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.

Sustained firing in auditory cortex evoked by preferred stimuli

Abstract

It has been well documented that neurons in the auditory cortex of anaesthetized animals generally display transient responses to acoustic stimulation, and typically respond to a brief stimulus with one or fewer action potentials1,2,3,4,5. The number of action potentials evoked by each stimulus usually does not increase with increasing stimulus duration1,5,6,7. Such observations have long puzzled researchers across disciplines and raised serious questions regarding the role of the auditory cortex in encoding ongoing acoustic signals. Contrary to these long-held views, here we show that single neurons in both primary (area A1) and lateral belt areas of the auditory cortex of awake marmoset monkeys (Callithrix jacchus) are capable of firing in a sustained manner over a prolonged period of time, especially when they are driven by their preferred stimuli. In contrast, responses become more transient or phasic when auditory cortex neurons respond to non-preferred stimuli. These findings suggest that when the auditory cortex is stimulated by a sound, a particular population of neurons fire maximally throughout the duration of the sound. Responses of other, less optimally driven neurons fade away quickly after stimulus onset. This results in a selective representation of the sound across both neuronal population and time.

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

Relevant articles

Open Access articles citing this article.

Access options

Buy article

Get time limited or full article access on ReadCube.

$32.00

All prices are NET prices.

Figure 1: Examples of sustained firing of single neurons evoked by long-duration stimuli.
Figure 2: Temporal firing patterns evoked by preferred and non-preferred stimuli.
Figure 3: Quantitative analysis of sustained and onset responses.
Figure 4: Quantitative measures of single-neuron responses to brief tones.

References

  1. Phillips, D. P. Temporal response features of cat auditory cortex neurons contributing to sensitivity to tones delivered in the presence of continuous noise. Hear. Res. 19, 253–268 (1985)

    ADS  CAS  Article  PubMed  Google Scholar 

  2. Calford, M. B. & Semple, M. N. Monaural inhibition in cat auditory cortex. J. Neurophysiol. 73, 1876–1891 (1995)

    CAS  Article  PubMed  Google Scholar 

  3. Heil, P. Auditory cortical onset responses revisited. II. Response strength. J. Neurophysiol. 77, 2642–2660 (1997)

    ADS  CAS  Article  PubMed  Google Scholar 

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

    ADS  CAS  Article  PubMed  Google Scholar 

  5. DeWeese, M. R., Wehr, M. & Zador, A. M. Binary spiking in auditory cortex. J. Neurosci. 23, 7940–7949 (2003)

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  6. deCharms, R. C. & Merzenich, M. M. Primary cortical representation of sounds by the coordination of action-potential timing. Nature 381, 610–613 (1996)

    ADS  CAS  Article  PubMed  Google Scholar 

  7. Eggermont, J. J. Firing rate and firing synchrony distinguish dynamic from steady state sound. Neuroreport 8, 2709–2713 (1997)

    CAS  Article  PubMed  Google Scholar 

  8. Zurita, P., Villa, A. E., de Ribaupierre, Y., de Ribaupierre, F. & Rouiller, E. M. Changes of single unit activity in the cat's auditory thalamus and cortex associated to different anesthetic conditions. Neurosci. Res. 19, 303–316 (1994)

    CAS  Article  PubMed  Google Scholar 

  9. Gaese, B. H. & Ostwald, J. Anesthesia changes frequency tuning of neurons in the rat primary auditory cortex. J. Neurophysiol. 86, 1062–1066 (2001)

    CAS  Article  PubMed  Google Scholar 

  10. Cheung, S. W., Nagarajan, S. S., Bedenbaugh, P. H., Schreiner, C. E., Wang, X. & Wong, A. Auditory cortical neuron response differences under isoflurane versus pentobarbital anesthesia. Hear. Res. 156, 115–127 (2001)

    CAS  Article  PubMed  Google Scholar 

  11. Bar-Yosef, O., Rotman, Y. & Nelken, I. Responses of neurons in cat primary auditory cortex to bird chirps: effects of temporal and spectral context. J. Neurosci. 22, 8619–8632 (2002)

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  12. Phillips, D. P. Neural representation of stimulus times in the primary auditory cortex. Ann. NY Acad. Sci. 682, 104–118 (1993)

    ADS  CAS  Article  PubMed  Google Scholar 

  13. Bieser, A. & Müller-Preuss, P. Auditory responsive cortex in the squirrel monkey: neural responses to amplitude-modulated sounds. Exp. Brain Res. 108, 273–284 (1996)

    CAS  Article  PubMed  Google Scholar 

  14. Recanzone, G. H. Response profiles of auditory cortical neurons to tones and noise in behaving macaque monkeys. Hear. Res. 150, 104–118 (2000)

    CAS  Article  PubMed  Google Scholar 

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

    CAS  Article  PubMed  Google Scholar 

  16. Mickey, B. J. & Middlebrooks, J. C. Representation of auditory space by cortical neurons in awake cats. J. Neurosci. 23, 8649–8663 (2003)

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  17. Malone, B. J., Scott, B. H. & Semple, M. N. Context-dependent adaptive coding of interaural phase disparity in the auditory cortex of awake macaques. J. Neurosci. 22, 4625–4638 (2002)

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  18. Brugge, J. F. & Merzenich, M. M. Responses of neurons in auditory cortex of the macaque monkey to monaural and binaural stimulation. J. Neurophysiol. 36, 1138–1158 (1973)

    CAS  Article  PubMed  Google Scholar 

  19. Liang, L., Lu, T. & Wang, X. Neural representations of sinusoidal amplitude and frequency modulations in the primary auditory cortex of awake primates. J. Neurophysiol. 87, 2237–2261 (2002)

    Article  PubMed  Google Scholar 

  20. Rauschecker, J. P., Tian, B. & Hauser, M. Processing of complex sounds in the macaque nonprimary auditory cortex. Science 268, 111–114 (1995)

    ADS  CAS  Article  PubMed  Google Scholar 

  21. Shadlen, M. N. & Newsome, W. T. Noise, neural codes and cortical organization. Curr. Opin. Neurobiol. 4, 569–579 (1994)

    CAS  Article  PubMed  Google Scholar 

  22. Rhode, W. S. & Smith, P. H. Encoding timing and intensity in the ventral cochlear nucleus of the cat. J. Neurophysiol. 56, 261–286 (1986)

    CAS  Article  PubMed  Google Scholar 

  23. 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)

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  24. Lu, T. & Wang, X. Information content of auditory cortical responses to time-varying acoustic stimuli. J. Neurophysiol. 91, 301–313 (2004)

    Article  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  26. 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)

    ADS  CAS  Article  PubMed  Google Scholar 

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

    ADS  CAS  Article  PubMed  PubMed Central  Google Scholar 

  28. Aitkin, L. M., Merzenich, M. M., Irvine, D. R., Clarey, J. C. & Nelson, J. E. Frequency representation in auditory cortex of the common marmoset (Callithrix jacchus jacchus). J. Comp. Neurol. 252, 175–185 (1986)

    CAS  Article  PubMed  Google Scholar 

  29. 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)

    CAS  Article  PubMed  Google Scholar 

  30. Pfingst, B. E. & O'Connor, T. A. Characteristics of neurons in auditory cortex of monkeys performing a simple auditory task. J. Neurophysiol. 45, 16–34 (1981)

    CAS  Article  PubMed  Google Scholar 

Download references

Acknowledgements

We thank A. Pistorio for assistance with animal training and care, S. Eliades for technical assistance, R. Adams for help with maintaining the marmoset colony, and C. Wen for support throughout this work. This work was supported by an NIH grant and a US Presidential Early Career Award for Scientists and Engineers (X.W.).Author Contributions X.W. led the development of the chronic recording preparation for awake marmosets with contributions from co-authors. R.K.S. and T.L. co-designed the Xblaster stimulus delivery and data acquisition system used in this study. X.W., L.L. and T.L. carried out the electrophysiological recording experiments. X.W. and T.L. analysed the data and wrote the manuscript.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Xiaoqin Wang.

Ethics declarations

Competing interests

Reprints and permissions information is available at npg.nature.com/reprintsandpermissions. The authors declare no competing financial interests.

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Wang, X., Lu, T., Snider, R. et al. Sustained firing in auditory cortex evoked by preferred stimuli. Nature 435, 341–346 (2005). https://doi.org/10.1038/nature03565

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1038/nature03565

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