Tuning to Binaural Cues in Human Auditory Cortex

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• 作者：Susan A. McLaughlin ; Nathan C. Higgins…
• 关键词：auditory space ; fMRI ; ILD ; ITD ; hemispheric asymmetry ; interaural differences
• 刊名：JARO - Journal of the Association for Research in Otolaryngology
• 出版年：2016
• 出版时间：February 2016
• 年：2016
• 卷：17
• 期：1
• 页码：37-53
• 全文大小：2,716 KB
• 参考文献：Aguirre GK (2007) Continuous carry-over designs for fMRI. Neuroimage 35(4):1480–1494PubMedCentral CrossRef PubMed
  Ahveninen J, Jääskeläinen IP, Raij T, Bonmassar G, Devore S, Hämäläinen M, Levänen 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):14608–14613PubMedCentral CrossRef PubMed
  Altman JA, Balonov LJ, Deglin VL (1979) Effects of unilateral disorder of the brain hemisphere function in man on directional hearing. Neuropsychologia 17(3–4):295–301CrossRef PubMed
  Altmann CF, Terada S, Kashino M, Goto K, Mima T, Fukuyama H, Furukawa S (2014) Independent or integrated processing of interaural time and level differences in human auditory cortex? Hear Res 312:121–127CrossRef PubMed
  Baumann S, Petkov CI, Griffiths TD (2013) A unified framework for the organization of the primate auditory cortex. Front Syst Neurosci 7:11PubMedCentral CrossRef PubMed
  Beckmann CF, Smith SM (2004) Probabilistic independent component analysis for functional magnetic resonance imaging. IEEE Trans Med Imaging 23(2):137–152CrossRef PubMed
  Belliveau LAC, Lyamzin DR, Lesica NA (2014) The neural representation of interaural time differences in gerbils is transformed from midbrain to cortex. J Neurosci 34(50):16796–16808PubMedCentral CrossRef PubMed
  Benjamini Y, Hochberg Y (1995) Controlling the false discovery rate: a practical and powerful approach to multiple testing. J Roy Stat Soc B 57(1):289–300
  Bisiach E, Cornacchia L, Sterzi R, Vallar G (1984) Disorders of perceived auditory lateralization after lesions of the right hemisphere. Brain 107(Pt 1):37–52CrossRef PubMed
  Blauert J (1983) Spatial hearing. MIT Press, Cambridge
  Boester L (1994) Binaural time and intensity discrimination following unilateral auditory cortex ablation in Japanese macaques (Macaca fuscata). Master’s thesis, University of Toledo, Toledo
  Briley PM, Kitterick PT, Summerfield AQ (2013) Evidence for opponent process analysis of sound source location in humans. J Assoc Res Otolaryngol 14(1):83–101PubMedCentral CrossRef PubMed
  Brungart DS, Rabinowitz WM (1999) Auditory localization of nearby sources: head-related transfer functions. J Acoust Soc Am 106(3 Pt 1):1465–1479CrossRef PubMed
  Campbell RAA, Schnupp JWH, Shial A, King AJ (2006) Binaural-level functions in ferret auditory cortex: evidence for a continuous distribution of response properties. J Neurophysiol 95(6):3742–3755CrossRef PubMed
  Corbetta M, Patel G, Shulman GL (2008) The reorienting system of the human brain: from environment to theory of mind. Neuron 58(3):306–324PubMedCentral CrossRef PubMed
  Culling JF, Hawley ML, Litovsky RY (2004) The role of head-induced interaural time and level differences in the speech reception threshold for multiple interfering sound sources. J Acoust Soc Am 116(2):1057–1065CrossRef PubMed
  Deouell L, Heller A, Malach R, D’Esposito M, Knight R (2007) Cerebral responses to change in spatial location of unattended sounds. Neuron 55(6):985–996CrossRef PubMed
  Desikan RS, Ségonne F, Fischl B, Quinn BT, Dickerson BC, Blacker D, Buckner RL, Dale AM, Maguire RP, Hyman BT, Albert MS, Killiany RJ (2006) An automated labeling system for subdividing the human cerebral cortex on MRI scans into gyral based regions of interest. Neuroimage 31(3):968–980CrossRef PubMed
  Downar J, Crawley AP, Mikulis DJ, Davis KD (2000) A multimodal cortical network for the detection of changes in the sensory environment. Nat Neurosci 3(3):277–283CrossRef PubMed
  Edmonds BA, Krumbholz K (2014) Are interaural time and level differences represented by independent or integrated codes in the human auditory cortex? J Assoc Res Otolaryngol 15(1):103–114PubMedCentral CrossRef PubMed
  Fitzpatrick DC, Kuwada S, Batra R (2000) Neural sensitivity to interaural time differences: beyond the Jeffress model. J Neurosci 20(4):1605–1615PubMed
  Friston KJ, Holmes AP, Poline JB, Grasby PJ, Williams SC, Frackowiak RS, Turner R (1995) Analysis of fMRI time-series revisited. Neuroimage 2(1):45–53CrossRef PubMed
  Furukawa S, Middlebrooks JC (2002) Cortical representation of auditory space: information-bearing features of spike patterns. J Neurophysiol 87(4):1749–1762PubMed
  Genovese CR, Lazar NA, Nichols T (2002) Thresholding of statistical maps in functional neuroimaging using the false discovery rate. Neuroimage 15(4):870–878CrossRef PubMed
  Griffiths T, Buchel C, Frackowiak R, Patterson R (1998) Analysis of the temporal structure of sound by the human brain. Nat Neurosci 1(5):422–427CrossRef PubMed
  Griffiths TD, Uppenkamp S, Johnsrude I, Josephs O, Patterson R (2001) Encoding of the temporal regularity of sound in the human brainstem. Nat Neurosci 4(6):633–637CrossRef PubMed
  Hackett T, Stepniewska I, Kaas J (1998) Subdivisions of auditory cortex and ipsilateral cortical connections of the parabelt auditory cortex in macaque monkeys. J Comp Neurol 394(4):475–495CrossRef PubMed
  Hall DA, Haggard M, Akeroyd M, Palmer AR, Summerfield AQ, Elliott M, Gurney E, Bowtell R (1999) Sparse temporal sampling in auditory fMRI. Hum Brain Mapp 7(3):213–223CrossRef PubMed
  Hall D, Barrett D, Akeroyd M, Summerfield A (2005) Cortical representations of temporal structure in sound. J Neurophysiol 94(5):3181–3191CrossRef PubMed
  Harrington IA, Stecker GC, Macpherson EA, Middlebrooks JC (2008) Spatial sensitivity of neurons in the anterior, posterior, and primary fields of cat auditory cortex. Hear Res 240:22–41PubMedCentral CrossRef PubMed
  Haynes J-D, Rees G (2005) Predicting the orientation of invisible stimuli from activity in human primary visual cortex. Nat Neurosci 8(5):686–690CrossRef PubMed
  Heffner HE (1997) The role of macaque auditory cortex in sound localization. Acta Otolaryngol Suppl 532:22–27CrossRef PubMed
  Higgins NC, Storace DA, Escabi MA, Read HL (2010) Specialization of binaural responses in ventral auditory cortices. J Neurosci 30(43):14522–14532PubMedCentral CrossRef PubMed
  Imig TJ, Adrián HO (1977) Binaural columns in the primary field (A1) of cat auditory cortex. Brain Res 138(2):241–257CrossRef PubMed
  Jäncke L, Wüstenberg T, Schulze K, Heinze HJ (2002) Asymmetric hemodynamic responses of the human auditory cortex to monaural and binaural stimulation. Hear Res 170(1–2):166–178CrossRef PubMed
  Jenkins WM, Masterton RB (1982) Sound localization: effects of unilateral lesions in central auditory system. J Neurophysiol 47(6):987–1016PubMed
  Johnson BW, Hautus MJ (2010) Processing of binaural spatial information in human auditory cortex: neuromagnetic responses to interaural timing and level differences. Neuropsychologia 48(9):2610–2619CrossRef PubMed
  Kaas J, Hackett T (2000) Subdivisions of auditory cortex and processing streams in primates. Proc Natl Acad Sci U S A 97(22):11793–11799PubMedCentral CrossRef PubMed
  Kamitani Y, Tong F (2005) Decoding the visual and subjective contents of the human brain. Nat Neurosci 8(5):679–685PubMedCentral CrossRef PubMed
  Kavanagh GL, Kelly JB (1987) Contribution of auditory cortex to sound localization by the ferret (Mustela putorius). J Neurophysiol 57(6):1746–1766PubMed
  Kelly RE Jr, Alexopoulos GS, Wang Z, Gunning FM, Murphy CF, Morimoto SS, Kanellopoulos D, Jia Z, Lim KO, Hoptman MJ (2010) Visual inspection of independent components: defining a procedure for artifact removal from fMRI data. J Neurosci Methods 189(2):233–245PubMedCentral CrossRef PubMed
  Kitzes L (2008) Binaural interactions shape binaural response structures and frequency response functions in primary auditory cortex. Hear Res 238(1–2):68–76CrossRef PubMed
  Krumbholz K, Schönwiesner M, von Cramon DY, Rübsamen R, Shah NJ, Zilles K, Fink GR (2005a) Representation of interaural temporal information from left and right auditory space in the human planum temporale and inferior parietal lobe. Cereb Cortex 15(3):317–324CrossRef PubMed
  Krumbholz K, Schönwiesner S, Rübsamen R, Zilles K, Fink G, von Cramon DY (2005b) Hierarchical processing of sound location and motion in the human brainstem and planum temporale. Eur J Neurosci 21(1):230–238CrossRef PubMed
  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(2):1649–1655CrossRef PubMed
  Kucyi A, Hodaie M, Davis KD (2012) Lateralization in intrinsic functional connectivity of the temporoparietal junction with salience- and attention-related brain networks. J Neurophysiol 108(12):3382–3392CrossRef PubMed
  Kuhn G (1977) Model for interaural time differences in the azimuthal plane. J Acoust Soc Am 62(157–67)
  Langers DRM, Backes WH, van Dijk P (2007) Representation of lateralization and tonotopy in primary versus secondary human auditory cortex. Neuroimage 34(1):264–273CrossRef PubMed
  Lau C, Zhang JW, Cheng JS, Zhou IY, Cheung MM, Wu EX (2013) Noninvasive fMRI investigation of interaural level difference processing in the rat auditory subcortex. PLoS One 8(8), e70706PubMedCentral CrossRef PubMed
  Licklider J (1948) The influence of interaural phase relations upon the masking of speech by white noise. J Acoust Soc Am 20(2):150–159CrossRef
  Lomber SG, Malhotra S, Hall AJ (2007) Functional specialization in non-primary auditory cortex of the cat: areal and laminar contributions to sound localization. Hear Res 229(1–2):31–45CrossRef PubMed
  Lui LL, Mokri Y, Reser DH, Rosa MGP, Rajan R (2015) Responses of neurons in the marmoset primary auditory cortex to interaural level differences: comparison of pure tones and vocalizations. Front Neurosci 9:132PubMedCentral CrossRef PubMed
  Macaulay EJ, Hartmann WM, Rakerd B (2010) The acoustical bright spot and mislocalization of tones by human listeners. J Acoust Soc Am 127(3):1440–1449PubMedCentral CrossRef PubMed
  Macpherson EA, Middlebrooks JC (2002) Listener weighting of cues for lateral angle: the duplex theory of sound localization revisited. J Acoust Soc Am 111(5 Pt 1):2219–2236CrossRef PubMed
  Magezi DA, Krumbholz K (2010) Evidence for opponent-channel coding of interaural time differences in human auditory cortex. J Neurophysiol 104(4):1997–2007PubMedCentral CrossRef PubMed
  Malhotra S, Hall AJ, Lomber SG (2004) Cortical control of sound localization in the cat: unilateral cooling deactivation of 19 cerebral areas. J Neurophysiol 92(3):1625–1643CrossRef PubMed
  McAlpine D, Jiang D, Palmer AR (2001) A neural code for low-frequency sound localization in mammals. Nat Neurosci 4(4):396–401CrossRef PubMed
  McLaughlin SA (2013) Functional magnetic resonance imaging of human auditory cortical tuning to interaural level and time differences. PhD thesis, University of Washington
  Middlebrooks JC, Bremen P (2013) Spatial stream segregation by auditory cortical neurons. J Neurosci 33(27):10986–11001PubMedCentral CrossRef PubMed
  Middlebrooks JC, Pettigrew JD (1981) Functional classes of neurons in primary auditory cortex of the cat distinguished by sensitivity to sound location. J Neurosci 1(1):107–120PubMed
  Nakamoto KT, Zhang J, Kitzes LM (2004) Response patterns along an isofrequency contour in cat primary auditory cortex (AI) to stimuli varying in average and interaural levels. J Neurophysiol 91(1):118–135CrossRef PubMed
  Nichols TE, Holmes AP (2002) Nonparametric permutation tests for functional neuroimaging: a primer with examples. Hum Brain Mapp 15(1):1–25CrossRef PubMed
  Nourski KV, Steinschneider M, McMurray B, Kovach CK, Oya H, Kawasaki H, Howard MA 3rd (2014) Functional organization of human auditory cortex: investigation of response latencies through direct recordings. Neuroimage 101:598–609PubMedCentral CrossRef PubMed
  Oldfield R (1971) The assessment and analysis of handedness: the Edinburgh inventory. Neuropsychologia 9:97–113CrossRef PubMed
  Palmer A, Kuwada S (2005) Binaural and spatial coding in the inferior colliculus. In: Winer JA, S. C. (eds) The inferior colliculus. Springer, New York, chapter 13, 377–410
  Palomäki KJ, Tiitinen H, Mäkinen V, May PJC, Alku P (2005) Spatial processing in human auditory cortex: the effects of 3D, ITD, and ILD stimulation techniques. Brain Res Cogn Brain Res 24(3):364–379CrossRef PubMed
  Patterson RD, Uppenkamp S, Johnsrude IS, Griffiths TD (2002) The processing of temporal pitch and melody information in auditory cortex. Neuron 36(4):767–776CrossRef PubMed
  Phillips DP, Hall SE (2005) Psychophysical evidence for adaptation of central auditory processors for interaural differences in time and level. Hear Res 202(1–2):188–199CrossRef PubMed
  Phillips DP, Irvine DR (1981) Responses of single neurons in physiologically defined area A1 of cat cerebral cortex: sensitivity to interaural intensity differences. Hear Res 4(3–4):299–307CrossRef PubMed
  Poldrack RA (2007) Region of interest analysis for fMRI. Soc Cogn Affect Neurosci 2(1):67–70PubMedCentral CrossRef PubMed
  Rauschecker J, Tian B (2000) Mechanisms and streams for processing of “what” and “where” in auditory cortex. Proc Natl Acad Sci U S A 97(22):11800–11806PubMedCentral CrossRef PubMed
  Reale RA, Brugge JF (1990) Auditory cortical neurons are sensitive to static and continuously changing interaural phase cues. J Neurophysiol 64(4):1247–1260PubMed
  Ruff RM, Hersh NA, Pribram KH (1981) Auditory spatial deficits in the personal and extrapersonal frames of reference due to cortical lesions. Neuropsychologia 19(3):435–443CrossRef PubMed
  Salminen NH (2015) Human cortical sensitivity to interaural level differences in low- and high-frequency sounds. J Acoust Soc Am 137(2):EL190–EL193CrossRef PubMed
  Salminen NH, Tiitinen H, Miettinen I, Alku P, May PJC (2010) Asymmetrical representation of auditory space in human cortex. Brain Res 1306:93–99CrossRef PubMed
  Salminen NH, Altoè A, Takanen M, Santala O, Pulkki V (2015a) Human cortical sensitivity to interaural time difference in high-frequency sounds. Hear Res 323:99–106CrossRef PubMed
  Salminen NH, Takanen M, Santala O, Alku P, Pulkki V (2015b) Neural realignment of spatially separated sound components. J Acoust Soc Am 137(6):3356CrossRef PubMed
  Salminen NH, Takanen M, Santala O, Lamminsalo J, Altoè A, Pulkki V (2015c) Integrated processing of spatial cues in human auditory cortex. Hear Res 327:143–152CrossRef PubMed
  Schröger E (1996) Interaural time and level differences: integrated or separated processing? Hear Res 96(1–2):191–198CrossRef PubMed
  Smith SM, Jenkinson M, Woolrich MW, Beckmann CF, Behrens TEJ, Johansen Berg H, Bannister PR, De Luca M, Drobnjak I, Flitney DE, Niazy RK, Saunders J, Vickers J, Zhang Y, De Stefano N, Brady JM, Matthews PM (2004) Advances in functional and structural MR image analysis and implementation as FSL. Neuroimage 23(Suppl 1):S208–S219CrossRef PubMed
  Spierer L, Bellmann-Thiran A, Maeder P, Murray MM, Clarke S (2009) Hemispheric competence for auditory spatial representation. Brain 132(Pt 7):1953–1966CrossRef PubMed
  Stecker GC (2010) More modeling of temporal weighting functions for interaural time and level differences. Assoc Res Otolaryngol Abs 33:831
  Stecker GC, Middlebrooks JC (2003) Distributed coding of sound locations in the auditory cortex. Biol Cybern 89(5):341–349CrossRef PubMed
  Stecker GC, Mickey B, Macpherson E, Middlebrooks J (2003) Spatial sensitivity in field PAF of cat auditory cortex. J Neurophysiol 89:2889–2903CrossRef PubMed
  Stecker GC, Harrington I, Macpherson E, Middlebrooks J (2005a) Spatial sensitivity in the dorsal zone (area DZ) of cat auditory cortex. J Neurophysiol 94(2):1267–1280CrossRef PubMed
  Stecker GC, Harrington IA, Middlebrooks JC (2005b) Location coding by opponent neural populations in the auditory cortex. PLoS Biol 3(3):e78PubMedCentral CrossRef PubMed
  Stecker GC, McLaughlin SA, Higgins NC (2015) Monaural and binaural contributions to interaural-level-difference sensitivity in human auditory cortex. Neuroimage
  Stevens MC, Calhoun VD, Kiehl KA (2005) Hemispheric differences in hemodynamics elicited by auditory oddball stimuli. Neuroimage 26(3):782–792PubMedCentral CrossRef PubMed
  Tardif E, Murray MM, Meylan R, Spierer L, Clarke S (2006) The spatiotemporal brain dynamics of processing and integrating sound localization cues in humans. Brain Res 1092(1):161–176CrossRef PubMed
  Thompson GC, Cortez AM (1983) The inability of squirrel monkeys to localize sound after unilateral ablation of auditory cortex. Behav Brain Res 8(2):211–216CrossRef PubMed
  Tiitinen H, Salminen NH, Palomäki KJ, Mäkinen VT, Alku P, May PJC (2006) Neuromagnetic recordings reveal the temporal dynamics of auditory spatial processing in the human cortex. Neurosci Lett 396(1):17–22CrossRef PubMed
  Trahiotis C, Stern RM (1989) Lateralization of bands of noise: effects of bandwidth and differences of interaural time and phase. J Acoust Soc Am 86(4):1285–1293CrossRef PubMed
  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(3):485–498CrossRef PubMed
  von Kriegstein K, Griffiths TD, Thompson SK, McAlpine D (2008) Responses to interaural time delay in human cortex. J Neurophysiol 100(5):2712–2718CrossRef
  Warren JD, Griffiths TD (2003) Distinct mechanisms for processing spatial sequences and pitch sequences in the human auditory brain. J Neurosci 23(13):5799–5804PubMed
  Werner-Reiss U, Groh JM (2008) A rate code for sound azimuth in monkey auditory cortex: implications for human neuroimaging studies. J Neurosci 28(14):3747–3758PubMedCentral CrossRef PubMed
  Wise LZ, Irvine DR (1985) Topographic organization of interaural intensity difference sensitivity in deep layers of cat superior colliculus: implications for auditory spatial representation. J Neurophysiol 54(2):185–211PubMed
  Woldorff MG, Tempelmann C, Fell J, Tegeler C, Gaschler-Markefski B, Hinrichs H, Heinz HJ, Scheich H (1999) Lateralized auditory spatial perception and the contralaterality of cortical processing as studied with functional magnetic resonance imaging and magnetoencephalography. Hum Brain Mapp 7(1):49–66CrossRef PubMed
  Woods TM, Lopez SE, Long JH, Rahman JE, Recanzone GH (2006) Effects of stimulus azimuth and intensity on the single-neuron activity in the auditory cortex of the alert macaque monkey. J Neurophysiol 96(6):3323–3337CrossRef PubMed
  Woods D, Stecker GC, Rinne T, Herron T, Cate A, Yund EW, Liao I, Kang X (2009) Functional maps of human auditory cortex: effects of acoustic features and attention. PLoS One 4(4), e5183PubMedCentral CrossRef PubMed
  Yost WA, Dye RH, Sheft S (2007) Interaural time difference processing of broadband and narrow-band noise by inexperienced listeners. J Acoust Soc Am 121(3):EL103–EL109PubMedCentral CrossRef PubMed
  Zatorre RJ, Penhune VB (2001) Spatial localization after excision of human auditory cortex. J Neurosci 21(16):6321–6328PubMed
  Zhang J, Nakamoto KT, Kitzes LM (2004) Binaural interaction revisited in the cat primary auditory cortex. J Neurophysiol 91(1):101–117CrossRef PubMed
  
• 作者单位：Susan A. McLaughlin (1)
  Nathan C. Higgins (2)
  G. Christopher Stecker (2)
  
  1. Institute for Learning and Brain Sciences, University of Washington, Seattle, WA, USA
  2. Department of Hearing and Speech Sciences, Vanderbilt University School of Medicine, 1215 21st Ave South, Room 8310, Nashville, TN, 37232-8242, USA
  
• 刊物类别：Medicine
• 刊物主题：Medicine & Public Health
  Otorhinolaryngology
  Neurosciences
  Neurobiology
  
• 出版者：Springer New York
• ISSN：1438-7573

文摘

Interaural level and time differences (ILD and ITD), the primary binaural cues for sound localization in azimuth, are known to modulate the tuned responses of neurons in mammalian auditory cortex (AC). The majority of these neurons respond best to cue values that favor the contralateral ear, such that contralateral bias is evident in the overall population response and thereby expected in population-level functional imaging data. Human neuroimaging studies, however, have not consistently found contralaterally biased binaural response patterns. Here, we used functional magnetic resonance imaging (fMRI) to parametrically measure ILD and ITD tuning in human AC. For ILD, contralateral tuning was observed, using both univariate and multivoxel analyses, in posterior superior temporal gyrus (pSTG) in both hemispheres. Response-ILD functions were U-shaped, revealing responsiveness to both contralateral and—to a lesser degree—ipsilateral ILD values, consistent with rate coding by unequal populations of contralaterally and ipsilaterally tuned neurons. In contrast, for ITD, univariate analyses showed modest contralateral tuning only in left pSTG, characterized by a monotonic response-ITD function. A multivoxel classifier, however, revealed ITD coding in both hemispheres. Although sensitivity to ILD and ITD was distributed in similar AC regions, the differently shaped response functions and different response patterns across hemispheres suggest that basic ILD and ITD processes are not fully integrated in human AC. The results support opponent-channel theories of ILD but not necessarily ITD coding, the latter of which may involve multiple types of representation that differ across hemispheres. Keywords auditory space fMRI ILD ITD hemispheric asymmetry interaural differences