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.

  • Perspective
  • Published:

Unraveling the principles of auditory cortical processing: can we learn from the visual system?

Abstract

Studies of auditory cortex are often driven by the assumption, derived from our better understanding of visual cortex, that basic physical properties of sounds are represented there before being used by higher-level areas for determining sound-source identity and location. However, we only have a limited appreciation of what the cortex adds to the extensive subcortical processing of auditory information, which can account for many perceptual abilities. This is partly because of the approaches that have dominated the study of auditory cortical processing to date, and future progress will unquestionably profit from the adoption of methods that have provided valuable insights into the neural basis of visual perception. At the same time, we propose that there are unique operating principles employed by the auditory cortex that relate largely to the simultaneous and sequential processing of previously derived features and that therefore need to be studied and understood in their own right.

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

Access options

Buy this article

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

Similar content being viewed by others

References

  1. Brown, C.H. & May, B.J. Comparative mammalian sound localization. in Sound Source Localization, Springer Handbook of Auditory Research (eds. Popper, A.N. & Fay, R.R.) 124–178 (Springer, New York, 2005).

    Chapter  Google Scholar 

  2. DeValois, R.L. & DeValois, K.K. Spatial Vision. Oxford Psychology Series 14 (Oxford University Press, Oxford, UK, 1990).

    Google Scholar 

  3. Tyler, C.W. & Hamer, R.D. Analysis of visual modulation sensitivity. IV. Validity of the Ferry-Porter law. J. Opt. Soc. Am. A 7, 743–758 (1990).

    Article  CAS  Google Scholar 

  4. Viemeister, N.F. & Plack, C.J. Time analysis. in Human Psychophysics, Springer Handbook of Auditory Research (eds. Yost, W.A., Popper, A.N. & Fay, R.R.) 116–154 (Springer, New York, 1993).

    Google Scholar 

  5. Hirsch, J.A. & Martinez, L.M. Circuits that build visual cortical receptive fields. Trends Neurosci. 29, 30–39 (2006).

    Article  CAS  Google Scholar 

  6. Palmer, A.R. Anatomy and physiology of the auditory brainstem. in Auditory Evoked Potentials (eds. Burkard, R.F., Don, M. & Eggermont, J.J.) 200–228 (Lippincott Williams and Wilkins, Baltimore, 2007).

    Google Scholar 

  7. Nelken, I., Fishbach, A., Las, L., Ulanovsky, N. & Farkas, D. Primary auditory cortex of cats: feature detection or something else? Biol. Cybern. 89, 397–406 (2003).

    Article  Google Scholar 

  8. 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).

    Article  CAS  Google Scholar 

  9. Clarey, J.C., Barone, P. & Imig, T.J. Physiology of thalamus and cortex. in The Mammalian Auditory Pathway: Neurophysiology. Springer Handbook of Auditory Research (eds. Popper, A.N. & Fay, R.R.) 232–335 (Springer, New York, 1992).

    Chapter  Google Scholar 

  10. Wang, X., Lu, T., Snider, R.K. & Liang, L. Sustained firing in auditory cortex evoked by preferred stimuli. Nature 435, 341–346 (2005).

    Article  CAS  Google Scholar 

  11. Hromádka, T., Deweese, M.R. & Zador, A.M. Sparse representation of sounds in the unanesthetized auditory cortex. PLoS Biol. 6, e16 (2008).

    Article  Google Scholar 

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

    Article  CAS  Google Scholar 

  13. Schnupp, J.W.H., Mrsic-Flogel, T.D. & King, A.J. Linear processing of spatial cues in primary auditory cortex. Nature 414, 200–204 (2001).

    Article  CAS  Google Scholar 

  14. Fritz, J.B., Elhilali, M. & Shamma, S.A. Differential dynamic plasticity of A1 receptive fields during multiple spectral tasks. J. Neurosci. 25, 7623–7635 (2005).

    Article  CAS  Google Scholar 

  15. Bar-Yosef, O. & Nelken, I. The effects of background noise on the neural responses to natural sounds in cat primary auditory cortex. Front. Comput. Neurosci. 1, 1–14 (2007).

    Article  Google Scholar 

  16. Machens, C.K., Wehr, M.S. & Zador, A.M. Linearity of cortical receptive fields measured with natural sounds. J. Neurosci. 24, 1089–1100 (2004).

    Article  CAS  Google Scholar 

  17. Serre, T., Oliva, A. & Poggio, T. A feedforward architecture accounts for rapid categorization. Proc. Natl. Acad. Sci. USA 104, 6424–6429 (2007).

    Article  CAS  Google Scholar 

  18. Kiani, R., Esteky, H., Mirpour, K. & Tanaka, K. Object category structure in response patterns of neuronal population in monkey inferior temporal cortex. J. Neurophysiol. 97, 4296–4309 (2007).

    Article  Google Scholar 

  19. Martinez, L.M. et al. Receptive field structure varies with layer in the primary visual cortex. Nat. Neurosci. 8, 372–379 (2005).

    Article  CAS  Google Scholar 

  20. Ohki, K. et al. Highly ordered arrangement of single neurons in orientation pinwheels. Nature 442, 925–928 (2006).

    Article  CAS  Google Scholar 

  21. Schreiner, C.E. & Winer, J.A. Auditory cortex mapmaking: principles, projections and plasticity. Neuron 56, 356–365 (2007).

    Article  CAS  Google Scholar 

  22. Linden, J.F. & Schreiner, C.E. Columnar transformations in auditory cortex? A comparison to visual and somatosensory cortices. Cereb. Cortex 13, 83–89 (2003).

    Article  Google Scholar 

  23. Tanaka, K. Inferotemporal cortex and object vision. Annu. Rev. Neurosci. 19, 109–139 (1996).

    Article  CAS  Google Scholar 

  24. Wollberg, Z. & Newman, J.D. Auditory cortex of squirrel monkey: response patterns of single cells to species-specific vocalizations. Science 175, 212–214 (1972).

    Article  CAS  Google Scholar 

  25. Chechik, G. et al. Reduction of information redundancy in the ascending auditory pathway. Neuron 51, 359–368 (2006).

    Article  CAS  Google Scholar 

  26. Suga, N. Principles of auditory information-processing derived from neuroethology. J. Exp. Biol. 146, 277–286 (1989).

    CAS  PubMed  Google Scholar 

  27. Joris, P.X., Schreiner, C.E. & Rees, A. Neural processing of amplitude-modulated sounds. Physiol. Rev. 84, 541–577 (2004).

    Article  CAS  Google Scholar 

  28. Chi, T., Ru, P. & Shamma, S.A. Multiresolution spectrotemporal analysis of complex sounds. J. Acoust. Soc. Am. 118, 887–906 (2005).

    Article  Google Scholar 

  29. Ulanovsky, N., Las, L. & Nelken, I. Processing of low-probability sounds by cortical neurons. Nat. Neurosci. 6, 391–398 (2003).

    Article  CAS  Google Scholar 

  30. Weinberger, N.M. Specific long-term memory traces in primary auditory cortex. Nat. Rev. Neurosci. 5, 279–290 (2004).

    Article  CAS  Google Scholar 

  31. King, A.J. et al. Physiological and behavioral studies of spatial coding in the auditory cortex. Hear. Res. 229, 106–115 (2007).

    Article  Google Scholar 

  32. Polley, D.B., Steinberg, E.E. & Merzenich, M.M. Perceptual learning directs auditory cortical map reorganization through top-down influences. J. Neurosci. 26, 4970–4982 (2006).

    Article  CAS  Google Scholar 

  33. Schnupp, J.W.H., Hall, T.M., Kokelaar, R.F. & Ahmed, B. Plasticity of temporal pattern codes for vocalization stimuli in primary auditory cortex. J. Neurosci. 26, 4785–4795 (2006).

    Article  CAS  Google Scholar 

  34. Kobatake, E., Wang, G. & Tanaka, K. Effects of shape-discrimination training on the selectivity of inferotemporal cells in adult monkeys. J. Neurophysiol. 80, 324–330 (1998).

    Article  CAS  Google Scholar 

  35. Yang, T. & Maunsell, J.H. The effect of perceptual learning on neuronal responses in monkey visual area V4. J. Neurosci. 24, 1617–1626 (2004).

    Article  Google Scholar 

  36. Suga, N. Role of corticofugal feedback in hearing. J. Comp. Physiol. A Neuroethol. Sens. Neural. Behav. Physiol. 194, 169–183 (2008).

    Article  Google Scholar 

  37. Ungerleider, L.G. & Haxby, J.V. 'What' and 'where' in the human brain. Curr. Opin. Neurobiol. 4, 157–165 (1994).

    Article  CAS  Google Scholar 

  38. Alain, C., Arnott, S.R., Hevenor, S., Graham, S. & Grady, C.L. 'What' and 'where' in the human auditory system. Proc. Natl. Acad. Sci. USA 98, 12301–12306 (2001).

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  40. Kaas, J.H. & Hackett, T.A. 'What' and 'where' processing in auditory cortex. Nat. Neurosci. 2, 1045–1047 (1999).

    Article  CAS  Google Scholar 

  41. Lomber, S.G. & Malhotra, S. Double dissociation of 'what' and 'where' processing in auditory cortex. Nat. Neurosci. 11, 609–616 (2008).

    Article  CAS  Google Scholar 

  42. Ghazanfar, A.A. & Schroeder, C.E. Is neocortex essentially multisensory? Trends Cogn. Sci. 10, 278–285 (2006).

    Article  Google Scholar 

  43. Harrington, I.A., Stecker, G.C., Macpherson, E.A. & Middlebrooks, J.C. Spatial sensitivity of neurons in the anterior, posterior, and primary fields of cat auditory cortex. Hear. Res. 240, 22–41 (2008).

    Article  Google Scholar 

  44. Recanzone, G.H. Representation of con-specific vocalizations in the core and belt areas of the auditory cortex in the alert macaque monkey. J. Neurosci. 28, 13184–13193 (2008).

    Article  CAS  Google Scholar 

  45. Bizley, J.K., Walker, K.M.M., Silverman, B.W., King, A.J. & Schnupp, J.W.H. Interdependent encoding of pitch, timbre and spatial location in auditory cortex. J. Neurosci. 29, 2064–2075 (2009).

    Article  CAS  Google Scholar 

  46. Salzman, C.D., Britten, K.H. & Newsome, W.T. Cortical microstimulation influences perceptual judgments of motion direction. Nature 346, 174–177 (1990).

    Article  CAS  Google Scholar 

  47. Otto, K.J., Rousche, P.J. & Kipke, D.R. Microstimulation in auditory cortex provides a substrate for detailed behaviors. Hear. Res. 210, 112–117 (2005).

    Article  Google Scholar 

  48. Yang, Y., DeWeese, M.R., Otazu, G.H. & Zador, A.M. Millisecond-scale differences in neural activity in auditory cortex can drive decisions. Nat. Neurosci. 11, 1262–1263 (2008).

    Article  CAS  Google Scholar 

  49. Huber, D. et al. Sparse optical microstimulation in barrel cortex drives learned behavior in freely moving mice. Nature 451, 61–64 (2008).

    Article  CAS  Google Scholar 

  50. Hubel, D.H., Henson, C.O., Rupert, A. & Galambos, R. Attention units in the auditory cortex. Science 129, 1279–1280 (1959).

    Article  CAS  Google Scholar 

Download references

Acknowledgements

We are grateful to B. Willmore for discussions. Financial support was provided by the Wellcome Trust (a Principal Research Fellowship to A.J.K.) and by the Israeli Science Foundation (I.N.).

Author information

Authors and Affiliations

Authors

Corresponding authors

Correspondence to Andrew J King or Israel Nelken.

Rights and permissions

Reprints and permissions

About this article

Cite this article

King, A., Nelken, I. Unraveling the principles of auditory cortical processing: can we learn from the visual system?. Nat Neurosci 12, 698–701 (2009). https://doi.org/10.1038/nn.2308

Download citation

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/nn.2308

This article is cited by

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