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Encoding of the temporal regularity of sound in the human brainstem

Nature Neuroscience volume 4, pages 633–637 (2001)Cite this article

Abstract

We measured the neural activity associated with the temporal structure of sound in the human auditory pathway from cochlear nucleus to cortex. The temporal structure includes regularities at the millisecond level and pitch sequences at the hundreds-of-milliseconds level. Functional magnetic resonance imaging (fMRI) of the whole brain with cardiac triggering allowed simultaneous observation of activity in the brainstem, thalamus and cerebrum. This work shows that the process of recoding temporal patterns into a more stable form begins as early as the cochlear nucleus and continues up to auditory cortex.

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Figure 1: Experimental protocol.
Figure 2: Activation of structures in the ascending auditory pathway with sound stimuli using cardiac triggering and sparse imaging (contrast between all sound stimuli and silence shown in relation to average structural MRI).
Figure 3: Activation during the processing of the pitch changes between sounds and the temporal structure within sounds.

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References

  1. Nobili, R., Mammano, F. & Ashmore, J. How well do we understand the cochlea? Trends Neurosci. 21, 159–167 (1998).

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  3. Rouilly, E., deRibaupierre, Y. & deRibaupierre, F. Phase-locked responses to low frequency tones in the medial geniculate body. Hear. Res. 1, 213–226 (1979).

    Article  Google Scholar 

  4. Yost, W. A., Patterson, R. D. & Sheft, S. A time domain description for the pitch strength of iterated rippled noise. J. Acoust. Soc. Am. 99, 1066–1078 (1996).

    Article  CAS  Google Scholar 

  5. Patterson, R. D., Yost, W. A., Handel, S. & Datta, A. J. The perceptual tone/noise ratio of merged iterated rippled noises. J. Acoust. Soc. Am. 107, 1578–1588 (2000).

    Article  CAS  Google Scholar 

  6. Patterson, R. D., Anderson, T. & Allerhand, M. in Proceedings of the International Conference on Spoken Language Processing 1994, 1395–1398 (Yokohama, Japan, 1994).

    Google Scholar 

  7. Langner, G. Periodicity encoding in the auditory system. Hear. Res. 60, 115–142 (1992).

    Article  CAS  Google Scholar 

  8. Patterson, R. D., Allerhand, M. H. & Giguère, C. Time-domain modeling of peripheral auditory processing: a modular architecture and a software platform. J. Acoust. Soc. Am. 98, 1890–1894 (1995).

    Article  CAS  Google Scholar 

  9. Langner, G. & Schreiner, C. E. Periodicity coding in the inferior colliculus of the cat. I. Neuronal mechanisms. J. Neurophysiol. 60, 1799–1822 (1988).

    Article  CAS  Google Scholar 

  10. Moore, J. K. T. in Neurotology (eds. Jackier, R. K. & Brackmann, D. E.) 1–17 (Mosby, St. Louis, 1994).

    Google Scholar 

  11. Griffiths, T. D., Buechel, C., Frackowiak, R. S. J. & Patterson, R. D. Analysis of temporal structure in sound by the human brain. Nat. Neurosci. 1, 421–427 (1998).

    Google Scholar 

  12. Guimares, A. R. et al. Imaging subcortical activity in humans. Hum. Brain. Mapp. 6, 33–41 (1998).

    Article  Google Scholar 

  13. Hall, D. A. et al. “Sparse” temporal sampling in auditory fMRI. Hum. Brain. Mapp. 7, 213–223 (1999).

    Article  CAS  Google Scholar 

  14. Rees, G., Friston, K. & Koch, C. A direct quantitative relationship between the functional properties of human and macaque V5. Nat. Neurosci. 3, 716–723 (2000).

    Article  CAS  Google Scholar 

  15. Wiegrebe, L. & Winter, I. M. Temporal representation of iterated rippled noise as a function of delay and sound level in the ventral cochlear nucleus. J. Neurophysiol. 85, 1206–1219 (2001).

    Article  CAS  Google Scholar 

  16. Chawla, D., Lumer, E. D. & Friston, K. J. The relationship between synchronization among neuronal populations and their mean activity levels. Neural Comput. 11, 1389–411 (1999).

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  18. Zatorre, R. J., Evans, A. C. & Meyer, E. Neural mechanisms underlying melodic perception and memory for pitch. J. Neurosci. 14, 1908–1919 (1994).

    Article  CAS  Google Scholar 

  19. Griffiths, T. D., Johnsrude, I., Dean, J. L. & Green, G. G. R. A common neural substrate for the analysis of pitch and duration pattern in segmented sound? Neuroreport 18, 3825–3830 (1999).

    Article  Google Scholar 

  20. Patterson, R. D., Handel, S., Yost, W. A. & Datta, A. J. The relative strength of the tone and the noise components in iterated rippled noise. J. Acoust. Soc. Am. 100, 3286–3294 (1996).

    Article  Google Scholar 

  21. Duvernoy, H. M. The Human Brain (Springer, New York, 1999).

    Book  Google Scholar 

Download references

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Author notes

  1. Timothy D. Griffiths and Stefan Uppenkamp: The first two authors contributed equally to this work

Authors and Affiliations

  1. Physiology Department, Centre for the Neural Basis of Hearing, University of Cambridge, Downing Street, Cambridge, UK, CB2 3EG

    Timothy D. Griffiths, Stefan Uppenkamp & Roy D. Patterson

  2. Wellcome Department of Cognitive Neurology, Institute of Neurology, 12 Queen Square, London, WC1N 3BG, UK

    Timothy D. Griffiths & Oliver Josephs

  3. Department of Physiological Sciences, Auditory Group, Newcastle University Medical School, Newcastle upon Tyne, NE2 4HH, UK

    Timothy D. Griffiths

  4. MRC Cognition and Brain Sciences Unit, 15 Chaucer Road, Cambridge, CB2 2EF, UK

    Ingrid Johnsrude

Authors
  1. Timothy D. Griffiths
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  2. Stefan Uppenkamp
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  3. Ingrid Johnsrude
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  4. Oliver Josephs
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  5. Roy D. Patterson
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Correspondence to Timothy D. Griffiths.

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Griffiths, T., Uppenkamp, S., Johnsrude, I. et al. Encoding of the temporal regularity of sound in the human brainstem. Nat Neurosci 4, 633–637 (2001). https://doi.org/10.1038/88459

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