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.

  • Article
  • Published:

Modality-specific frontal and parietal areas for auditory and visual spatial localization in humans

Nature Neuroscience volume 2, pages 759–766 (1999)Cite this article

Abstract

Although the importance of the posterior parietal and prefrontal regions in spatial localization of visual stimuli is well established, their role in auditory space perception is less clear. Using positron emission tomography (PET) during auditory and visual spatial localization in the same subjects, modality-specific areas were identified in the superior parietal lobule, middle temporal and lateral prefrontal cortices. These findings suggest that, similar to the visual system, the hierarchical organization of the auditory system extends beyond the temporal lobe to include areas in the posterior parietal and prefrontal regions specialized in auditory spatial processing. Our results may explain the dissociation of visual and auditory spatial localization deficits following lesions involving these regions.

This is a preview of subscription content, access via your institution

Access options

Buy this article

  • Purchase on Springer Link
  • Instant access to full article PDF
Buy now

Prices may be subject to local taxes which are calculated during checkout

Figure 1: Areas for auditory and visual spatial localization.
Figure 2: Modality-specific spatial localization areas.

Similar content being viewed by others

References

  1. Blauert, J. Spatial Hearing: The Psychophysics of Human Sound Localisation (MIT press, Cambridge, 1983).

    Google Scholar 

  2. King, A. J. & Palmer, A. R. Cells responsive to free-field auditory stimuli in guinea-pig superior colliculus: distribution and response properties. J. Physiol. (Lond.) 342, 361 –381 (1983).

    Article  CAS  Google Scholar 

  3. Knudsen, E. I. & Konishi, M. A neural map of auditory space in the owl. Science 200, 795– 797 (1978).

    Article  CAS  Google Scholar 

  4. Rauschecker, J. P. Cortical processing of complex sounds. Curr. Opin. Neurobiol. 8, 516–521 (1998).

    Article  CAS  Google Scholar 

  5. Cranford, J., Ravizza, R., Diamond, I. T. & Whitfield, I. C. Unilateral ablation of the auditory cortex in the cat impairs complex sound localization. Science 172, 286– 288 (1971).

    Article  CAS  Google Scholar 

  6. Heffner, H. & Masterton, B. Contribution of auditory cortex to sound localization in the monkey (Macaca mulatta). J. Neurophysiol. 38, 1340–1358 (1975).

    Article  CAS  Google Scholar 

  7. Jenkins, W. M. & Merzenich, M. M. Role of cat primary auditory cortex for sound-localization behavior. J. Neurophysiol. 52, 819–847 (1984).

    Article  CAS  Google Scholar 

  8. Wegener, J. The sound locating behaviour of brain damaged monkeys. J. Aud. Res. 13, 191–219 ( 1973).

    Google Scholar 

  9. Middlebrooks, J. C., Clock, A. E., Xu, L. & Green, D. M. A panoramic code for sound location by cortical neurons. Science 264 , 842–844 (1994).

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  11. Vaadia, E. Single-unit activity related to active localization of acoustic and visual stimuli in the frontal cortex of the rhesus monkey. Brain Behav. Evol. 33, 127–131 ( 1989).

    Article  CAS  Google Scholar 

  12. Mazzoni, P., Bracewell, R. M., Barash, S. & Andersen, R. A. Spatially tuned auditory responses in area LIP of macaques performing delayed memory saccades to acoustic targets. J. Neurophysiol. 75, 1233–1241 (1996).

    Article  CAS  Google Scholar 

  13. Azuma, M. & Suzuki, H. Properties and distribution of auditory neurons in the dorsolateral prefrontal cortex of the alert monkey. Brain Res. 298, 343–346 (1984).

    Article  CAS  Google Scholar 

  14. Sanchez-Longo, L. P. & Forster, F. M. Clinical significance of sound localization. Neurology 8, 119– 125 (1958).

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  16. Bender, M. & Diamond, S. An analysis of auditory perceptual defects with observations on the localization of dysfunction. Brain 88, 675–686 ( 1965).

    Article  Google Scholar 

  17. Heilman, K. M., Pandya, D. N., Karol, E. A. & Geschwind, N. Auditory inattention. Arch. Neurol. 24, 323–325 (1971).

    Article  CAS  Google Scholar 

  18. De Renzi, E., Gentilini, M. & Pattacini, F. Auditory extinction following hemisphere damage. Neuropsychologia 22, 733–744 (1984).

    Article  CAS  Google Scholar 

  19. De Renzi, E., Gentilini, M. & Barbieri, C. Auditory neglect. J. Neurol. Neurosurg. Psychiatry 52, 613–617 ( 1989).

    Article  CAS  Google Scholar 

  20. Weeks, R. et al. A PET study of auditory spatial processing. Neurosci. Lett. (in press).

  21. Griffiths, T. et al. Right parietal cortex is involved in the perception of sound movement in humans. Nat. Neurosci. 1, 74 –79 (1998).

    Article  CAS  Google Scholar 

  22. Corbetta, M., Miezin, F. M., Shulman, G. L. & Petersen, S. E. A PET study of visuospatial attention. J. Neurosci. 13, 1202–1226 (1993).

    Article  CAS  Google Scholar 

  23. Haxby, J. V. et al. The functional organization of human extrastriate cortex: a PET-rCBF study of selective attention to faces and locations. J. Neurosci. 14, 6336–6353 (1994).

    Article  CAS  Google Scholar 

  24. Nobre, A. C. et al. Functional localization of the system for visuospatial attention using positron emission tomography. Brain 120, 515–533 (1997).

    Article  Google Scholar 

  25. Andersen, R. A., Snyder, L. H., Bradley, D. C. & Xing, J. Multimodal representation of space in the posterior parietal cortex and its use in planning movements. Annu. Rev. Neurosci. 20, 303–330 (1997).

    Article  CAS  Google Scholar 

  26. Wightman, F. L. & Kistler, D. J. Headphone simulation of free-field listening. I: Stimulus synthesis. II: Psychophysical validation. J. Acoust. Soc. Am. 85, 858– 878 (1989).

    Article  CAS  Google Scholar 

  27. 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).

    Article  CAS  Google Scholar 

  28. Brugge, J. F., Reale, R. A. & Hind, J. E. The structure of spatial receptive fields of neurons in primary auditory cortex of the cat. J. Neurosci. 16, 4420–4437 (1996).

    Article  CAS  Google Scholar 

  29. Sweeney, J. A. et al. Positron emission tomography study of voluntary saccadic eye movements and spatial working memory. J. Neurophysiol. 75, 454–468 (1996).

    Article  CAS  Google Scholar 

  30. Milner, A. Neglect, Extinction, and the Cortical Streams of Visual Processing (Springer, Heidelberg, 1997).

    Book  Google Scholar 

  31. Young, A. W., Hellawell, D. J. & Welch, J. Neglect and visual recognition. Brain 115, 51–71 (1992).

    Article  Google Scholar 

  32. Harrington, D. L., Haaland, K. Y. & Knight, R. T. Cortical networks underlying mechanisms of time perception. J. Neurosci. 18, 1085– 1095 (1998).

    Article  CAS  Google Scholar 

  33. Pardo, J. V., Fox, P. T. & Raichle, M. E. Localization of a human system for sustained attention by positron emission tomography. Nature 349, 61–64 (1991).

    Article  CAS  Google Scholar 

  34. Maquet, P. et al. Brain activation induced by estimation of duration: a PET study. Neuroimage 3, 119– 126 (1996).

    Article  CAS  Google Scholar 

  35. Watson, R. T., Valenstein, E., Day, A. & Heilman, K. M. Posterior neocortical systems subserving awareness and neglect. Neglect associated with superior temporal sulcus but not area 7 lesions. Arch. Neurol. 51, 1014–1021 (1994).

    Article  CAS  Google Scholar 

  36. Fink, G. R., Dolan, R. J., Halligan, P. W., Marshall, J. C. & Frith, C. D. Space-based and object-based visual attention: shared and specific neural domains. Brain 18, 2013–2028 (1997).

    Article  Google Scholar 

  37. McCarthy, G. et al. Functional magnetic resonance imaging of human prefrontal cortex activation during a spatial working memory task. Proc. Natl. Acad. Sci. USA 91, 8690–8694 (1994).

    Article  CAS  Google Scholar 

  38. Courtney, S. M., Petit, L., Maisog, J. M., Ungerleider, L. G. & Haxby, J. V. An area specialized for spatial working memory in human frontal cortex. Science 279, 1347– 1351 (1998).

    Article  CAS  Google Scholar 

  39. Russo, G. S. & Bruce, C. J. Frontal eye field activity preceding aurally guided saccades. J. Neurophysiol. 71, 1250–1253 (1994).

    Article  CAS  Google Scholar 

  40. Ungerleider, L. G., Courtney, S. M. & Haxby, J. V. A neural system for human visual working memory. Proc. Natl. Acad. Sci. USA 95, 883– 890 (1998).

    Article  CAS  Google Scholar 

  41. Zatorre, R. J., Perry, D. W., Beckett, C. A., Westbury, C. F. & Evans, A. C. Functional anatomy of musical processing in listeners with absolute pitch and relative pitch. Proc. Natl. Acad. Sci. USA 95, 3172–3177 (1998).

    Article  CAS  Google Scholar 

  42. Ahissar, M., Ahissar, E., Bergman, H. & Vaadia, E. Encoding of sound-source location and movement: activity of single neurons and interactions between adjacent neurons in the monkey auditory cortex. J. Neurophysiol. 67, 203–215 ( 1992).

    Article  CAS  Google Scholar 

  43. Ward, L. M. Supramodal and modality-specific mechanisms for stimulus-driven shifts of auditory and visual attention. Can. J. Exp. Psychol. 48, 242–259 (1994).

    Article  CAS  Google Scholar 

  44. Farah, M. J., Wong, A. B., Monheit, M .A. & Morrow, L. A. Parietal lobe mechanisms of spatial attention: modality-specific or supramodal? Neuropsychologia 27, 461– 470 (1989).

    Article  CAS  Google Scholar 

  45. Soroker, N., Calamaro, N., Glicksohn, J. & Myslobodsky, M. S. Auditory inattention in right-hemisphere-damaged patients with and without visual neglect. Neuropsychologia 35, 249 –256 (1997).

    Article  CAS  Google Scholar 

  46. Herscovitch, P., Markham, J. & Raichle, M. E. Brain blood flow measured with intravenous H2(15)O. I. Theory and error analysis. J. Nucl. Med. 24, 782–789 (1983).

    CAS  PubMed  Google Scholar 

  47. Woods, R. P., Cherry, S. R. & Mazziotta, J. C. Rapid automated algorithm for aligning and reslicing PET images. J. Comput. Assist. Tomogr. 16, 620–633 (1992).

    Article  CAS  Google Scholar 

  48. Lacquaniti, F. et al. Visuomotor transformations for reaching to memorized targets: a PET study. Neuroimage 5, 129– 146 (1997).

    Article  CAS  Google Scholar 

  49. Friston, K.J. Testing for anatomically specified regional effects. Hum. Brain Mapp. 5, 133–136 ( 1997).

    Article  CAS  Google Scholar 

  50. Price, C. J. & Friston, K. J. Cognitive conjunction: a new approach to brain activation experiments. Neuroimage 5, 261–270 (1997).

    Article  CAS  Google Scholar 

Download references

Acknowledgements

We thank Devera G. Schoenberg for editing the manuscript and Nguyet Dang and George Dold for their assistance with computer programming.

Author information

Authors and Affiliations

  1. Human Motor Control Section, Medical Neurology Branch, National Institute of Neurological Disorders and Stroke, National Institutes of Health, Building 10, Room 5N226, MSC 1428, 10 Center Drive, Bethesda, 20892, Maryland

    Khalafalla O. Bushara, Robert A. Weeks, Kenji Ishii, Maria-Jose Catalan & Mark Hallett

  2. Institute for Cognitive and Computational Sciences, Georgetown University Medical Center, 3970 Reservoir Road, N.W. , Washington, 20007 , District of Columbia, USA

    Biao Tian & Josef P. Rauschecker

Authors
  1. Khalafalla O. Bushara
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Robert A. Weeks
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Kenji Ishii
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Maria-Jose Catalan
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Biao Tian
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Josef P. Rauschecker
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Mark Hallett
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Mark Hallett.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Bushara, K., Weeks, R., Ishii, K. et al. Modality-specific frontal and parietal areas for auditory and visual spatial localization in humans. Nat Neurosci 2, 759–766 (1999). https://doi.org/10.1038/11239

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1038/11239

This article is cited by

Search

Advanced 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