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Modulation of cochlear hair cells by the auditory cortex in the mustached bat

An Erratum to this article was published on 01 February 2002

Abstract

The corticofugal (descending) auditory system forms multiple feedback loops, and adjusts and improves auditory signal processing in the subcortical auditory nuclei. However, the mechanism by which the corticofugal system modulates cochlear hair cells has been unexplored. We found that electric stimulation of cortical neurons via the corticofugal system modulates cochlear hair cells in a highly specific way according to the relationship in terms of best frequency between cortical neurons and hair cells. Such frequency-specific effects can be explained by selective corticofugal modulation of individual olivocochlear efferent fibers.

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Figure 1: Cortical over-representation of and sharply tuned hair cell responses to a 61 kHz sound.
Figure 2: Corticofugal modulation of cochlear microphonic (CM) responses.
Figure 3: Corticofugal modulation of cochlear microphonic responses.
Figure 4: Distribution of cortical Doppler-shifted constant frequency (DSCF) neurons that evoked either centrifugal or centripetal best frequency (BF) shift of the cochlear microphonic potential (CM).
Figure 5: Effect of cortical inactivation on frequency tuning of cochlear microphonic response.

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References

  1. Huffman, R. F. & Henson O. W. Jr. The descending auditory pathway and acousticomotor systems: connections with the inferior colliculus. Brain Res. Rev. 15, 295–323 (1990).

    Article  CAS  Google Scholar 

  2. Warr, W. B. in The Mammalian Auditory Pathway: Neuroanatomy (eds. Webster, D. B., Popper, A. N. & Fay, R. R.) 410–448 (Springer, New York, 1992).

    Book  Google Scholar 

  3. Bishop, A. L. & Henson, O. W. Jr. The efferent cochlear projections of the superior olivary complex in the mustached bat. Hear Res. 31, 175–182 (1987).

    Article  CAS  Google Scholar 

  4. Schnitzler, H. U. Echoortung bei der Fledermaus Chilonycteris rubiginosa. Z. Vergl. Physiol. 68, 25–38 (1970).

    Article  Google Scholar 

  5. Henson, O. W. Jr., Henson, M. M., Kobler, J. B. & Pollack, G. D. in Animal Sonar Systems (eds. Busnel, R. G. & Fish, J. F.) 913–916 (Plenum, New York, 1980).

    Book  Google Scholar 

  6. Gaioni, S. J., Riquimaroux, H. & Suga, N. Biosonar behavior of mustached bats swung on a pendulum prior to cortical ablation. J. Neurophysiol. 64, 1801–1817 (1990).

    Article  CAS  Google Scholar 

  7. Goldman, L. J. & Henson, O. W. Jr. Prey recognition and selection by the constant frequency bat, Pteronotus P. parnellii. Beh. Ecol. Sociobiol. 2, 411–419 (1977).

    Article  Google Scholar 

  8. Suga, N. & Jen, P. H. Further studies on the peripheral auditory system of 'CF-FM' bats specialized for fine frequency analysis of Doppler-shifted echoes. J. Exp. Biol. 69, 207–232 (1977).

    CAS  PubMed  Google Scholar 

  9. Suga, N. & Manabe, T. Neural basis of amplitude-spectrum representation in auditory cortex of the mustached bat. J. Neurophysiol. 47, 225–255 (1982).

    Article  CAS  Google Scholar 

  10. Yan, J. & Suga, N. Corticofugal modulation of time-domain processing of biosonar information in bats. Science 273, 1100–1103 (1996).

    Article  CAS  Google Scholar 

  11. Zhang, Y., Suga, N. & Yan, J. Corticofugal modulation of frequency processing in bat auditory system. Nature 387, 900–903 (1997).

    Article  CAS  Google Scholar 

  12. Zhang, Y. & Suga, N. Modulation of responses and frequency tuning of thalamic and collicular neurons by cortical activation in mustached bats. J. Neurophysiol. 84, 325–333 (2000).

    Article  CAS  Google Scholar 

  13. Pollak, G., Henson, O. W. Jr. & Novick, A. Cochlear microphonic audiograms in the “pure tone” bat chilonycteris parnellii parnellii. Science 176, 66–68 (1972).

    Article  CAS  Google Scholar 

  14. Xie, D. H. & Henson, O. W. Jr. Tonic efferent-induced cochlear damping in roosting and echolocating mustached bats. Hear. Res. 124, 60–68 (1998).

    Article  CAS  Google Scholar 

  15. Suga, N., Gao, E., Zhang, Y., Ma, X. & Olsen, J. F. The corticofugal system for hearing: recent progress. Proc. Natl. Acad. Sci. USA 97, 11807–11814 (2000).

    Article  CAS  Google Scholar 

  16. Suga, N. & Jen, P. H. Peripheral control of acoustic signals in the auditory system of echolocating bats. J. Exp. Biol. 62, 277–311 (1975).

    CAS  PubMed  Google Scholar 

  17. Huffman, R. F. & Henson, O. W. Jr. Labile cochlear tuning in the mustached bat. I. Concomitant shifts in biosonar emission frequency. J. Comp. Physiol. A 171, 725–734 (1993).

    Article  CAS  Google Scholar 

  18. Huffman, R. F. & Henson, O. W. Jr. Cochlear and CNS tonotopy: normal physiological shifts in the mustached bat. Hear. Res. 56, 79–85 (1991).

    Article  CAS  Google Scholar 

  19. Manabe, T., Suga, N. & Ostwald, J. Aural representation in the Doppler-shifted-CF processing area of the auditory cortex of the mustache bat. Science 200, 339–342 (1978).

    Article  CAS  Google Scholar 

  20. Liu, W. & Suga, N. Binaural and commissural organization of the primary auditory cortex of the mustached bat. J. Comp. Physiol. A 181, 599–605 (1997).

    Article  CAS  Google Scholar 

  21. Desmedt, J. E. & Monaco, P. Mode of action of the efferent olivocochlear bundle in the inner ear. Nature 193, 1263–1268 (1961).

    Article  Google Scholar 

  22. Mulders, W. H. & Robertson, D. Effects on cochlear responses of activation of descending pathways from the inferior colliculus. Hear. Res. 149, 11–23 (2000).

    Article  CAS  Google Scholar 

  23. Ma, X. & Suga, N. Plasticity of bat's central auditory system evoked by focal electric stimulation of auditory and/or somatosensory cortices. J. Neurophysiol. 85, 1078–1087 (2001).

    Article  CAS  Google Scholar 

  24. Gao, E. & Suga, N. Experience-dependent corticofugal adjustment of midbrain frequency map in bat auditory system. Proc. Natl. Acad. Sci. USA 95, 12663–12670 (1998).

    Article  CAS  Google Scholar 

  25. Gao, E. & Suga, N. Experience-dependent plasticity in the auditory cortex and the inferior colliculus of bats: role of the corticofugal system. Proc. Natl. Acad. Sci. USA 97, 8081–8086 (2000).

    Article  CAS  Google Scholar 

  26. Yan, W. & Suga, N. Corticofugal modulation of the midbrain frequency map in the bat auditory system. Nat. Neurosci. 1, 54–58 (1998).

    Article  CAS  Google Scholar 

  27. Goldberg, R. L. & Henson, O. W. Jr. Changes in cochlear mechanics during vocalization: evidence for a phasic medial efferent effect. Hear. Res. 122, 71–81 (1998).

    Article  CAS  Google Scholar 

  28. Khalfa, S. et al. Evidence of peripheral auditory activity modulation by the auditory cortex in humans. Neuroscience 104, 347–358 (2001).

    Article  CAS  Google Scholar 

  29. Puel, J. L., Bonfils, P. & Pujol, R. Selective attention modifies the active micromechanical properties of the cochlea. Brain Res. 447, 380–383 (1988).

    Article  CAS  Google Scholar 

  30. Maison, S., Micheyl, C. & Collet, L. Influence of focused auditory attention on cochlear activity in humans. Psychophysiology 38, 35–40 (2001).

    Article  CAS  Google Scholar 

  31. Riquimaroux, H., Gaioni, S. J. & Suga, N. Cortical computational maps control auditory perception. Science 251, 565–568 (1991).

    Article  CAS  Google Scholar 

  32. Zhang, Y. & Suga, N. Corticofugal amplification of subcortical responses to single tone stimuli in the mustached bat. J. Neurophysiol. 78, 3489–3492 (1997).

    Article  CAS  Google Scholar 

  33. Henson, O. W. Jr., Pollak, G. D., Kobler, J. B., Henson, M. M. & Goldman, L. J. Cochlear microphonic potentials elicited by biosonar signals in flying bats, Pteronotus p. parnellii. Hear. Res. 7, 127–147 (1982).

    Article  Google Scholar 

  34. Dewson, J. H. III. Efferent of olivocochlear bund. some relationships to stimulus discrimination in noise. J. Neurophysiol. 31, 122–130 (1968).

    Article  Google Scholar 

  35. Nieder, P. & Nieder, I. Stimulation of efferent olivocochlear bundle causes release from low level masking. Nature 227, 184–185 (1970).

    Article  CAS  Google Scholar 

  36. Dolan, D. F. & Nuttall, A. L. Masked cochlear whole-nerve response intensity functions altered by electrical stimulation of the crossed olivocochlear bundle. J. Acoust. Soc. Am. 83, 1081–1086 (1988).

    Article  CAS  Google Scholar 

  37. Kawase, T., Delgutte, B. & Liberman, M. C. Antimasking effects of the olivocochlear reflex. II. Enhancement of auditory-nerve response to masked tones. J. Neurophysiol. 70, 2533–2549 (1993).

    Article  CAS  Google Scholar 

  38. Geisler, C. D. Hypothesis on the function of the crossed olivocochlear bundle. J. Acoust. Soc. Am. 56, 1908–1909 (1974).

    Article  CAS  Google Scholar 

  39. Oatman, L. C. & Anderson, B. W. Effects of visual attention on tone burst evoked auditory potentials. Exp. Neurol. 57, 200–211 (1977)

    Article  CAS  Google Scholar 

  40. Wiederhold, M. L. Variations in the effects of electric stimulation of the crossed olivocochlear bundle on cat single auditory-nerve-fiber responses to tone bursts. J. Acoust. Soc. Am. 48, 966–977 (1970).

    Article  CAS  Google Scholar 

  41. Mountain, D. C. Changes in endolymphatic potential and crossed olivocochlear bundle stimulation alter cochlear mechanics. Science 210, 71–72 (1980).

    Article  CAS  Google Scholar 

  42. Siegel, J. H. & Kim, D. O. Efferent neural control of cochlear mechanics? Olivocochlear bundle stimulation affects cochlear biomechanical nonlinearity. Hear. Res. 6, 171–182 (1982).

    Article  CAS  Google Scholar 

  43. Rajan, R. Electrical stimulation of the inferior colliculus at low rates protects the cochlea from auditory desensitization. Brain Res. 506, 192–204 (1990).

    Article  CAS  Google Scholar 

  44. Henson, O. W. Jr. & Pollak, G. D. A technique for chronic implantation of electrodes in the cochleae of bats. Physiol. Behav. 8, 1185–1187 (1972).

    Article  Google Scholar 

  45. Suga, N., Niwa, H., Taniguchi, I. & Margoliash, D. The personalized auditory cortex of the mustached bat: adaptation for echolocation. J. Neurophysiol. 58, 643–654 (1987).

    Article  CAS  Google Scholar 

  46. 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 

  47. Olsen, J. F. & Suga, N. Combination-sensitive neurons in the medial geniculate body of the mustached bat: encoding of target range information. J. Neurophysiol. 65, 1275–1296 (1991).

    Article  CAS  Google Scholar 

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Acknowledgements

We thank O.W. Henson, S. Kuwada, N. Laleman and M.C. Liberman for their comments, the Ministry of Agriculture, Land and Marine Resources in Trinidad and Tobago for permitting us to collect the mustached bats, and F. Muradali for exporting them to the USA. This work was supported by a research grant from the National Institute on Deafness and Other Communicative Disorders (DC-00175).

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Correspondence to Nobuo Suga.

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Xiao, Z., Suga, N. Modulation of cochlear hair cells by the auditory cortex in the mustached bat. Nat Neurosci 5, 57–63 (2002). https://doi.org/10.1038/nn786

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