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:

Temporal plasticity in the primary auditory cortex induced by operant perceptual learning

Abstract

Processing of rapidly successive acoustic stimuli can be markedly improved by sensory training. To investigate the cortical mechanisms underlying such temporal plasticity, we trained rats in a 'sound maze' in which navigation using only auditory cues led to a target location paired with food reward. In this task, the repetition rate of noise pulses increased as the distance between the rat and target location decreased. After training in the sound maze, neurons in the primary auditory cortex (A1) showed greater responses to high-rate noise pulses and stronger phase-locking of responses to the stimuli; they also showed shorter post-stimulation suppression and stronger rebound activation. These improved temporal dynamics transferred to trains of pure-tone pips. Control animals that received identical sound stimulation but were given free access to food showed the same results as naive rats. We conclude that this auditory perceptual learning results in improvements in temporal processing, which may be mediated by enhanced cortical response dynamics.

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

Figure 1: Learning a temporal rate discrimination task.
Figure 2: Training enhances cortical responses to high-rate noise pulses.
Figure 3: Training enhances cortical phase-locked responses.
Figure 4: Training effects on cortical responses to repetitive tone pips.
Figure 5: Spectral tuning bandwidth measured at 30 dB above the threshold.

Similar content being viewed by others

References

  1. Singh, N.C. & Theunissen, F.E. Modulation spectra of natural sounds and ethological theories of auditory processing. J. Acoust. Soc. Am. 114, 3394–3411 (2003).

    Article  Google Scholar 

  2. Shannon, R.V., Zeng, F.G., Kamath, V., Wygonski, J. & Ekelid, M. Speech recognition with primarily temporal cues. Science 270, 303–304 (1995).

    Article  CAS  Google Scholar 

  3. Nagarajan, S.S. et al. Representation of spectral and temporal envelope of twitter vocalizations in common marmoset primary auditory cortex. J. Neurophysiol. 87, 1723–1737 (2002).

    Article  Google Scholar 

  4. Wang, X., Merzenich, M.M., Beitel, R. & Schreiner, C.E. Representation of a species-specific vocalization in the primary auditory cortex of the common marmoset: temporal and spectral characteristics. J. Neurophysiol. 74, 2685–2706 (1995).

    Article  CAS  Google Scholar 

  5. Kanwal, J.S., Matsumura, S., Ohlemiller, K. & Suga, N. Analysis of acoustic elements and syntax in communication sounds emitted by mustached bats. J. Acoust. Soc. Am. 96, 1229–1254 (1994).

    Article  CAS  Google Scholar 

  6. Rosen, S. Temporal information in speech: acoustic, auditory and linguistic aspects. Phil. Trans. R. Soc. Lond. B Biol. Sci. 336, 367–373 (1992).

    Article  CAS  Google Scholar 

  7. Rose, J.E., Brugge, J.F., Anderson, D.J. & Hind, J.E. Phase-locked response to low-frequency tones in single auditory nerve fibers of the squirrel monkey. J. Neurophysiol. 30, 769–793 (1967).

    Article  CAS  Google Scholar 

  8. Johnson, D.H. The relationship between spike rate and synchrony in responses of auditory-nerve fibers to single tones. J. Acoust. Soc. Am. 68, 1115–1122 (1980).

    Article  CAS  Google Scholar 

  9. Joris, P.X. & Yin, T.C. Responses to amplitude-modulated tones in the auditory nerve of the cat. J. Acoust. Soc. Am. 91, 215–232 (1992).

    Article  CAS  Google Scholar 

  10. Frisina, R.D. Subcortical neural coding mechanisms for auditory temporal processing. Hear. Res. 158, 1–27 (2001).

    Article  CAS  Google Scholar 

  11. Schulze, H. & Langner, G. Periodicity coding in the primary auditory cortex of the Mongolian gerbil (Meriones unguiculatus): two different coding strategies for pitch and rhythm? J. Comp. Physiol. [A] 181, 651–663 (1997).

    Article  CAS  Google Scholar 

  12. Schreiner, C.E., Mendelson, J., Raggio, M.W., Brosch, M. & Krueger, K. Temporal processing in cat primary auditory cortex. Acta Otolaryngol. Suppl. 532, 54–60 (1997).

    Article  CAS  Google Scholar 

  13. Eggermont, J.J. Temporal modulation transfer functions in cat primary auditory cortex: separating stimulus effects from neural mechanisms. J. Neurophysiol. 87, 305–321 (2002).

    Article  Google Scholar 

  14. Eggermont, J.J. The magnitude and phase of temporal modulation transfer functions in cat auditory cortex. J. Neurosci. 19, 2780–2788 (1999).

    Article  CAS  Google Scholar 

  15. Lu, T., Liang, L. & Wang, X. Temporal and rate representations of time-varying signals in the auditory cortex of awake primates. Nat. Neurosci. 4, 1131–1138 (2001).

    Article  CAS  Google Scholar 

  16. Ahissar, E. et al. Speech comprehension is correlated with temporal response patterns recorded from auditory cortex. Proc. Natl. Acad. Sci. USA 98, 13367–13372 (2001).

    Article  CAS  Google Scholar 

  17. Nagarajan, S. et al. Cortical auditory signal processing in poor readers. Proc. Natl. Acad. Sci. USA 96, 6483–6488 (1999).

    Article  CAS  Google Scholar 

  18. Temple, E. et al. Disrupted neural responses to phonological and orthographic processing in dyslexic children: an fMRI study. Neuroreport 12, 299–307 (2001).

    Article  CAS  Google Scholar 

  19. Wright, B.A. et al. Deficits in auditory temporal and spectral resolution in language-impaired children. Nature 387, 176–178 (1997).

    Article  CAS  Google Scholar 

  20. Tallal, P. et al. Language comprehension in language-learning impaired children improved with acoustically modified speech. Science 271, 81–84 (1996).

    Article  CAS  Google Scholar 

  21. Merzenich, M.M. et al. Temporal processing deficits of language-learning impaired children ameliorated by training. Science 271, 77–81 (1996).

    Article  CAS  Google Scholar 

  22. Merzenich, M.M. et al. Pervasive Developmental Disorders: Listening Training and Language Abilities in the Changing Nervous System: Neurobehavioral Consequences of Early Brain Disorders (eds. S.H. Broman & J.M. Fletcher) 365–385 (Oxford University Press, Oxford, 1999).

    Google Scholar 

  23. Chang, E.F. & Merzenich, M.M. Environmental noise retards auditory cortical development. Science 300, 498–502 (2003).

    Article  CAS  Google Scholar 

  24. Shepherd, R.K., Hartmann, R., Heid, S., Hardie, N. & Klinke, R. The central auditory system and auditory deprivation: experience with cochlear implants in the congenitally deaf. Acta Otolaryngol. Suppl. 532, 28–33 (1997).

    Article  CAS  Google Scholar 

  25. Ponton, C.W. et al. Auditory system plasticity in children after long periods of complete deafness. Neuroreport 8, 61–65 (1996).

    Article  CAS  Google Scholar 

  26. Ponton, C.W., Moore, J.K. & Eggermont, J.J. Prolonged deafness limits auditory system developmental plasticity: evidence from an evoked potentials study in children with cochlear implants. Scand. Audiol. Suppl. 51, 13–22 (1999).

    CAS  PubMed  Google Scholar 

  27. Kilgard, M.P. & Merzenich, M.M. Plasticity of temporal information processing in the primary auditory cortex. Nat. Neurosci. 1, 727–731 (1998).

    Article  CAS  Google Scholar 

  28. Beitel, R.E., Schreiner, C.E., Cheung, S.W., Wang, X. & Merzenich, M.M. Reward-dependent plasticity in the primary auditory cortex of adult monkeys trained to discriminate temporally modulated signals. Proc. Natl. Acad. Sci. USA 100, 11070–11075 (2003).

    Article  CAS  Google Scholar 

  29. Mardia, K.V. & Jupp, P.E. Directional Statistics (John Wiley and Sons, New York, 2000).

    Google Scholar 

  30. Kilgard, M.P. & Merzenich, M.M. Distributed representation of spectral and temporal information in rat primary auditory cortex. Hear. Res. 134, 16–28 (1999).

    Article  CAS  Google Scholar 

  31. Garabedian, C.E., Jones, S.R., Merzenich, M.M., Dale, A. & Moore, C.I. Band-pass response properties of rat SI neurons. J. Neurophysiol. 90, 1379–1391 (2003).

    Article  Google Scholar 

  32. Krukowski, A.E. & Miller, K.D. Thalamocortical NMDA conductances and intracortical inhibition can explain cortical temporal tuning. Nat. Neurosci. 4, 424–430 (2001).

    Article  CAS  Google Scholar 

  33. Elhilali, M., Fritz, J.B., Klein, D.J., Simon, J.Z. & Shamma, S.A. Dynamics of precise spike timing in primary auditory cortex. J. Neurosci. 24, 1159–1172 (2004).

    Article  CAS  Google Scholar 

  34. Recanzone, G.H., Merzenich, M.M. & Schreiner, C.E. Changes in the distributed temporal response properties of SI cortical neurons reflect improvements in performance on a temporally based tactile discrimination task. J. Neurophysiol. 67, 1071–1091 (1992).

    Article  CAS  Google Scholar 

  35. Bakin, J.S. & Weinberger, N.M. Classical conditioning induces CS-specific receptive field plasticity in the auditory cortex of the guinea pig. Brain Res. 536, 271–286 (1990).

    Article  CAS  Google Scholar 

  36. Ji, W., Gao, E. & Suga, N. Effects of acetylcholine and atropine on plasticity of central auditory neurons caused by conditioning in bats. J. Neurophysiol. 86, 211–225 (2001).

    Article  CAS  Google Scholar 

  37. Ohl, F.W. & Scheich, H. Differential frequency conditioning enhances spectral contrast sensitivity of units in auditory cortex (field Al) of the alert Mongolian gerbil. Eur. J. Neurosci. 8, 1001–1017 (1996).

    Article  CAS  Google Scholar 

  38. Blake, D.T., Strata, F., Churchland, A.K. & Merzenich, M.M. Neural correlates of instrumental learning in primary auditory cortex. Proc. Natl. Acad. Sci. USA 99, 10114–10119 (2002).

    Article  CAS  Google Scholar 

  39. Bakin, J.S. & Weinberger, N.M. Induction of a physiological memory in the cerebral cortex by stimulation of the nucleus basalis. Proc. Natl. Acad. Sci. USA 93, 11219–11224 (1996).

    Article  CAS  Google Scholar 

  40. Bao, S., Chan, V.T. & Merzenich, M.M. Cortical remodelling induced by activity of ventral tegmental dopamine neurons. Nature 412, 79–83 (2001).

    Article  CAS  Google Scholar 

  41. Bao, S., Chan, V.T., Zhang, L.I. & Merzenich, M.M. Suppression of cortical representation through backward conditioning. Proc. Natl. Acad. Sci. USA 100, 1405–1408 (2003).

    Article  CAS  Google Scholar 

  42. Bao, S., Chang, E.F., Davis, J.D., Gobeske, K.T. & Merzenich, M.M. Progressive degradation and subsequent refinement of acoustic representations in the adult auditory cortex. J. Neurosci. 23, 10765–10775 (2003).

    Article  CAS  Google Scholar 

Download references

Acknowledgements

This research was supported by National Institutes of Health grants NS-10414 and NS-34835, the Coleman Fund, the Sandler Fund, the Mental Insight Foundation and the National Organization for Hearing Research Foundation. We thank J. Davis for help with the experiments. We thank D. Polley and C.-L. Teng for comments on this manuscript.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Shaowen Bao.

Ethics declarations

Competing interests

The authors declare no competing financial interests.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Bao, S., Chang, E., Woods, J. et al. Temporal plasticity in the primary auditory cortex induced by operant perceptual learning. Nat Neurosci 7, 974–981 (2004). https://doi.org/10.1038/nn1293

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/nn1293

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