Gain, nonlinearity and regulation in the mammalian cochlea
Abstract
Apart from acute conductive problems, we normally think of a person’s pure- tone audiogram as relatively fixed, changing rapidly only rarely (e.g. stroke, stula, Ménière’s syndrome). Given that outer hair cells (OHCs) actively enhance cochlear vibration 50-60dB by cancelling internal friction, we should expect cochlear gain to be very sensitive to changes in component parts, as in any positive feedback system. This is especially true when the components are highly nonlinear, with their small-signal efficiency depending on the slope of their transfer curve at the operating point. As a result, it seems inescapa- ble that cochlear gain is regulated in some way. Indeed there is evidence that it is usually maintained within a tolerance of a few decibel by good 'design' to reject disturbances, and by a dynamic servo-loop to stabilize gain. For example, after intense but non-traumatic low-frequency tones, the audiogram can slowly oscillate up and down by as much as 30 dB, suggesting underdamped gain stabilization. How the cochlea's design minimizes large perturbations and how OHCs stabilize their gain are discussed using experimental data from animals and humans, and with mathematical modelling of the feedback systems controlling the highly nonlinear OHCs. This suggests that co-evolution of the cochlea's geometry, electro-anatomy and membrane proteins has produced a robust system to stabilize the OHC feedback forces against changes in the cochlea's internal battery (endocochlear potential), against slow changes in pressure within the cochlea, and ultimately against unavoidable variations in the density of the OHC's own membrane proteins.
References
Farahbakhsh, N. A. Narins, P. M., (2006). “Slow motility in hair cells of the frog amphibian papilla:Ca2+-dependent shape changes,” Hear. Res. 212:140–159.
Franchinia, L. F., and Elgoyhena, A. B., (2006). “Adaptive evolution in mammalian proteins involved in cochlear outer hair cell electromotility”. Molecular Phylogenetics and Evolution 41, 622-635.
Frolenkov, G. I., (2006). “Regulation of electromotility in the cochlear outer hair cell,” J. Physiol. 576, 43-48.
Frolenkov, G. I., Mammano, F. Belyantseva, I. A., Coling, D., Kachar, B., (2000). “Two distinct Ca2+-dependent signaling pathways regulate the motor output of cochlear outer hair cells,” J. Neurosci. 20, 5940–5948.
Holton, T., Hudspeth, A. J., (1986). “The transduction channel of hair cells from the bull-frog characterized by noise analysis,” J. Physiol. (Lond.), 375, 195-227.
Housley, G. D., Ashmore, J. F., (1992). “Ionic currents of outer hair cells isolated from the guinea-pig cochlea,” J. Physiol. (Lond.), 448, 73-98.
Kemp, D. T., (1986). “Otoacoustic emissions, travelling waves and cochlear mechanisms,” Hear. Res. 22, 95-104.
Kirk, D. L., Moleirinho, A., and Patuzzi, R. B., (1997) “Microphonic and DPOAE measurements suggest a micromechanical mechanism for the ‘bounce’ phenomenon following low frequency tones,” Hear. Res., 112, 69-86.
Kirk, D. L., Patuzzi, R. B., (1997). “Transient changes in cochlear potentials and DPOAEs after low-frequency tones: the ‘two-minute’ bounce revisited,” Hear. Res. 112, 49-68.
O'Beirne, G. A., Patuzzi, R. B., (2003). “Mathematical modelling of the role of outer hair cells in cochlear homeostasis,” Biophysics of the Cochlea. World Scientific, Singapore, 434-435.
O'Beirne, G. A., Patuzzi, R. B., (2007). “Mathematical model of outer hair cell regulation including ion transport and cell motility,” Hear. Res. (in press).
Patuzzi, R., (2002). “Outer hair cells, EP regulation and tinnitus,” in. Proceedings of the Seventh International Tinnitus Seminar. University of Western Australia, Crawley, 16-24.
Patuzzi, R., and Sellick, P. M., (1984). “The modulation of the sensitivity of the mammalian cochlea by low frequency tones. II. Inner hair cell receptor potentials,” Hear. Res. 13, 9-18.
Patuzzi, R., and Robertson, D. (1988). “Tuning in the mammalian cochlea,” Physiol. Rev. 68, 1009-1082.
Patuzzi, R., Sellick, P. M., and Johnstone, B.M., (1984) “The modulation of the sensitivity of the mammalian cochlea by low frequency tones. III. Basilar membrane motion”, Hear. Res. 13, 19-27.
Patuzzi, R., Sellick, P. M., Johnstone, B. M., (1984). “The modulation of the sensitivity of the mammalian cochlea by low frequency tones. I. Primary afferent activ- ity,” Hear. Res. 13:1-8.
Patuzzi, R., Wareing, N., (2002). “Generation of transient tinnitus in humans using low-frequency tones and its mechanism,” in Proceedings of the Seventh International Tinnitus Seminar. University of Western Australia, Crawley, 71-73.
Patuzzi, R. B., (1996). “Cochlear micromechanics and macromechanics,” in The Cochlea. Springer-Verlag, New York, NY, pp. 186-257.
Patuzzi, R. B., (2003). “Low-frequency oscillations in outer hair cells and homeostatic regulation of the organ of Corti,” in Biophysics of the Cochlea. World Scienti c, Singapore, 292-299.
Patuzzi, R. B., O'Beirne, G.A., (1999). “Boltzmann analysis of CM waveforms using virtual instrument software,” Hear. Res., 133, 155-159.
Patuzzi, R. B., Yates, G. K., and Johnstone, B. M., (1989). “Outer hair cell receptor current and sensorineural hearing loss”, Hear. Res. 42, 47-72.
Robles, L., Ruggero, M. A., (2001). “Mechanics of the Mammalian Cochlea,” Physiol. Rev. 81, 1305-1352.
Sellick, P. M., Patuzzi, R., and Johnstone, B. M., (1982). “Modulation of responses of spiral ganglion cells in the guinea pig cochlea by low frequency sound,” Hear. Res. 7, 199-221.
Zheng, J., Shen, W., He, D.Z., Long, K.B., Madison, L.D., Dallos, P., (2000). “Prestin is the motor protein of cochlear outer hair cells,” Nature 405, 149-155.
Zwicker, E. (1976). “Psychoacoustic equivalent of period histograms [in memoriam Dr. Russell Pfeiffer],” J. Acoust. Soc. Am., 59, 166-175.
Zwicker, E. (1979). “A model describing nonlinearities in hearing by active processes with saturation at 40 dB,” Biological Cybernetics, 35, 243-250.
Zwicker, E., Hesse, A., (1984). “Temporary threshold shifts after onset and offset of moderately loud low-frequency maskers,” J. Acoust. Soc. Am. 75, 545-549.
Additional Files
Published
How to Cite
Issue
Section
License
Authors who publish with this journal agree to the following terms:
a. Authors retain copyright* and grant the journal right of first publication with the work simultaneously licensed under a Creative Commons Attribution License that allows others to share the work with an acknowledgement of the work's authorship and initial publication in this journal.
b. Authors are able to enter into separate, additional contractual arrangements for the non-exclusive distribution of the journal's published version of the work (e.g., post it to an institutional repository or publish it in a book), with an acknowledgement of its initial publication in this journal.
c. Authors are permitted and encouraged to post their work online (e.g., in institutional repositories or on their website) prior to and during the submission process, as it can lead to productive exchanges, as well as earlier and greater citation of published work (See The Effect of Open Access).
*From the 2017 issue onward. The Danavox Jubilee Foundation owns the copyright of all articles published in the 1969-2015 issues. However, authors are still allowed to share the work with an acknowledgement of the work's authorship and initial publication in this journal.
