Plasticity in human pitch perception induced by tonotopically mismatched electro-acoustic stimulation

Under normal conditions, the acoustic pitch percept of a pure tone is determined mainly by the tonotopic place of the stimulation along the cochlea. Unlike acoustic stimulation, electric stimulation of a cochlear implant (CI) allows for the direct manipulation of the place of stimulation in human subjects. CI sound processors analyze the range of frequencies needed for speech perception and allocate portions of this range to the small number of electrodes distributed in the cochlea. Because the allocation is assigned independently of the original resonant frequency of the basilar membrane associated with the location of each electrode, CI users who have access to residual hearing in either or both ears often have tonotopic mismatches between the acoustic and electric stimulation. Here we demonstrate plasticity of place pitch representations of up to three octaves in Hybrid CI users after experience with combined electro-acoustic stimulation. The pitch percept evoked by single CI electrodes, measured relative to acoustic tones presented to the non-implanted ear, changed over time in directions that reduced the electro-acoustic pitch mismatch introduced by the CI programming. This trend was particularly apparent when the allocations of stimulus frequencies to electrodes were changed over time, with pitch changes even reversing direction in some subjects. These findings show that pitch plasticity can occur more rapidly and on a greater scale in the mature auditory system than previously thought possible. Overall, the results suggest that the adult auditory system can impose perceptual order on disordered arrays of inputs.

[1]  Do tests for cochlear dead regions provide important information for fitting hearing aids? , 2004, The Journal of the Acoustical Society of America.

[2]  J. Eggermont,et al.  Cortical tonotopic map plasticity and behavior , 2011, Neuroscience & Biobehavioral Reviews.

[3]  G. Stratton Some preliminary experiments on vision without inversion of the retinal image. , 1896 .

[4]  Patricia A. Leake,et al.  Frequency Map for the Human Cochlear Spiral Ganglion: Implications for Cochlear Implants , 2007, Journal for the Association for Research in Otolaryngology.

[5]  R. Shannon,et al.  Effects of electrode configuration and frequency allocation on vowel recognition with the Nucleus-22 cochlear implant. , 1999, Ear and hearing.

[6]  G. Recanzone Rapidly induced auditory plasticity: the ventriloquism aftereffect. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[7]  Bruce J Gantz,et al.  Integration of acoustic and electrical hearing. , 2008, Journal of rehabilitation research and development.

[8]  Robert Tibshirani,et al.  An Introduction to the Bootstrap , 1994 .

[9]  Bruce J Gantz,et al.  Effects of Extreme Tonotopic Mismatches Between Bilateral Cochlear Implants on Electric Pitch Perception: A Case Study , 2011, Ear and hearing.

[10]  James G. Taylor The behavioral basis of perception , 1962 .

[11]  Bruce J Gantz,et al.  Combining acoustic and electrical hearing. , 2003, The Laryngoscope.

[12]  Eric I Knudsen,et al.  Hunting Increases Adaptive Auditory Map Plasticity in Adult Barn Owls , 2005, The Journal of Neuroscience.

[13]  Bruce J. Gantz,et al.  Changes in Pitch with a Cochlear Implant Over Time , 2007, Journal for the Association for Research in Otolaryngology.

[14]  C. Turner,et al.  Combining acoustic and electrical hearing , 2003 .

[15]  Donald K. Eddington,et al.  Depth of Electrode Insertion and Postoperative Performance in Humans with Cochlear Implants: A Histopathologic Study , 2010, Audiology and Neurotology.

[16]  Hugh J. McDermott,et al.  Comparison of two frequency-to-electrode maps for acoustic-electric stimulation , 2009, International journal of audiology.

[17]  C. Turner,et al.  Hearing Loss and the Limits of Amplification , 2006, Audiology and Neurotology.

[18]  C. Turner,et al.  Effects of Lower Frequency-to-Electrode Allocations on Speech and Pitch Perception with the Hybrid Short-Electrode Cochlear Implant , 2012, Audiology and Neurotology.

[19]  Qian-Jie Fu,et al.  Auditory Training with Spectrally Shifted Speech: Implications for Cochlear Implant Patient Auditory Rehabilitation , 2005, Journal of the Association for Research in Otolaryngology.

[20]  Bruce J. Gantz,et al.  Combining acoustic and electric hearing: Simulations and real‐patient results , 2000 .

[21]  J. Fritz,et al.  Rapid task-related plasticity of spectrotemporal receptive fields in primary auditory cortex , 2003, Nature Neuroscience.

[22]  D. D. Greenwood A cochlear frequency-position function for several species--29 years later. , 1990, The Journal of the Acoustical Society of America.

[23]  Felix Wichmann,et al.  The psychometric function: II. Bootstrap-based confidence intervals and sampling , 2001, Perception & psychophysics.

[24]  A. Faulkner,et al.  Adaptation by normal listeners to upward spectral shifts of speech: implications for cochlear implants. , 1999, The Journal of the Acoustical Society of America.