Skip to main content

Advertisement

Log in

Reorganisation of the Right Occipito-Parietal Stream for Auditory Spatial Processing in Early Blind Humans. A Transcranial Magnetic Stimulation Study

  • Original Paper
  • Published:
Brain Topography Aims and scope Submit manuscript

Abstract

It is well known that, following an early visual deprivation, the neural network involved in processing auditory spatial information undergoes a profound reorganization. In particular, several studies have demonstrated an extensive activation of occipital brain areas, usually regarded as essentially “visual”, when early blind subjects (EB) performed a task that requires spatial processing of sounds. However, little is known about the possible consequences of the activation of occipitals area on the function of the large cortical network known, in sighted subjects, to be involved in the processing of auditory spatial information. To address this issue, we used event-related transcranial magnetic stimulation (TMS) to induce virtual lesions of either the right intra-parietal sulcus (rIPS) or the right dorsal extrastriate occipital cortex (rOC) at different delays in EB subjects performing a sound lateralization task. Surprisingly, TMS applied over rIPS, a region critically involved in the spatial processing of sound in sighted subjects, had no influence on the task performance in EB. In contrast, TMS applied over rOC 50 ms after sound onset, disrupted the spatial processing of sounds originating from the contralateral hemifield. The present study shed new lights on the reorganisation of the cortical network dedicated to the spatial processing of sounds in EB by showing an early contribution of rOC and a lesser involvement of rIPS.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • Allman BL, Keniston LP, Meredith MA (2008) Subthreshold auditory inputs to extrastriate visual neurons are responsive to parametric changes in stimulus quality: sensory-specific versus non-specific coding. Brain Res 1242:95–101

    Google Scholar 

  • Amedi A, Floel A, Knecht S, Zohary E, Cohen LG (2004) Transcranial magnetic stimulation of the occipital pole interferes with verbal processing in blind subjects. Nat Neurosci 7:1266–1270

    Article  PubMed  CAS  Google Scholar 

  • Andersen RA (1997) Multimodal integration for the representation of space in the posterior parietal cortex. Philos Trans R Soc Lond B Biol Sci 352:1421–1428

    Article  PubMed  CAS  Google Scholar 

  • Andersen RA, Buneo CA (2002) Intentional maps in posterior parietal cortex. Annu Rev Neurosci 25:189–220

    Article  PubMed  CAS  Google Scholar 

  • Arno P, De Volder AG, Vanlierde A, Wanet-Defalque MC, Streel E, Robert A, Sanabria-Bohorquez S, Veraart C (2001) Occipital activation by pattern recognition in the early blind using auditory substitution for vision. Neuroimage 13:632–645

    Article  PubMed  CAS  Google Scholar 

  • Avillac M, Deneve S, Olivier E, Pouget A, Duhamel JR (2005) Reference frames for representing visual and tactile locations in parietal cortex. Nat Neurosci 8:941–949

    PubMed  CAS  Google Scholar 

  • Bavelier D, Neville HJ (2002) Cross-modal plasticity: where and how? Nat Rev Neurosci 3:443–452

    PubMed  CAS  Google Scholar 

  • Belmaker B, Fitzgerald P, George MS, Lisanby SH, Pascual-Leone A, Schlaepfer TE, Wassermann E (2003) Managing the risks of repetitive transcranial stimulation. CNS Spectr 8:489

    PubMed  Google Scholar 

  • Blauert J (1997) Spatial hearing: the psychophysics of human sound localization. MIT Press, Cambridge

  • Bremmer F, Schlack A, Shah NJ, Zafiris O, Kubischik M, Hoffmann K, Zilles K, Fink GR (2001) Polymodal motion processing in posterior parietal and promotor cortex: a human fMRI study strongly implies equivalencies between humans and monkeys. Neuron 29:287–296

    Article  PubMed  CAS  Google Scholar 

  • Carriere BN, Royal DW, Perrault TJ, Morrison SP, Vaughan JW, Stein BE, Wallace MT (2007) Visual deprivation alters the development of cortical multisensory integration. J Neurophysiol 98:2858–2867

    Article  PubMed  Google Scholar 

  • Cohen LG, Celnik P, Pascual-Leone A, Corwell B, Falz L, Dambrosia J, Honda M, Sadato N, Gerloff C, Catala MD, Hallett M (1997) Functional relevance of cross-modal plasticity in blind humans. Nature 389:180–183

    Article  PubMed  CAS  Google Scholar 

  • Collignon O, Renier L, Bruyer R, Tranduy D, Veraart C (2006) Improved selective and divided spatial attention in early blind subjects. Brain Res 1075:175–182

    Article  PubMed  CAS  Google Scholar 

  • Collignon O, Lassonde M, Lepore F, Bastien D, Veraart C (2007) Functional cerebral reorganization for auditory spatial processing and auditory substitution of vision in early blind subjects. Cereb Cortex 17:457–465

    Article  PubMed  Google Scholar 

  • Collignon O, Davare M, De Volder AG, Poirier C, Olivier E, Veraart C (2008a) Time-course of posterior parietal and occipital cortex contribution to sound localization. J Cogn Neurosci 20:1454–1463

    Article  PubMed  Google Scholar 

  • Collignon O, Voss P, Lassonde M, Lepore F (2008b) Cross-modal plasticity for the spatial processing of sounds in visually deprived subjects. Exp Brain Res 192(3):343–358

    Google Scholar 

  • Davare M, Andres M, Cosnard G, Thonnard JL, Olivier E (2006) Dissociating the role of ventral and dorsal promotor cortex in precision grasping. J Neurosci 26:2260–2268

    Article  PubMed  Google Scholar 

  • De Volder AG, Catalan-Ahumada M, Robert A, Bol A, Labar D, Coppens A, Michel C, Veraart C (1999) Changes in occipital cortex activity in early blind humans using a sensory substitution device. Brain Res 826:128–134

    Article  PubMed  Google Scholar 

  • Eimer M (2001) Crossmodal links in spatial attention between vision, audition, and touch: evidence from event-related brain potentials. Neuropsychologia 39:1292–1303

    Article  PubMed  CAS  Google Scholar 

  • Falchier A, Clavagnier S, Barone P, Kennedy H (2002) Anatomical evidence of multimodal integration in primate striate cortex. J Neurosci 22:5749–5759

    PubMed  CAS  Google Scholar 

  • Fishman MC, Michael P (1973) Integration of auditory information in the cat’s visual cortex. Vision Res 13:1415–1419

    Article  PubMed  CAS  Google Scholar 

  • Giard MH, Peronnet F (1999) Auditory-visual integration during multimodal object recognition in humans: a behavioral and electrophysiological study. J Cogn Neurosci 11:473–490

    Article  PubMed  CAS  Google Scholar 

  • Gougoux F, Zatorre RJ, Lassonde M, Voss P, Lepore F (2005) A functional neuroimaging study of sound localization: visual cortex activity predicts performance in early-blind individuals. PLoS Biol 3:e27

    Article  PubMed  Google Scholar 

  • Grefkes C, Fink GR (2005) The functional organization of the intraparietal sulcus in humans and monkeys. J Anat 207:3–17

    Article  PubMed  Google Scholar 

  • Griffiths TD, Rees G, Rees A, Green GG, Witton C, Rowe D, Buchel C, Turner R, Frackowiak RS (1998) Right parietal cortex is involved in the perception of sound movement in humans. Nat Neurosci 1:74–79

    Article  PubMed  CAS  Google Scholar 

  • Haxby JV, Grady CL, Horwitz B, Ungerleider LG, Mishkin M, Carson RE, Herscovitch P, Schapiro MB, Rapoport SI (1991) Dissociation of object and spatial visual processing pathways in human extrastriate cortex. Proc Natl Acad Sci USA 88:1621–1625

    Article  PubMed  CAS  Google Scholar 

  • Kennett S, Eimer M, Spence C, Driver J (2001) Tactile-visual links in exogenous spatial attention under different postures: convergent evidence from psychophysics and ERPs. J Cogn Neurosci 13:462–478

    Article  PubMed  CAS  Google Scholar 

  • Kujala T, Alho K, Paavilainen P, Summala H, Naatanen R (1992) Neural plasticity in processing of sound location by the early blind: an event-related potential study. Electroencephalogr Clin Neurophysiol 84:469–472

    Article  PubMed  CAS  Google Scholar 

  • Leclerc C, Saint-Amour D, Lavoie ME, Lassonde M, Lepore F (2000) Brain functional reorganization in early blind humans revealed by auditory event-related potentials. NeuroReport 11:545–550

    Article  PubMed  CAS  Google Scholar 

  • Leclerc C, Segalowitz SJ, Desjardins J, Lassonde M, Lepore F (2005) EEG coherence in early-blind humans during sound localization. Neurosci Lett 376:154–159

    Article  PubMed  CAS  Google Scholar 

  • Lewald J, Foltys H, Topper R (2002) Role of the posterior parietal cortex in spatial hearing. J Neurosci. 22: RC207

  • Lewald J, Meister IG, Weidemann J, Topper R (2004a) Involvement of the superior temporal cortex and the occipital cortex in spatial hearing: evidence from repetitive transcranial magnetic stimulation. J Cogn Neurosci 16:828–838

    Article  PubMed  Google Scholar 

  • Lewald J, Wienemann M, Boroojerdi B (2004b) Shift in sound localization induced by rTMS of the posterior parietal lobe. Neuropsychologia 42:1598–1607

    Article  PubMed  Google Scholar 

  • Merabet LB, Rizzo JF, Amedi A, Somers DC, Pascual-Leone A (2005) What blindness can tell us about seeing again: merging neuroplasticity and neuroprostheses. Nat Rev Neurosci 6:71–77

    Article  PubMed  CAS  Google Scholar 

  • Molholm S, Ritter W, Murray MM, Javitt DC, Schroeder CE, Foxe JJ (2002) Multisensory auditory-visual interactions during early sensory processing in humans: a high-density electrical mapping study. Brain Res Cogn Brain Res 14:115–128

    Article  PubMed  Google Scholar 

  • Morrell F (1972) Visual system’s view of acoustic space. Nature 238:44–46

    Article  PubMed  CAS  Google Scholar 

  • Mullette-Gillman OA, Cohen YE, Groh JM (2005) Eye-centered, head-centered, and complex coding of visual and auditory targets in the intraparietal sulcus. J Neurophysiol 94:2331–2352

    Article  PubMed  Google Scholar 

  • Noirhomme Q, Ferrant M, Vandermeeren Y, Olivier E, Macq B, Cuisenaire O (2004) Registration and real-time visualization of transcranial magnetic stimulation with 3-D MR images. IEEE Trans Biomed Eng 51:1994–2005

    Google Scholar 

  • O’Shea J, Taylor PC, Rushworth MF (2008) Imaging causal interactions during sensorimotor processing. Cortex 44:598–608

    Article  PubMed  Google Scholar 

  • Pascual-Leone A, Amedi A, Fregni F, Merabet LB (2005) The plastic human brain cortex. Annu Rev Neurosci 28:377–401

    Article  PubMed  CAS  Google Scholar 

  • Piche M, Chabot N, Bronchti G, Miceli D, Lepore F, Guillemot JP (2007) Auditory responses in the visual cortex of neonatally enucleated rats. Neuroscience 145:1144–1156

    Article  PubMed  CAS  Google Scholar 

  • Poirier C, Collignon O, de Volder AG, Renier L, Vanlierde A, Tranduy D, Scheiber C (2005) Specific activation of the V5 brain area by auditory motion processing: an fMRI study. Brain Res Cogn Brain Res 25:650–658

    Article  PubMed  Google Scholar 

  • Poirier C, Collignon O, Scheiber C, Renier L, Vanlierde A, Tranduy D, Veraart C, De Volder AG (2006) Auditory motion perception activates visual motion areas in early blind subjects. Neuroimage 15:279–285

    Article  Google Scholar 

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

    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

    Google Scholar 

  • Roder B, Teder-Salejarvi W, Sterr A, Rosler F, Hillyard SA, Neville HJ (1999) Improved auditory spatial tuning in blind humans. Nature 400:162–166

    Article  PubMed  CAS  Google Scholar 

  • Romanski LM, Tian B, Fritz J, Mishkin M, Goldman-Rakic PS, Rauschecker JP (1999) Dual streams of auditory afferents target multiple domains in the primate prefrontal cortex. Nat Neurosci 2:1131–1136

    Google Scholar 

  • Schlack A, Sterbing-D’Angelo SJ, Hartung K, Hoffmann KP, Bremmer F (2005) Multisensory space representations in the macaque ventral intraparietal area. J Neurosci 25:4616–4625

    Article  PubMed  CAS  Google Scholar 

  • Spence C, Driver J (2004) Crossmodal space and crossmodal attention. Oxford University Press, New York

    Google Scholar 

  • Stricanne B, Andersen RA, Mazzoni P (1996) Eye-centered, head-centered, and intermediate coding of remembered sound locations in area LIP. J Neurophysiol 76:2071–2076

    PubMed  CAS  Google Scholar 

  • Vanlierde A, De Volder AG, Wanet-Defalque MC, Veraart C (2003) Occipito-parietal cortex activation during visuo-spatial imagery in early blind humans. Neuroimage 19:698–709

    Article  PubMed  Google Scholar 

  • Voss P, Gougoux F, Zatorre RJ, Lassonde M, Lepore F (2008) Differential occipital responses in early- and late-blind individuals during a sound-source discrimination task. Neuroimage 40:746–758

    Article  PubMed  Google Scholar 

  • Walsh V, Cowey A (2000) Transcranial magnetic stimulation and cognitive neuroscience. Nat Rev Neurosci 1:73–79

    Article  PubMed  CAS  Google Scholar 

  • Wasserman EM, Greenberg BD, Murphy DL, Nguyen MB, Smith MJ (2000) A relationship between personality traits and cortical synaptic transmission measured with transcranial magnetic stimulation. Ann Neurol 48:420

    Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Zimmer U, Lewald J, Erb M, Grodd W, Karnath HO (2004) Is there a role of visual cortex in spatial hearing? Eur J Neurosci 20:3148–3156

    Article  PubMed  Google Scholar 

Download references

Acknowledgements

We wish to thank the blind volunteers for their participation. Thanks are also due to C. Veraart for discussions and to B. Gerard for technical help. This experiment was supported by an FRSM Grant #3.4505.04 (ADV). ADV is senior research associate and MD and OC are postdoctoral researchers at the National Funds for Scientific Research (NFSR; Belgium).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to O. Collignon.

Additional information

This article is published as part of the Special Issue on Multisensory Integration.

Electronic supplementary material

Below is the link to the electronic supplementary material.

(DOC 13 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Collignon, O., Davare, M., Olivier, E. et al. Reorganisation of the Right Occipito-Parietal Stream for Auditory Spatial Processing in Early Blind Humans. A Transcranial Magnetic Stimulation Study. Brain Topogr 21, 232–240 (2009). https://doi.org/10.1007/s10548-009-0075-8

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10548-009-0075-8

Keywords

Navigation