Skip to main content

Temporal Considerations for Stimulating Spiral Ganglion Neurons with Cochlear Implants

Abstract

A wealth of knowledge about different types of neural responses to electrical stimulation has been developed over the past 100 years. However, the exact forms of neural response properties can vary across different types of neurons. In this review, we survey four stimulus-response phenomena that in recent years are thought to be relevant for cochlear implant stimulation of spiral ganglion neurons (SGNs): refractoriness, facilitation, accommodation, and spike rate adaptation. Of these four, refractoriness is the most widely known, and many perceptual and physiological studies interpret their data in terms of refractoriness without incorporating facilitation, accommodation, or spike rate adaptation. In reality, several or all of these behaviors are likely involved in shaping neural responses, particularly at higher stimulation rates. A better understanding of the individual and combined effects of these phenomena could assist in developing improved cochlear implant stimulation strategies. We review the published physiological data for electrical stimulation of SGNs that explores these four different phenomena, as well as some of the recent studies that might reveal the biophysical bases of these stimulus-response phenomena.

This is a preview of subscription content, access via your institution.

FIG. 1
FIG. 2
FIG. 3
FIG. 4
FIG. 5

References

  1. Adamson CL, Reid MA, Mo ZL, Bowne-English J, Davis RL (2002) Firing features and potassium channel content of murine spiral ganglion neurons vary with cochlear location. J Comp Neurol 447(4):331–350

    CAS  PubMed  Article  Google Scholar 

  2. Arora K, Dawson P, Dowell R, Vandali A (2009) Electrical stimulation rate effects on speech perception in cochlear implants. Int J Audiol 48(8):561–567

    PubMed  Article  Google Scholar 

  3. Avissar M, Wittig JH, Saunders JC, Parsons TD (2013) Refractoriness enhances temporal coding by auditory nerve fibers. J Neurosci 33(18):7681–7690

    PubMed Central  CAS  PubMed  Article  Google Scholar 

  4. Balkany T, Hodges A, Menapace C, Hazard L, Driscoll C, Gantz B, Kelsall D, Luxford W, McMenomy S, Neely JG, Peters B, Pillsbury H, Roberson J, Schramm D, Telian S, Waltzman S, Westerberg B, Payne S (2007) Nucleus Freedom North American clinical trial. Otolaryngol Head Neck Surg 136(5):757–762

    PubMed  Article  Google Scholar 

  5. Baylor DA, Nicholls JG (1969) Changes in extracellular potassium concentration produced by neuronal activity in the central nervous system of the leech. J Physiol 203(3):555–569

    PubMed Central  CAS  PubMed  Article  Google Scholar 

  6. Benarroch EE (2013) HCN channels: function and clinical implications. Neurology 80(3):304–310

    PubMed  Article  Google Scholar 

  7. Benda J, Herz AVM (2003) A universal model for spike-frequency adaptation. Neural Comput 15(11):2523–2564

    PubMed  Article  Google Scholar 

  8. Bi Q (1989) A closed-form solution for removing the dead time effects from the poststimulus time histograms. J Acoust Soc Am 85(6):2504

    CAS  PubMed  Article  Google Scholar 

  9. Biel M, Wahl-Schott C, Michalakis S, Zong X (2009) Hyperpolarization-activated cation channels: from genes to function. Physiol Rev 89(3):847–885

    CAS  PubMed  Article  Google Scholar 

  10. Bortone DS, Mitchell K, Manis PB (2006) Developmental time course of potassium channel expression in the rat cochlear nucleus. Hear Res 211(1-2):114–125

    CAS  PubMed  Article  Google Scholar 

  11. Botros A, Psarros C (2010) Neural response telemetry reconsidered: II. The influence of neural population on the ECAP recovery function and refractoriness. Ear Hear 31(3):380–391

    PubMed  Article  Google Scholar 

  12. Brette R, Gerstner W (2005) Adaptive exponential integrate-and-fire model as an effective description of neuronal activity. J Neurophysiol 94(5):3637–3642

    PubMed  Article  Google Scholar 

  13. Brew HM, Hallows JL, Tempel BL (2003) Hyperexcitability and reduced low threshold potassium currents in auditory neurons of mice lacking the channel subunit Kv1.1. J Physiol 548(1):1–20

    PubMed Central  CAS  PubMed  Article  Google Scholar 

  14. Brown DA, Adams PR (1980) Muscarinic suppression of a novel voltage-sensitive K+ current in a vertebrate neuron. Nature 283(5748):673–676

    CAS  PubMed  Article  Google Scholar 

  15. Bruce IC, White MW, Irlicht LS, O’Leary SJ, Dynes S, Javel E, Clark GM (1999) A stochastic model of the electrically stimulated auditory nerve: single-pulse response. IEEE Trans Biomed Eng 46(6):617–629

    CAS  PubMed  Article  Google Scholar 

  16. Brunel N, van Rossum M (2007) Quantitative investigations of electrical nerve excitation treated as polarization. Biol Cybern 97(5-6):341–349

    Article  Google Scholar 

  17. Burkitt AN (2006) A review of the integrate-and-fire neuron model: I. Homogeneous synaptic input. Biol Cybern 95(1):1–19

    CAS  PubMed  Article  Google Scholar 

  18. Butikofer R, Lawrence PD (1979) Electrocutaneous nerve stimulation-II: stimulus waveform selection. IEEE Trans Biomed Eng BME-26(2):69–75

    Article  Google Scholar 

  19. Campbell LJ, Sly DJ, O’Leary SJ (2012) Prediction and control of neural responses to pulsatile electrical stimulation. J Neural Eng 9(2):026,023

    Article  Google Scholar 

  20. Cartee LA (2000) Evaluation of a model of the cochlear neural membrane. II: Comparison of model and physiological measures of membrane properties measured in response to intrameatal electrical stimulation. Hear Res 146(1-2):153–166

    CAS  PubMed  Article  Google Scholar 

  21. Cartee LA (2006) Spiral ganglion cell site of excitation II: numerical model analysis. Hear Res 215(1-2):22–30

    PubMed  Article  Google Scholar 

  22. Cartee LA, van den Honert C, Finley CC, Miller RL (2000) Evaluation of a model of the cochlear neural membrane. I. Physiological measurement of membrane characteristics in response to intrameatal electrical stimulation. Hear Res 146(1-2):143–152

    CAS  PubMed  Article  Google Scholar 

  23. Cartee LA, Miller CA, van den Honert C (2006) Spiral ganglion cell site of excitation I: comparison of scala tympani and intrameatal electrode responses. Hear Res 215(1-2):10–21

    PubMed  Article  Google Scholar 

  24. Chen C (1997) Hyperpolarization-activated current (I h) in primary auditory neurons. Hear Res 110(1-2):179–190

    CAS  PubMed  Article  Google Scholar 

  25. Chow CC, White JA (1996) Spontaneous action potentials due to channel fluctuations. Biophys J 71(6):3013–3021

    PubMed Central  CAS  PubMed  Article  Google Scholar 

  26. Cohen LT (2009) Practical model description of peripheral neural excitation in cochlear implant recipients: 5. Refractory recovery and facilitation. Hear Res 248(1-2):1–14

    PubMed  Article  Google Scholar 

  27. Dynes SBC (1996) Discharge characteristics of auditory nerve fibers for pulsatile electrical stimuli. PhD thesis, Massachusetts Institute of Technology, Cambridge, Massachusetts

  28. Fleidervish IA, Friedman A, Gutnick MJ (1996) Slow inactivation of Na+ current and slow cumulative spike adaptation in mouse and guinea-pig neocortical neurones in slices. J Physiol Lond 493(1):83–97

    PubMed Central  CAS  PubMed  Article  Google Scholar 

  29. Frankenhaeuser B, Vallbo AB (1965) Accommodation in myelinated nerve fibres of Xenopus laevis as computed on the basis of voltage clamp data. Acta Physiol Scand 63(1-2):1–20

    CAS  PubMed  Article  Google Scholar 

  30. Friesen LM, Shannon RV, Cruz RJ (2005) Effects of stimulation rate on speech recognition with cochlear implants. Audiol Neurootol 10(3):169–184

    PubMed  Article  Google Scholar 

  31. Glowatzki E, Fuchs PA (2002) Transmitter release at the hair cell ribbon synapse. Nat Neurosci 5(2):147–154

    CAS  PubMed  Article  Google Scholar 

  32. Goldwyn JH, Rubinstein JT, Shea-Brown E (2012) A point process framework for modeling electrical stimulation of the auditory nerve. J Neurophysiol 108(5):1430–1452

    PubMed Central  PubMed  Article  Google Scholar 

  33. Gulledge AT, Dasari S, Onoue K, Stephens EK, Hasse JM, Avesar D (2013) A sodium-pump-mediated afterhyperpolarization in pyramidal neurons. J Neurosci 33(32):13,025–13,041

    CAS  Article  Google Scholar 

  34. Hardie NA, Shepherd RK (1999) Sensorineural hearing loss during development: morphological and physiological response of the cochlea and auditory brainstem. Hear Res 128(1-2):147–165

    CAS  PubMed  Article  Google Scholar 

  35. Hartmann R, Topp G, Klinke R (1984) Discharge patterns of cat primary auditory fibers with electrical-stimulation of the cochlea. Hear Res 13(1):47–62

    CAS  PubMed  Article  Google Scholar 

  36. Heffer LF (2010) High rate electrical stimulation of the auditory nerve: examining the effects of sensorineural hearing loss. PhD thesis, The University of Melbourne, Melbourne, Victoria

  37. Heffer LF, Sly DJ, Fallon JB, White MW, Shepherd RK, O’Leary SJ (2010) Examining the auditory nerve fiber response to high rate cochlear implant stimulation: chronic sensorineural hearing loss and facilitation. J Neurophysiol 104(6):3124–3135

    PubMed Central  PubMed  Article  Google Scholar 

  38. Heil P, Neubauer H, Irvine DRF, Brown M (2007) Spontaneous activity of auditory-nerve fibers: insights into stochastic processes at ribbon synapses. J Neurosci 27(31):8457–8474

    CAS  PubMed  Article  Google Scholar 

  39. Hill AV (1936) Excitation and accommodation in nerve. Proc R Soc B 119(814):305–355

    Article  Google Scholar 

  40. Hodgkin AL (1938) The subthreshold potentials in a crustacean nerve fibre. Proc R Soc B 126(842):87–121

    Article  Google Scholar 

  41. Hodgkin AL, Huxley AF (1952) A quantitative description of membrane current and its application to conduction and excitation in nerve. J Physiol 117(4):500–544

    PubMed Central  CAS  PubMed  Article  Google Scholar 

  42. Holden LK, Skinner MW, Holden TA, Demorest ME (2002) Effects of stimulation rate with the Nucleus 24 ACE speech coding strategy. Ear Hear 23(5):463–476

    PubMed  Article  Google Scholar 

  43. van den Honert C, Kelsall DC (2007) Focused intracochlear electric stimulation with phased array channels. J Acoust Soc Am 121(6):3703–3716

    PubMed  Article  Google Scholar 

  44. Hossain WA, Antic SD, Yang Y, Rasband MN, Morest DK (2005) Where is the spike generator of the cochlear nerve? Voltage-gated sodium channels in the mouse cochlea. J Neurosci 25(29):6857–6868

    PubMed Central  CAS  PubMed  Article  Google Scholar 

  45. Howells J, Trevillion L, Bostock H, Burke D (2012) The voltage dependence of I(I h) in human myelinated axons. J Physiol Lond 590(Pt 7):1625–1640

    PubMed Central  CAS  PubMed  Article  Google Scholar 

  46. Imennov NS, Rubinstein JT (2009) Stochastic population model for electrical stimulation of the auditory nerve. IEEE Trans Biomed Eng 56(10):2493–2501

    PubMed  Article  Google Scholar 

  47. Izhikevich EM (2003) Simple model of spiking neurons. IEEE Trans Neural Netw 14(6):1569–1572

    CAS  PubMed  Article  Google Scholar 

  48. Javel E, Viemeister NF (2000) Stochastic properties of cat auditory nerve responses to electric and acoustic stimuli and application to intensity discrimination. J Acoust Soc Am 107(2):908

    CAS  PubMed  Article  Google Scholar 

  49. June L, Young ED (1993) Discharge-rate dependence of refractory behavior of cat auditory-nerve fibers. Hear Res 69(1-2):151–162

    Article  Google Scholar 

  50. Kandel ER, Schwartz J, Jessell T (2000) Principles of neural science, 4th edn. McGraw-Hill Medical

  51. Katz B (1936) Multiple response to constant current in frog’s medullated nerve. J Physiol 88(2):239–255

    PubMed Central  CAS  PubMed  Article  Google Scholar 

  52. Kiefer J, von Ilberg C, Rupprecht V, Hubner-Egner J, Knecht R (2000) Optimized speech understanding with the continuous interleaved sampling speech coding strategy in patients with cochlear implants: effect of variations in stimulation rate and number of channels. Ann Otol Rhinol Laryngol 109(11):1009–1020

    CAS  PubMed  Article  Google Scholar 

  53. Knight BW (1972) Dynamics of encoding in a population of neurons. J Gen Physiol 59(6):734–766

    PubMed Central  CAS  PubMed  Article  Google Scholar 

  54. Lai HC, Jan LY (2006) The distribution and targeting of neuronal voltage-gated ion channels. Nat Rev Neurosci 7(7):548–562

    CAS  PubMed  Article  Google Scholar 

  55. Lapicque L (1907) Recherches quantitatives sur l’excitation électrique des nerfs traitée comme une polarisation. J Physiol Pathol Gen 9:620–635

    Google Scholar 

  56. Litvak LM, Delgutte B, Eddington DK (2001) Auditory nerve fiber responses to electric stimulation: modulated and unmodulated pulse trains. J Acoust Soc Am 110(1):368–379

    PubMed Central  CAS  PubMed  Article  Google Scholar 

  57. Litvak LM, Smith ZM, Delgutte B, Eddington DK (2003) Desynchronization of electrically evoked auditory-nerve activity by high-frequency pulse trains of long duration. J Acoust Soc Am 114(4 Pt 1):2066–2078

    PubMed Central  PubMed  Article  Google Scholar 

  58. Liu Q, Lee E, Davis RL (2014a) Heterogeneous intrinsic excitability of murine spiral ganglion neurons is determined by Kv1 and HCN channels. Neuroscience 257:96–110

    PubMed Central  CAS  PubMed  Article  Google Scholar 

  59. Liu Q, Manis PB, Davis RL (2014b) I h and HCN channels in murine spiral ganglion neurons: tonotopic variation, local heterogeneity, and kinetic model. J Assoc Res Otolaryngol 15(4):585–599

    PubMed Central  PubMed  Article  Google Scholar 

  60. Loizou PC (1998) Mimicking the human ear. IEEE Signal Process Mag 15(5):101–130

    Article  Google Scholar 

  61. Loizou PC, Poroy O, Dorman M (2000) The effect of parametric variations of cochlear implant processors on speech understanding. J Acoust Soc Am 108(2):790–802

    CAS  PubMed  Article  Google Scholar 

  62. Lucas K (1910) Quantitative researches on the summation of inadequate stimuli in muscle and nerve, with observations on the time-factor in electric excitation. J Physiol 39(6):461–475

    PubMed Central  CAS  PubMed  Article  Google Scholar 

  63. Macherey O, Carlyon RP, van Wieringen A, Deeks JM, Wouters J (2008) Higher sensitivity of human auditory nerve fibers to positive electrical currents. J Assoc Res Otolaryngol 9(2):241–251

    PubMed Central  PubMed  Article  Google Scholar 

  64. Madison DV, Nicoll RA (1984) Control of the repetitive discharge of rat CA 1 pyramidal neurones in vitro. J Physiol 354:319–331

    PubMed Central  CAS  PubMed  Article  Google Scholar 

  65. Mark KE, Miller MI (1992) Bayesian model selection and minimum description length estimation of auditory-nerve discharge rates. J Acoust Soc Am 91(2):989–1002

    CAS  PubMed  Article  Google Scholar 

  66. Matsuoka AJ, Rubinstein JT, Abbas PJ, Miller CA (2001) The effects of interpulse interval on stochastic properties of electrical stimulation: models and measurements. IEEE Trans Biomed Eng 48(4):416–424

    CAS  PubMed  Article  Google Scholar 

  67. Merzenich MM, White MW (1977) Cochlear implants: the interface problem. In: Hambrecht FT, Reswick JB (eds) Functional electrical stimulation: applications in neural prostheses. Marcel Dekker, Inc., New York, pp 321–340

    Google Scholar 

  68. Miller C, Abbas PJ, Nourski KV, Hu N, Robinson BK (2003) Electrode configuration influences action potential initiation site and ensemble stochastic response properties. Hear Res 175(1-2):200–214

    PubMed  Article  Google Scholar 

  69. Miller CA, Abbas PJ, Robinson B (2001) Response properties of the refractory auditory nerve fiber. J Assoc Res Otolaryngol 2(3):216–232

    PubMed Central  CAS  PubMed  Article  Google Scholar 

  70. Miller CA, Woo J, Abbas PJ, Hu N, Robinson BK (2011) Neural masking by sub-threshold electric stimuli: animal and computer model results. J Assoc Res Otolaryngol 12(2):219–232

    PubMed Central  PubMed  Article  Google Scholar 

  71. Miller MI (1985) Algorithms for removing recovery-related distortion from auditory-nerve discharge patterns. J Acoust Soc Am 77(4):1452–1464

    CAS  PubMed  Article  Google Scholar 

  72. Miller MI, Mark KE (1992) A statistical study of cochlear nerve discharge patterns in response to complex speech stimuli. J Acoust Soc Am 92(1):202–209

    CAS  PubMed  Article  Google Scholar 

  73. Mino H, Rubinstein JT, Miller CA, Abbas PJ (2004) Effects of electrode-to-fiber distance on temporal neural response with electrical stimulation. IEEE Trans Biomed Eng 51(1):13–20

    PubMed  Article  Google Scholar 

  74. Mo ZL, Adamson CL, Davis RL (2002) Dendrotoxin-sensitive K+ currents contribute to accommodation in murine spiral ganglion neurons. J Physiol 542(3):763–778

    PubMed Central  CAS  PubMed  Article  Google Scholar 

  75. Negm MH, Bruce IC (2008) Effects of and on the response of the auditory nerve to electrical stimulation in a stochastic Hodgkin-Huxley model. Proc 30th Annu Int Conf IEEE Eng Med Biol Soc pp 5539–5542

  76. Negm MH, Bruce IC (2014) The effects of HCN and KLT ion channels on adaptation and refractoriness in a stochastic auditory nerve model. IEEE Trans Biomed Eng 61(11):2749–2759

    PubMed  Article  Google Scholar 

  77. Nernst W (1908) Zur theorie des elektrischen reizes. Pfluger Arch 122(7-9):275–314

    Article  Google Scholar 

  78. Nie K, Barco A, Zeng FG (2006) Spectral and temporal cues in cochlear implant speech perception. Ear Hear 27(2):208–217

    PubMed  Article  Google Scholar 

  79. Phan TT, White MW, Finley CC, Cartee LA (1994) Neural membrane model responses to sinusoidal electrical stimuli. In: Hochmair-Desoyer IJ, Hochmair ES (eds) Advances in cochlear implants. Manz, Vienna, Austria, pp 342–347

    Google Scholar 

  80. Plant K, Holden L, Skinner M, Arcaroli J, Whitford L, Law MA, Nel E (2007) Clinical evaluation of higher stimulation rates in the nucleus research platform 8 system. Ear Hear 28(3):381–393

    PubMed  Article  Google Scholar 

  81. Plant KL, Whitford LA, Psarros CE, Vandali AE (2002) Parameter selection and programming recommendations for the ACE and CIS speech-processing strategies in the Nucleus 24 cochlear implant system. Cochlear Implants Int 3(2):104–125

    PubMed  Article  Google Scholar 

  82. Plourde E, Delgutte B, Brown EN (2011) A point process model for auditory neurons considering both their intrinsic dynamics and the spectrotemporal properties of an extrinsic signal. IEEE Trans Biomed Eng 58(6):1507–1510

    PubMed Central  PubMed  Article  Google Scholar 

  83. Prijs VF, Keijzer J, Versnel H, Schoonhoven R (1993) Recovery characteristics of auditory nerve fibres in the normal and noise-damaged guinea pig cochlea. Hear Res 71(1-2):190–201

    CAS  PubMed  Article  Google Scholar 

  84. Rasband MN, Shrager P (2000) Ion channel sequestration in central nervous system axons. J Physiol 525(Pt 1):63–73

    PubMed Central  CAS  PubMed  Article  Google Scholar 

  85. Rattay F (2000) Basics of hearing theory and noise in cochlear implants. Chaos Soliton Fract 11(12):1875–1884

    Article  Google Scholar 

  86. Rattay F, Danner SM (2014) Peak I of the human auditory brainstem response results from the somatic regions of type I spiral ganglion cells: evidence from computer modeling. Hear Res 315:67–79

    PubMed Central  PubMed  Article  Google Scholar 

  87. Rattay F, Lutter P, Felix H (2001) A model of the electrically excited human cochlear neuron. Hear Res 153(1-2):43–63

    CAS  PubMed  Article  Google Scholar 

  88. Rattay F, Potrusil T, Wenger C, Wise AK, Glueckert R, Schrott-Fischer A (2013) Impact of morphometry, myelinization and synaptic current strength on spike conduction in human and cat spiral ganglion neurons. PLoS One 8(11):e79,256

    CAS  Article  Google Scholar 

  89. Reid MA, Flores-Otero J, Davis RL (2004) Firing patterns of type II spiral ganglion neurons in vitro. J Neurosci 24(3):733–742

    CAS  PubMed  Article  Google Scholar 

  90. Robinson RB, Siegelbaum SA (2003) Hyperpolarization-activated cation currents: from molecules to physiological function. Annu Rev Physiol 65:453–480

    CAS  PubMed  Article  Google Scholar 

  91. Rothman JS, Manis PB (2003) Kinetic analyses of three distinct potassium conductances in ventral cochlear nucleus neurons. J Neurophysiol 89(6):3083–3096

    CAS  PubMed  Article  Google Scholar 

  92. Rubinstein JT (1995) Threshold fluctuations in an N sodium channel model of the node of Ranvier. Biophys J 68(3):779–785

    PubMed Central  CAS  PubMed  Article  Google Scholar 

  93. Safieddine S, El-Amraoui A, Petit C (2012) The auditory hair cell ribbon synapse: from assembly to function. Annu Rev Neurosci 35(1):509–528

    CAS  PubMed  Article  Google Scholar 

  94. Sigworth FJ (1981) Covariance of nonstationary sodium current fluctuations at the node of Ranvier. Biophys J 34(1):111–133

    PubMed Central  CAS  PubMed  Article  Google Scholar 

  95. Sly DJ, Heffer LF, White MW, Shepherd RK, Birch MGJ, Minter RL, Nelson NE, Wise AK, O’Leary SJ (2007) Deafness alters auditory nerve fibre responses to cochlear implant stimulation. Eur J Neurosci 26(2):510–522

    PubMed Central  PubMed  Article  Google Scholar 

  96. Smit JE, Hanekom T, Hanekom JJ (2008) Predicting action potential characteristics of human auditory nerve fibres through modification of the Hodgkin-Huxley equations. S Afr J Sc 104(7-8):284–292

    Google Scholar 

  97. Smit JE, Hanekom T, van Wieringen A, Wouters J, Hanekom JJ (2010) Threshold predictions of different pulse shapes using a human auditory nerve fibre model containing persistent sodium and slow potassium currents. Hear Res 269(1-2):12–22

    PubMed  Article  Google Scholar 

  98. Solandt DY (1936) The measurement of “accommodation” in nerve. Proc R Soc B 119(814):355–379

    CAS  Article  Google Scholar 

  99. Tait J (1910) The relation between refractory phase and electrical change. Exp Physiol 3(3):221–232

    Article  Google Scholar 

  100. Trevino A, Coleman TP, Allen J (2010) A dynamical point process model of auditory nerve spiking in response to complex sounds. J Comput Neurosci 29(1-2):193–201

    PubMed Central  PubMed  Article  Google Scholar 

  101. Vandali AE, Whitford LA, Plant KL, Clarke GM (2000) Speech perception as a function of electrical stimulation rate: using the nucleus 24 cochlear implant system. Ear Hear 21(6):608–624

    CAS  PubMed  Article  Google Scholar 

  102. Verschuur CA (2005) Effect of stimulation rate on speech perception in adult users of the Med-El CIS speech processing strategy. Int J Audiol 44(1):58–63

    CAS  PubMed  Article  Google Scholar 

  103. Verveen AA (1961) Fluctuation in excitability. PhD thesis, Netherlands Central Institute for Brain Research, Amsterdam, Netherlands

  104. Verveen AA (1962) Axon diameter and fluctuation in excitability. Acta Morphol Neerl Scand 5:79–85

    CAS  PubMed  Google Scholar 

  105. Verveen AA, Derksen HE (1968) Fluctuation phenomena in nerve membrane. Proc IEEE 56(6):906–916

    Article  Google Scholar 

  106. Weber BP, Lai WK, Dillier N, von Wallenberg EL, Killian MJP, Pesch J, Battmer RD, Lenarz T (2007) Performance and preference for ACE stimulation rates obtained with nucleus RP 8 and freedom system. Ear Hear 28(2):46S–48S

    CAS  PubMed  Article  Google Scholar 

  107. Webster M, Webster DB (1981) Spiral ganglion neuron loss following organ of Corti loss: a quantitative study. Brain Res 212(1):17–30

    CAS  PubMed  Article  Google Scholar 

  108. White MW (1984) Psychophysical and neuropsychological considerations in the design of a cochlear prosthesis. Audiol Ital 1:77–117

    Google Scholar 

  109. Wilson BS, Finley CC, Farmer JC, Lawson DT, Weber BA, Wolford RD, Kenan PD, White MW, Merzenich MM, Schindler RA (1988) Comparative studies of speech processing strategies for cochlear implants. Laryngoscope 98(10):1069–1077

    CAS  PubMed  Google Scholar 

  110. Wilson BS, Finley CC, Lawson DT, Wolford RD, Zerbi M (1993) Design and evaluation of a continuous interleaved sampling (CIS) processing strategy for multichannel cochlear implants. J Rehabil Res Dev 30(1):110–116

    CAS  PubMed  Google Scholar 

  111. Woo J, Miller CA, Abbas PJ (2009a) Biophysical model of an auditory nerve fiber with a novel adaptation component. IEEE Trans Biomed Eng 56(9):2177–2180

    PubMed  Article  Google Scholar 

  112. Woo J, Miller CA, Abbas PJ (2009b) Simulation of the electrically stimulated cochlear neuron: modeling adaptation to trains of electric pulses. IEEE Trans Biomed Eng 56(5):1348–1359

    PubMed  Article  Google Scholar 

  113. Woo J, Miller CA, Abbas PJ (2009c) The dependence of auditory nerve rate adaptation on electric stimulus parameters, electrode position, and fiber diameter: a computer model study. J Assoc Res Otolaryngol 11(2):283–296

    PubMed Central  PubMed  Article  Google Scholar 

  114. Yi E, Roux I, Glowatzki E (2010) Dendritic HCN channels shape excitatory postsynaptic potentials at the inner hair cell afferent synapse in the mammalian cochlea. J Neurophysiol 103(5):2532–2543

    PubMed Central  CAS  PubMed  Article  Google Scholar 

  115. Zhang F, Miller CA, Robinson BK, Abbas PJ, Hu N (2007) Changes across time in spike rate and spike amplitude of auditory nerve fibers stimulated by electric pulse trains. J Assoc Res Otolaryngol 8(3):356–372

    PubMed Central  PubMed  Article  Google Scholar 

Download references

Acknowledgments

We would like to thank Drs. Paul Abbas, Lianne Cartee, and Elisabeth Glowatzki for allowing the use of their figures in this paper. We would also like to thank members of the Bruce laboratory for the feedback on earlier versions of the manuscript. Finally, we would like to thank Associate Editor Dr. George Spirou and the two anonymous reviewers for the helpful comments. This work was supported by NSERC Discovery Grant 261736 (ICB).

Compliance with Ethical Standards

Conflict of Interest

The authors declare that they have no competing interests.

Author information

Affiliations

Authors

Corresponding author

Correspondence to Jason Boulet.

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Boulet, J., White, M. & Bruce, I.C. Temporal Considerations for Stimulating Spiral Ganglion Neurons with Cochlear Implants. JARO 17, 1–17 (2016). https://doi.org/10.1007/s10162-015-0545-5

Download citation

Keywords

  • auditory nerve fiber
  • ion channel
  • refractoriness
  • facilitation
  • accommodation
  • spike rate adaptation