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Journal of the Association for Research in Otolaryngology

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01-03-2007

A Dual-Process Integrator–Resonator Model of the Electrically Stimulated Human Auditory Nerve

Authors: Olivier Macherey, Robert P. Carlyon, Astrid van Wieringen, Jan Wouters

Published in: Journal of the Association for Research in Otolaryngology | Issue 1/2007

Abstract

A phenomenological dual-process model of the electrically stimulated human auditory nerve is presented and compared to threshold and loudness data from cochlear implant users. The auditory nerve is modeled as two parallel processes derived from linearized equations of conductance-based models. The first process is an integrator, which dominates stimulation for short-phase duration biphasic pulses and high-frequency sinusoidal stimuli. It has a relatively short time constant (0.094 ms) arising from the passive properties of the membrane. The second process is a resonator, which induces nonmonotonic functions of threshold vs frequency with minima around 80 Hz. The ion channel responsible for this trend has a relatively large relaxation time constant of about 1 ms. Membrane noise is modeled as a Gaussian noise, and loudness sensation is assumed to relate to the probability of firing of a neuron during a 20-ms rectangular window. Experimental psychophysical results obtained in seven previously published studies can be interpreted with this model. The model also provides a physiologically based account of the nonmonotonic threshold vs frequency functions observed in biphasic and sinusoidal stimulation, the large threshold decrease obtained with biphasic pulses having a relatively long inter-phase gap and the effects of asymmetric pulses.

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Bruce IC, White MW, Irlicht LS, O’Leary SJ, Dynes S, Javel E, Clark GM. A Stochastic model of the electrically stimulated auditory nerve: Single-pulse response. IEEE Trans. Biomed. Eng. 46:617–629, 1999a.PubMedCrossRef

Bruce IC, White MW, Irlicht LS, O’Leary SJ, Clark GM. The effects of stochastic neural activity in a model predicting intensity perception with cochlear implants: Low-rate stimulation. IEEE Trans. Biomed. Eng. 46:1393–1404, 1999b.PubMedCrossRef

Brunel N, Hakim V, Richardson MEJ. Firing-rate resonance in a generalized integrate-and-fire neuron with subthreshold resonance. Phys. Rev. 67:051916.1–051916.23, 2003.

Carlyon RP, van Wieringen A, Deeks JM, Long CJ, Lyzenga J, Wouters J. Effect of inter-phase gap on the sensitivity of cochlear implant users to electrical stimulation. Hear. Res. 205:210–224, 2005.PubMedCrossRef

Cartee LA. 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. 146:153–166, 2000.PubMedCrossRef

Chen C. Hyperpolarization-activated current (Ih) in primary auditory neurons. Hear. Res. 110:179–190, 1997.PubMedCrossRef

Clopton BM, Spelman FA, Glass I, Pfingst BE, Miller JM, Lawrence PD, Dean DP. Neural encoding of electrical signals. In cochlear prostheses. New York, Annals of New York Academy of Sciences, pp. 146–158, 1983.

Colombo J, Parkins CW. A model of electrical excitation of the mammalian auditory-nerve neuron. Hear. Res. 31:287–311, 1987.PubMedCrossRef

de Balthasar C, Boex C, Cosendai G, Valentini G, Sigrist A, Pelizzone M. Channel interactions with high-rate biphasic electrical stimulation in cochlear implant subjects. Hear. Res. 182:77–87, 2003.PubMedCrossRef

Donaldson GS, Viemeister NF, Nelson DA. Psychometric functions and temporal integration in electric hearing. J. Acoust. Soc. Am. 101:3706–3721, 1997.PubMedCrossRef

Eddington DK, Noel VA, Rabinowitz WM, Svirsky MA, Tierney J, Zissman MA. Speech processors for auditory prostheses. Eighth quarterly progress report, NIH contract N01-DC-2-2402, 1994.

Finley CC, Wilson BS, White MW. Models of neural responsiveness to electrical stimulation. In: Miller JM and Spelman FA (eds) Cochlear Implants: Models of the electrically stimulated ear. New York, Springler-Verlag, pp. 55–96, 1990.

Frankenhauser B, Huxley AF. The action potential in the myelinated nerve fiber of Xenopus laevis as computed on the basis of voltage clamp data. J. Physiol. 171:302–315, 1964.

French AS. The frequency response function and sinusoidal threshold properties of the Hodgkin–Huxley model of action potential encoding. Biol. Cybern. 49:169–174, 1984.PubMedCrossRef

Frijns JHM, de Snoo SL, ten Kate JH. Spatial selectivity in a rotationally symmetric model of the electrically stimulated cochlea. Hear. Res. 95:33–48, 1996.PubMedCrossRef

Gerstner W, Kistler WM. Formal spiking neuron models. In: Spiking Neuron Models. Cambridge, MA, Cambridge University Press, pp. 93–145, 2002.

Guttman R, Hachmeister L. Effect of calcium, temperature, and polarizing currents upon alternating current excitation of space-clamped squid axons. J. Gen. Physiol. 58:304–321, 1971.PubMedCrossRef

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

Hutcheon B, Yarom Y. Resonance, oscillation and the intrinsic frequency preferences of neurons. Trends Neurosci. 23:216–222, 2000.PubMedCrossRef

Izhikevich EM. Resonate-and-fire neurons. Neural Netw. 14:883–894, 2001.PubMedCrossRef

Koch C. Cable theory in neurons with active, linearized membranes. Biol. Cybern. 50:15–33, 1984.PubMedCrossRef

Kreft HA, Donaldson GS, Nelson DA. Effects of pulse rate on threshold and dynamic range in Clarion cochlear-implant users. J. Acoust. Soc. Am. 115:1885–1888, 2004.PubMedCrossRef

Levitt H. Transformed up-down methods in psychoacoustics. J. Acoust. Soc. Am. 49:467–477, 1971.PubMedCrossRef

Longnion JK, Rubinstein JT. A biophysical population model of an auditory nerve: response to electrically-encoded speech. Abstracts of the 29th Midwinter Research Meeting, Association for Research in Otolaryngology, p. 219, 2006.

Macherey O, van Wieringen A, Carlyon RP, Deeks JM, Wouters J. Asymmetric pulses in cochlear implants: effects of pulse shape, polarity and rate. J. Assoc. Res. Otolaryngol. 7:253–266, 2006.PubMedCrossRef

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

Mauro A, Conti F, Dodge F, Schor R. Subthreshold behavior and phenomenological impedance of the squid giant axon. J. Gen. Physiol. 55:497–523, 1970.PubMedCrossRef

McIntyre CC, Richardson AG, Grill WM. Modeling the excitability of mammalian nerve fibers: Influence of afterpotentials on the recovery cycle. J. Neurophysiol. 87:995–1006, 2002.PubMed

McKay CM, Henshall KR. The perceptual effects of interphase gap duration in cochlear implant stimulation. Hear. Res. 181:94–99, 2003.PubMedCrossRef

McKay CM, Henshall KR, Farrell RJ, McDermott HJ. A practical method of predicting the loudness of complex electrical stimuli. J. Acoust. Soc. Am. 113:2054–2063, 2003.PubMedCrossRef

Middlebrooks JC. Effects of cochlear-implant pulse rate and inter-channel timing on channel interactions and thresholds. J. Acoust. Soc. Am. 116:452–468, 2004.PubMedCrossRef

Miller AL, Morris DJ, Pfingst BE. Interactions between pulse separation and pulse polarity order in cochlear implants. Hear. Res. 109:21–33, 1997.PubMedCrossRef

Miller AL, Smith DW, Pfingst BE. Across-species comparisons of psychophysical detection thresholds for electrical stimulation of the cochlea: I. Sinusoidal stimuli. Hear. Res. 134:89–104, 1999a.PubMedCrossRef

Miller AL, Smith DW, Pfingst BE. Across-species comparisons of psychophysical detection thresholds for electrical stimulation of the cochlea: II. Strength–duration functions for single, biphasic pulses. Hear. Res. 135:47–55, 1999b.PubMedCrossRef

Miller CA, Abbas PJ, Robinson BK, Rubinstein JT, Matsuoka AJ. Electrically evoked single-fiber action potentials from cat: Responses to monopolar, monophasic stimulation. Hear. Res. 130:197–218, 1999c.PubMedCrossRef

Mo Z, Davis RL. Heterogeneous voltage dependence of inward Rectifier currents in spiral ganglion neurons. J. Neurophysiol. 78:3019–3027, 1997.PubMed

Moon AK, Zwolan TA, Pfingst BE. Effects of phase duration on detection of electrical stimulation of the human cochlea. Hear. Res. 67:166–178, 1993.PubMedCrossRef

Moore BCJ, Glasberg BR, Plack CJ, Biswas AK. The shape of the ear’s temporal window. J. Acoust. Soc. Am. 83:1102–1116, 1988.PubMedCrossRef

Moore BCJ, Peters RW, Glasberg BR. Detection of decrements and increments in sinusoids at high overall levels. J. Acoust. Soc. Am. 99:3669–3677, 1996.PubMedCrossRef

Morse RP, Evans EF. The sciatic nerve of the toad Xenopus Laevis as a physiological model of the human cochlear nerve. Hear. Res. 182:97–118, 2003.PubMedCrossRef

Pfingst BE. Comparisons of psychophysical and neurophysiological studies of cochlear implants. Hear. Res. 34:243–251, 1988.PubMedCrossRef

Pfingst BE, Holloway LA, Razzaque SA. Effects of pulse separation on detection thresholds for electrical stimulation of the human cochlea. Hear. Res. 98:77–92, 1996.PubMedCrossRef

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

Rattay F. Analysis of models for extracellular fiber stimulation. IEEE Trans. Biomed. Eng. 36:676–682, 1989.PubMedCrossRef

Rattay F, Lutter P, Felix H. 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, 2001.PubMedCrossRef

Richardson MJ, Brunel N, Hakim V. From subthreshold to firing-rate resonance. J. Neurophysiol. 89:2538–2554, 2003.PubMedCrossRef

Rubinstein JT. Threshold fluctuations in an N-sodium channel model of the node of Ranvier. Biophys. J. 68:779–785, 1995.PubMedCrossRef

Rubinstein JT, Miller CA, Mino H, Abbas PJ. Analysis of monophasic and biphasic electrical stimulation of nerve. IEEE Trans. Biomed. Eng. 48:1065–1070, 2001.PubMedCrossRef

Schwarz DW, Dezso A, Neufeld PR. Frequency selectivity of central auditory neurons without inner ear. Acta Otolaryngol. 113:266–270, 1993.PubMed

Shannon RV. Multichannel electrical stimulation of the auditory nerve in man. I. Basic psychophysics. Hear. Res. 11:157–189, 1983.PubMedCrossRef

Shannon RV. Threshold and loudness functions for pulsatile stimulation of cochlear implants. Hear. Res. 18:135–143, 1985.PubMedCrossRef

Shannon RV. A model of threshold for pulsatile electrical stimulation of cochlear implants. Hear. Res. 40:197–204, 1989.PubMedCrossRef

Shepherd RK, Javel E. Electrical stimulation of the auditory nerve: II. Effect of stimulus waveshape on single fibre response properties. Hear. Res. 130:171–188, 1999.PubMedCrossRef

St Hilaire M, Longtin, A. Comparison of coding capabilities of type I and type II neurons. J. Comput. Neurosci. 16:299–313, 2004.PubMedCrossRef

Strohmann B, Schwarz DW, Puil E. Electrical resonances in central auditory neurons. Acta Otolaryngol. 115:168–172, 1995.PubMed

van den Honert C, Mortimer JT. The response of the myelinated nerve fiber to short duration biphasic stimulating currents. Ann. Biomed. Eng. 7:117–125, 1979.PubMedCrossRef

van Wieringen A, Carlyon RP, Macherey O, Wouters J. Effects of pulse rate on thresholds and loudness of biphasic and alternating monophasic pulse trains in electrical hearing. Hear. Res. 220:49–60, 2006.PubMedCrossRef

Verveen AA. Fluctuation in excitability. Ph.D. dissertation, University of Amsterdam, Amsterdam, The Netherlands, 1961.

Viemeister NF, Wakefield GH. Temporal integration and multiple looks. J. Acoust. Soc. Am. 90:858–865, 1991.PubMedCrossRef

Weiss TF. Cellular biophysics: teaching and learning with computer simulations. http://umech.mit.edu/weiss/announce.html, 2000.

Xu Y, Collins LM. Predicting the threshold of pulse-train electrical stimuli using a stochastic auditory nerve model: The effects of stimulus noise. IEEE Trans. Biomed. Eng. 51:590–603, 2004.PubMedCrossRef

Xu Y, Collins LM. Predicting dynamic range and intensity discrimination for electrical pulse-train stimuli using a stochastic auditory nerve model: The effects of stimulus noise. IEEE Trans. Biomed. Eng. 52:1040–1049, 2005.PubMedCrossRef

Zeng FG, Fu QJ, Morse R. Human hearing enhanced by noise. Brain Res. 869:251–255, 2000.PubMedCrossRef

Title: A Dual-Process Integrator–Resonator Model of the Electrically Stimulated Human Auditory Nerve
Authors: Olivier Macherey
Robert P. Carlyon
Astrid van Wieringen
Jan Wouters
Publication date: 01-03-2007
Publisher: Springer-Verlag
Published in: Journal of the Association for Research in Otolaryngology / Issue 1/2007
Print ISSN: 1525-3961
Electronic ISSN: 1438-7573
DOI: https://doi.org/10.1007/s10162-006-0066-3

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A Dual-Process Integrator–Resonator Model of the Electrically Stimulated Human Auditory Nerve

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