Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

Relearning sound localization with new ears

Abstract

Because the inner ear is not organized spatially, sound localization relies on the neural processing of implicit acoustic cues. To determine a sound's position, the brain must learn and calibrate these cues, using accurate spatial feedback from other sensorimotor systems. Experimental evidence for such a system has been demonstrated in barn owls, but not in humans. Here, we demonstrate the existence of ongoing spatial calibration in the adult human auditory system. The spectral elevation cues of human subjects were disrupted by modifying their outer ears (pinnae) with molds. Although localization of sound elevation was dramatically degraded immediately after the modification, accurate performance was steadily reacquired. Interestingly, learning the new spectral cues did not interfere with the neural representation of the original cues, as subjects could localize sounds with both normal and modified pinnae.

Your institute does not have access to this article

Relevant articles

Open Access articles citing this article.

Access options

Buy article

Get time limited or full article access on ReadCube.

$32.00

All prices are NET prices.

Figure 2: Adaptation to altered spectral cues.
Figure 1: Effect of molds on pinna acoustic transfer.
Figure 3: Summary of the results for all four subjects.

References

  1. Middlebrooks, J. C. Narrow-band sound localization related to external ear acoustics. J. Acoust. Soc. Am. 61, 2607–2624 (1992).

    Article  Google Scholar 

  2. Zakarouskas, P. & Cynader, M. S. A computational theory of spectral cue localization. J. Acoust. Soc. Am. 94, 1323–1331 (1993).

    Article  Google Scholar 

  3. Oldfield, S. R. & Parker, S. P. Acuity of sound localization: a topography of auditory space. I. Normal hearing conditions. Perception 13, 581–600 (1994).

    Article  Google Scholar 

  4. Frens, M. A. & Van Opstal, A. J. A quantitative study of auditory-evoked saccadic eye movements in two dimensions. Exp. Brain Res. 107, 103–117 (1995).

    CAS  Article  Google Scholar 

  5. Knudsen, E. I. & Konishi, M. Mechanism of sound localization in the barn owl (Tyto alba). J. Comp. Physiol. A 133, 13–21 (1979).

    Article  Google Scholar 

  6. Batteau, D. W. The role of pinna in human localization. Proc. R. Soc. Lond. B 168, 158–180 (1967).

    CAS  Article  Google Scholar 

  7. Blauert, J. Spatial Hearing. The Psychophysics of Human Sound Localization. (MIT Press, Cambridge, Massachusetts, 1996).

    Google Scholar 

  8. Teranishi, R. & Shaw, E. A. G. External-ear acoustic models with simple geometry. J. Acoust. Soc. Am. 44, 257–263 (1968).

    CAS  Article  Google Scholar 

  9. Lopez-Poveda, E. A. & Meddis, R. A physical model of sound diffraction and reflections in the human concha. J. Acoust. Soc. Am. 100, 3248–3259 (1996).

    CAS  Article  Google Scholar 

  10. Wightman, F. L. & Kistler, D. J. Headphone simulation of free-field listening. I. Stimulus synthesis. J. Acoust. Soc. Am. 85, 858–867 (1989).

    CAS  Article  Google Scholar 

  11. Oldfield, S. R. & Parker, S. P. Acuity of sound localization: a topography of auditory space. II. Pinna cues absent. Perception 13, 601–617 (1984).

    CAS  Article  Google Scholar 

  12. Wenzel, E. M., Arruda, M., Kistler, D. J. & Wightman, F. L. Localization using nonindividualized head-related transfer functions. J. Acoust. Soc. Am. 94, 111–123 (1993).

    CAS  Article  Google Scholar 

  13. Hofman, P. M. & Van Opstal, A. J. Spectro-temporal factors in two-dimensional human sound localization. J. Acoust. Soc. Am. 103, 2634–2648 (1998).

    CAS  Article  Google Scholar 

  14. Knudsen, E. I. & Knudsen, P. F. Vision guides the adjustment of auditory localization in young barn owls. Science 230, 545–548 (1985).

    CAS  Article  Google Scholar 

  15. Knudsen, E. I. & Knudsen, P. F. Vision calibrates sound localization in developing barn owl. J. Neurosci. 9, 3306–3313 (1989).

    CAS  Article  Google Scholar 

  16. Knudsen, E. I. & Mogdans, J. Vision-independent adjustment of unit tuning to sound localization cues in response to monaural occlusion in developing owl optic tectum. J. Neurosci. 12, 3485–3493 (1992).

    CAS  Article  Google Scholar 

  17. Brainard, M. S. & Knudsen, E. I. Experience-dependent plasticity in the inferior colliculus: a site for visual calibration of the neural representation of auditory space in the barn owl. J. Neurosci. 13, 4590–4608 (1993).

    Article  Google Scholar 

  18. King, A. J., Hutchings, M. E., Moore, D. R. & Blakemore, C. Developmental plasticity in the visual and auditory representation in the mammalian superior colliculus. Nature 332, 73–76 (1988).

    CAS  Article  Google Scholar 

  19. Withington-Wray D. J., Binns, K. E. & Keating, M. J. The maturation of the superior collicular map of auditory space in the guinea pig is disrupted by developmental visual deprivation. Eur. J. Neurosci. 2, 682–692 (1990).

    Article  Google Scholar 

  20. Javer, A. R. & Schwarz, D. W. F. Plasticity in human directional hearing. J. Otolaryngol. 24, 111–117 (1995).

    CAS  Google Scholar 

  21. Knudsen, E. I., Esterly, S. D. & Olsen, J. F. Adaptive plasticity of the auditory space map in the optic tectum of adult and baby barn owls in response to external ear modification. J. Neurophysiol. 71, 79–94 (1994).

    CAS  Article  Google Scholar 

  22. Knudsen, E. I. & Knudsen, P. F. The sensitive period for auditory localization in barn owls is limited by age, not by experience. J. Neurosci. 6, 1918–1924 (1986).

    CAS  Article  Google Scholar 

  23. King, A. J. & Moore, D. R. Plasticity of auditory maps in the brain. Trends Neurosci. 14, 31–37 (1991).

    CAS  Article  Google Scholar 

  24. Knudsen, E. I. Capacity for plasticity in the adult owl auditory system expanded by juvenile experience. Science 279, 1531–1533 (1998).

    CAS  Article  Google Scholar 

  25. Stein, B. E. & Meredith, A. M. The Merging of the Senses (MIT Press, Cambridge, Massachusetts, 1993).

    Google Scholar 

  26. Perrett, S. & Noble, W. The contribution of head motion cues to localization of low pass-noise. Percept. Psychophys. 59, 1018–1026 (1997).

    CAS  Article  Google Scholar 

  27. Schröder, M. R. Synthesis of low-peak factor signals and binary sequences with low autocorrelation. IEEE Trans. Inform. Theory 16, 85–89 (1970).

    Article  Google Scholar 

  28. Robinson, D. A. A method of measuring eye movement using a scleral search coil in a magnetic field. IEEE Trans. Biomed. Eng. 10, 137–145 (1963).

    CAS  Google Scholar 

  29. Collewijn, H., Van der Mark, F. & Janssen, T. J. Precise recording of human eye movements. Vision Res. 15, 447–450 (1975).

    CAS  Article  Google Scholar 

  30. Press, W. H., Flannery, B. P., Teukolsky, S. A. & Vettering, W. T. Numerical Recipes in C, 2nd edn (Cambridge Univ. Press, Cambridge, 1992).

    Google Scholar 

  31. Efron, B. & Tibshirani, R. Statistical analysis in the computer age. Science Wash. D.C. 253, 390–395 (1991).

    CAS  Article  Google Scholar 

Download references

Acknowledgements

This research was supported by the Dutch Foundation for the Life Sciences (SLW 805-33.705-P; PMH), the University of Nijmegen, the Netherlands (AJVO), and the Human Frontiers Science Program (RG0174/1998-B; AJVO).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to A. John Van Opstal.

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Hofman, P., Van Riswick, J. & Van Opstal, A. Relearning sound localization with new ears. Nat Neurosci 1, 417–421 (1998). https://doi.org/10.1038/1633

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1038/1633

Further reading

Search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing