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Auditory evoked visual awareness following sudden ocular blindness: an EEG and TMS investigation

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Abstract

Neurophysiological and neuroanatomical studies have provoked controversy about whether the visual cortex may be more modifiable than previously believed. Auditory processing is enhanced in blind compared to sighted people, and the enhancement might reflect encroachment of auditory transmission onto visual cortex. To address this issue, we recorded the auditory event-related potentials (ERPs) correlated with auditory related paradoxical visual awareness in a subject with traumatic total late-onset blindness. We found that (1) there was auditory related brain activity over the occipital visual scalp regions starting from a very early stage (< 80 ms) and (2) this occipital activity was significantly different between “visually aware” and “visually unaware” responses in the P1 (40–80 ms) component following meaningful stimuli. There was also a significant difference between responses with and without visual awareness in the N1 (100–120 ms) component following either tones or meaningful stimuli. The phosphenes accompanying auditory stimuli in the ERP experiment were always perceived to be directly in front of the subject and this was reproduced by transcranial magnetic stimulation over the blind primary visual cortex and by sudden sounds delivered to the side or behind the subject. The TMS induced phosphenes were restricted to the central part of the space and were, at least qualitatively, the same as those induced by sounds. The results are clear evidence that human perceptual functions can be reorganized after sudden, late-onset, total ocular blindness.

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References

  • AEEGS (1991) American electroencephalographic society guidelines for standard electrode position nomenclature. J Clin Neurophysiol 8:200–202

    Article  Google Scholar 

  • Aleman A, Rutten G-JM, Sitskoorn MM, Dautzenberg G, Ramsey NF (2001) Activation of striate cortex in the absence of visual stimulation: an fMRI study of synesthesia. NeuroReport 12:2827–2830

    Article  PubMed  CAS  Google Scholar 

  • Amedi A, Raz N, Pianka P, Malach R, Zohary E (2003) Early ‘visual’ cortex activation correlates with superior verbal memory performance in the blind. Nat Neurosci 6:758–766

    Article  PubMed  CAS  Google Scholar 

  • Armel KC, Ramachandran VS (1999) Acquired synaesthesia in retinitis pigmentosa. Neurocase 5:293–296

    Article  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 

  • Büchel C (2003) Cortical hierarchy turned on its head. Nat Neurosci 6:657–658

    Article  PubMed  CAS  Google Scholar 

  • Büchel C, Price C, Frackowiak RS, Friston K (1998a) Different activation patterns in the visual cortex of late and congenitally blind subjects. Brain 121(Pt 3):409–419

    Article  Google Scholar 

  • Büchel C, Price C, Friston K (1998b) A multimodal language region in the ventral visual pathway. Nature 394:274–277

    Article  Google Scholar 

  • Burton H, Snyder AZ, Diamond JB, Raichle ME (2002) Adaptive changes in early and late blind: a FMRI study of verb generation to heard nouns. J Neurophysiol 88:3359–3371

    Article  PubMed  CAS  Google Scholar 

  • Cohen LG, Celnik P, Pascual-Leone A, Corwell B, Faiz L, Dambrosio J, Honda M, Sadato M, 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 

  • Cowey A, Walsh V (2000) Magnetically induced phosphenes in sighted, blind and blindsighted observers. Neuroreport 11:3269–3273

    Article  PubMed  CAS  Google Scholar 

  • De Volder AG, Toyama H, Kimura Y, Kiyosawa M, Nakano H, Vanlierde A, Wanet-Defalque MC, Mishina M, Oda K, Ishiwata K, Senda M (2001) Auditory triggered mental imagery of shape involves visual association areas in early blind humans. Neuroimage 14:129–139

    Article  PubMed  Google Scholar 

  • Doucet ME, Guillemot JP, Lassonde M, Gagne JP, Leclerc C, Lepore F (2005) Blind subjects process auditory spectral cues more efficiently than sighted individuals. Exp Brain Res 160:194–202

    Article  PubMed  Google Scholar 

  • Dumoulin SO, Bittar RG, Kabani NJ, Baker CL Jr, Le Goualher G, Pike GB, Evans AG (2000) A new anatomical landmark for reliable identification of human area V5/MT: a quantitative analysis of sulcal patterning. Cereb Cortex 10:454–463

    Article  PubMed  CAS  Google Scholar 

  • Escera C, Alho K, Winkler I (1998) Neural mechanisms of involuntary attention to acoustic novelty and change. J Cogn Neurosci 10(5):590–604

    Article  PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Foxe JJ, Simpson GV (2002) Flow of activation from V1 to frontal cortex in humans. A framework for defining “early” visual processing. Exp Brain Res 142:139–150

    Article  PubMed  Google Scholar 

  • Foxe JJ, Doniger GM, Javitt DC (2001) Early visual processing deficits in schizophrenia: impaired P1 generation revealed by high-density electrical mapping. Neuroreport 12:3815–3820

    Article  PubMed  CAS  Google Scholar 

  • Foxe JJ, Murray MM, Javitt DC (2005) Filling-in in schizophrenia: a high-density electrical mapping and source-analysis investigation of illusory contour processing. Cereb Cortex

  • Hotting K, Rösler F, Röder B (2004) Altered auditory-tactile interactions in congenitally blind humans: an event-related potential study. Exp Brain Res 159:370–381

    Article  PubMed  Google Scholar 

  • Jacobs L, Karpik A, Bozian D, Gothgen S (1981) Auditory-visual synesthesia: sound induced photisms. Arch Neurol 38:211–216

    PubMed  CAS  Google Scholar 

  • Martinez A, DiRusso F, Anllo-Vento L, Sereno MI, Buxton RB, Hillyard SA (2001) Putting spatial attention on the map: timing and localization of stimulus selection processes in striate and extrastriate visual areas. Vision Res 41:1437–1457

    Article  PubMed  CAS  Google Scholar 

  • Mecklinger A, Opitz B, Friederici AD (1997) Semantic aspects of novelty detection in humans. Neurosci Lett 235:65–68

    Article  PubMed  CAS  Google Scholar 

  • Nunn JA, Gregory LJ, Brammer M, Williams SCR, Parslow DM, Morgan MJ, Morris RG, Bullmore ET, Baron-Cohen S, Gray JA (2002) Functional magnetic resonance imaging of synesthesia: activation of V4/V8 by spoken words. Nature Neurosci 5:371–375

    Article  PubMed  CAS  Google Scholar 

  • Rakic P, Suner I, Williams RW (1991) A novel cytoarchitectonic area induced experimentally within the primate visual cortex. Proc Natl Acad Sci USA 88: 2083–2087

    Article  PubMed  CAS  Google Scholar 

  • Rao A, Nobre AC, Cowey A (2001) Disruption of visual evoked potentials following a V1 lesion: implications for blindsight,. In: De Gelder B, De Haan EHF, Heywood CA (eds) Out of mind: varieties of unconscious processes, vol 5. Oxford University Press, Oxford pp 69–86

    Google Scholar 

  • Röder B, Rösler F, Hennighausen E, Nacker F (1996) Event-related potentials during auditory and somatosensory discrimination in sighted and blind human subjects. Brain Res Cogn Brain Res 4:77–93

    PubMed  Google Scholar 

  • Röder B, Rösler F, Neville HJ (1999) Effects of interstimulus interval on auditory event-related potentials in congenitally blind and normally sighted humans. Neurosci Lett 264:53–56

    Article  PubMed  Google Scholar 

  • Röder B, Rösler F, Neville HJ (2001) Auditory memory in congenitally blind adults: a behavioral-electrophysiological investigation. Brain Res Cogn Brain Res 11:289–303

    Article  PubMed  Google Scholar 

  • Röder B, Stock O, Bien S, Neville H, Rösler F (2002) Speech processing activates visual cortex in congenitally blind humans. Eur J Neurosci 16:930–936

    Article  PubMed  Google Scholar 

  • Sadato N, Pascual-Leone A, Grafman J, Ibanez V, Deiber MP, Dold G, Hallett M (1996) Activation of the primary visual cortex by Braille reading in blind subjects. Nature 380:526–528

    Article  PubMed  CAS  Google Scholar 

  • Sparing R, Mottaghy FM, Ganis G, Thompon WL, Topper R, Kosslyn SM, Pascua-Leone A (2002) Visual cortex excitability increases during visual mental imagery—a TMS study in healthy human subjects. Brain Res 938:92–97

    Article  PubMed  CAS  Google Scholar 

  • Steven MS, Blakemore C (2004) Visual synaesthesia in the blind. Perception 33:855–868

    Article  PubMed  Google Scholar 

  • Theoret H, Merabet L, Pascual-Leone A (2004) Behavioral and neuroplastic changes in the blind: evidence for functionally relevant cross-modal interactions. J Physiol Paris 98:221–233

    Article  PubMed  Google Scholar 

  • Voss P, Lassonde M, Gougoux F, Fortin M, Guillemot JP, Lepore F (2004) Early- and late-onset blind individuals show supra-normal auditory abilities in far-space. Curr Biol 14:1734–1738

    Article  PubMed  CAS  Google Scholar 

  • Walsh V, Cowey A (1998) Magnetic stimulation studies of visual cognition. Trends Cogn Sci 2:103–110

    Article  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 

  • Weiskrantz L, Warrington EK, Sanders MD, Marshall J (1974) Visual capacity in the hemianopic field following a restricted occipital ablation. Brain 97:709–728

    Article  PubMed  CAS  Google Scholar 

  • Weiskrantz L, Rao A, Hodinott-Hill I, Nobre AC, Cowey A (2003) Brain potentials associated with conscious aftereffects induced by unseen stimuli in a blindsight subject. Proc Natl Acad Sci USA 100:10500–10505

    Article  PubMed  CAS  Google Scholar 

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Acknowledgments

We thank PS and the sighted volunteers for their enthusiasm and patience during hours of recording.

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Correspondence to Alan Cowey.

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Rao, A., Nobre, A.C., Alexander, I. et al. Auditory evoked visual awareness following sudden ocular blindness: an EEG and TMS investigation. Exp Brain Res 176, 288–298 (2007). https://doi.org/10.1007/s00221-006-0616-2

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  • DOI: https://doi.org/10.1007/s00221-006-0616-2

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