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.

  • Letter
  • Published:

Laminar fine structure of frequency organization in auditory midbrain

Nature volume 388, pages 383–386 (1997)Cite this article

Abstract

The perception of sound is based on signal processing by a bank of frequency-selective auditory filters, the so-called critical bands1,2,3. Here we investigate how the internal frequency organization of the main auditory midbrain station, the central nucleus of the inferior colliculus (ICC), might contribute to the generation of the critical-band behaviour of its neurons. We find a unique spatial arrangement of the frequency distribution in the ICC that correlates with psychophysical critical-band characteristics. Systematic frequency discontinuities along the main tonotopic axis, in combination with a smooth frequency gradient orthogonal to the main tonotopic organization of cat ICC, reflect a layering of the frequency organization paralleling its anatomical laminae. This layered frequency organization is characterized by constant frequency ratios of corresponding locations on neighbouring laminae and may provide a spatial framework for the generation of critical bands and for signal processing within4 and across5 frequency bands for the analysis of sound.

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: Stepwise progression of characteristic frequency (CF) along the main tonotopic axis in ICC.
Figure 2: Spatial and frequency spacing of frequency plateaux along dorso–ventral electrode tracks in the ICC.
Figure 3: a, Reconstruction of functional frequency-band lamina in the ICC.

Similar content being viewed by others

References

  1. Fletcher, H. Auditory patterns. Rev. Mod. Physiol. 12, 47–65 (1940).

    Article  ADS  Google Scholar 

  2. Zwicker, E. et al. Critical bandwidth in loudness summation. J. Acoust. Soc. Am. 29, 548–557 (1957).

    Article  ADS  Google Scholar 

  3. Greenwood, D. D. Critical bandwidth and the frequency coordinates of the basilar membrane. J. Acoust. Soc. Am. 33, 1344–1356 (1961).

    Article  ADS  Google Scholar 

  4. Watson, C. S. Masking of tones by noise for the cat. J. Acoust. Soc. Am. 62, 167–172 (1963).

    Article  ADS  Google Scholar 

  5. Yost, W. A. & Sheft, S. Across-critical band processing of amplitude modulated tones. J. Acoust. Soc. Am. 85, 848–857 (1989).

    Article  ADS  CAS  Google Scholar 

  6. Ehret, G. & Merzenich, M. M. Auditory midbrain responses parallel spectral integration phenomena. Science 227, 1245–1247 (1985).

    Article  ADS  CAS  Google Scholar 

  7. 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. 13, 139–163 (1988).

    Article  Google Scholar 

  8. Pickles, J. O. Normal critical bands in the cat. Acta Otolaryngol. 80, 245–254 (1975).

    Article  CAS  Google Scholar 

  9. Pickles, J. O. & Comis, S. D. Auditory-nerve-fiber bandwidths and critical bandwidths in the cat. J. Acoust. Soc. Am. 60, 1151–1156 (1976).

    Article  ADS  CAS  Google Scholar 

  10. Ehret, G. Critical bands and filter characteristics in the ear of the house mouse (Mus musculus). Biol. Cybern. 24, 35–42 (1976).

    Article  CAS  Google Scholar 

  11. Ehret, G. & Moffat, A. J. M. Noise masking of tone responses and critical ratios of the mouse cochlear nerve and cochlear nucleus. Hearing Res. 14, 45–57 (1984).

    Article  CAS  Google Scholar 

  12. Pickles, J. O. Psychophysical frequency resolution in the cat as determined by simultaneous masking and its relation to auditory-nerve resolution. J. Acoust. Soc. Am. 66, 1725–1732 (1979).

    Article  ADS  CAS  Google Scholar 

  13. Evans, E. F. et al. Correspondence between behavioural and physiological frequency selectivity in the guinea pig. Br. J. Audiol. 23, 151–152 (1989).

    Google Scholar 

  14. Nienhyus, G. W. & Clark, G. M. Critical bands following the selective destruction of cochlear inner and outer haircells. Acta Otolaryngol. 88, 350–358 (1979).

    Article  Google Scholar 

  15. Suga, N. & Tsuzuki, K. Inhibition and level-tolerant frequency tuning in the auditory cortex of the mustached bat. J. Neurophysiol. 53, 1109–1145 (1985).

    Article  CAS  Google Scholar 

  16. Suga, N. Sharpening of frequency tuning by inhibition in the central auditory system: tribute to Yasuji Katsuki. Neurosci. Res. 21, 287–299 (1995).

    Article  CAS  Google Scholar 

  17. Merzenich, M. M. & Reid, M. D. Representation of the cochlea within the inferior colliculus of the cat. Brain. Res. 77, 397–415 (1974).

    Article  CAS  Google Scholar 

  18. Roth, G. L. et al. Some features of the spatial organization of the central nucleus of the inferior colliculus of the cat. J. Comp. Neurol. 182, 661–680 (1978).

    Article  CAS  Google Scholar 

  19. Semple, M. N. & Aitkin, L. M. Representation of sound frequency and laterality by units in the central nucleus of the cat inferior colliculus. J. Neurophysiol. 42, 1626–1639 (1979).

    Article  CAS  Google Scholar 

  20. Rockel, A. J. & Jones, E. G. The neuronal organization of the inferior colliculus of the adult cat: I. The central nucleus. J. Comp. Neurol. 147, 11–60 (1973).

    Article  CAS  Google Scholar 

  21. Oliver, D. L. & Morest, D. K. The central nucleus of the inferior colliculus in the cat. J. Comp. Neurol. 222, 237–264 (1984).

    Article  CAS  Google Scholar 

  22. Oliver, D. L. Dorsal cochlear nucleus projections to the inferior colliculus in the cat: A light and electron microscope study. J. Comp. Neurol. 224, 155–172 (1984).

    Article  CAS  Google Scholar 

  23. Shneiderman, A. & Henkel, C. K. Banding of lateral superior olivary nucleus afferents in the inferior colliculus: a possible substrate for sensory integration. J. Comp. Neurol. 266, 519–534 (1987).

    Article  CAS  Google Scholar 

  24. Malmierca, M. S. et al. The central nucleus of the inferior colliculus in rat: A Golgi and computer reconstruction study of neuronal and laminar structure. J. Comp. Neurol. 333, 1–27 (1993).

    Article  CAS  Google Scholar 

  25. Chan, J. L. & Yin, T. C. T. Topographical relationships along the isofrequency laminae of the cat inferior colliculus: correlation with the anatomical lamination and representation of binaural response properties. Soc. Neurosci. Abstr. 8, 348 (1982).

    Google Scholar 

  26. Schreiner, C. E. & Langner, G. Periodicity coding in the inferior colliculus of the cat. II. Topographical organization. J. Neurophysiol. 60, 1823–1840 (1988).

    Article  CAS  Google Scholar 

  27. Serviere, J. & Webster, W. R. A. Acombined electrophysiological and [14C]2-deoxyglucose study of the frequency organization of the inferior colliculus of the cat. Neurosci. Lett. 27, 113–118 (1981).

    Article  CAS  Google Scholar 

  28. Ehret, G. & Fischer, R. Neuronal activity and tonotopy in the auditory system visualized by c-fos gene expression. Brain Res. 567, 350–354 (1991).

    Article  CAS  Google Scholar 

  29. Pollak, G. D. & Park, T. J. The effects of GABAergic inhibition on monaural response properties of neurons in the mustache bat's inferior colliculus. Hearing Res. 65, 99–117 (1993).

    Article  CAS  Google Scholar 

  30. Palombi, P. S. & Caspary, D. M. GABA inputs control discharge rate primarily within frequency receptive fields of inferior colliculus neurons. J. Neurophysiol. 75, 2211–2219 (1996).

    Article  CAS  Google Scholar 

Download references

Acknowledgements

Supported by the Office of Naval Research (C.E.S.) and the Deutsche Forschungsgemeinschaft (G.L.). We thank J. A. Winer for comments on the manuscript.

Author information

Authors and Affiliations

  1. *W. M. Keck Center for Integrative Neuroscience, Sloan Center for Theoretical Neuroscience, Coleman Laboratory, University of California at San Francisco, 513 Parnassus Avenue, San Francisco, 94143-0732, California, USA

    Christoph E. Schreiner

  2. †Zoologisches Institut, Technische Hochschule Darmstadt, D-64287, Darmstadt, Germany

    Gerald Langner

Authors
  1. Christoph E. Schreiner
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Gerald Langner
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Christoph E. Schreiner.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Schreiner, C., Langner, G. Laminar fine structure of frequency organization in auditory midbrain. Nature 388, 383–386 (1997). https://doi.org/10.1038/41106

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1038/41106

This article is cited by

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

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