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:

Neural correlates of categorical perception in learned vocal communication

Nature Neuroscience volume 12, pages 221–228 (2009)Cite this article

Abstract

The division of continuously variable acoustic signals into discrete perceptual categories is a fundamental feature of vocal communication, including human speech. Despite the importance of categorical perception to learned vocal communication, the neural correlates underlying this phenomenon await identification. We found that individual sensorimotor neurons in freely behaving swamp sparrows expressed categorical auditory responses to changes in note duration, a learned feature of their songs, and that the neural response boundary accurately predicted the categorical perceptual boundary measured in field studies of the same sparrow population. Furthermore, swamp sparrow populations that learned different song dialects showed different categorical perceptual boundaries that were consistent with the boundary being learned. Our results extend the analysis of the neural basis of perceptual categorization into the realm of vocal communication and advance the learned vocalizations of songbirds as a model for investigating how experience shapes categorical perception and the activity of categorically responsive neurons.

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: Earlier behavioral tests with swamp sparrows reveal categorical perception of changes in individual song notes.
Figure 2: Extracellular recordings reveal differences in the auditory response of identified single units in nucleus HVC.
Figure 3: Manipulation of song note duration reveals categorical auditory responses of HVCX neurons.
Figure 4: The perceptual boundary in swamp sparrows' categorization of note duration was predicted by the categorical boundary evident in auditory responses of HVCX neurons.
Figure 5: Categorical responses were evoked by changes in specific features of individual notes in the syllable.

Similar content being viewed by others

References

  1. Miller, E.K., Nieder, A., Freedman, D.J. & Wallis, J.D. Neural correlates of categories and concepts. Curr. Opin. Neurobiol. 13, 198–203 (2003).

    Article  CAS  Google Scholar 

  2. Bregman, A. Auditory Scene Analysis (MIT Press, Cambridge, Massachusetts, 1990).

    Book  Google Scholar 

  3. Liberman, A.M., Harris, K.S., Hoffman, H.S. & Griffith, B.C. The discrimination of speech sounds within and across phoneme boundaries. J. Exp. Psychol. 54, 358–368 (1957).

    Article  CAS  Google Scholar 

  4. Liberman, A.M., Harris, K.S., Kinney, J.A. & Lane, H. The discrimination of relative onset-time of the components of certain speech and nonspeech patterns. J. Exp. Psychol. 61, 379–388 (1961).

    Article  CAS  Google Scholar 

  5. May, B., Moody, D.B. & Stebbins, W.C. Categorical perception of conspecific communication sounds by Japanese macaques, Macaca fuscata. J. Acoust. Soc. Am. 85, 837–847 (1989).

    Article  CAS  Google Scholar 

  6. Kuhl, P.K. & Miller, J.D. Speech-perception by chinchilla: phonetic boundaries for synthetic VOT stimuli. J. Acoust. Soc. Am. 57, S49–S50 (1975).

    Article  Google Scholar 

  7. Nelson, D.A. & Marler, P. Categorical perception of a natural stimulus continuum: birdsong. Science 244, 976–978 (1989).

    Article  CAS  Google Scholar 

  8. Baugh, A.T., Akre, K.L. & Ryan, M.J. Categorical perception of a natural, multivariate signal: mating call recognition in tungara frogs. Proc. Natl. Acad. Sci. USA 105, 8985–8988 (2008).

    Article  CAS  Google Scholar 

  9. Nowak, M.A. & Krakauer, D.C. The evolution of language. Proc. Natl. Acad. Sci. USA 96, 8028–8033 (1999).

    Article  CAS  Google Scholar 

  10. Marler, P. & Peters, S. Sparrows learn adult song and more from memory. Science 213, 780–782 (1981).

    Article  CAS  Google Scholar 

  11. Catchpole, C.K. & Slater, P.J.B. Birdsong: Biological Themes and Variations (Cambridge University Press, New York, 1995).

  12. Marler, P. & Pickert, R. Species-universal microstructure in the learned song of the swamp sparrow (Melospiza georgiana). Anim. Behav. 32, 673–689 (1984).

    Article  Google Scholar 

  13. Clark, C.W., Marler, P. & Beeman, K. Quantitative analysis of animal vocal phonology: an application to swamp sparrow song. Ethology 76, 101–115 (1987).

    Article  Google Scholar 

  14. Nottebohm, F., Stokes, T.M. & Leonard, C.M. Central control of song in the canary, Serinus canarius. J. Comp. Neurol. 165, 457–486 (1976).

    Article  CAS  Google Scholar 

  15. Gentner, T.Q., Hulse, S.H., Bentley, G.E. & Ball, G.F. Individual vocal recognition and the effect of partial lesions to HVc on discrimination, learning and categorization of conspecific song in adult songbirds. J. Neurobiol. 42, 117–133 (2000).

    Article  CAS  Google Scholar 

  16. Brenowitz, E.A. Altered perception of species-specific song by female birds after lesions of a forebrain nucleus. Science 251, 303–305 (1991).

    Article  CAS  Google Scholar 

  17. Yu, A.C. & Margoliash, D. Temporal hierarchical control of singing in birds. Science 273, 1871–1875 (1996).

    Article  CAS  Google Scholar 

  18. Bottjer, S.W., Miesner, E.A. & Arnold, A.P. Forebrain lesions disrupt development, but not maintenance of song in passerine birds. Science 224, 901–903 (1984).

    Article  CAS  Google Scholar 

  19. Hahnloser, R.H., Kozhevnikov, A.A. & Fee, M.S. An ultra-sparse code underlies the generation of neural sequences in a songbird. Nature 419, 65–70 (2002).

    Article  CAS  Google Scholar 

  20. Prather, J.F., Peters, S., Nowicki, S. & Mooney, R. Precise auditory-vocal mirroring in neurons for learned vocal communication. Nature 451, 305–310 (2008).

    Article  CAS  Google Scholar 

  21. Mooney, R., Hoese, W. & Nowicki, S. Auditory representation of the vocal repertoire in a songbird with multiple song types. Proc. Natl. Acad. Sci. USA 98, 12778–12783 (2001).

    Article  CAS  Google Scholar 

  22. Scharff, C., Nottebohm, F. & Cynx, J. Conspecific and heterospecific song discrimination in male zebra finches with lesions in the anterior forebrain pathway. J. Neurobiol. 36, 81–90 (1998).

    Article  CAS  Google Scholar 

  23. Rizzolatti, G. & Craighero, L. The mirror-neuron system. Annu. Rev. Neurosci. 27, 169–192 (2004).

    Article  CAS  Google Scholar 

  24. Fee, M.S. & Leonardo, A. Miniature motorized microdrive and commutator system for chronic neural recording in small animals. J. Neurosci. Methods 112, 83–94 (2001).

    Article  CAS  Google Scholar 

  25. Studdert-Kennedy, M., Liberman, A.M., Harris, K.S. & Cooper, F.S. Theoretical notes. Motor theory of speech perception: a reply to Lane's critical review. Psychol. Rev. 77, 234–249 (1970).

    Article  CAS  Google Scholar 

  26. Wyttenbach, R.A., May, M.L. & Hoy, R.R. Categorical perception of sound frequency by crickets. Science 273, 1542–1544 (1996).

    Article  CAS  Google Scholar 

  27. Freedman, D.J., Riesenhuber, M., Poggio, T. & Miller, E.K. Categorical representation of visual stimuli in the primate prefrontal cortex. Science 291, 312–316 (2001).

    Article  CAS  Google Scholar 

  28. Diehl, R.L., Lotto, A.J. & Holt, L.L. Speech perception. Annu. Rev. Psychol. 55, 149–179 (2004).

    Article  Google Scholar 

  29. Balaban, E. Cultural and genetic variation in swamp sparrows (Melospiza georgiana). Behaviour 105, 250–290 (1988).

    Article  Google Scholar 

  30. Eimas, P.D., Siqueland, E.R., Jusczyk, P. & Vigorito, J. Speech perception in infants. Science 171, 303–306 (1971).

    Article  CAS  Google Scholar 

  31. Ballentine, B., Searcy, W.A. & Nowicki, S. Reliable aggressive signaling in swamp sparrows. Anim. Behav. 75, 693–703 (2008).

    Article  Google Scholar 

  32. Eifuku, S., De Souza, W.C., Tamura, R., Nishijo, H. & Ono, T. Neuronal correlates of face identification in the monkey anterior temporal cortical areas. J. Neurophysiol. 91, 358–371 (2004).

    Article  Google Scholar 

  33. Etcoff, N.L. & Magee, J.J. Categorical perception of facial expressions. Cognition 44, 227–240 (1992).

    Article  CAS  Google Scholar 

  34. Marler, P. & Tamura, M. Culturally transmitted patterns of vocal behavior in sparrows. Science 146, 1483–1486 (1964).

    Article  CAS  Google Scholar 

  35. Kuhl, P.K., Tsao, F.M. & Liu, H.M. Foreign-language experience in infancy: effects of short-term exposure and social interaction on phonetic learning. Proc. Natl. Acad. Sci. USA 100, 9096–9101 (2003).

    Article  CAS  Google Scholar 

  36. Freedman, D.J. & Assad, J.A. Experience-dependent representation of visual categories in parietal cortex. Nature 443, 85–88 (2006).

    Article  CAS  Google Scholar 

  37. Coleman, M.J. & Mooney, R. Synaptic transformations underlying highly selective auditory representations of learned birdsong. J. Neurosci. 24, 7251–7265 (2004).

    Article  CAS  Google Scholar 

  38. Rosen, M.J. & Mooney, R. Synaptic interactions underlying song-selectivity in the avian nucleus HVC revealed by dual intracellular recordings. J. Neurophysiol. 95, 1158–1175 (2006).

    Article  Google Scholar 

  39. Rosen, M.J. & Mooney, R. Inhibitory and excitatory mechanisms underlying auditory responses to learned vocalizations in the songbird nucleus HVC. Neuron 39, 177–194 (2003).

    Article  CAS  Google Scholar 

  40. Mooney, R. & Prather, J.F. The HVC microcircuit: the synaptic basis for interactions between song motor and vocal plasticity pathways. J. Neurosci. 25, 1952–1964 (2005).

    Article  CAS  Google Scholar 

  41. Theunissen, F.E. & Doupe, A.J. Temporal and spectral sensitivity of complex auditory neurons in the nucleus HVc of male zebra finches. J. Neurosci. 18, 3786–3802 (1998).

    Article  CAS  Google Scholar 

  42. Margoliash, D. Acoustic parameters underlying the responses of song-specific neurons in the white-crowned sparrow. J. Neurosci. 3, 1039–1057 (1983).

    Article  CAS  Google Scholar 

  43. Margoliash, D. & Fortune, E.S. Temporal and harmonic combination-sensitive neurons in the zebra finch's HVc. J. Neurosci. 12, 4309–4326 (1992).

    Article  CAS  Google Scholar 

  44. Lewicki, M.S. & Konishi, M. Mechanisms underlying the sensitivity of songbird forebrain neurons to temporal order. Proc. Natl. Acad. Sci. USA 92, 5582–5586 (1995).

    Article  CAS  Google Scholar 

  45. Mooney, R. Different subthreshold mechanisms underlie song selectivity in identified HVc neurons of the zebra finch. J. Neurosci. 20, 5420–5436 (2000).

    Article  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Neurobiology, 101 Research Drive, Duke University Medical Center, Durham, 27710, North Carolina, USA

    Jonathan F Prather, Stephen Nowicki & Richard Mooney

  2. Department of Biology, 125 Science Drive, Duke University, Durham, 27710, North Carolina, USA

    Stephen Nowicki, Rindy C Anderson & Susan Peters

Authors
  1. Jonathan F Prather
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Stephen Nowicki
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Rindy C Anderson
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Susan Peters
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Richard Mooney
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

J.F.P. collected and analyzed neural and behavioral data and wrote the manuscript. S.N. supervised the project, collected behavioral data and edited the manuscript. R.C.A. collected and analyzed behavioral data. S.P. collected and analyzed songs and created acoustic stimuli. R.M. supervised the project and wrote and edited the manuscript.

Corresponding author

Correspondence to Richard Mooney.

Supplementary information

Supplementary Text and Figures

Supplementary Figures 1–6 and Supplementary Methods (PDF 1026 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Prather, J., Nowicki, S., Anderson, R. et al. Neural correlates of categorical perception in learned vocal communication. Nat Neurosci 12, 221–228 (2009). https://doi.org/10.1038/nn.2246

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/nn.2246

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