Linear processing of spatial cues in primary auditory cortex

Abstract

To determine the direction of a sound source in space, animals must process a variety of auditory spatial cues, including interaural level and time differences, as well as changes in the sound spectrum caused by the direction-dependent filtering of sound by the outer ear1. Behavioural deficits observed when primary auditory cortex (A1) is damaged have led to the widespread view that A1 may have an essential role in this complex computational task2,3,4,5. Here we show, however, that the spatial selectivity exhibited by the large majority of A1 neurons is well predicted by a simple linear model, which assumes that neurons additively integrate sound levels in each frequency band and ear. The success of this linear model is surprising, given that computing sound source direction is a necessarily nonlinear operation6,7,8,9. However, because linear operations preserve information, our results are consistent with the hypothesis that A1 may also form a gateway to higher, more specialized cortical areas10,11.

Access options

Rent or Buy article

Get time limited or full article access on ReadCube.

from$8.99

All prices are NET prices.

Figure 1: Predicting spatial responses from frequency-filtering characteristics.
Figure 2: Examples of binaural FTRFs, shown alongside observed and predicted SRFs for six units.
Figure 3
Figure 4: Predicting changes in SRF structure for own-ear and foreign-ear stimuli.

References

  1. 1

    King, A. J., Schnupp, J. W. H. & Doubell, T. P. The shape of ears to come: dynamic coding of auditory space. Trends Cogn. Sci. 5, 261–270 (2001).

    Article  Google Scholar 

  2. 2

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

    CAS  Article  Google Scholar 

  3. 3

    Kavanagh, G. L. & Kelly, J. B. Contribution of auditory cortex to sound localization by the ferret (Mustela putorius). J. Neurophysiol. 57, 1746–1766 (1987).

    CAS  Article  Google Scholar 

  4. 4

    Masterton, R. B. in Acoustical Signal Processing in the Central Auditory System (ed. Syka, J.) 1–17 (Plenum, New York, 1997).

    Google Scholar 

  5. 5

    Heffner, H. E. & Heffner, R. S. Effect of bilateral auditory cortex lesions on sound localization in Japanese macaques. J. Neurophysiol. 64, 915–931 (1990).

    CAS  Article  Google Scholar 

  6. 6

    Goldberg, J. M. & Brown, P. B. Response of binaural neurons of dog superior olivary complex to dichotic tonal stimuli: some physiological mechanisms of sound localisation. J. Neurophysiol. 32, 613–636 (1969).

    CAS  Article  Google Scholar 

  7. 7

    Kitzes, L. M., Wrege, K. S. & Cassady, J. M. Patterns of responses of cortical cells to binaural stimulation. J. Comp. Neurol. 192, 455–472 (1980).

    CAS  Article  Google Scholar 

  8. 8

    Yu, J. J. & Young, E. D. Linear and nonlinear pathways of spectral information transmission in the cochlear nucleus. Proc. Natl Acad. Sci. USA 97, 11780–11786 (2000).

    ADS  CAS  Article  Google Scholar 

  9. 9

    Peña, J. L. & Konishi, M. Auditory spatial receptive fields created by multiplication. Science 292, 249–252 (2001).

    ADS  Article  Google Scholar 

  10. 10

    Tian, B., Reser, D., Durham, A., Kustov, A. & Rauschecker, J. P. Functional specialization in rhesus monkey auditory cortex. Science 292, 290–293 (2001).

    ADS  CAS  Article  Google Scholar 

  11. 11

    Recanzone, G. H., Guard, D. C., Phan, M. L. & Su, T. K. Correlation between the activity of single auditory cortical neurons and sound-localization behavior in the macaque monkey. J. Neurophysiol. 83, 2723–2739 (2000).

    CAS  Article  Google Scholar 

  12. 12

    Wightman, F. L. & Kistler, D. J. in Human Psychophysics (eds Yost, W. A., Popper, A. N. & Fay, R. R.) 155–192 (Springer, New York, 1993).

    Google Scholar 

  13. 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).

    ADS  CAS  Article  Google Scholar 

  14. 14

    Wightman, F. L. & Kistler, D. J. Monaural sound localization revisited. J. Acoust. Soc. Am. 101, 1050–1063 (1997).

    ADS  CAS  Article  Google Scholar 

  15. 15

    Clarke, S., Bellmann, A., Meuli, R. A., Assal, G. & Steck, A. J. Auditory agnosia and auditory spatial deficits following left hemispheric lesions: evidence for distinct processing pathways. Neuropsychologia 38, 797–807 (2000).

    CAS  Article  Google Scholar 

  16. 16

    deCharms, R. C., Blake, D. T. & Merzenich, M. M. Optimizing sound features for cortical neurons. Science 280, 1439–1443 (1998).

    ADS  CAS  Article  Google Scholar 

  17. 17

    Kowalski, N., Depireux, D. A. & Shamma, S. A. Analysis of dynamic spectra in ferret primary auditory cortex. II. Prediction of unit responses to arbitrary dynamic spectra. J. Neurophysiol. 76, 3524–3534 (1996).

    CAS  Article  Google Scholar 

  18. 18

    Movshon, J. A., Thompson, I. D. & Tolhurst, D. J. Spatial summation in the receptive fields of simple cells in the cat's striate cortex. J. Physiol. Lond. 283, 53–77 (1978).

    CAS  Article  Google Scholar 

  19. 19

    Phillips, D. P., Judge, P. W. & Kelly, J. B. Primary auditory cortex in the ferret (Mustela putorius): neural response properties and topographic organization. Brain Res. 443, 281–294 (1988).

    CAS  Article  Google Scholar 

  20. 20

    Carlile, S. The auditory periphery of the ferret. II: The spectral transformations of the external ear and their implications for sound localization. J. Acoust. Soc. Am. 88, 2196–2204 (1990).

    ADS  CAS  Article  Google Scholar 

  21. 21

    Clarey, J. C., Barone, P. & Imig, T. J. in The Mammalian Auditory Pathway: Neurophysiology (eds Popper, A. & Fay, R.) 232–334 (Springer, New York, 1992).

    Google Scholar 

  22. 22

    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).

    CAS  Article  Google Scholar 

  23. 23

    Brugge, J. F. et al. Simulation of free-field sound sources and its application to studies of cortical mechanisms of sound localization in the cat. Hear. Res. 73, 67–84 (1994).

    CAS  Article  Google Scholar 

  24. 24

    Middlebrooks, J. C. & Pettigrew, J. D. Functional classes of neurons in primary auditory cortex of the cat distinguished by sensitivity to sound location. J. Neurosci. 1, 107–120 (1981).

    CAS  Article  Google Scholar 

  25. 25

    Samson, F. K., Barone, P., Clarey, J. C. & Imig, T. J. Effects of ear plugging on single-unit azimuth sensitivity in cat primary auditory cortex. II. Azimuth tuning dependent upon binaural stimulation. J. Neurophysiol. 71, 2194–2216 (1994).

    CAS  Article  Google Scholar 

  26. 26

    Ruggero, M. A. in The Mammalian Auditory Pathway: Neurophysiology (eds Popper, A. N. & Fay, R. R.) 34–93 (Springer, New York, 1992).

    Google Scholar 

  27. 27

    Schreiner, C. E. Spatial distribution of responses to simple and complex sounds in the primary auditory cortex. Audiol. Neurootol. 3, 104–122 (1998).

    CAS  Article  Google Scholar 

  28. 28

    Read, H. L., Winer, J. A. & Schreiner, C. E. Modular organization of intrinsic connections associated with spectral tuning in cat auditory cortex. Proc. Natl Acad. Sci. USA 98, 8042–8047 (2001).

    ADS  CAS  Article  Google Scholar 

  29. 29

    Wang, X. On cortical coding of vocal communication sounds in primates. Proc. Natl Acad. Sci. USA 97, 11843–11849 (2000).

    ADS  CAS  Article  Google Scholar 

  30. 30

    Nelken, I., Rotman, Y. & Bar Yosef, O. Responses of auditory-cortex neurons to structural features of natural sounds. Nature 397, 154–157 (1999).

    ADS  CAS  Article  Google Scholar 

Download references

Acknowledgements

We are grateful to D. Moore and A. Parker for comments on an earlier draft of this manuscript. This work was supported by Defeating Deafness (Dunhill Research Fellowship to J.W.H.S.) and by the Wellcome Trust (Wellcome Prize Studentship to T.D.M.F. and Wellcome Senior Research Fellowship to A.J.K.).

Author information

Affiliations

Authors

Corresponding author

Correspondence to Jan W. H. Schnupp.

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Schnupp, J., Mrsic-Flogel, T. & King, A. Linear processing of spatial cues in primary auditory cortex. Nature 414, 200–204 (2001). https://doi.org/10.1038/35102568

Download citation

Further reading

Comments

By submitting a comment you agree to abide by our Terms and Community Guidelines. If you find something abusive or that does not comply with our terms or guidelines please flag it as inappropriate.

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