Abstract
We examine the functional characteristics of auditory cortical areas that are sensitive to spatial cues in the human brain, and determine whether they can be dissociated from parietal lobe mechanisms. Three positron emission tomography (PET) experiments were conducted using a speaker array permitting quasi free-field sound presentation within the scanner. Posterior auditory cortex responded to sounds that varied in their spatial distribution, but only when multiple complex stimuli were presented simultaneously, implicating this cortical system in disambiguation of overlapping auditory sources. We also found that the right inferior parietal cortex is specifically recruited in localization tasks, and that its activity predicts behavioral performance, consistent with its involvement in sensorimotor integration and spatial transformation. These findings clarify the functional roles of posterior auditory and parietal cortices, and help to reconcile competing models of auditory cortical organization.
This is a preview of subscription content, access via your institution
Access options
Subscribe to this journal
Receive 12 print issues and online access
$209.00 per year
only $17.42 per issue
Buy this article
- Purchase on Springer Link
- Instant access to full article PDF
Prices may be subject to local taxes which are calculated during checkout
Similar content being viewed by others
References
Rauschecker, J.P. & Tian, B. Mechanisms and streams for processing of “what” and “where” in auditory cortex. Proc. Nat. Acad. Sci. USA 97, 11800–11806 (2000).
Ungerleider, L. & Haxby, J. “What” and “where” in the human brain. Curr. Biol. 4, 157–165 (1994).
Rauschecker, J.P., Tian, B., Pons, T. & Mishkin, M. Serial and parallel processing in Rhesus monkey auditory cortex. J. Comp. Neurol. 382, 89–103 (1997).
Romanski, L. et al. Dual streams of auditory afferents target multiple domains in the primate prefrontal cortex. Nat. Neurosci. 2, 1131–1136 (1999).
Rauschecker, J.P., Tian, B. & Hauser, M. Processing of complex sounds in the Macaque nonprimary auditory cortex. Science 268, 111–114 (1995).
Recanzone, G.H., Guard, D.C., Phan, M.L. & Su, T.-I.K. Correlation between the activity of single auditory cortical neurons and sound-localization behavior in the Macaque monkey. J. Neurophysiol. 83, 2723–2739 (2000).
Tian, B., Reser, D., Durham, A., Kustov, A. & Rauschecker, J.P. Functional specialization in Rhesus monkey auditory cortex. Science 292, 290–293 (2001).
Clarke, S., Bellman, A., Meuli, R., Assal, G. & Steck, A. Auditory agnosia and auditory spatial deficits following left hemispheric lesions: evidence for distinct processing pathways. Neuropsychologia 38, 797–807 (2000).
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).
Furukawa, S., Xu, L. & Middlebrooks, J.C. Coding of sound-source location by ensembles of cortical neurons. J. Neurosci. 20, 1216–1228 (2000).
Brugge, J., Reale, R., Jenison, R. & Schnupp, J.W.H. Auditory cortical spatial receptive fields. Audiol. Neurootol. 6, 173–177 (2001).
Cohen, Y.E. & Wessinger, C.M. Who goes there? Neuron 24, 769–771 (1999).
Belin, P. & Zatorre, R.J. What, where and how in auditory cortex. Nat. Neurosci. 3, 965–966 (2000).
Griffiths, T.D., Green, G.G.R., Rees, A. & Rees, G. Human brain areas involved in the analysis of auditory movement. Hum. Brain Mapp. 9, 72–80 (2000).
Bushara, K. et al. Modality-specific frontal and parietal areas for auditory and visual spatial localization in humans. Nat. Neurosci. 2, 759–766 (1999).
Weeks, R. et al. A positron emission tomographic study of auditory localization in the congenitally blind. J. Neurosci. 20, 2664–2672 (2000).
Alain, C., Arnott, S.R., Hevenor, S., Graham, S. & Grady, C.L. “What” and “where” in the human auditory system. Proc. Nat. Acad. Sci. USA 98, 12301–12306 (2001).
Maeder, P. et al. Distinct pathways involved in sound recognition and localization: a human fMRI study. Neuroimage 14, 802–816 (2001).
Zatorre, R.J., Mondor, T.A. & Evans, A.C. Functional activation of right parietal and frontal cortex during auditory attention to space and frequency. Neuroimage 10, 544–554 (1999).
Andersen, R.A. Encoding of intention and spatial location in the posterior parietal cortex. Cereb. Cortex 5, 457–469 (1995).
Wightman, F.L. & Kistler, D.J. Headphone simulation of free-field listening: II. Psychophysical validation. J. Acoust. Soc. Am. 85, 868–878 (1989).
Middlebrooks, J. Virtual localization improved by scaling nonindividualized external-ear transfer functions in frequency. J. Acoust. Soc. Am. 106, 1493–1510 (1999).
Mrsic-Flogel, T.D., King, A.J., Jenison, R.L. & Schnupp, J.W.H. Listening through different ears alters spatial response fields in ferret primary auditory cortex. J. Neurophysiol. 86, 1043–1046 (2001).
Grill-Spector, K. & Malach, R. fMR-adaptation: a tool for studying the functional properties of human cortical neurons. Acta Psychol. 107, 293–321 (2001).
Penhune, V.B., Zatorre, R.J., MacDonald, J.D. & Evans, A.C. Interhemispheric anatomical differences in human primary auditory cortex: probabilistic mapping and volume measurement from magnetic resonance scans. Cereb. Cortex 6, 661–672 (1996).
Westbury, C.F., Zatorre, R.J. & Evans, A.C. Quantifying variability in the planum temporale: a probability map. Cereb. Cortex 9, 392–405 (1999).
Galaburda, A.M. & Sanides, F. Cytoarchitectonic organization of the human auditory cortex. J. Comp. Neurol. 190, 597–610 (1980).
Mesulam, M. Spatial attention and neglect: parietal, frontal and cingulate contributions to the mental representation and attentional targeting of salient extrapersonal events. Phil. Transac. Roy. Soc. Lon. 354, 1325–1346 (1999).
Zatorre, R.J. & Penhune, V.B. Spatial localization after excision of human auditory cortex. J. Neurosci. 21, 6321–6328 (2001).
Thivard, L., Belin, P., Zilbovicius, M., Poline, J. & Samson, Y. A cortical region sensitive to auditory spectral motion. Neuroreport 11, 2969–2972 (2000).
Warren, J., Zielinski, B., Green, G., Rauschecker, J. & Griffiths, T. Analysis of sound source motion by the human brain. Neuron 34, 139–148 (2002).
Sereno, A. & Maunsell, J. Shape selectivity in primate lateral intraparietal cortex. Nature 395, 500–503 (1998).
Mondor, T.A., Zatorre, R.J. & Terrio, N.A. Constraints on the selection of auditory information. J. Exp. Psychol. Hum. Percept. Perform. 24, 66–79 (1998).
Bregman, A. Auditory Scene Analysis (MIT Press, Cambridge, Massachusetts, 1990).
Baumgart, F., Gaschler-Markefski, B., Woldorff, M., Heinze, H.-J. & Scheich, H. A movement-sensitive area in auditory cortex. Nature 400, 724–725 (1999).
Efron, R., Crandall, P., Koss, B., Divenyi, P. & Yund, E. Central auditory processing III. The “cocktail party” effect and anterior temporal lobectomy. Brain Lang. 19, 254–263 (1983).
Lewis, J. & Van Essen, D. Corticocortical connections of visual, sensorimotor, and multimodal processing areas in the parietal lobe of the macaque monkey. J. Comp. Neurol. 428, 112–137 (2000).
Whitfield, I. in Cerebral Cortex. (eds. Peters, A. & Jones, E.) 329–351 (Plenum, New York, 1985).
Griffiths, T.D. et al. Right parietal cortex is involved in the perception of sound movement in humans. Nat. Neurosci. 1, 74–79 (1998).
Brungart, D.S. & Rabinowitz, W.M. Auditory localization of nearby sources. Head-related transfer functions. J. Acoust. Soc. Am. 106, 1465–1479 (1999).
Brungart, D.S., Durlach, N.I. & Rabinowitz, W.M. Auditory localization of nearby sources. II. Localization of a broadband source. J. Acoust. Soc. Am. 106, 1956–1968 (1999).
Worsley, K., Evans, A., Marrett, S. & Neelin, P. A three-dimensional statistical analysis for CBF activation studies in human brain. J. Cereb. Blood Flow Metab. 12, 900–918 (1992).
Paus, T., Perry, D., Zatorre, R., Worsley, K. & Evans, A. Modulation of cerebral blood-flow in the human auditory cortex during speech: role of motor-to-sensory discharges. Eur. J. Neurosci. 8, 2236–2246 (1996).
Talairach, J. & Tournoux, P. Co-Planar Stereotaxic Atlas of the Human Brain (Thieme Medical, New York, 1988).
Acknowledgements
This work was supported by operating grants from the Canadian Institutes of Health Research and the McDonnell-Pew Cognitive Neuroscience Program. We thank A.C. Evans, B. Pike and the staff of the McConnell Brain Imaging Centre for their assistance, and J. Rauschecker for comments on an earlier version of this manuscript.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Competing interests
The authors declare no competing financial interests.
Supplementary information
Rights and permissions
About this article
Cite this article
Zatorre, R., Bouffard, M., Ahad, P. et al. Where is 'where' in the human auditory cortex?. Nat Neurosci 5, 905–909 (2002). https://doi.org/10.1038/nn904
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1038/nn904
This article is cited by
-
Audiovisual adaptation is expressed in spatial and decisional codes
Nature Communications (2022)
-
Cortical mechanisms of spatial hearing
Nature Reviews Neuroscience (2019)
-
Phenomenology of Voice-Hearing in Psychosis Spectrum Disorders: a Review of Neural Mechanisms
Current Behavioral Neuroscience Reports (2019)
-
Neural Representation of Interaural Time Differences in Humans—an Objective Measure that Matches Behavioural Performance
Journal of the Association for Research in Otolaryngology (2016)
-
Neural Mechanisms Underlying Musical Pitch Perception and Clinical Applications Including Developmental Dyslexia
Current Neurology and Neuroscience Reports (2015)