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. 2008 Jul 19;24(3):173–182. doi: 10.1007/s12264-008-1226-8

The dual-pathway model of auditory signal processing

听觉信号加工的双通路模型

Wen-Jie Wang 1, Xi-Hong Wu 1, Liang Li 1,
PMCID: PMC5552542  PMID: 18500391

Abstract

Similar to the visual dual-pathway model, neurophysiological studies in non-human primates have suggested that the dual-pathway model is also applicable for explaining auditory cortical processing, including the ventral “what” pathway for object identification and the dorsal “where” pathway for spatial localization. This review summarizes evidence from human neuroimaging studies supporting the dual-pathway model for auditory cortical processing in humans.

Keywords: auditory perception, auditory localization, auditory pattern recognition, functional MRI

References

  • [1].Bregman A.S. Auditory Scene Analysis. Cambridge, MA: MIT Press; 1990. [Google Scholar]
  • [2].Felleman D.J., Van Essen D.C. Distributed hierarchical processing in the primate cerebral cortex. Cereb Cortex. 1991;1:1–47. doi: 10.1093/cercor/1.1.1-a. [DOI] [PubMed] [Google Scholar]
  • [3].Ungerleider L.G., Mishkin M. Two cortical visual systems. In: Ingle D., Goodale M., Mansfield R., editors. Analysis of Visual Behavior. Cambridge, MA: MIT Press; 1982. pp. 49–86. [Google Scholar]
  • [4].Ungerleider L.G. Functional brain imaging studies of cortical mechanisms for memory. Science. 1995;270:769–775. doi: 10.1126/science.270.5237.769. [DOI] [PubMed] [Google Scholar]
  • [5].Goodale M.A., Milner A.D. Separate visual pathways for perception and action. Trends Neurosci. 1992;15:20–25. doi: 10.1016/0166-2236(92)90344-8. [DOI] [PubMed] [Google Scholar]
  • [6].Desimone R., Ungerleider L.G. Neural mechanisms of visual processing in monkeys. In: Boller F., Grafman J., editors. Handbook of Neuropsychology. Amsterdam: Elsevier; 1989. pp. 267–299. [Google Scholar]
  • [7].Goldberg M.E., Colby C. The neurophysiology of spatial vision. In: Boller F., Grafman J., editors. Handbook of Neuropsychology. Amsterdam: Elsevier; 1989. pp. 301–315. [Google Scholar]
  • [8].Kwong K.K., Belliveau J.W., Chesler D.A., Goldberg I.E., Weisskoff R.M., Poncelet B.P., et al. Dynamic magnetic resonance imaging of human brain activity during primary sensory stimulation. Proc Natl Acad Sci. 1992;89:5675–5679. doi: 10.1073/pnas.89.12.5675. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • [9].Ogawa S., Tank D.W., Menon R., Ellermann J.M., Kim S.G., Merkle H., et al. Intrinsic signal changes accompanying sensory stimulation: functional brain mapping with magnetic resonance imaging. Proc Natl Acad Sci. 1992;89:5951–5955. doi: 10.1073/pnas.89.13.5951. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • [10].Haxby J.V., Horwitz B., Ungerleider L.G., Maisog J.M., Pietrini P., Grady C.L. The functional organization of human extrastriate cortex: a PET-rCBF study of selective attention to faces and locations. J Neurosci. 1994;14:6336–6353. doi: 10.1523/JNEUROSCI.14-11-06336.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • [11].Ungerleider L.G., Haxby J.V. “what” and “where” in the human brain. Curr Opin Neurobiol. 1994;4:157–165. doi: 10.1016/0959-4388(94)90066-3. [DOI] [PubMed] [Google Scholar]
  • [12].Kastner S., Ungerleider L.G. Mechanisms of visual attention in the human cortex. Annu Rev Neurosci. 2000;23:315–341. doi: 10.1146/annurev.neuro.23.1.315. [DOI] [PubMed] [Google Scholar]
  • [13].Atzori M., Lei S., Evans D.I., Kanold P.O., Phillips-Tansey E., McIntyre O., et al. Differential synaptic processing separates stationary from transient inputs to the auditory cortex. Nat Neurosci. 2001;4:1230–1237. doi: 10.1038/nn760. [DOI] [PubMed] [Google Scholar]
  • [14].Miller L.M., Escabi M.A., Read H.L., Schreiner C.E. Functional convergence of response properties in the auditory thalamocortical system. Neuron. 2001;32:151–160. doi: 10.1016/S0896-6273(01)00445-7. [DOI] [PubMed] [Google Scholar]
  • [15].Zatorre R.J., Belin P., Penhune V.B. Structure and function of auditory cortex: music and speech. Trends Cogn Sci. 2002;6:37–46. doi: 10.1016/S1364-6613(00)01816-7. [DOI] [PubMed] [Google Scholar]
  • [16].Romanski L.M., Tian B., Fritz J.B., Mishkin M., Goldman-Rakic P.S., Rauschecker J.P. Dual streams of auditory afferents target multiple domains in the primate prefrontal cortex. Nat Neurosci. 1999;2:1131–1136. doi: 10.1038/16056. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • [17].Romanski L.M., Bates J.F., Goldman-Rakic P.S. Auditory belt and parabelt projections to the prefrontal cortex in the rhesus monkey. J Comp Neurol. 1999;403:141–157. doi: 10.1002/(SICI)1096-9861(19990111)403:2<141::AID-CNE1>3.0.CO;2-V. [DOI] [PubMed] [Google Scholar]
  • [18].Kaas J.H., Hackett T.A. Subdivisions of auditory cortex and processing streams in primates. Proc Natl Acad Sci. 2000;97:11793–11799. doi: 10.1073/pnas.97.22.11793. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • [19].Poremba A., Saunders R.C., Crane A.M., Cook M., Sokoloff L. Functional mapping of the primate auditory system. Science. 2003;299:568–572. doi: 10.1126/science.1078900. [DOI] [PubMed] [Google Scholar]
  • [20].Jones E.G., Dellanna M.E., Molinari M., Rausell E., Hashikawa T. Subdivisions of macaque monkey auditory cortex revealed by calcium-binding protein immunoreactivity. J Comp Neurol. 1995;362:153–170. doi: 10.1002/cne.903620202. [DOI] [PubMed] [Google Scholar]
  • [21].Hackett T.A., Stepniewska I., Kaas J.H. Subdivisions of auditory cortex and ipsilateral cortical connections of the parabelt auditory cortex in macaque monkeys. J Comp Neurol. 1998;394:475–495. doi: 10.1002/(SICI)1096-9861(19980518)394:4<475::AID-CNE6>3.0.CO;2-Z. [DOI] [PubMed] [Google Scholar]
  • [22].Hackett T.A., Stepniewska I., Kaas J.H. Thalamocortical connections of the parabelt auditory cortex in macaque monkeys. J Comp Neurol. 1998;400:271–286. doi: 10.1002/(SICI)1096-9861(19981019)400:2<271::AID-CNE8>3.0.CO;2-6. [DOI] [PubMed] [Google Scholar]
  • [23].Rauschecker J.P. Parallel processing in the auditory cortex of primates. Audiol Neurootol. 1998;3:86–103. doi: 10.1159/000013784. [DOI] [PubMed] [Google Scholar]
  • [24].Rauschecker J.P., Tian B. Mechanisms and streams for processing of “what” and “where” in auditory cortex. Proc Natl Acad Sci. 2000;97:11800–11806. doi: 10.1073/pnas.97.22.11800. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • [25].Tian B., Reser D., Durham A., Kustov A., Rauschecker J.P. Functional specialization in rhesus monkey auditory cortex. Science. 2001;292:290–293. doi: 10.1126/science.1058911. [DOI] [PubMed] [Google Scholar]
  • [26].Woods T.M., Lopez S.E., Long J.H., Rahman J.E., Recanzone G.H. Effects of stimulus azimuth and intensity on the single-neuron activity in the auditory cortex of the alert macaque monkey. J Neurophysiol. 2006;96:3323–3337. doi: 10.1152/jn.00392.2006. [DOI] [PubMed] [Google Scholar]
  • [27].Kaas J.H., Hackett T.A. “what” and “where” processing in auditory cortex. Nat Neurosci. 1999;2:1045–1047. doi: 10.1038/15967. [DOI] [PubMed] [Google Scholar]
  • [28].Romanski L.M., Tian B., Fritz J.B., Mishkin M., Goldman-Rakic P.S., Rauschecker J.P. Reply to “what”, “where” and “how” in auditory cortex. Nat Neurosci. 2000;3:966. doi: 10.1038/79892. [DOI] [PubMed] [Google Scholar]
  • [29].Hamalainen M., Hari R., Ilmoniemi R.J., Knuutila J., Lounasmaa O.V. Magnetoencephalography-theory, instrumentation, and applications to noninvasive studies of the working human brain. Reviews of Modern Physics. 1993;65:413–497. doi: 10.1103/RevModPhys.65.413. [DOI] [Google Scholar]
  • [30].Hackett T.A., Preuss T.M., Kaas J.H. Architectonic identification of the core region in auditory cortex of macaques, chimpanzees, and humans. J Comp Neurol. 2001;441:197–222. doi: 10.1002/cne.1407. [DOI] [PubMed] [Google Scholar]
  • [31].Fullerton B.C., Pandya D.N. Architectonic analysis of the auditory-related areas of the superior temporal region in human brain. J Comp Neurol. 2007;504:470–498. doi: 10.1002/cne.21432. [DOI] [PubMed] [Google Scholar]
  • [32].Wallace M.N., Johnston P.W., Palmer A.R. Histochemical identification of cortical areas in the auditory region of the human brain. Exp Brain Res. 2002;143:499–508. doi: 10.1007/s00221-002-1014-z. [DOI] [PubMed] [Google Scholar]
  • [33].Ratnanather J.T., Barta P.E., Honeycutt N.A., Lee N., Morris H.M., Dziorny A.C., et al. Dynamic programming generation of boundaries of local coordinatized submanifolds in the neocortex: application to the planum temporale. Neuroimage. 2003;20:359–377. doi: 10.1016/S1053-8119(03)00238-6. [DOI] [PubMed] [Google Scholar]
  • [34].Warren J.D., Griffiths T.D. Distinct mechanisms for processing spatial sequences and pitch sequences in the human auditory brain. J Neurosci. 2003;23:5799–5804. doi: 10.1523/JNEUROSCI.23-13-05799.2003. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • [35].Alain C., Arnott S.R., Hevenor S., Graham S., Grady C.L. “what” and “where” in the human auditory system. Proc Natl Acad Sci. 2001;98:12301–12306. doi: 10.1073/pnas.211209098. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • [36].Anurova I., Artchakov D., Korvenoja A., Ilmoniemi R.J., Aronen H.J., Carlson Sv. Cortical generators of slow evoked responses elicited by spatial and nonspatial auditory working memory tasks. Clin Neurophysiol. 2005;116:1644–1654. doi: 10.1016/j.clinph.2005.02.029. [DOI] [PubMed] [Google Scholar]
  • [37].Rämä P., Poremba A., Sala J.B., Yee L., Malloy M., Mishkin M., et al. Dissociable functional cortical topographies for working memory maintenance of voice identity and location. Cereb Cortex. 2004;14:768–780. doi: 10.1093/cercor/bhh037. [DOI] [PubMed] [Google Scholar]
  • [38].Arnott S.R., Grady C.L., Hevenor S.J., Graham S., Alain C. The functional organization of auditory working memory as revealed by fMRI. J Cogn Neurosci. 2005;17:819–831. doi: 10.1162/0898929053747612. [DOI] [PubMed] [Google Scholar]
  • [39].Maeder P.P., Meuli R.A., Adriani M., Bellmann A., Fornari E., Thiran J.P., et al. Distinct pathways involved in sound recognition and localization: A human fMRI study. Neuroimage. 2001;14:802–816. doi: 10.1006/nimg.2001.0888. [DOI] [PubMed] [Google Scholar]
  • [40].Warren J.D., Zielinski B.A., Green G.G., Rauschecker J.P., Griffiths T.D. Perception of sound-source motion by the human brain. Neuron. 2002;34:139–148. doi: 10.1016/S0896-6273(02)00637-2. [DOI] [PubMed] [Google Scholar]
  • [41].Griffiths T.D., Warren J.D. The planum temporale as a computational hub. Trends Neurosci. 2002;25:348–353. doi: 10.1016/S0166-2236(02)02191-4. [DOI] [PubMed] [Google Scholar]
  • [42].Barrett D.J.K., Hall D.A. Response preferences for “what” and “where” in human non-primary auditory cortex. Neuroimage. 2006;32:968–977. doi: 10.1016/j.neuroimage.2006.03.050. [DOI] [PubMed] [Google Scholar]
  • [43].Bar M., Kassam K.S., Ghuman A.S., Boshyan J., Schmid A.M., Dale A.M., et al. Top-down facilitation of visual recognition. Proc Natl Acad Sci. 2006;103:449–454. doi: 10.1073/pnas.0507062103. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • [44].Chen C.M., Lakatos P., Shah A.S., Mehta A.D., Givre S.J., Javitt D.C., et al. Functional anatomy and interaction of fast and slow visual pathways in macaque monkeys. Cereb Cortex. 2007;17:1561–1569. doi: 10.1093/cercor/bhl067. [DOI] [PubMed] [Google Scholar]
  • [45].Freyman R.L., Helfer K.S., McCall D.D., Clifton R.K. The role of perceived spatial separation in the unmasking of speech. J Acoust Soc Am. 1999;106:3578–3588. doi: 10.1121/1.428211. [DOI] [PubMed] [Google Scholar]
  • [46].Wu Y., Li W., Chen J., Wang C., Qu H., Wu X., et al. Informational masking of Chinese speech under perceived spatial separation. Chinese J. Acoustics (in Chinese) 2005;30:462–467. doi: 10.1016/j.heares.2004.03.010. [DOI] [PubMed] [Google Scholar]
  • [47].Jääskeläinen I.P., Ahveninen J., Bonmassar G., Dale A.M., Ilmoniemi R.J., Levänen S., et al. Human posterior auditory cortex gates novel sounds to consciousness. Proc Natl Acad Sci. 2004;101:6809–6814. doi: 10.1073/pnas.0303760101. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • [48].Ahveninen J., Jääskeläinen I.P., Raij T., Bonmassar G., Devore S., Hämäläinen M., et al. Task-modulated “what” and “where” pathways in human auditory cortex. Proc Natl Acad Sci. 2006;103:14608–14613. doi: 10.1073/pnas.0510480103. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • [49].De Santis L., Clarke S., Murray M.M. Automatic and intrinsic auditory “what” and “where” processing in humans revealed by electrical neuroimaging. Cereb Cortex. 2007;17:9–17. doi: 10.1093/cercor/bhj119. [DOI] [PubMed] [Google Scholar]
  • [50].Altmann C.F., Bledowski C., Wibral M., Kaiser J. Processing of location and pattern changes of natural sounds in the human auditory cortex. Neuroimage. 2007;35:1192–1200. doi: 10.1016/j.neuroimage.2007.01.007. [DOI] [PubMed] [Google Scholar]
  • [51].Sestieri C., Di Matteo R., Ferretti A., Del Gratta C., Caulo M., Tartaro A., et al. “What” versus “where” in the audiovisual domain: An fMRI study. Neuroimage. 2006;33:672–680. doi: 10.1016/j.neuroimage.2006.06.045. [DOI] [PubMed] [Google Scholar]
  • [52].Clarke S., Bellmann A., Meuli R.A., Assal G., Steck A.J. Auditory agnosia and auditory spatial deficits following left hemispheric lesions: evidence for distinct processing pathways. Neuropsychologia. 2000;38:797–807. doi: 10.1016/S0028-3932(99)00141-4. [DOI] [PubMed] [Google Scholar]
  • [53].Clarke S., Bellmann Thiran A., Maeder P., Adriani M., Vernet O., Regli L., et al. What and where in human audition: selective deficits following focal hemispheric lesions. Exp Brain Res. 2002;147:8–15. doi: 10.1007/s00221-002-1203-9. [DOI] [PubMed] [Google Scholar]
  • [54].Krumbholz K., Schönwiesner M., von Cramon D.Y., Rübsamen R., Shah N.J., Zilles K., et al. Representation of interaural temporal information from left and right auditory space in the human planum temporale and inferior parietal lobe. Cereb Cortex. 2005;15:317–324. doi: 10.1093/cercor/bhh133. [DOI] [PubMed] [Google Scholar]
  • [55].Rushworth M.F., Krams M., Passingham R.E. The attentional role of the left parietal cortex: The distinct lateralization and localization of motor attention in the human brain. J Cogn Neurosci. 2001;13:698–710. doi: 10.1162/089892901750363244. [DOI] [PubMed] [Google Scholar]
  • [56].Federspiel A., Volpe U., Horn H., Dierks T., Franck A., Vannini P., et al. Motion standstill leads to activation of inferior parietal lobe. Hum Brain Mapp. 2006;27:340–349. doi: 10.1002/hbm.20189. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • [57].Griffiths T.D., Rees G., Rees A., Green G.G., Witton C., Rowe D., et al. Right parietal cortex is involved in the perception of sound movement in humans. Nat Neurosci. 1998;1:74–79. doi: 10.1038/276. [DOI] [PubMed] [Google Scholar]
  • [58].Bushara K.O., Weeks R.A., Ishii K., Catalan M.J., Tian B., Rauschecker J.P., et al. Modality-specific frontal and parietal areas for auditory and visual spatial localization in humans. Nat Neurosci. 1999;2:759–766. doi: 10.1038/11239. [DOI] [PubMed] [Google Scholar]
  • [59].Warren J.D., Jennings A.R., Griffiths T.D. Analysis of the spectral envelope of sounds by the human brain. Neuroimage. 2005;24:1052–1057. doi: 10.1016/j.neuroimage.2004.10.031. [DOI] [PubMed] [Google Scholar]
  • [60].Belin P., Zatorre R.J., Lafaille P., Ahad P., Pike B. Voice-selective areas in human auditory cortex. Nature. 2000;403:309–312. doi: 10.1038/35002078. [DOI] [PubMed] [Google Scholar]
  • [61].Specht K., Reul J. Functional segregation of the temporal lobes into highly differentiated subsystems for auditory perception: an auditory rapid event-related fMRI-task. Neuroimage. 2003;20:1944–1954. doi: 10.1016/j.neuroimage.2003.07.034. [DOI] [PubMed] [Google Scholar]
  • [62].Arnott S.R., Binns M.A., Grady C.L., Alain C. Assessing the auditory dual-pathway model in humans. Neuroimage. 2004;22:401–408. doi: 10.1016/j.neuroimage.2004.01.014. [DOI] [PubMed] [Google Scholar]
  • [63].Belin P., Zatorre R.J. “What”, “where” and “how” in auditory cortex. Nat Neurosci. 2000;3:965–966. doi: 10.1038/79890. [DOI] [PubMed] [Google Scholar]

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