Abstract
Stimulus polarity can affect both physiological and perceptual measures in cochlear-implant recipients. Large differences between polarities for various outcome measures (e.g., eCAP threshold, amplitude, or slope) theoretically reflect poorer neural health, whereas smaller differences reflect better neural health. Therefore, we expect large polarity effects to be correlated with other measures shown to contribute to poor neural health, such as advanced age or prolonged deafness. Our earlier studies using the electrically evoked compound action potential (eCAP) demonstrated differences in polarity effects between users of Cochlear and Advanced Bionics devices when device-specific clinical pulse designs were used. Since the stimuli differed slightly between devices, the first goal of this study was to determine whether small, clinically relevant differences in pulse phase duration (PD) have a significant impact on eCAP polarity effects to potentially explain the device differences observed previously. Polarity effects were quantified as the difference in eCAP thresholds, mean normalized amplitudes, and slope of the amplitude growth function obtained for anodic-first versus cathodic-first biphasic pulses. The results showed that small variations in PD did not explain the observed differences in eCAP polarity effects between devices. Therefore, eCAP polarity sensitivity measures are relatively robust to small differences in pulse parameters. However, it remains unclear what underlies the observed manufacturer differences, which may limit the utility of eCAP polarity sensitivity measures. The second goal was to characterize polarity sensitivity in a large group of CI recipients (65 ears) to relate polarity sensitivity to age and duration of deafness as a proxy for neural health. The same pulse parameters were used for both device groups. The only significant predictors of eCAP polarity effects were age for threshold and amplitude polarity effects for Cochlear recipients and age and duration of deafness for slope for AB recipients. However, three of these four correlations were in the opposite direction of what was expected. These results suggest that eCAP polarity sensitivity measures likely reflect different mechanisms than the effects that age and duration of deafness induce on the peripheral auditory system.
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References
Abbas B, Shallop F, Hughes H, Staller SJ (1999) Summary of results using the nucleus CI24M implant to record the electrically evoked compound action potential. Ear Hear 20(1):45–59
Brochier G, Deeks G, Bance C (2021) Evaluating and comparing behavioral and electrophysiological estimates of neural health in cochlear implant users. J Assoc Res Otolaryngol 22(1):67–80
Brochier T, McKay CM, Carlyon RP (2021) Interpreting the effect of stimulus parameters on the electrically evoked compound action potential and on neural health estimates. J Assoc Res Otolaryngol 22(1):81–94
Carlyon RP, Cosentino S, Deeks JM, Parkinson W, Arenberg JA (2018) Effect of stimulus polarity on detection thresholds in cochlear implant users: relationships with average threshold, gap detection, and rate discrimination. J Assoc Res Otolaryngol 19:559–567
Carlyon RP, Deeks JM, Macherey O (2013) Polarity effects on place pitch and loudness for three cochlear-implant designs and at different cochlear sites. J Acoust Soc Am 134:503–509
Coste RL, Pfingst BE (1996) Stimulus features affecting psychophysical detection thresholds for electrical stimulation of the cochlea. III. Pulse polarity. J Acoust Soc Am 99(5):3099–3108
Glueckert P, Kinnefors RA, Schrott-Fischer A (2005) The human spiral ganglion: new insights into ultrastructure, survival rate and implications for cochlear implants. Audiol Neurotol 10:258–273
Hughes G, Baudhuin JL (2017) Effects of stimulus polarity and artifact reduction method on the electrically evoked compound action potential. Ear Hear 38(3):332–343
Hughes C, Glickman E (2018) What can stimulus polarity and interphase gap tell us about auditory nerve function in cochlear-implant recipients? Hear Res 359:50–63
Jahn A (2019) Evaluating psychophysical polarity sensitivity as an indirect estimate of neural status in cochlear implant listeners. J Assoc Res Otolaryngol 20:415–430
Joshi D, Epp B (2017) A model of electrically stimulated auditory nerve fiber responses with peripheral and central sites of spike generation. J Assoc Res Otolaryngol 18:323–342
Loeb W, Jenkins WM (1983) Biophysical considerations in electrical stimulation of the auditory nervous system. Ann NY Acad Sci 405:123–136
Macherey C (2012) Place-pitch manipulations with cochlear implants. J Acoust Soc Am 131:2225–2236
Macherey C, van Wieringen D, Wouters J (2008) Higher sensitivity of human auditory nerve fibers to positive electrical currents. J Assoc Res Otolaryngol 9:241–251
Macherey D, Carlyon RP (2011) Extending the limits of place and temporal pitch perception in cochlear implant users. J Assoc Res Otolaryngol 12:233–251
Macherey O, Van Wieringen A, Carlyon RP, Deeks JM, Wouters J (2006) Asymmetric pulses in cochlear implants: effects of pulse shape, polarity, and rate. J Assoc Res Otolaryngol 7:253–266
Macherey O, Van Wieringen A, Carlyon RP, Dhooge I, Wouters J (2010) Forward-masking patterns produced by symmetric and asymmetric pulse shapes in electric hearing. J Acoust Soc Am 127:326–338
McKay H (2003) The perceptual effects of interphase gap duration in cochlear implant stimulation. Hear Res 181:94–99
Mesnildrey Q, Venail F, Carlyon RP, Macherey O (2020) Polarity sensitivity as a potential correlate of neural degeneration in cochlear implant users. J Assoc Res Otolaryngol 89–104
Nadol Jr JB (1979) Electron microscopic findings in presbycusic degeneration of the basal turn of the human cochlea. Otolaryngol Head Neck Surg 87:818–836
Nadol Jr JB, Hsu W (1991) Histopathologic correlation of spiral ganglion cell count and new bone formation in the cochlea following meningogenic labyrinthitis and deafness. Ann Otol Rhinol Laryngol 100(9):712–716
Nadol Jr. (1997) Patterns of neural degeneration in the human cochlea and auditory nerve: Implications for cochlear implantation. Otolaryngol Head Neck Surg 117(3):220-228
Nadol Jr JB, Glynn Y (1989) Survival of spiral ganglion cells in profound sensorineural hearing loss: Implications for cochlear implantation. Ann Otol Rhinol Laryngol 98:411–416
Parkins C (1987) Auditory-nerve single-neuron thresholds to electrical stimulation from scala tympani electrodes. Hear Res 31:267–286
Parkins C (1989) Temporal response patterns of auditory nerve fibers to electrical stimulation in deafened squirrel monkeys. Hear Res 41:137–168
Prado-Guitierrez P, Fewster LM, Heasman JM, McKay CM, Shepherd RK (2006) Effect of interphase gap and pulse duration on electrically evoked potentials is correlated with auditory nerve survival. Hear Res 215(1-2):47-55
Ramekers V, Strahl S, Klis G (2014) Auditory-nerve responses to varied inter-phase gap and phase duration of the electric pulse stimulus as predictors for neuronal degeneration. J Assoc Res Otolaryngol 15:187–202
Rattay L, Felix H (2001a) A model of the electrically excited human cochlear neuron. I. Contribution of neural substructures to the generation and propagation of spikes. Hear Res 153:43–63
Rattay L, Felix H (2001b) A model of the electrically excited human cochlear neuron. II. Influence of the three-dimensional cochlear structure on neural excitability. Hear Res 153:64–79
Riggs V, Skidmore C, Pellittieri C, Stegman CJ, He S (2021) The sensitivity of the electrically stimulated auditory nerve to amplitude modulation cues declines with advanced age. Ear Hear 42(5):1358–1372
Rubinstein M, Mino A (2001) Analysis of monophasic and biphasic electrical stimulation of nerve. IEEE Trans Biomed Eng 48(10):1065–1070
Schmidt-Clay B (2007) Adaptation of the electrically evoked compound action potential (ECAP) recorded from Nucleus CI24 cochlear implant users. Ear Hear 28:850–861
Shepherd J (1999) Electrical stimulation of the auditory nerve: II. Effect of stimulus waveshape on single fibre response properties. Hear Res 130:171–188
Spitzer C, Hughes ML (2019) The effect of stimulus polarity on the relation between pitch ranking and ECAP spread of excitation in cochlear implant users. J Assoc Res Otolaryngol 20(3):279–290
Spitzer H (2017) Effect of stimulus polarity on physiological spread of excitation in cochlear implants. J Am Acad Audiol 28:786–798
Undurraga C, Macherey W, van Wieringen A (2012) Spread of excitation varies for different electrical pulse shapes and stimulation modes in cochlear implants. Hear Res 290:21–36
Undurraga JA, Wouters J, van Wieringen A (2013) The polarity sensitivity of the electrically stimulated human auditory nerve measured at the level of the brainstem. J Assoc Res Otolaryngol 14:359–377
Undurraga JA, van Wieringen A, Carlyon RP, Macherey O, Wouters J (2010) Polarity effects on neural responses of the electrically stimulated auditory nerve at different cochlear sites. Hear Res 269:146–161
van den Honert M (1979) The response of the myelinated nerve fiber to short duration biphasic stimulating currents. Ann Biomed Eng 7:177–125
van den Honert S (1984) Physiological properties of the electrically stimulated auditory nerve. II Single Fiber Recordings Hear Res 14:225–243
Zilberstein L, Corfas G (2012) Inner hair cells are not required for survival of spiral ganglion neurons in the adult cochlea. J Neurosci 32(2):405–410
ACKNOWLEDGEMENTS
This research was supported by NIH/NIDCD grant R01 DC009595. Data collection was completed at Boys Town National Research Hospital in Omaha, NE, and analysis was completed at the University of Nebraska-Lincoln. The content of this project is solely the responsibility of the author and does not necessarily represent the official views of the National Institute on Deafness and Other Communication Disorders or the National Institutes of Health. The author thanks Jenny Goehring, Jacquelyn Baudhuin, Rachel Scheperle, Sangsook Choi, and Josh Sevier for data collection; Elysa Binger and Jamie Petersen for managing data fidelity; Tim Brochier for sharing his Matlab analysis code; and Donna Chen and Lorey Wheeler for assistance with statistical analyses.
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This project was approved by the Boys Town National Research Hospital Institutional Review Board under study protocol 03-07-XP. All participants (or parents/guardians for minors) provided written informed consent.
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Hughes, M.L. Characterizing Polarity Sensitivity in Cochlear Implant Recipients: Demographic Effects and Potential Implications for Estimating Neural Health. JARO 23, 301–318 (2022). https://doi.org/10.1007/s10162-021-00824-0
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DOI: https://doi.org/10.1007/s10162-021-00824-0