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Sound recognition and localization in man: specialized cortical networks and effects of acute circumscribed lesions

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Abstract

Functional imaging studies have shown that information relevant to sound recognition and sound localization are processed in anatomically distinct cortical networks. We have investigated the functional organization of these specialized networks by evaluating acute effects of circumscribed hemispheric lesions. Thirty patients with a primary unilateral hemispheric lesion, 15 with right-hemispheric damage (RHD) and 15 with left-hemispheric damage (LHD), were evaluated for their capacity to recognise environmental sounds, to localize sounds in space and to perceive sound motion. One patient with RHD and 2 with LHD had a selective deficit in sound recognition; 3 with RHD a selective deficit in sound localization; 2 with LHD a selective deficit in sound motion perception; 4 with RHD and 3 with LHD a combined deficit of sound localization and motion perception; 2 with RHD and 1 with LHD a combined deficit of sound recognition and motion perception; and 1 with LHD a combined deficit of sound recognition, localization and motion perception. Five patients with RHD and 6 with LHD had normal performance in all three domains. Deficient performance in sound recognition, sound localization and/or sound motion perception was always associated with a lesion that involved the shared auditory structures and the specialized What and/or Where networks, while normal performance was associated with lesions within or outside these territories. Thus, damage to regions known to be involved in auditory processing in normal subjects is necessary, but not sufficient for a deficit to occur. Lesions of a specialized network was not always associated with the corresponding deficit. Conversely, specific deficits tended not be associated predominantly with lesions of the corresponding network; e.g. deficits in auditory spatial tasks were observed in patients whose lesions involved to a larger extent the shared auditory structures and the specialized What network than the specialized Where network, and deficits in sound recognition in patients whose lesions involved mostly the shared auditory structures and to a varying degree the specialized What network. The human auditory cortex consists of functionally defined auditory areas, whose intrinsic organization is currently not understood. In particular, areas involved in the What and Where pathways can be conceived as: (1) specialized regions, in which lesions cause dysfunction limited to the damaged part; observed deficits should be then related to the specialization of the damaged region and their magnitude to the extent of the damage; or (2) specialized networks, in which lesions cause dysfunction that may spread over the two specialized networks; observed deficits may then not be related to the damaged region and their magnitude not proportional to the extent of the damage. Our results support strongly the network hypothesis.

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References

  • Alain C, Arnott SR, Hevenor S, Graham S, Grady CL (2001) "What" and "Where" in the human auditory system. Proc Natl Acad Sci USA 98:12301–12306

    Article  CAS  PubMed  Google Scholar 

  • Alexander MP, Warren RL (1988) Localization of callosal auditory pathways: a CT case study. Neurology 38:802–804

    CAS  PubMed  Google Scholar 

  • Altman J, Balanov L, Delgin V (1979) Effects of unilateral disorder of the brain hemispheric functions in man on directional hearing. Neuropsychologia 17:295–301

    CAS  PubMed  Google Scholar 

  • Anourova I, Nikouline VV, Ilmoniemi RJ, Hotta J, Aronen HJ, Carlson S (2001) Evidence for dissociation of spatial and nonspatial auditory information processing. Neuroimage 14:1268–1277

    CAS  PubMed  Google Scholar 

  • Baumgart F, Gaschler-Markefski B, Woldorff MG, Heinze H-J, Scheich H (1999) A movement-sensitive area in auditory cortex. Nature 400:724–726

    Google Scholar 

  • Belin P, Zatorre RJ (2000) "What," "where" and "how" in auditory cortex. Nat Neurosci 3(10):965–966

    CAS  PubMed  Google Scholar 

  • Belin P, Zilbovicius M, Crozier S, Thivard L, Fontaine A, Masure M-C, Samson Y (1998) Lateralization of speech and auditory temporal processing. J Cogn Neurosci 10:536–540

    Article  CAS  PubMed  Google Scholar 

  • Bellmann A (2001) Le traitement des données spatiales en audition: une approche neuropsychologique. Thèse de Doctorat en Psychologie, University of Geneva, Switzerland

  • Bellmann Thiran A, Clarke S (2003) Preserved use of spatial cues for sound segregation in a case of spatial deafness. Neuropsychologia 41:1254–1261

    Article  PubMed  Google Scholar 

  • Bellmann A, Meuli R, Clarke S (2001) Two types of auditory neglect. Brain 124:676–687

    CAS  PubMed  Google Scholar 

  • Binder JR, Frost JA, Hammeke TA, Bellgowan PSF, Springer JA, Kaufman JN, Possing ET (2000) Human temporal lobe activation by speech and nonspeech sounds. Cereb Cortex 10:512–528

    Article  CAS  PubMed  Google Scholar 

  • Bisiach E, Cornacchia L, Sterzi R, Vallar G (1984) Disorders of perceived auditory lateralization after lesions of the right hemisphere. Brain 107:37–52

    PubMed  Google Scholar 

  • Chiry O, Tardif E, Magistretti P, Clarke S (2003) Patterns of calcium binding proteins support parallel and hierarchical organization of human auditory areas. Eur J Neurosci 17(2):397–410

    Article  PubMed  Google Scholar 

  • Clarke S, Bellmann Thiran A (2003) Auditory neglect: What and Where in auditory space. Cortex (In press)

    Google Scholar 

  • Clarke S, Bellmann A, Ribaupierre F de, Assal G (1996) Non-verbal auditory recognition in normal subjects and brain-damaged patients: evidence for parallel processing. Neuropsychologia 34:587–603

    CAS  PubMed  Google Scholar 

  • Clarke S, Adriani M, Bellmann A (1998) Distinct short-term memory systems for sound content and sound localization. Neuroreport 9:3433–3437

    CAS  PubMed  Google Scholar 

  • 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 38:797–807

    CAS  PubMed  Google Scholar 

  • Clarke S, Bellmann Thiran A, Maeder P, Adriani M, Vernet O, Regli L, Cuisenaire O, Thiran J-Ph (2002) What and Where in human audition: selective deficits following focal hemispheric lesions. Exp Brain Res 147:8–15 DOI: 10.1007/s00221–002–1203–9

    Google Scholar 

  • Di Virgilio G, Clarke S (1997) Direct interhemispheric visual input to human speech areas. Hum Brain Mapp 5:347–354

    Article  Google Scholar 

  • Ducommun C, Murray MM, Thut G, Bellmann A, Viaud-Delmon I, Clarke S, Michel CM (2002) Segregated processing of auditory motion and auditory location: an ERP mapping study. Neuroimage 16:76–88

    Article  PubMed  Google Scholar 

  • Engelien A, Silbersweig D, Stern E, Huber W, Döring W, Frith C, Frackowiak RSJ (1995) The functional anatomy of recovery from auditory agnosia. A PET study of sound categorization in a neurological patient and normal controls. Brain 111:1395–1409

    Google Scholar 

  • Faglioni P, Spinnler H, Vignolo LA (1969) Contrasting behavior of right and left hemisphere-damaged patients on a discriminative and a semantic task of auditory recognition. Cortex 5:366–389

    CAS  PubMed  Google Scholar 

  • Frith CD, Friston KJ (1996) The role of the thalamus in "Top Down" modulation of attention to sound. Neuroimage 4:210–215

    Article  CAS  PubMed  Google Scholar 

  • Fujii T, Fukatsu R, Watabe S, Ohnuma A, Teramura K, Kimura I, Saso S, Kogure K (1990) Auditory sound agnosia without aphasia following a right lobe lesion. Cortex 26:263–268

    CAS  PubMed  Google Scholar 

  • Griffiths TD, Green GGR (1999) Cortical activation during perception of rotating wide-field acoustic stimulus. Neuroimage 10:84–90

    CAS  PubMed  Google Scholar 

  • Griffiths TD, Warren JD (2002) The planum temporale as a computational hub. Trends Neurosci 25:348–353

    Article  CAS  PubMed  Google Scholar 

  • Griffiths TD, Rees A, Witton C, Shakir RA, Henning GB, Green GGR (1996) Evidence for a sound movement area in the human cerebral cortex. Nature 383:425–427

    Google Scholar 

  • Griffiths TD, Rees A, Witton C, Cross PM, Shakir RA, Green GG (1997) Spatial and temporal auditory processing deficits following right hemisphere infarction. A psychophysical study. Brain 120:785–794

    PubMed  Google Scholar 

  • Hossmann KA (1994) Viability thresholds and the penumbra of focal ischemia. Ann Neurol 36:557–65

    CAS  PubMed  Google Scholar 

  • Jerger J, Loverling L, Wertz M (1972) Auditory disorder following bilateral temporal lobe insult: report of a case. J Speech Hear Disord 37:523–535

    CAS  PubMed  Google Scholar 

  • Kaas JH, Hackett TA, Tramo MJ (1999) Auditory processing in primate cerebral cortex. Curr Opin Neurobiol 9:164–170

    CAS  PubMed  Google Scholar 

  • Liepert J, Storch P, Fritsch A, Weiller C (2000) Motor cortex disinhibition in acute stroke. Clin Neurophysiol 111:671–676

    Article  CAS  PubMed  Google Scholar 

  • Maeder P, Meuli R, Adriani M, Bellmann A, Fornari E, Thiran J-Ph, Pittet A, Clarke S (2001) Distinct pathways involved in sound recognition and localization: a human fMRI study. Neuroimage 14:802–816

    CAS  PubMed  Google Scholar 

  • Musso M, Weiller C, Kiebel S Muller SP, Bulau P, Rijntjes M (1999) Training-induced brain plasticity in aphasia. Brain 122:1781–1790

    PubMed  Google Scholar 

  • Pavani F, Macaluso E, Warren JD, Driver J, Griffiths TD (2002) A common cortical substrate activated horizontal and vertical sound movement in the human brain. Curr Biol 12:1584–1590

    CAS  PubMed  Google Scholar 

  • Price CJ, Warburton EA, Moore CJ, Frackowiak RS, Friston KJ (2001) Dynamic diaschisis: anatomically remote and context-sensitive human brain lesions. J Cogn Neurosci 13:419–29

    Article  CAS  PubMed  Google Scholar 

  • Rauschecker JP (1998) Parallel processing in the auditory cortex of primates. Audiol Neurootol 3:86–103

    CAS  PubMed  Google Scholar 

  • Rauschecker JP, Tian B (2000) Mechanisms and streams for processing of "what" and "where" in auditory cortex. Proc Natl Acad Sci USA 97:11800–11806

    Article  CAS  PubMed  Google Scholar 

  • Rauschecker JP, Tian B, Hauser M (1995) Processing of complex sounds in the macaque non primary auditory cortex. Science 268:111–114

    CAS  PubMed  Google Scholar 

  • Recanzone GH (2000) Spatial processing in the auditory cortex of the macaque monkey. Proc Natl Acad Sci USA 97:11829–11835

    Article  CAS  PubMed  Google Scholar 

  • Rivier F, Clarke S (1997) Cytochrome oxidase, acetylcholinesterase, and NADPH-diaphorase staining in human supratemporal and insular cortex: evidence for multiple auditory areas. Neuroimage 6:288–304

    Article  CAS  PubMed  Google Scholar 

  • Spreen O, Benton AL, Fincham RW (1965) Auditory agnosia without aphasia. Arch Neurol 13:84–92

    CAS  Google Scholar 

  • Talairach J, Tournoux P (1988) Co-planar stereotaxic atlas of the human brain. Thieme Medical, New York

  • Tardif E, Clarke S (2000) Intrinsic connectivity of human auditory areas: a tracing study with Dil. Eur J Neurosci 13:1045–1050

    Article  Google Scholar 

  • Thivard L, Belin P, Zilbovicius M, Poline JB, Samson Y (2000) A cortical region sensitive to auditory spectral motion. Neuroreport 11:2969–2972

    CAS  PubMed  Google Scholar 

  • Tian B, Reser D, Durham A, Kustov A, Rauschecker JP (2001) Functional specialization in rhesus monkey auditory cortex. Science 292:290–293

    Google Scholar 

  • Vignolo LA (1982) Auditory agnosia. Philos Trans R Soc Lond B Biol 298:49–57

    CAS  Google Scholar 

  • Wallace MN, Johnston PW, Palmer AR (2002) Histochemical identification of cortical areas in the auditory region of the human brain. Exp Brain Res 143:499–508

    Article  CAS  PubMed  Google Scholar 

  • Warren JD, Zielinski BA, Green GGR, Rauschecker JP, Griffiths TD (2002) Perception of sound-source motion by the human brain. Neuron 34:139–148

    CAS  PubMed  Google Scholar 

  • Weeks RA, Aziz-Sultan A, Bushara KO, Tian B, Wessinger CM, Dang N, Rauschecker JP, Hallet M (1999) A PET study of human auditory spatial processing. Neurosci Lett 262:155–158

    CAS  PubMed  Google Scholar 

  • Weeks R, Horwitz B, Aziz-Sultan A, Tian B, Wessinger CM, Cohen LG, Hallet M, Rauschecker JP (2000) A positron emission tomography study of auditory localization in congenitally blind. J Neurosci 20:2664–2672

    CAS  PubMed  Google Scholar 

  • Wessinger CM, VanMeter J, Tian B, Van Lare J, Pekar J, Rauschecker JP (2001) Hierarchical organization of the human auditory cortex revealed by functional magnetic resonance imaging. J Cogn Neurosci 13:1–7

    CAS  PubMed  Google Scholar 

  • Witte OW, Bidmon HJ, Schiene K, Redecker C, Hagemann G (2000) Functional differentiation of multiple perilesional zones after focal cerebral ischemia. J Cereb Blood Flow Metab 20:1149–65

    CAS  PubMed  Google Scholar 

  • Zatorre RJ, Mondor TA, Evans AC (1999) Auditory attention to space and frequency activates similar cerebral systems. Neuroimage 10:544–554

    Article  CAS  PubMed  Google Scholar 

  • Zatorre RJ, Bouffard M, Ahad P, Belin P (2002) Where is "where" in the human auditory cortex? Nat Neurosci 5(9):905–909

    Article  CAS  PubMed  Google Scholar 

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Acknowledgements

This study was supported by Swiss National Science Foundation grants 3138-51173.97 and 3238-064604.01 and by the Lausanne Medical Faculty RATP grant to S.C.

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Authors and Affiliations

  1. Division de Neuropsychologie, CHUV, 1011, Lausanne, Switzerland

    Michela Adriani, Anne Bellmann Thiran & Stephanie Clarke

  2. Service de Radiodiagnostic et Radiologie Interventionnelle, CHUV, Lausanne, Switzerland

    Philippe Maeder, Reto Meuli & Eleonora Fornari

  3. Service de Rhumatologie et Médecine Réhabilitative, CHUV, Lausanne, Switzerland

    Rolf Frischknecht

  4. Service de Neurochirurgie, CHUV, Lausanne, Switzerland

    Jean-Guy Villemure

  5. Service de Neurologie, HCU, Geneva, Switzerland

    James Mayer & Jean-Marie Annoni

  6. Service de Neurologie, CHUV, Lausanne, Switzerland

    Julien Bogousslavsky

  7. Institut de Traitement des Signaux, EPFL, Lausanne, Switzerland

    Jean-Philippe Thiran

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  1. Michela Adriani
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Correspondence to Stephanie Clarke.

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Adriani, M., Maeder, P., Meuli, R. et al. Sound recognition and localization in man: specialized cortical networks and effects of acute circumscribed lesions. Exp Brain Res 153, 591–604 (2003). https://doi.org/10.1007/s00221-003-1616-0

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