Skip to main content
Key Specialties
Cardiology Diabetology Endocrinology Gastroenterology Geriatrics and Gerontology Gynecology and Obstetrics Hematology Infectious Disease Internal Medicine Nephrology Neurology Oncology Pediatrics Respiratory Medicine Rheumatology Surgery
Congress Coverage
2024 ACC Congress 2023 ESMO Congress 2023 EASD Congress 2023 ERS Congress 2023 ESC Congress
Clinical Collections
Advances in Alzheimer’s

At a glance: The STEP trials

A round-up of the STEP phase 3 clinical trials evaluating semaglutide for weight loss in people with overweight or obesity.
ADVANCED SEARCH
Log in
Top
Journal of the Association for Research in Otolaryngology
Published in: Journal of the Association for Research in Otolaryngology 1/2016

01-02-2016 | Review Article

Temporal Considerations for Stimulating Spiral Ganglion Neurons with Cochlear Implants

Authors: Jason Boulet, Mark White, Ian C. Bruce

Published in: Journal of the Association for Research in Otolaryngology | Issue 1/2016

Login to get access

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.
Literature
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):331–350PubMedCrossRef
Arora K, Dawson P, Dowell R, Vandali A (2009) Electrical stimulation rate effects on speech perception in cochlear implants. Int J Audiol 48(8):561–567PubMedCrossRef
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):757–762PubMedCrossRef
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):555–569PubMedCentralPubMedCrossRef
Benda J, Herz AVM (2003) A universal model for spike-frequency adaptation. Neural Comput 15(11):2523–2564PubMedCrossRef
Bi Q (1989) A closed-form solution for removing the dead time effects from the poststimulus time histograms. J Acoust Soc Am 85(6):2504PubMedCrossRef
Biel M, Wahl-Schott C, Michalakis S, Zong X (2009) Hyperpolarization-activated cation channels: from genes to function. Physiol Rev 89(3):847–885PubMedCrossRef
Bortone DS, Mitchell K, Manis PB (2006) Developmental time course of potassium channel expression in the rat cochlear nucleus. Hear Res 211(1-2):114–125PubMedCrossRef
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):380–391PubMedCrossRef
Brette R, Gerstner W (2005) Adaptive exponential integrate-and-fire model as an effective description of neuronal activity. J Neurophysiol 94(5):3637–3642PubMedCrossRef
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):1–20PubMedCentralPubMedCrossRef
Brown DA, Adams PR (1980) Muscarinic suppression of a novel voltage-sensitive K+ current in a vertebrate neuron. Nature 283(5748):673–676PubMedCrossRef
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):617–629PubMedCrossRef
Brunel N, van Rossum M (2007) Quantitative investigations of electrical nerve excitation treated as polarization. Biol Cybern 97(5-6):341–349CrossRef
Burkitt AN (2006) A review of the integrate-and-fire neuron model: I. Homogeneous synaptic input. Biol Cybern 95(1):1–19PubMedCrossRef
Butikofer R, Lawrence PD (1979) Electrocutaneous nerve stimulation-II: stimulus waveform selection. IEEE Trans Biomed Eng BME-26(2):69–75CrossRef
Campbell LJ, Sly DJ, O’Leary SJ (2012) Prediction and control of neural responses to pulsatile electrical stimulation. J Neural Eng 9(2):026,023CrossRef
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):153–166PubMedCrossRef
Cartee LA (2006) Spiral ganglion cell site of excitation II: numerical model analysis. Hear Res 215(1-2):22–30PubMedCrossRef
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):143–152PubMedCrossRef
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):10–21PubMedCrossRef
Chen C (1997) Hyperpolarization-activated current (I h) in primary auditory neurons. Hear Res 110(1-2):179–190PubMedCrossRef
Cohen LT (2009) Practical model description of peripheral neural excitation in cochlear implant recipients: 5. Refractory recovery and facilitation. Hear Res 248(1-2):1–14PubMedCrossRef
Dynes SBC (1996) Discharge characteristics of auditory nerve fibers for pulsatile electrical stimuli. PhD thesis, Massachusetts Institute of Technology, Cambridge, Massachusetts
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):83–97PubMedCentralPubMedCrossRef
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):1–20PubMedCrossRef
Friesen LM, Shannon RV, Cruz RJ (2005) Effects of stimulation rate on speech recognition with cochlear implants. Audiol Neurootol 10(3):169–184PubMedCrossRef
Glowatzki E, Fuchs PA (2002) Transmitter release at the hair cell ribbon synapse. Nat Neurosci 5(2):147–154PubMedCrossRef
Goldwyn JH, Rubinstein JT, Shea-Brown E (2012) A point process framework for modeling electrical stimulation of the auditory nerve. J Neurophysiol 108(5):1430–1452PubMedCentralPubMedCrossRef
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):13,025–13,041CrossRef
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):147–165PubMedCrossRef
Hartmann R, Topp G, Klinke R (1984) Discharge patterns of cat primary auditory fibers with electrical-stimulation of the cochlea. Hear Res 13(1):47–62PubMedCrossRef
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
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):3124–3135PubMedCentralPubMedCrossRef
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):8457–8474PubMedCrossRef
Hill AV (1936) Excitation and accommodation in nerve. Proc R Soc B 119(814):305–355CrossRef
Hodgkin AL (1938) The subthreshold potentials in a crustacean nerve fibre. Proc R Soc B 126(842):87–121CrossRef
Hodgkin AL, Huxley AF (1952) A quantitative description of membrane current and its application to conduction and excitation in nerve. J Physiol 117(4):500–544PubMedCentralPubMedCrossRef
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):463–476PubMedCrossRef
van den Honert C, Kelsall DC (2007) Focused intracochlear electric stimulation with phased array channels. J Acoust Soc Am 121(6):3703–3716PubMedCrossRef
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):6857–6868PubMedCentralPubMedCrossRef
Imennov NS, Rubinstein JT (2009) Stochastic population model for electrical stimulation of the auditory nerve. IEEE Trans Biomed Eng 56(10):2493–2501PubMedCrossRef
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):908PubMedCrossRef
June L, Young ED (1993) Discharge-rate dependence of refractory behavior of cat auditory-nerve fibers. Hear Res 69(1-2):151–162CrossRef
Kandel ER, Schwartz J, Jessell T (2000) Principles of neural science, 4th edn. McGraw-Hill Medical
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):1009–1020PubMedCrossRef
Lai HC, Jan LY (2006) The distribution and targeting of neuronal voltage-gated ion channels. Nat Rev Neurosci 7(7):548–562PubMedCrossRef
Lapicque L (1907) Recherches quantitatives sur l’excitation électrique des nerfs traitée comme une polarisation. J Physiol Pathol Gen 9:620–635
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):368–379PubMedCentralPubMedCrossRef
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):2066–2078PubMedCentralPubMedCrossRef
Liu Q, Lee E, Davis RL (2014a) Heterogeneous intrinsic excitability of murine spiral ganglion neurons is determined by Kv1 and HCN channels. Neuroscience 257:96–110PubMedCentralPubMedCrossRef
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):585–599PubMedCentralPubMedCrossRef
Loizou PC (1998) Mimicking the human ear. IEEE Signal Process Mag 15(5):101–130CrossRef
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):790–802PubMedCrossRef
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):461–475PubMedCentralPubMedCrossRef
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):241–251PubMedCentralPubMedCrossRef
Mark KE, Miller MI (1992) Bayesian model selection and minimum description length estimation of auditory-nerve discharge rates. J Acoust Soc Am 91(2):989–1002PubMedCrossRef
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):416–424PubMedCrossRef
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
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):200–214PubMedCrossRef
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):219–232PubMedCentralPubMedCrossRef
Miller MI (1985) Algorithms for removing recovery-related distortion from auditory-nerve discharge patterns. J Acoust Soc Am 77(4):1452–1464PubMedCrossRef
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):202–209PubMedCrossRef
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):13–20PubMedCrossRef
Mo ZL, Adamson CL, Davis RL (2002) Dendrotoxin-sensitive K+ currents contribute to accommodation in murine spiral ganglion neurons. J Physiol 542(3):763–778PubMedCentralPubMedCrossRef
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
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):2749–2759PubMedCrossRef
Nernst W (1908) Zur theorie des elektrischen reizes. Pfluger Arch 122(7-9):275–314CrossRef
Nie K, Barco A, Zeng FG (2006) Spectral and temporal cues in cochlear implant speech perception. Ear Hear 27(2):208–217PubMedCrossRef
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
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):381–393PubMedCrossRef
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):104–125PubMedCrossRef
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):1507–1510PubMedCentralPubMedCrossRef
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):190–201PubMedCrossRef
Rattay F (2000) Basics of hearing theory and noise in cochlear implants. Chaos Soliton Fract 11(12):1875–1884CrossRef
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 315:67–79PubMedCentralPubMedCrossRef
Rattay F, Lutter P, Felix H (2001) A model of the electrically excited human cochlear neuron. Hear Res 153(1-2):43–63PubMedCrossRef
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):e79,256CrossRef
Reid MA, Flores-Otero J, Davis RL (2004) Firing patterns of type II spiral ganglion neurons in vitro. J Neurosci 24(3):733–742PubMedCrossRef
Robinson RB, Siegelbaum SA (2003) Hyperpolarization-activated cation currents: from molecules to physiological function. Annu Rev Physiol 65:453–480PubMedCrossRef
Rothman JS, Manis PB (2003) Kinetic analyses of three distinct potassium conductances in ventral cochlear nucleus neurons. J Neurophysiol 89(6):3083–3096PubMedCrossRef
Safieddine S, El-Amraoui A, Petit C (2012) The auditory hair cell ribbon synapse: from assembly to function. Annu Rev Neurosci 35(1):509–528PubMedCrossRef
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):510–522PubMedCentralPubMedCrossRef
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
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):12–22PubMedCrossRef
Solandt DY (1936) The measurement of “accommodation” in nerve. Proc R Soc B 119(814):355–379CrossRef
Tait J (1910) The relation between refractory phase and electrical change. Exp Physiol 3(3):221–232CrossRef
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):193–201PubMedCentralPubMedCrossRef
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):608–624PubMedCrossRef
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):58–63PubMedCrossRef
Verveen AA (1961) Fluctuation in excitability. PhD thesis, Netherlands Central Institute for Brain Research, Amsterdam, Netherlands
Verveen AA (1962) Axon diameter and fluctuation in excitability. Acta Morphol Neerl Scand 5:79–85PubMed
Verveen AA, Derksen HE (1968) Fluctuation phenomena in nerve membrane. Proc IEEE 56(6):906–916CrossRef
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–48SPubMedCrossRef
Webster M, Webster DB (1981) Spiral ganglion neuron loss following organ of Corti loss: a quantitative study. Brain Res 212(1):17–30PubMedCrossRef
White MW (1984) Psychophysical and neuropsychological considerations in the design of a cochlear prosthesis. Audiol Ital 1:77–117
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):1069–1077PubMed
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):110–116PubMed
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):2177–2180PubMedCrossRef
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):1348–1359PubMedCrossRef
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):283–296PubMedCentralPubMedCrossRef
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):2532–2543PubMedCentralPubMedCrossRef
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):356–372PubMedCentralPubMedCrossRef
Metadata
Title
Temporal Considerations for Stimulating Spiral Ganglion Neurons with Cochlear Implants
Authors
Jason Boulet
Mark White
Ian C. Bruce
Publication date
01-02-2016
Publisher
Springer US
Published in
Journal of the Association for Research in Otolaryngology / Issue 1/2016
Print ISSN: 1525-3961
Electronic ISSN: 1438-7573
DOI
https://doi.org/10.1007/s10162-015-0545-5

Other articles of this Issue 1/2016

Journal of the Association for Research in Otolaryngology 1/2016 Go to the issue

Research Article

Channel Interaction and Current Level Affect Across-Electrode Integration of Interaural Time Differences in Bilateral Cochlear-Implant Listeners

Research Article

Pitch Discrimination in Musicians and Non-Musicians: Effects of Harmonic Resolvability and Processing Effort

Research Article

Tuning to Binaural Cues in Human Auditory Cortex

Research Article

Loss of Afferent Vestibular Input Produces Central Adaptation and Increased Gain of Vestibular Prosthetic Stimulation