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Published in: Journal of the Association for Research in Otolaryngology 3/2007

01-09-2007

Changes Across Time in Spike Rate and Spike Amplitude of Auditory Nerve Fibers Stimulated by Electric Pulse Trains

Authors: Fawen Zhang, Charles A. Miller, Barbara K. Robinson, Paul J. Abbas, Ning Hu

Published in: Journal of the Association for Research in Otolaryngology | Issue 3/2007

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Abstract

We undertook a systematic evaluation of spike rates and spike amplitudes of auditory nerve fiber (ANF) responses to trains of electric current pulses. Measures were obtained from acutely deafened cats to examine time-related changes free from the effects of hair-cell and synaptic adaptation. Such data relate to adaptation that likely occurs in ANFs of cochlear-implant users. A major goal was to determine and compare rate adaptation observed at different pulse rates (primarily 250, 1000, and 5000 pulse/s) and describe them using decaying exponential models similar to those used in acoustic studies. Rate-vs.-time functions were best described by two-exponent models and produced time constants similar to (although slightly greater than) the “rapid” and “short-term” components described in acoustic studies. There was little dependence of these time constants on onset spike rate, but pulse-rate effects were noted. Spike amplitude changes followed a time course different from that of rate adaptation consistent with a process related to ANF interspike intervals. The fact that two time constants governed rate adaptation in electrically stimulated and deafened fibers suggests that future computational models of adaptation should not only include hair cell and synapse components, but also components determined by fiber membrane characteristics.
Literature
go back to reference Babalian AL, Ryugo DK, Rouiller EM. Discharge properties of identified cochlear nucleus neurons and auditory nerve fibers in response to repetitive electrical stimulation of the auditory nerve. Exp Brain Res. 153:452–460, 2003.PubMedCrossRef Babalian AL, Ryugo DK, Rouiller EM. Discharge properties of identified cochlear nucleus neurons and auditory nerve fibers in response to repetitive electrical stimulation of the auditory nerve. Exp Brain Res. 153:452–460, 2003.PubMedCrossRef
go back to reference BeMent SL, Ranck JB, Jr. A quantitative study of electrical stimulation of central myelinated fibers. Exp. Neurol. 24:147–170, 1969a.PubMedCrossRef BeMent SL, Ranck JB, Jr. A quantitative study of electrical stimulation of central myelinated fibers. Exp. Neurol. 24:147–170, 1969a.PubMedCrossRef
go back to reference BeMent SL, Ranck JB, Jr. A model for electrical stimulation of central myelinated fibers with monopolar electrodes. Exp. Neurol. 24:171–186, 1969b.PubMedCrossRef BeMent SL, Ranck JB, Jr. A model for electrical stimulation of central myelinated fibers with monopolar electrodes. Exp. Neurol. 24:171–186, 1969b.PubMedCrossRef
go back to reference Bevington PR. Data Reduction and Error Analysis for the Physical Sciences. New York, McGraw-Hill, 1969. Bevington PR. Data Reduction and Error Analysis for the Physical Sciences. New York, McGraw-Hill, 1969.
go back to reference Briaire JJ, Frijns JH. Unraveling the electrically evoked compound action potential. Hear Res. 205:143–156, 2005.PubMedCrossRef Briaire JJ, Frijns JH. Unraveling the electrically evoked compound action potential. Hear Res. 205:143–156, 2005.PubMedCrossRef
go back to reference 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, 1999.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, 1999.PubMedCrossRef
go back to reference Cartee LA. Spiral ganglion cell site of excitation: II. Numerical model analysis. Hear Res. 215:22–30, 2006.PubMedCrossRef Cartee LA. Spiral ganglion cell site of excitation: II. Numerical model analysis. Hear Res. 215:22–30, 2006.PubMedCrossRef
go back to reference Cartee LA, van den Honert C, Finley CC, Miller RL. Evaluation of a model of the cochlear neural membrane. I. Physiological measurement of membrane characteristics in response to intrameatal electrical stimulation. Hear Res. 146:143–152, 2000.PubMedCrossRef Cartee LA, van den Honert C, Finley CC, Miller RL. Evaluation of a model of the cochlear neural membrane. I. Physiological measurement of membrane characteristics in response to intrameatal electrical stimulation. Hear Res. 146:143–152, 2000.PubMedCrossRef
go back to reference Chimento TC, Schreiner CE. Adaptation and recovery from adaptation in single fiber responses of the cat auditory nerve. J. Acoust. Soc. Am. 90:263–273, 1991.PubMedCrossRef Chimento TC, Schreiner CE. Adaptation and recovery from adaptation in single fiber responses of the cat auditory nerve. J. Acoust. Soc. Am. 90:263–273, 1991.PubMedCrossRef
go back to reference Colombo J, Parkins CW. A model of electrical excitation of the mammalian auditory-nerve neuron. Hear Res. 31:287–311, 1987.PubMedCrossRef Colombo J, Parkins CW. A model of electrical excitation of the mammalian auditory-nerve neuron. Hear Res. 31:287–311, 1987.PubMedCrossRef
go back to reference Cooper NP, Robertson D, Yates GK. Cochlear nerve fiber responses to amplitude-modulated stimuli: variations with spontaneous rate and other response characteristics. J. Neurophysiol. 70:370–386, 1993.PubMed Cooper NP, Robertson D, Yates GK. Cochlear nerve fiber responses to amplitude-modulated stimuli: variations with spontaneous rate and other response characteristics. J. Neurophysiol. 70:370–386, 1993.PubMed
go back to reference Dynes SB, Delgutte B. Phase-locking of auditory-nerve discharges to sinusoidal electric stimulation of the cochlea. Hear Res. 58:79–90, 1992.PubMedCrossRef Dynes SB, Delgutte B. Phase-locking of auditory-nerve discharges to sinusoidal electric stimulation of the cochlea. Hear Res. 58:79–90, 1992.PubMedCrossRef
go back to reference Dynes SBC. Discharge characteristics of auditory nerve fibers for pulsatile electrical stimuli Ph.D. Thesis, Massachusetts Institute of Technology, 1996. Dynes SBC. Discharge characteristics of auditory nerve fibers for pulsatile electrical stimuli Ph.D. Thesis, Massachusetts Institute of Technology, 1996.
go back to reference Eggermont JJ. Peripheral auditory adaptation and fatigue: a model oriented review. Hear Res. 18:57–71, 1985.PubMedCrossRef Eggermont JJ. Peripheral auditory adaptation and fatigue: a model oriented review. Hear Res. 18:57–71, 1985.PubMedCrossRef
go back to reference 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, Springer-Verlag, 1990. 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, Springer-Verlag, 1990.
go back to reference Frijns JH, Briaire JJ, Grote JJ. The importance of human cochlear anatomy for the results of modiolus-hugging multichannel cochlear implants. Otol. Neurotol. 22:340–349, 2001.PubMedCrossRef Frijns JH, Briaire JJ, Grote JJ. The importance of human cochlear anatomy for the results of modiolus-hugging multichannel cochlear implants. Otol. Neurotol. 22:340–349, 2001.PubMedCrossRef
go back to reference Gaumond RP, Kim DO, Molnar CE. Response of cochlear nerve fibers to brief acoustic stimuli: role of discharge-history effects. J. Acoust. Soc. Am. 74:1392–1398, 1983.PubMedCrossRef Gaumond RP, Kim DO, Molnar CE. Response of cochlear nerve fibers to brief acoustic stimuli: role of discharge-history effects. J. Acoust. Soc. Am. 74:1392–1398, 1983.PubMedCrossRef
go back to reference Hartmann R, Topp G, Klinke R. Discharge patterns of cat primary auditory fibers with electrical stimulation of the cochlea. Hear Res. 13:47–62, 1984.PubMedCrossRef Hartmann R, Topp G, Klinke R. Discharge patterns of cat primary auditory fibers with electrical stimulation of the cochlea. Hear Res. 13:47–62, 1984.PubMedCrossRef
go back to reference Javel E, Tong YC, Shepherd RK, Clark GM. Responses of cat auditory nerve fibers to biphasic electrical current pulses. Ann. Otol. Rhinol. Laryngol. 96 (Suppl. 128):26–30, 1987. Javel E, Tong YC, Shepherd RK, Clark GM. Responses of cat auditory nerve fibers to biphasic electrical current pulses. Ann. Otol. Rhinol. Laryngol. 96 (Suppl. 128):26–30, 1987.
go back to reference Javel E. Acoustic and electrical encoding of temporal information. In: Miller JM and Spelman FA (eds) Cochlear Implants. Models of the Electrically Stimulated Ear. New York, Springer-Verlag, pp. 247–295, 1990. Javel E. Acoustic and electrical encoding of temporal information. In: Miller JM and Spelman FA (eds) Cochlear Implants. Models of the Electrically Stimulated Ear. New York, Springer-Verlag, pp. 247–295, 1990.
go back to reference Javel E. Long-term adaptation in cat auditory-nerve fiber responses. J. Acoust. Soc. Am. 99:1040–1052, 1996.PubMedCrossRef Javel E. Long-term adaptation in cat auditory-nerve fiber responses. J. Acoust. Soc. Am. 99:1040–1052, 1996.PubMedCrossRef
go back to reference Javel E, Shepherd RK. Electrical stimulation of the auditory nerve. III. Response initiation sites and temporal fine structure. Hear Res. 140:45–76, 2000.PubMedCrossRef Javel E, Shepherd RK. Electrical stimulation of the auditory nerve. III. Response initiation sites and temporal fine structure. Hear Res. 140:45–76, 2000.PubMedCrossRef
go back to reference Kiang NY, Watanabe T, Thomas EC, Clark LF. Discharge Patterns of Single Fibers in the Cat's Auditory Nerve. Cambridge, MIT Press, 1965. Kiang NY, Watanabe T, Thomas EC, Clark LF. Discharge Patterns of Single Fibers in the Cat's Auditory Nerve. Cambridge, MIT Press, 1965.
go back to reference Killian MJP (1994) Excitability of the electrically stimulated auditory nerve. Doctoral thesis, Utrecht University. Killian MJP (1994) Excitability of the electrically stimulated auditory nerve. Doctoral thesis, Utrecht University.
go back to reference Liang DH, Lusted HS, White RL. The nerve–electrode interface of the cochlear implant: current spread. IEEE Trans. Biomed. Eng. 46:35–43, 1999.PubMedCrossRef Liang DH, Lusted HS, White RL. The nerve–electrode interface of the cochlear implant: current spread. IEEE Trans. Biomed. Eng. 46:35–43, 1999.PubMedCrossRef
go back to reference Liberman MC, Oliver ME. Morphometry of intracellularly labeled neurons of the auditory nerve: correlations with functional properties. J. Comp. Neurol. 223:163–176, 1984.PubMedCrossRef Liberman MC, Oliver ME. Morphometry of intracellularly labeled neurons of the auditory nerve: correlations with functional properties. J. Comp. Neurol. 223:163–176, 1984.PubMedCrossRef
go back to reference Litvak L, Delgutte B, Eddington D. Auditory nerve fiber responses to electric stimulation: modulated and unmodulated pulse trains. J. Acoust. Soc. Am. 110:368–379, 2001.PubMedCrossRef Litvak L, Delgutte B, Eddington D. Auditory nerve fiber responses to electric stimulation: modulated and unmodulated pulse trains. J. Acoust. Soc. Am. 110:368–379, 2001.PubMedCrossRef
go back to reference Litvak LM. Towards a better sound processor for cochlear implants: Auditory-nerve responses to high-rate electric pulse trains. Doctoral thesis. Cambridge, Massachusetts Institute of Technology, 2002. Litvak LM. Towards a better sound processor for cochlear implants: Auditory-nerve responses to high-rate electric pulse trains. Doctoral thesis. Cambridge, Massachusetts Institute of Technology, 2002.
go back to reference Litvak LM, Smith ZM, Delgutte B, Eddington DK. Desynchronization of electrically evoked auditory-nerve activity by high-frequency pulse trains of long duration. J. Acoust. Soc. Am. 114:2066–2078, 2003.PubMedCrossRef Litvak LM, Smith ZM, Delgutte B, Eddington DK. Desynchronization of electrically evoked auditory-nerve activity by high-frequency pulse trains of long duration. J. Acoust. Soc. Am. 114:2066–2078, 2003.PubMedCrossRef
go back to reference McNeal DR. Analysis of a model for excitation of myelinated nerve. IEEE Trans. Biomed. Eng. 23:329–337, 1976.PubMedCrossRef McNeal DR. Analysis of a model for excitation of myelinated nerve. IEEE Trans. Biomed. Eng. 23:329–337, 1976.PubMedCrossRef
go back to reference Meddis R. Simulation of mechanical to neural transduction in the auditory receptor. J. Acoust. Soc. Am. 79:702–711, 1986.PubMedCrossRef Meddis R. Simulation of mechanical to neural transduction in the auditory receptor. J. Acoust. Soc. Am. 79:702–711, 1986.PubMedCrossRef
go back to reference 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, 1999.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, 1999.PubMedCrossRef
go back to reference Miller CA, Abbas PJ, Robinson BK. Response properties of the refractory auditory nerve fiber. J. Assoc. Res. Otolaryngol. 2:216–232, 2001.PubMed Miller CA, Abbas PJ, Robinson BK. Response properties of the refractory auditory nerve fiber. J. Assoc. Res. Otolaryngol. 2:216–232, 2001.PubMed
go back to reference Miller CA, Abbas PJ, Nourski KV, Hu N, Robinson BK. Electrode configuration influences action potential initiation site and ensemble stochastic response properties. Hear Res. 175:200–214, 2003.PubMedCrossRef Miller CA, Abbas PJ, Nourski KV, Hu N, Robinson BK. Electrode configuration influences action potential initiation site and ensemble stochastic response properties. Hear Res. 175:200–214, 2003.PubMedCrossRef
go back to reference Mino H, Rubinstein JT, Miller CA, Abbas PJ. Effects of electrode-to-fiber distance on temporal neural response with electrical stimulation. IEEE Trans. Biomed. Eng. 51:13–20, 2004.PubMedCrossRef Mino H, Rubinstein JT, Miller CA, Abbas PJ. Effects of electrode-to-fiber distance on temporal neural response with electrical stimulation. IEEE Trans. Biomed. Eng. 51:13–20, 2004.PubMedCrossRef
go back to reference Nourski KV, Abbas PJ, Miller CA. Effects of Remaining Hair Cells on Cochlear Implant Function, 15th Quarterly Progress Report, NIH Contract N01-DC-2-1005, 2006. Nourski KV, Abbas PJ, Miller CA. Effects of Remaining Hair Cells on Cochlear Implant Function, 15th Quarterly Progress Report, NIH Contract N01-DC-2-1005, 2006.
go back to reference Parkins CW, Colombo J. Auditory-nerve single-neuron thresholds to electrical stimulation from scala tympani electrodes. Hear Res. 31:267–285, 1987.PubMedCrossRef Parkins CW, Colombo J. Auditory-nerve single-neuron thresholds to electrical stimulation from scala tympani electrodes. Hear Res. 31:267–285, 1987.PubMedCrossRef
go back to reference Parkins CW. Temporal response patterns of auditory nerve fibers to electrical stimulation in deafened squirrel monkeys. Hear Res. 41:137–168, 1989.PubMedCrossRef Parkins CW. Temporal response patterns of auditory nerve fibers to electrical stimulation in deafened squirrel monkeys. Hear Res. 41:137–168, 1989.PubMedCrossRef
go back to reference Rebscher SJ, Snyder RL, Leake PA. The effect of electrode configuration and duration of deafness on threshold and selectivity of responses to intracochlear electrical stimulation. J. Acoust. Soc. Am. 109:2035–2048, 2001.PubMedCrossRef Rebscher SJ, Snyder RL, Leake PA. The effect of electrode configuration and duration of deafness on threshold and selectivity of responses to intracochlear electrical stimulation. J. Acoust. Soc. Am. 109:2035–2048, 2001.PubMedCrossRef
go back to reference Relkin EM, Doucet JR. Recovery from prior stimulation. I: Relationship to spontaneous firing rates of primary auditory neurons. Hear Res. 55:215–222, 1991.PubMedCrossRef Relkin EM, Doucet JR. Recovery from prior stimulation. I: Relationship to spontaneous firing rates of primary auditory neurons. Hear Res. 55:215–222, 1991.PubMedCrossRef
go back to reference Rubinstein JT, Wilson BS, Finley CC, Abbas PJ. Pseudospontaneous activity: stochastic independence of auditory nerve fibers with electrical stimulation. Hear Res. 127:108–118, 1999.PubMedCrossRef Rubinstein JT, Wilson BS, Finley CC, Abbas PJ. Pseudospontaneous activity: stochastic independence of auditory nerve fibers with electrical stimulation. Hear Res. 127:108–118, 1999.PubMedCrossRef
go back to reference Smith RL. Short-term adaptation in single auditory nerve fibers: some poststimulatory effects. J. Neurophysiol. 40:1098–1111, 1977.PubMed Smith RL. Short-term adaptation in single auditory nerve fibers: some poststimulatory effects. J. Neurophysiol. 40:1098–1111, 1977.PubMed
go back to reference Smith RL, Brachman ML. Adaptation in auditory-nerve fibers: a revised model. Biol. Cybern. 44:107–120, 1982.PubMedCrossRef Smith RL, Brachman ML. Adaptation in auditory-nerve fibers: a revised model. Biol. Cybern. 44:107–120, 1982.PubMedCrossRef
go back to reference van den Honert C, Stypulkowski PH. Physiological properties of the electrically stimulated auditory nerve. II. Single fiber recordings. Hear Res. 14:225–243, 1984.PubMedCrossRef van den Honert C, Stypulkowski PH. Physiological properties of the electrically stimulated auditory nerve. II. Single fiber recordings. Hear Res. 14:225–243, 1984.PubMedCrossRef
go back to reference van den Honert C, Stypulkowski PH. Single fiber mapping of spatial excitation patterns in the electrically stimulated auditory nerve. Hear Res. 29:195–206, 1987a.PubMedCrossRef van den Honert C, Stypulkowski PH. Single fiber mapping of spatial excitation patterns in the electrically stimulated auditory nerve. Hear Res. 29:195–206, 1987a.PubMedCrossRef
go back to reference van den Honert C, Stypulkowski PH. Temporal response patterns of single auditory nerve fibers elicited by periodic electrical stimuli. Hear Res. 29:207–222, 1987b.PubMedCrossRef van den Honert C, Stypulkowski PH. Temporal response patterns of single auditory nerve fibers elicited by periodic electrical stimuli. Hear Res. 29:207–222, 1987b.PubMedCrossRef
go back to reference Verveen AA. Fluctuation in Excitability. Drukkerij Holland N.V., Amsterdam, 1961. Verveen AA. Fluctuation in Excitability. Drukkerij Holland N.V., Amsterdam, 1961.
go back to reference Westerman LA, Smith RL. Rapid and short-term adaptation in auditory nerve responses. Hear Res. 15:249–260, 1984.PubMedCrossRef Westerman LA, Smith RL. Rapid and short-term adaptation in auditory nerve responses. Hear Res. 15:249–260, 1984.PubMedCrossRef
go back to reference Wilson BS, Finley CC, Lawson DT, Zerbi M. Speech Processors for Auditory Prostheses. Eleventh Quarterly Progress Report. NIH Contract N01-DC-2-2401. Research Triangle Park, Research Triangle Institute, 1995. Wilson BS, Finley CC, Lawson DT, Zerbi M. Speech Processors for Auditory Prostheses. Eleventh Quarterly Progress Report. NIH Contract N01-DC-2-2401. Research Triangle Park, Research Triangle Institute, 1995.
go back to reference Zhang X, Carney LH. Analysis of models for the synapse between the inner hair cell and the auditory nerve. J. Acoust. Soc. Am. 118:1540–1553, 2005.PubMedCrossRef Zhang X, Carney LH. Analysis of models for the synapse between the inner hair cell and the auditory nerve. J. Acoust. Soc. Am. 118:1540–1553, 2005.PubMedCrossRef
Metadata
Title
Changes Across Time in Spike Rate and Spike Amplitude of Auditory Nerve Fibers Stimulated by Electric Pulse Trains
Authors
Fawen Zhang
Charles A. Miller
Barbara K. Robinson
Paul J. Abbas
Ning Hu
Publication date
01-09-2007
Publisher
Springer-Verlag
Published in
Journal of the Association for Research in Otolaryngology / Issue 3/2007
Print ISSN: 1525-3961
Electronic ISSN: 1438-7573
DOI
https://doi.org/10.1007/s10162-007-0086-7

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