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Ultra-fine frequency tuning revealed in single neurons of human auditory cortex

Nature volume 451, pages 197–201 (2008)Cite this article

Abstract

Just-noticeable differences of physical parameters are often limited by the resolution of the peripheral sensory apparatus. Thus, two-point discrimination in vision is limited by the size of individual photoreceptors. Frequency selectivity is a basic property of neurons in the mammalian auditory pathway1,2. However, just-noticeable differences of frequency are substantially smaller than the bandwidth of the peripheral sensors3. Here we report that frequency tuning in single neurons recorded from human auditory cortex in response to random-chord stimuli is far narrower than that typically described in any other mammalian species (besides bats), and substantially exceeds that attributed to the human auditory periphery. Interestingly, simple spectral filter models failed to predict the neuronal responses to natural stimuli, including speech and music. Thus, natural sounds engage additional processing mechanisms beyond the exquisite frequency tuning probed by the random-chord stimuli.

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Figure 1: Response selectivity.
Figure 2: Frequency tuning in the responses to the random-chord stimulus.
Figure 3: Frequency discrimination based on single-trial responses.
Figure 4: Natural versus artificial responses.

References

  1. Howard, M. A. et al. A chronic microelectrode investigation of the tonotopic organization of human auditory cortex. Brain Res. 724, 260–264 (1996)

    Article  CAS  Google Scholar 

  2. Nelken, I. in Integrative Functions in the Mammalian Auditory Pathway (eds Oertel, D., Popper, A. N. & Fay, R. R.) 358–416 (Springer, New York, 2002)

    Book  Google Scholar 

  3. Moore, B. C. J. An Introduction to the Psychology of Hearing Ch. 3 74–114 (Academic Press, London, 1982)

    Google Scholar 

  4. Evans, E. F. in Psychophysics and Physiology of Hearing (eds Evans, E. F. & Wilson, J. P.) 185–196 (Academic Press, London, 1977)

    Google Scholar 

  5. Ehret, G. & Schreiner, C. E. Frequency resolution and spectral integration (critical band analysis) in single units of the cat primary auditory cortex. J. Comp. Physiol. A 181, 635–650 (1997)

    Article  CAS  Google Scholar 

  6. Ehret, G. & Merzenich, M. M. Complex sound analysis (frequency resolution, filtering and spectral integration) by single units of the inferior colliculus of the cat. Brain Res. 472, 139–163 (1988)

    Article  CAS  Google Scholar 

  7. Heinz, M. G., Colburn, H. S. & Carney, L. H. Evaluating auditory performance limits: I. One-parameter discrimination using a computational model for the auditory nerve. Neural Comput. 13, 2273–2316 (2001)

    Article  CAS  Google Scholar 

  8. Fried, I. et al. Cerebral microdialysis combined with single-neuron and electroencephalographic recording in neurosurgical patients. J. Neurosurg. 91, 697–705 (1999)

    Article  CAS  Google Scholar 

  9. Banai, K. & Ahissar, M. Poor frequency discrimination probes dyslexics with particularly impaired working memory. Audiol. Neurootol. 9, 328–340 (2004)

    Article  Google Scholar 

  10. Theunissen, F. E., Sen, K. & Doupe, A. J. Spectral-temporal receptive fields of nonlinear auditory neurons obtained using natural sounds. J. Neurosci. 20, 2315–2331 (2000)

    Article  CAS  Google Scholar 

  11. Woolley, S. M., Gill, P. R. & Theunissen, F. E. Stimulus-dependent auditory tuning results in synchronous population coding of vocalizations in the songbird midbrain. J. Neurosci. 26, 2499–2512 (2006)

    Article  CAS  Google Scholar 

  12. Hsu, A., Borst, A. & Theunissen, F. E. Quantifying variability in neural responses and its application for the validation of model predictions. Network 15, 91–109 (2004)

    Article  Google Scholar 

  13. 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  ADS  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  15. Qin, L., Kitama, T., Chimoto, S., Sakayori, S. & Sato, Y. Time course of tonal frequency-response-area of primary auditory cortex neurons in alert cats. Neurosci. Res. 46, 145–152 (2003)

    Article  Google Scholar 

  16. Moshitch, D., Las, L., Ulanovsky, N., Bar-Yosef, O. & Nelken, I. Responses of neurons in primary auditory cortex (A1) to pure tones in the halothane-anesthetized cat. J. Neurophysiol. 95, 3756–3769 (2006)

    Article  Google Scholar 

  17. Recanzone, G. H., Guard, D. C. & Phan, M. L. Frequency and intensity response properties of single neurons in the auditory cortex of the behaving macaque monkey. J. Neurophysiol. 83, 2315–2331 (2000)

    Article  CAS  Google Scholar 

  18. Schwarz, D. W. & Tomlinson, R. W. Spectral response patterns of auditory cortex neurons to harmonic complex tones in alert monkey (Macaca mulatta). J. Neurophysiol. 64, 282–298 (1990)

    Article  CAS  Google Scholar 

  19. Miller, L. M., Escabi, M. A., Read, H. L. & Schreiner, C. E. Spectrotemporal receptive fields in the lemniscal auditory thalamus and cortex. J. Neurophysiol. 87, 516–527 (2002)

    Article  Google Scholar 

  20. Tramo, M. J., Shah, G. D. & Braida, L. D. Functional role of auditory cortex in frequency processing and pitch perception. J. Neurophysiol. 87, 122–139 (2002)

    Article  Google Scholar 

  21. Quiroga, R. Q., Reddy, L., Kreiman, G., Koch, C. & Fried, I. Invariant visual representation by single neurons in the human brain. Nature 435, 1102–1107 (2005)

    Article  ADS  CAS  Google Scholar 

  22. Benasich, A. A. & Tallal, P. Infant discrimination of rapid auditory cues predicts later language impairment. Behav. Brain Res. 136, 31–49 (2002)

    Article  Google Scholar 

  23. Banai, K. & Ahissar, M. Auditory processing deficits in dyslexia: task or stimulus related? Cereb. Cortex 16, 1718–1728 (2006)

    Article  Google Scholar 

  24. McArthur, G. M. & Bishop, D. V. Speech and non-speech processing in people with specific language impairment: a behavioural and electrophysiological study. Brain Lang. 94, 260–273 (2005)

    Article  CAS  Google Scholar 

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

    Article  ADS  CAS  Google Scholar 

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

    Article  ADS  CAS  Google Scholar 

  27. Theunissen, F. E. et al. Estimating spatio-temporal receptive fields of auditory and visual neurons from their responses to natural stimuli. Network 12, 289–316 (2001)

    Article  CAS  Google Scholar 

  28. Mukamel, R. et al. Coupling between neuronal firing, field potentials, and FMRI in human auditory cortex. Science 309, 951–954 (2005)

    Article  ADS  CAS  Google Scholar 

  29. Bleeck, S., Ives, T. & Patterson, R. D. Aim-mat: the auditory image model in MATLAB. Acta Acustica 90, 781–788 (2004)

    Google Scholar 

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Acknowledgements

We thank the patients for their cooperation in participating in the experiments. We thank E. Behnke, T. A. Fields, E. Ho and C. Wilson for technical assistance. This work was supported by an ISF grant (to I.N.), a NINDS grant (to I.F.), the US-Israel BSF fund (R.M. and I.F.) and a European Molecular Biology Organization and Human Frontier Science Program fellowship (R.M.).

Author information

Authors and Affiliations

  1. Department of Neurobiology, Life Science Institute,

    Y. Bitterman & I. Nelken

  2. Interdisciplinary Center for Neural Computation, Hebrew University, Jerusalem 91904, Israel ,

    Y. Bitterman & I. Nelken

  3. Ahmanson-Lovelace Brain Mapping Center, David Geffen School of Medicine,,

    R. Mukamel

  4. Division of Neurosurgery, David Geffen School of Medicine and Semel Institute for Neuroscience and Human Behaviour, University of California Los Angeles (UCLA), Los Angeles, California 90095, USA,

    R. Mukamel & I. Fried

  5. Department of Neurobiology, Weizmann Institute of Science, Rehovot 76100, Israel

    R. Malach

  6. Functional Neurosurgery Unit, Tel Aviv Sourasky Medical Center and Sackler School of Medicine, Tel Aviv University, Tel Aviv 69978, Israel

    I. Fried

Authors
  1. Y. Bitterman
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  2. R. Mukamel
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  3. R. Malach
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  4. I. Fried
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  5. I. Nelken
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Corresponding authors

Correspondence to I. Fried or I. Nelken.

Supplementary information

Supplementary Information

The file contains Supplementary Notes and Supplementary Figure 1 with Legend, on the subjects of response reproducibility and evaluation of STRFs predictive power. (PDF 234 kb)

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Bitterman, Y., Mukamel, R., Malach, R. et al. Ultra-fine frequency tuning revealed in single neurons of human auditory cortex. Nature 451, 197–201 (2008). https://doi.org/10.1038/nature06476

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