Neural coding of ITD with bilateral cochlear implants: Effects of auditory experience
Resumé
Human bilateral cochlear implant users do poorly on tasks involving interaural time differences (ITD), a cue which provides important bene ts to the normal hearing, especially in challenging acoustic environments. Yet the precision of neural ITD coding in acutely-deafened, bilaterally-implanted cats is essentially normal [Smith and Delgutte, J. Neurosci. 27, 6740-6750 (2007)]. One explanation for this discrepancy is that neural plasticity induced by the extended periods of binaural deprivation typically experienced by cochlear implant users degrades neural ITD sensitivity. To test this hypothesis, we recorded from single units in inferior colliculus (IC) of two groups of bilaterally-implanted, anesthetized cats: acutely-deafened cats, which had normal binaural hearing until experimentation, and congenitally deaf white cats, which received no auditory inputs until the experiment. Rate responses of only half as many neurons showed signi cant ITD sensitivity to low-rate pulse trains in congenitally deaf cats compared to acutely deafened cats. For neurons that were ITD sensitive, ITD tuning was broader and best ITDs were more variable in congenitally deaf cats. A signal detection model constrained by the observed physiology supports the idea that the degraded neural ITD coding resulting from deprivation of binaural experience contributes to poor ITD discrimination by human implantees.
Referencer
Grantham, D. W., Ashmead, D. H., Ricketts, T. A., Haynes, D. S., and Labadie, R. F. (2008). “Interaural time and level difference thresholds for acoustically presented signals in post-lingually deafened adults tted with bilateral cochlear implants using CIS+ processing”, Ear. Hear. 29, 33-44.
Green, D. M., and Swets, J. A. (1988). Signal Detection Theory and Psychophysics, (Los Altos, CA: Peninsula).
Hancock, K. E., and Delgutte, B. (2004). “A physiologically based model of interaural time difference discrimination,” J. Neurosci. 24, 7110-7117.
Hancock, K. E., and Noel, V. (2008). “A physiologically-based model of ITD discrimination in bilateral cochlear implant subjects,” Abstr. Assoc.
Res. Otolaryngol. 31, 301.
Heid, S., Hartmann, R., and Klinke, R. (1998). “A model for prelingual deafness, the congenitally deaf white cat--population statistics and degenerative changes,” Hear. Res. 115, 101-112.
Jean-Baptiste, M., and Morest, D. K. (1975). “Transneuronal changes of synaptic endings and nuclear chromatin in the trapezoid body following cochlear ablations in cats,” J. Comp. Neurol. 162, 111-134.
Joris, P. X., Van de Sande, B., Louage, D. H., and van der Heijden, M. (2006). “Binaural and cochlear disparities,” Proc. Natl. Acad. Sci. U.S.A. 103,12917-12922.
Kapfer, C., Seidl, A. H., Schweizer, H. and Grothe, B. (2002). “Experience-dependent re nement of inhibitory inputs to auditory coincidence-detector neurons,” Nat. Neurosci. 5, 247-253.
Kral, A., Tillein, J., Hubka, P., Syed, E., and Engel, A. K. (2009). “Cortical responses to bilateral cochlear implants in deaf cats,” in Conference on Implantable Auditory Prostheses, p 65. Lake Tahoe.
Kuwabara, N., and Zook, J. M. (1992). “Projections to the medial superior olive from the medial and lateral nuclei of the trapezoid body in rodents and bats,” J. Comp. Neurol. 324, 522-538.
Laback, B., Majdak, P., and Baumgartner, W. D. (2007). “Lateralization discrimination of interaural time delays in four-pulse sequences in electric and acoustic hearing,” J. Acoust. Soc. Am. 121, 2182-2191.
Laback, B., Pok, S. M., Baumgartner, W. D., Deutsch, W. A., and Schmid, K. (2004). “Sensitivity to interaural level and envelope time differences of two bilateral cochlear implant listeners using clinical sound processors,” Ear. Hear. 25, 488- 500.
Lawson, D. T., Wilson, B. S., Zerbi, M., van den Honert, C., Finley, C. C., Farmer, J. C., Jr., McElveen, J. T., Jr., and Roush, P. A. (1998). “Bilateral cochlear implants controlled by a single speech processor”, Am. J. Otol. 19, 758-761.
Lee, D. J., Cahill, H. B., and Ryugo, D. K. (2003). “Effects of congenital deafness in the cochlear nuclei of Shaker-2 mice: an ultrastructural analysis of synapse morphology in the endbulbs of Held,” J. Neurocytol. 32, 229-243.
Litovsky, R., Parkinson, A., Arcaroli, J., and Sammeth, C. (2006). “Simultaneous bilateral cochlear implantation in adults: a multicenter clinical study,” Ear. Hear. 27, 714-731.
McAlpine, D., Jiang, D., and Palmer, A. R. (2001). “A neural code for low-frequency sound localization in mammals,” Nat. Neurosci. 4, 396-401.
Mossop, J. E., and Culling, J. F. (1998). “Lateralization of large interaural delays,” J. Acoust. Soc. Am. 104, 1574-1579.
Ryugo, D. K., Pongstaporn, T., Huchton, D. M., and Niparko, J. K. (1997). “Ultrastructural analysis of primary endings in deaf white cats: morphologic alterations in endbulbs of Held,” J. Comp. Neurol. 385, 230-244.
Ryugo, D. K., Rosenbaum, B. T., Kim, P. J., Niparko, J. K., and Saada, A. A. (1998). “Single unit recordings in the auditory nerve of congenitally deaf white cats: morphological correlates in the cochlea and cochlear nucleus,” J. Comp. Neurol. 397, 532-548.
Smith, Z. M., and Delgutte, B. (2007). “Sensitivity to interaural time differences in the inferior colliculus with bilateral cochlear implants,” J. Neurosci. 27, 6740- 6750.
Tirko, N., Pongstaporn, T. and Ryugo, D. K. (2009). “Synaptic organization of MSO principal neurons in hearing, deaf, and cochlear-implanted cats,” Abstr. Assoc. Res. Otolaryngol. 32, 707.
van Hoesel, R. J. (2004). “Exploring the bene ts of bilateral cochlear implants,” Audiol. Neurootol. 9, 234-246.
van Hoesel, R. J. (2007). “Sensitivity to binaural timing in bilateral cochlear implant users,” J. Acoust. Soc. Am. 121, 2192-2206.
van Hoesel, R. J., and Tyler, R. S. (2003). “Speech perception, localization, and lateralization with bilateral cochlear implants,” J. Acoust. Soc. Am. 113, 1617- 1630.
West, C. D., and Harrison, J. M. (1973). “Transneuronal cell atrophy in the congenitally deaf white cat,” J. Comp. Neurol. 151, 377-398.
Xu, S. A., Shepherd, R. K., Chen, Y., and Clark, G. M. (1993). “Profound hearing loss in the cat following the single co-administration of kanamycin and ethacrynic acid,” Hear. Res. 70, 205-215.
Yin, T. C., Chan, J. C. and Irvine, D. R. (1986). “Effects of interaural time delays of noise stimuli on low-frequency cells in the cat’s inferior colliculus. I. Responses to wideband noise,” J. Neurophysiol. 55, 280-300.
Zurek, P. M. (1992). “Binaural advantages and directional effects in speech intelligibility,” in Acoustical factors affecting hearing aid performance, edited by G. A. Studebaker and I. Hochberg (Allyn and Bacon, Boston), pp. 255-276.
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