Skip to main content
SpringerLink
Log in

Sensory compensation in sound localization in people with one eye

  • Research Article
  • Published:
Experimental Brain Research Aims and scope Submit manuscript

Abstract

Some blind people are better at locating sounds than people with normal vision indicating cross-modal plasticity. People who have lost one eye have a unique form of visual deprivation that reduces visual afferent signals by half and can potentially also lead to cross-modal (as well as intra-modal) plasticity. To look for evidence of auditory-visual cross-modal compensation, we measured binaural and monaural sound localization in one-eyed people and compared them with normally sighted controls. One-eyed people showed significantly better binaural sound localization than controls in the central region of space (±78° from straight ahead), but they mislocalized sounds in the far periphery (on both the blind and intact side) by up to 15° towards the centre. One-eyed people showed significantly better monaural sound localization compared with controls. Controls’ performance became asymmetric when they had one eye patched. Patching improved accuracy in the viewing field but decreased accuracy in the occluded field. These results are discussed in terms of cross-modal sensory compensation and the possible contribution of visual depth to interpreting sound localization cues.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

Notes

  1. In the eyes closed condition, participants looked at the fixation point, closed their eyes during the stimulus presentation (90 ms) while maintaining fixation and then opened the eyes.

References

  • Abel SM, Tikuisis C (2005) Sound localization with monocular vision. Appl Acoust 66:932–944

    Article  Google Scholar 

  • Abel SM, Figuerido JC, Consoli A, Biri CM, Papsin BC (2002) The effect of blindness on horizontal plane sound source identification. Int J Audiol 41:285–292

    Article  PubMed  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 

  • Ashmead DH, Wall RS, Ebinger KA, Eaton SB, Snook-Hill MM, Yang X (1998) Spatial hearing in children with visual disabilities. Perception 27:105–122

    Article  PubMed  CAS  Google Scholar 

  • Carlile S, Leong P, Hyams S (1997) The nature and distribution of errors in sound localization by human listeners. Hear Res 114:179–196

    Article  PubMed  CAS  Google Scholar 

  • Ceyte H, Cian C, Trousselard M, Barraud PA (2009) Influence of perceived egocentric coordinates on the subjective visual vertical. Neurosci Lett 462:85–88

    Article  PubMed  CAS  Google Scholar 

  • Chen P, Erdahl L, Barrett AM (2009) Monocular patching may induce ipsilateral “where” spatial bias. Neuropsychologia 47:711–716

    Article  PubMed  Google Scholar 

  • Collignon O, Davare M, Olivier E, De Volder AG (2009a) 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

    Article  PubMed  CAS  Google Scholar 

  • Collignon O, Voss P, Lassonde M, Lepore F (2009b) Cross-modal plasticity for the spatial processing of sounds in visually deprived subjects. Exp Brain Res 192:343–358

    Article  PubMed  Google Scholar 

  • Collignon O et al (2011) Functional specialization for auditory-spatial processing in the occipital cortex of congenitally blind humans. Proc Natl Acad Sci USA 108:4435–4440

    Article  PubMed  CAS  Google Scholar 

  • Dengis CA, Steinbach MJ, Goltz HC, Stager C (1993a) Visual alignment from the midline: a declining developmental trend in normal, strabismic and monocularly enucleated children. J Pediat Ophthalmol Strabismus 30:323–326

    PubMed  CAS  Google Scholar 

  • Dengis CA, Steinbach MJ, Ono H, Kraft SP, Smith DR, Graham JE (1993b) Egocenter location in children with strabismus: in the median plane and unchanged by surgery. Invest Ophthalmol Vis Sci 34:2990–2995

    PubMed  CAS  Google Scholar 

  • Despres O, Candas V, Dufour A (2005) Spatial auditory compensation in early-blind humans: involvement of eye movements and/or attention orienting? Neuropsychologia 43:1955–1962

    Article  PubMed  CAS  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 

  • Faguet J, Maranhao B, Smith SL, Trachtenberg JT (2009) Ipsilateral eye cortical maps are uniquely sensitive to binocular plasticity. J Neurophysiol 101:855–861

    Article  PubMed  Google Scholar 

  • González EG, Steinbach MJ, Ono H, Wolf M (1989) Depth perception in humans enucleated at an early age. Clin Vis Sci 4:173–177

    Google Scholar 

  • González EG, Steinbach MJ, Gallie BL, Ono H (1999) Egocentric localization: visually directed alignment to projected head landmarks in binocular and monocular observers. Binocul Vis Stabismus Q 14:127–136

    Google Scholar 

  • Gougoux F, Lepore F, Lassonde M, Voss P, Zatorre RJ, Belin P (2004) Neuropsychology: pitch discrimination in the early blind. Nature 430:309

    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 

  • Hartmann WM (1983) Localization of sound in rooms. J Acoust Soc Am 74:1380–1391

    Article  PubMed  CAS  Google Scholar 

  • Hofman PM, Van Opstal AJ (1998) Spectrotemporal factors in 2-dimensional human sound localization. J Acoustic Soc Am 103:2634–2648

    Article  CAS  Google Scholar 

  • Hubbard TL, Ruppel SE (2000) Spatial memory averaging, the landmark attraction effect, and representational gravity. Psychol Res 64:41–55

    Article  PubMed  CAS  Google Scholar 

  • Jaekl PM, Harris LR (2010) Space constancy vs. shape constancy. See Perceiving 23:385–399

    Article  Google Scholar 

  • Kerzel D (2002) Memory for the position of stationary objects: disentangling foveal bias and memory averaging. Vision Res 42:159–167

    Article  PubMed  Google Scholar 

  • Kim DO, Moiseff A, Turner JB, Gull J (2008) Acoustic cues underlying auditory distance in barn owls. Acta Otolaryngol 128:382–387

    Article  PubMed  Google Scholar 

  • Kupers R, Pappens M, de Noordhout AM, Schoenen J, Ptito M, Fumal A (2007) rTMS of the occipital cortex abolishes Braille reading and repetition priming in blind subjects. Neurology 68:691–693

    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 

  • Lessard N, Pare M, Lepore F, Lassonde W (1998) Early-blind human subjects localize sound sources better than sighted subjects. Nature 395:278–280

    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, 1–5

    Google Scholar 

  • Makous JC, Middlebrooks JC (1990) Two-dimensional sound localization by human listeners. J Acoust Soc Am 87:2188–2200

    Article  PubMed  CAS  Google Scholar 

  • Marotta JJ, Perrot TS, Nicolle D, Goodale MA (1995) The development of adaptive head movements following enucleation. Eye 9(Pt 3):333–336

    Article  PubMed  Google Scholar 

  • Middlebrooks JC, Green DM (1991) Sound localization by human listeners. Annu Rev Psychol 42:135–159

    Article  PubMed  CAS  Google Scholar 

  • Moidell BG, Steinbach MJ, Ono H (1988) Egocenter location in children enucleated at an early age. Invest Ophth Vis Sci 29:1348–1351

    CAS  Google Scholar 

  • Niemeyer W, Starlinger I (1981) Do the blind hear better? Investigations on auditory processing in congenital or early acquired blindness. II. Central functions. Audiology 20:510–515

    Article  PubMed  CAS  Google Scholar 

  • Oldfield SR, Parker SP (1984) Acuity of sound localisation: a topography of auditory space. I. Normal hearing conditions. Perception 13:581–600

    Article  PubMed  CAS  Google Scholar 

  • Ono H, Mapp AP, Howard IP (2002) The cyclopean eye in vision: the new and old data continue to hit you right between the eyes. Vision Res 42:1307–1324

    Article  PubMed  Google Scholar 

  • Porac C, Coren S (1986) Sighting dominance and egocentric localization. Vision Res 26:1709–1713

    Article  PubMed  CAS  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 

  • Roth HL, Lora AN, Heilman KM (2002) Effects of monocular viewing and eye dominance on spatial attention. Brain 125:2023–2035

    Article  PubMed  Google Scholar 

  • Sheth BR, Shimojo S (2001) Compression of space in visual memory. Vision Res 41:329–341

    Article  PubMed  CAS  Google Scholar 

  • Smith SL, Trachtenberg JT (2007) Experience-dependent binocular competition in the visual cortex begins at eye opening. Nat Neurosci 10:370–375

    Article  PubMed  CAS  Google Scholar 

  • Steeves JK, Gonzalez EG, Steinbach MJ (2008) Vision with one eye: a review of visual function following unilateral enucleation. Spat Vis 21:509–529

    Article  PubMed  Google Scholar 

  • Van Brussel L, Gerits A, Arckens L (2011) Evidence for cross-modal plasticity in adult mouse visual cortex following monocular enucleation. Cereb Cortex 21:2133–2146

    Google Scholar 

  • Voss P, Lepore F, Gougoux F, Zatorre RJ (2011) Relevance of spectral cues for auditory spatial processing in the occipital cortex of the blind. Front Psychol 2:48

    Article  PubMed  Google Scholar 

  • Weeks R, Horwitz B, Aziz-Sultan1 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

    Google Scholar 

  • Wightman FL, Kistler DJ (1989) Headphone simulation of free-field listening. II: Psychophysical validation. J Acoust Soc Am 85:868–878

    Article  PubMed  CAS  Google Scholar 

  • Withington DJ, Binns KE, Ingham NJ, Thornton SK (1994) The effects of monocular enucleation on the representation of auditory space in the superior colliculus of the guinea-pig. Brain Res 636:348–352

    Article  PubMed  CAS  Google Scholar 

  • Zwiers MP, Van Opstal AJ, Cruysberg JR (2001) Two-dimensional sound-localization behavior of early-blind humans. Exp Brain Res 140:206–222

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

We would like to thank the one-eyed participants in this study for their continued enthusiasm and participation in our work. This work was supported by the Natural Sciences and Engineering Research Council of Canada (NSERC) grants to JKES and LRH. AENH held a PGS-M2 NSERC graduate scholarship.

Author information

Authors and Affiliations

  1. Department of Psychology and Centre for Vision Research, York University, 4700 Keele Street, Toronto, ON, M3J 1P3, Canada

    Adria E. N. Hoover, Laurence R. Harris & Jennifer K. E. Steeves

Authors
  1. Adria E. N. Hoover
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Laurence R. Harris
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Jennifer K. E. Steeves
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Jennifer K. E. Steeves.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Hoover, A.E.N., Harris, L.R. & Steeves, J.K.E. Sensory compensation in sound localization in people with one eye. Exp Brain Res 216, 565–574 (2012). https://doi.org/10.1007/s00221-011-2960-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00221-011-2960-0

Keywords

Search

Navigation