtell RW (1999) ‘Sparse’ temporal sampling in auditory fMRI. Hum Brain Mapp 7:213–223PubMedCrossRefGoogle Scholar
  22. 22.
    Bandettini PA, Jesmanowicz A, Van Kylen J, Birn RM, Hyde JS (1998) Functional MRI of brain activation induced by scanner acoustic noise. Magn Reson Med 39:410–416PubMedCrossRefGoogle Scholar
  23. 23.
    Bilecen D, Scheffler K, Schmid N, Tschopp K, Seelig J (1998) Tonotopic organization of the human auditory cortex as detected by BOLD-FMRI. Hear Res 126:19–27PubMedCrossRefGoogle Scholar
  24. 24.
    Hall DA, Summerfield AQ, Gonçalves MS, Foster JR, Palmer AR, Bowtell RW (2000) Time-course of the auditory BOLD response to scanner noise. Magn Reson Med 43:601–606PubMedCrossRefGoogle Scholar
  25. 25.
    Shah NJ, Jäncke L, Grosse-Ruyken M-L, Müller-Gärtner HW (1999) Influence of acoustic masking noise in fMRI of the auditory cortex during phonetic discrimination. J Magn Reson Imaging 9(1):19–25PubMedCrossRefGoogle Scholar
  26. 26.
    Talavage TM, Edmister WB, Ledden PJ, Weisskoff RM (1999) Quantitative assessment of auditory cortex responses induced by imager acoustic noise. Hum Brain Mapp 7(2):79–88PubMedCrossRefGoogle Scholar
  27. 27.
    Elliott MR, Bowtell RW, Morris PG (1999) The effect of scanner sound in visual, motor, and auditory functional MRI. Magn Reson Med 41(6):1230–1235PubMedCrossRefGoogle Scholar
  28. 28.
    Edmister WB, Talavage TM, Ledden PJ, Weisskoff RM (1999) Improved auditory cortex imaging using clustered volume acquisitions. Hum Brain Mapp 7:89–97PubMedCrossRefGoogle Scholar
  29. 29.
    Formisano E, Kim DS, Di Salle F, van de Moortele PF, Ugurbil K, Goebel R (2003) Mirror-symmetric tonotopic maps in human primary auditory cortex. Neuron 40(4):859–869PubMedCrossRefGoogle Scholar
  30. 30.
    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(3):107–119PubMedCrossRefGoogle Scholar
  31. 31.
    Hall DA, Haggard MP, Summerfield AQ, Akeroyd MA, Palmer AR, Bowtell RW (2001) Functional magnetic resonance imaging measurements of sound-level encoding in the absence of background scanner noise. J Acoust Soc Am 109(4):1559–1570PubMedCrossRefGoogle Scholar
  32. 32.
    Hart HC, Palmer AR, Hall DA (2004) Different areas of human non-primary auditory cortex are activated by sounds with spatial and nonspatial properties. Hum Brain Mapp 21:178–190PubMedCrossRefGoogle Scholar
  33. 33.
    Langers DRM, Backes WH, Van Dijk P (2007) Representation of lateralization and tonotopy in primary versus secondary human auditory cortex. Neuroimage 34:264–273PubMedCrossRefGoogle Scholar
  34. 34.
    Schwarzbauer C, Davis MH, Rodd JM, Johnsrude I (2006) Interleaved silent steady state (ISSS) imaging: a new sparse imaging method applied to auditory fMRI. Neuroimage 29(3):774–782PubMedCrossRefGoogle Scholar
  35. 35.
    Bregman AS (1990) Auditory scene analysis: the perceptual organisation of sound. MIT, Cambridge, MAGoogle Scholar
  36. 36.
    Fishman YI, Arezzo JC, Steinschneider M (2004) Auditory stream segregation in monkey auditory cortex: effects of frequency separation, presentation rate, and tone duration. J Acoust Soc Am 116(3):1656–1670PubMedCrossRefGoogle Scholar
  37. 37.
    Fishman YI, Reser DH, Arezzo JC, Steinschneider M (2001) Neural correlates of auditory stream segregation in primary auditory cortex of the awake monkey. Hear Res 151:167–187PubMedCrossRefGoogle Scholar
  38. 38.
    Brosch M, Schreiner CE (1997) Time course of forward masking tuning curves in cat primary auditory cortex. J Neurophysiol 77:923–943PubMedGoogle Scholar
  39. 39.
    Bartlett EL, Wang X (2005) Long-lasting modulation by stimulus context in primate auditory cortex. J Neurophysiol 94:83–104PubMedCrossRefGoogle Scholar
  40. 40.
    Harms MP, Guinan JJ, Sigalovsky IS, Melcher JR (2005) Short-term sound temporal envelope characteristics determine multisecond time patterns of activity in human auditory cortex as shown by fMRI. J Neurophysiol 93:210–222PubMedCrossRefGoogle Scholar
  41. 41.
    Palmer AR, Hall DA, Sumner C, Barrett DJK, Jones S, Nakamoto K, Moore DR (2007) Some investigations into non-passive listening. Hear Res 229:148–157PubMedCrossRefGoogle Scholar
  42. 42.
    Hall DA, Edmondson-Jones M, Fridriksson J (2006) Periodicity and frequency coding in human auditory cortex. Eur J Neurosci 24:3601–3610PubMedCrossRefGoogle Scholar
  43. 43.
    Hall DA, Johnsrude IS, Haggard MP, Palmer AR, Akeroyd MA, Summerfield AQ (2002) Spectral and temporal processing in human auditory cortex. Cereb Cortex 12:140–149PubMedCrossRefGoogle Scholar
  44. 44.
    Hart HC, Hall DA, Palmer AR (2003) The sound-level-dependent growth in the extent of fMRI activation in Heschl’s gyrus is different for low- and high-frequency tones. Hear Res 179(1–2):104–112PubMedCrossRefGoogle Scholar
  45. 45.
    Von Békésy G (1947) The variations of phase along the basilar membrane with sinusoidal vibrations. J Acoust Soc Am 19:452–460CrossRefGoogle Scholar
  46. 46.
    Kosaki H, Hashikawa T, He J, Jones EG (1997) Tonotopic organization of auditory cortical fields delineated by parvalbumin immunoreactivity in macaque monkeys. J Comp Neurol 386:304–316PubMedCrossRefGoogle Scholar
  47. 47.
    Merzenich MM, Brugge JF (1973) Representation of the cochlear partition on the superior temporal plane of the macaque monkey. Brain Res 50:275–296PubMedCrossRefGoogle Scholar
  48. 48.
    Petkov CL, Kayser C, Augath M, Logothetis NK (2006) Functional imaging reveals numerous fields in the monkey auditory cortex. PLoS Biol 4(7):213–226CrossRefGoogle Scholar
  49. 49.
    Hall DA, Hart HC, Johnsrude IS (2003) Relationships between human auditory cortical structure and function. Audiol Neurootol 8(1):1–18PubMedCrossRefGoogle Scholar
  50. 50.
    Schönwiesner M, Von Cramon DY, Rubsamen R (2002) Is it tonotopy after all? Neuroimage 17:1144–1161PubMedCrossRefGoogle Scholar
  51. 51.
    Talavage TM, Ledden PJ, Benson RR, Rosen BR, Melcher JR (2000) Frequency-dependent responses exhibited by multiple regions in human auditory cortex. Hear Res 150:225–244PubMedCrossRefGoogle Scholar
  52. 52.
    Talavage TM, Sereno MI, Melcher JR, Ledden PJ, Rosen BR, Dale AM (2004) Tonotopic organization in human auditory cortex revealed by progressions of frequency sensitivity. J Neurophysiol 91:1282–1296PubMedCrossRefGoogle Scholar
  53. 53.
    Kastner S, Ungerleider LG (2000) Mechanisms of visual attention in the human cortex. Annu Rev Neurosci 23(1):315–341PubMedCrossRefGoogle Scholar
  54. 54.
    Maunsell JHR, Treue S (2006) Feature-based attention in visual cortex. Trends Neurosci 29(6):317–322PubMedCrossRefGoogle Scholar
  55. 55.
    Scholl BJ (2001) Objects and attention: the state of the art. Cognition 80(1–2):1–46PubMedCrossRefGoogle Scholar
  56. 56.
    Griffiths TD, Warren JD (2004) What is an auditory object? Nat Rev Neurosci 5(11):887–892PubMedCrossRefGoogle Scholar
  57. 57.
    Johnson JA, Zatorre RJ (2005) Attention to simultaneous unrelated auditory and visual events: behavioral and neural correlates. Cereb Cortex 15(10):1609–1620PubMedCrossRefGoogle Scholar
  58. 58.
    Johnson JA, Zatorre RJ (2006) Neural substrates for dividing and focusing attention between simultaneous auditory and visual events. Neuroimage 31(4):1673–1681PubMedCrossRefGoogle Scholar
  59. 59.
    Lavie N (2005) Distracted and confused? Selective attention under load. Trends Cogn Sci 9(2):75–82PubMedCrossRefGoogle Scholar
  60. 60.
    Degerman A, Rinne T, Salmi J, Salonen O, Alho K (2006) Selective attention to sound location or pitch studied with fMRI. Brain Res 1077(1):123–134PubMedCrossRefGoogle Scholar
  61. 61.
    Petkov CI, Kang X, Alho K, Bertrand O, Yund EW, Woods DL (2004) Attentional modulation of human auditory cortex. Nat Neurosci 7(6):658–663PubMedCrossRefGoogle Scholar
  62. 62.
    Kayser C, Petkov CI, Augath M, Logothetis NK (2007) Functional imaging reveals visual modulation of specific fields in auditory cortex. J Neurosci 27(8):1824–1835PubMedCrossRefGoogle Scholar
  63. 63.
    Lehmann C, Herdener M, Esposito F, Hubl D, di Salle F, Scheffler K, Bach DR, Federspiel A, Kretz R, Dierks T, Seifritz E (2006) Differential patterns of multisensory interactions in core and belt areas of human auditory cortex. Neuroimage 31(1):294–300PubMedCrossRefGoogle Scholar
  64. 64.
    Ahveninen J, Jaaskelainen IP, Raij T, Bonmassar G, Devore S, Hamalainen M, Levanen S, Lin F-H, Sams M, Shinn-Cunningham BG, Witzel T, Belliveau JW (2006) Task-modulated “what” and “where” pathways in human auditory cortex. Proc Natl Acad Sci U S A 103(39):14608–14613PubMedPubMedCentralCrossRefGoogle Scholar
  65. 65.
    Lewald J, Meister IG, Weidemann J, Topper R (2004) Involvement of the superior temporal cortex and the occipital cortex in spatial hearing: evidence from repetitive transcranial magnetic stimulation. J Cogn Neurosci 16(5):828–838PubMedCrossRefGoogle Scholar
  66. 66.
    Degerman A, Rinne T, Pekkola J, Autti T, Jaaskelainen IP, Sams M, Alho K (2007) Human brain activity associated with audiovisual perception and attention. Neuroimage 34(4):1683–1691PubMedCrossRefGoogle Scholar
  67. 67.
    Greenberg GZ, Larkin WD (1968) Frequency-response characteristic of auditory observers detecting signals of a single frequency in noise: the probe-signal method. J Acoust Soc Am 44(6):1513–1523PubMedCrossRefGoogle Scholar
  68. 68.
    Schlauch RS, Hafter ER (1991) Listening bandwidths and frequency uncertainty in pure-tone signal detection. J Acoust Soc Am 90(3):1332–1339PubMedCrossRefGoogle Scholar
  69. 69.
    Fritz JB, Elhilali M, David SV, Shamma SA (2007) Does attention play a role in dynamic receptive field adaptation to changing acoustic salience in A1? Hear Res 229:186–203PubMedPubMedCentralCrossRefGoogle Scholar
  70. 70.
    Shackleton TM, Carlyon RP (1994) The role of resolved and unresolved harmonics in pitch perception and frequency modulation discrimination. J Acoust Soc Am 95:3529–3540PubMedCrossRefGoogle Scholar
  71. 71.
    Penagos H, Melcher JR, Oxenham AJ (2004) A neural representation of pitch salience in nonprimary human auditory cortex revealed with functional magnetic resonance imaging. J Neurosci 24(30):6810–6815PubMedPubMedCentralCrossRefGoogle Scholar
  72. 72.
    Griffiths TD, Büchel C, Frackowiak RSJ, Patterson RD (1998) Analysis of temporal structure in sound by the human brain. Nat Neurosci 1:422–427PubMedCrossRefGoogle Scholar
  73. 73.
    Blauert J, Lindemann W (1986) Spatial mapping of intracranial auditory events for various degrees of interaural coherence. J Acoust Soc Am 79(3):806–813PubMedCrossRefGoogle Scholar
  74. 74.
    Budd TW, Hall DA, Goncalves MS, Akeroyd MA, Foster JR, Palmer AR, Head K, Summerfield AQ (2003) Binaural specialisation in human auditory cortex: an fMRI investigation of interaural correlation sensitivity. Neuroimage 20(3):1783–1794PubMedCrossRefGoogle Scholar
  75. 75.
    Culling JF, Colburn HS, Spurchise M (2001) Interaural correlation sensitivity. J Acoust Soc Am 110(2):1020–1029PubMedCrossRefGoogle Scholar
  76. 76.
    Griffiths TD, Uppenkamp S, Johnsrude I, Josephs O, Patterson RD (2001) Encoding of the temporal regularity of sound in the human brainstem. Nat Neurosci 4:633–637PubMedCrossRefGoogle Scholar
  77. 77.
    Scheich H, Brechmann A, Brosch M, Budinger E, Ohl FW (2007) The cognitive auditory cortex: task-specificity of stimulus representations. Hear Res 229:213–224PubMedCrossRefGoogle Scholar
  78. 78.
    Brechmann A, Scheich H (2005) Hemispheric shifts of sound representation in auditory cortex with conceptual listening. Cereb Cortex 15(5):578–587PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2016

Authors and Affiliations

  1. 1.MRC Institute of Hearing ResearchNottinghamUK

Personalised recommendations