Further Evidence for Tuning Mechanisms of High Dynamic Order in Lower Vertebrates

  • Edwin R. Lewis
  • Michael G. Sneary
  • Xiaolong Yu
Part of the Lecture Notes in Biomathematics book series (LNBM, volume 87)


In recent years, data from individual hair cells have suggested that frequency selectivity in lower vertebrates is accomplished by the amplitude tuning peaks of underdamped electrical resonances (Crawford and Fettiplace, 1981; Lewis and Hudspeth, 1983; Pitchford and Ashmore, 1987). In the present study we have used the reverse-correlation (REVCOR) method (Evans, 1989; Eggermont et al, 1983; de Boer and Kuyper, 1968; de Boer and de Jongh, 1977) to study linear tuning responses from primary afferent axons of the three inner-ear organs in which these resonances were first reported -- the turtle basilar papilla and the frog sacculus and amphibian papilla. The characteristic signature of a single (undcrdamped) resonance comprises the following features: (I) impulse response in the fonn of a sinusoid with exponentially declining amplitude, (2) sinusoidal steady-state phase shift limited to one-half cycle, (3) convexity of the gain (amplitude) tuning curve limited to the highest three decibels (where the tuning curve is plotted on the conventional log-log coordinates), and (4) absolute values of the limiting slopes of the gain tuning curve which sum to two (decades per decade). If the outputs of resonances were added (not subtracted) in parallel, producing a tuning structure of high dynamic order, the characteristic signature of that structure would comprise features (2) and (4) from the previous list, plus (5) global concavity of the gain tuning curve (convexity only within approximately 3 dB of the tuning peaks). Among 155 axons included in this study, all displayed the following properties: (I) impulse responses that are more complex than exponentially decaying sinusoids, (2) sinusoidal steady-state phase shifts ranging over one or more cycles, (3) gain tuning curves exhibiting global convexity (with occasional, local concavity) and, (4) limiting gain-tuning-curve slopes whose absolute values sum to numbers considerably greater than two. We conclude that frequency selectivity in these axons is not accomplished by underdamped resonance peaks acting alone or in parallel combination (through positive addition), but rather by the asymptotic slopes of amplitude tuning curves, made steep by high dynamic order.


Hair Cell Impulse Response Tuning Curve Frequency Selectivity Lower Vertebrate 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.


Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.


  1. Art, J.J. and R.F. Fettiplace (1987) Variation of membrane properties in hair cells isolated from the turtle cochlea. 1. PhysioI. 385: 207–242.Google Scholar
  2. Capranica, R.R. and Moffat, A.J.M. (1975) Selectivity of the peripheral auditory system of spadefoot toads (Scaphiopus couchi) for sounds of biolOgical significance. J. Compo Physiol. 100: 231–249.Google Scholar
  3. Crawford, A.C. and Fettipiace, R.F. (1980) The frequncy selectivity of auditory nerve fibres and hair cells in the cochlea of the turtle. 1. Physiol. 306:79–125.Google Scholar
  4. Crawford, A.C. and Fettiplace, R.F. (1981) An electrical tuning mechanism in turtle cochlear hair cells. J. Physio!. 312: 377–412.Google Scholar
  5. de Boer, E. and de Jongh, H.R. (1977) On cochlear encoding: potentialities and limitations of the reverse–correlation technique. 1. Acoust. Soc. Am. 63(1), 115– 135.Google Scholar
  6. de Boer, E. and Kuyper, P. (1968) Triggered correlation. IEEE Trans Biomed. Engrg. 15:169–179.Google Scholar
  7. Eggermont, J.J., Johannesma, P.I.M. and Aertsen, A.M.H.J. (1983) Reversecorrelation method in auditory research. Quart Rev. Biophys. 16(3): 341–414.Google Scholar
  8. Evans, E.F. (1989) Cochlear filtering: a view seen through the temporal discharge patterns of single cochlear nerve fibres. In: Cochlear Mechanisms (Eds: Wilson, J.P and Kemp, D.T.) Plenum, New York, pp. 241–250.Google Scholar
  9. Fettiplace, R.F. and Crawford, A.C. (1978) The coding of sound pressure and frequency in cochlear hair cells of the terrapin. Proc. Roy. Soc. Lond. B. 203: 209–218.Google Scholar
  10. Frishkopf, L.S. and Goldstein, M.H. (1963) Responses to acoustic stimuli from single units in the eighth nerve of the bullfrog. J. Acoust. Soc. Am. 35: 1219–1228.Google Scholar
  11. Lewis, R.S. and Hudspeth, A.J. (1983) Frequency tuning and ionic conductance in hair cells of the bullfrog sacculus. In: Hearing ––Physiological Bases and Psychophysics. pp 17–24. (Eds: R. Klinke and Hartmann, R.) Springer–Verlag, Berlin.Google Scholar
  12. Pitchford, S. and Ashmore, J.F. (1987) An electrical resonance in hair cells of the amphibian papilla of the frog, Rana temporaria. Hearing Research 27, 75–84.Google Scholar
  13. van Dijk, P., Lewis, E.R. and Wit, H.P. (1990) Temperature effects on auditory nerve fiber response in the American bullfrog. Hear. Res. 44: 231–240.Google Scholar
  14. Weiss, T.F., Rose, C. (1988) A comparison of synchronization filters in different auditory receptor organs. Hearing Res. 33: 175–180.Google Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 1990

Authors and Affiliations

  • Edwin R. Lewis
    • 1
  • Michael G. Sneary
    • 1
  • Xiaolong Yu
    • 1
  1. 1.Department of Electrical Engineering and Computer ScienceUniversity of CaliforniaBerkeleyUSA

Personalised recommendations