Skip to main content
Top
Published in: Experimental Brain Research 3/2012

01-05-2012 | Research Article

Co-modulation of stimulus rate and current from elevated baselines expands head motion encoding range of the vestibular prosthesis

Authors: Natan S. Davidovics, Gene Y. Fridman, Charles C. Della Santina

Published in: Experimental Brain Research | Issue 3/2012

Login to get access

Abstract

An implantable prosthesis that stimulates vestibular nerve branches to restore sensation of head rotation and vision-stabilizing reflexes could benefit individuals disabled by bilateral loss of vestibular sensation. The normal vestibular system encodes head movement by increasing or decreasing firing rate of the vestibular afferents about a baseline firing rate in proportion to head rotation velocity. Our multichannel vestibular prosthesis emulates this encoding scheme by modulating pulse rate and pulse current amplitude above and below a baseline stimulation rate (BSR) and a baseline stimulation current. Unilateral baseline prosthetic stimulation that mimics normal vestibular afferent baseline firing results in vestibulo-ocular reflex (VOR) eye responses with a wider range of eye velocity in response to stimuli modulated above baseline (excitatory) than below baseline (inhibitory). Stimulus modulation about higher than normal baselines resulted in increased range of inhibitory eye velocity, but decreased range of excitatory eye velocity. Simultaneous modulation of rate and current (co-modulation) above all tested baselines elicited a significantly wider range of excitatory eye velocity than rate or current modulation alone. Time constants associated with the recovery of VOR excitability following adaptation to elevated BSRs implicate synaptic vesicle depletion as a possible mechanism for the small range of excitatory eye velocity elicited by rate modulation alone. These findings can be used toward selecting optimal baseline levels for vestibular stimulation that would result in large inhibitory eye responses while maintaining a wide range of excitatory eye velocity via co-modulation.
Literature
go back to reference Bagnall MW, McElvain L, Faulstich M, du Lac SV (2008) Frequency-independent synaptic transmission supports a linear vestibular behavior. Neuron 60:343–352PubMedCrossRef Bagnall MW, McElvain L, Faulstich M, du Lac SV (2008) Frequency-independent synaptic transmission supports a linear vestibular behavior. Neuron 60:343–352PubMedCrossRef
go back to reference Baird RA, Desmadryl G, Fernandez C, Goldberg JM (1988) The vestibular nerve of the chinchilla. 2. Relation between afferent response properties and peripheral innervation patterns in the semicircular canals. J Neurophysiol 60:182–203PubMed Baird RA, Desmadryl G, Fernandez C, Goldberg JM (1988) The vestibular nerve of the chinchilla. 2. Relation between afferent response properties and peripheral innervation patterns in the semicircular canals. J Neurophysiol 60:182–203PubMed
go back to reference BeMent SL, Ranck JB Jr (1969) A quantitative study of electrical stimulation of central myelinated fibers. Exp Neurol 24:147–170PubMedCrossRef BeMent SL, Ranck JB Jr (1969) A quantitative study of electrical stimulation of central myelinated fibers. Exp Neurol 24:147–170PubMedCrossRef
go back to reference Black FO, Wade SW, Nashner LM (1996) What is the minimal vestibular function required for compensation? Am J Otol 17:401–409PubMedCrossRef Black FO, Wade SW, Nashner LM (1996) What is the minimal vestibular function required for compensation? Am J Otol 17:401–409PubMedCrossRef
go back to reference Black FO, Gianna-Poulin C, Pesznecker SC (2001) Recovery from vestibular ototoxicity. Otol Neurotol 22:662–671PubMedCrossRef Black FO, Gianna-Poulin C, Pesznecker SC (2001) Recovery from vestibular ototoxicity. Otol Neurotol 22:662–671PubMedCrossRef
go back to reference Black FO, Pesznecker S, Stallings V (2004) Permanent gentamicin vestibulotoxicity. Otol Neurotol 25:559–569PubMedCrossRef Black FO, Pesznecker S, Stallings V (2004) Permanent gentamicin vestibulotoxicity. Otol Neurotol 25:559–569PubMedCrossRef
go back to reference Cohen B, Suzuki J, Bender MB (1964) Eye movements from semicircular canal nerve stimulation in cat. Ann Otol Rhinol Laryngol 73:153PubMed Cohen B, Suzuki J, Bender MB (1964) Eye movements from semicircular canal nerve stimulation in cat. Ann Otol Rhinol Laryngol 73:153PubMed
go back to reference Curthoys IS, Halmagyi GM (1995) Vestibular compensation: a review of the oculomotor, neural, and clinical consequences of unilateral vestibular loss. J Vestib Res 5:67–107PubMedCrossRef Curthoys IS, Halmagyi GM (1995) Vestibular compensation: a review of the oculomotor, neural, and clinical consequences of unilateral vestibular loss. J Vestib Res 5:67–107PubMedCrossRef
go back to reference Dai C, Fridman GY, Chiang B, Davidovics NS, Melvin T, Cullen KE, Della Santina CC (2011) Cross-axis adaptation improves 3D vestibulo-ocular reflex alignment during chronic stimulation via a head-mounted multichannel vestibular prosthesis. Exp Brain Res 210:595–606PubMedCrossRef Dai C, Fridman GY, Chiang B, Davidovics NS, Melvin T, Cullen KE, Della Santina CC (2011) Cross-axis adaptation improves 3D vestibulo-ocular reflex alignment during chronic stimulation via a head-mounted multichannel vestibular prosthesis. Exp Brain Res 210:595–606PubMedCrossRef
go back to reference Davidovics NS, Fridman GY, Chiang B, Della Santina CC (2011) Effects of biphasic current pulse frequency, amplitude, duration, and interphase gap on eye movement responses to prosthetic electrical stimulation of the vestibular nerve. IEEE Trans Neural Syst Rehabil Eng 19:84–94PubMedCrossRef Davidovics NS, Fridman GY, Chiang B, Della Santina CC (2011) Effects of biphasic current pulse frequency, amplitude, duration, and interphase gap on eye movement responses to prosthetic electrical stimulation of the vestibular nerve. IEEE Trans Neural Syst Rehabil Eng 19:84–94PubMedCrossRef
go back to reference Della Santina C, Migliaccio A, Patel A (2005) Electrical stimulation to restore vestibular function development of a 3-d vestibular prosthesis. Conf Proc IEEE Eng Med Biol Soc 7:7380–7385PubMed Della Santina C, Migliaccio A, Patel A (2005) Electrical stimulation to restore vestibular function development of a 3-d vestibular prosthesis. Conf Proc IEEE Eng Med Biol Soc 7:7380–7385PubMed
go back to reference Della Santina CC, Migliaccio AA, Patel AH (2007) A multichannel semicircular canal neural prosthesis using electrical stimulation to restore 3-D vestibular sensation. IEEE Trans Biomed Eng 54:1016–1030PubMedCrossRef Della Santina CC, Migliaccio AA, Patel AH (2007) A multichannel semicircular canal neural prosthesis using electrical stimulation to restore 3-D vestibular sensation. IEEE Trans Biomed Eng 54:1016–1030PubMedCrossRef
go back to reference Fridman G, Davidovics N, Dai C, Migliaccio A, Della Santina C (2010a) Vestibulo-ocular reflex responses to a multichannel vestibular prosthesis incorporating a 3D coordinate transformation for correction of misalignment. J Assoc Res Otolaryngol 11:367–381PubMedCrossRef Fridman G, Davidovics N, Dai C, Migliaccio A, Della Santina C (2010a) Vestibulo-ocular reflex responses to a multichannel vestibular prosthesis incorporating a 3D coordinate transformation for correction of misalignment. J Assoc Res Otolaryngol 11:367–381PubMedCrossRef
go back to reference Fridman GY, Blair HT, Blaisdell AP, Judy JW (2010b) A quantitative model for the perceived intensity of cortical electrical stimulation. Exp Brain Res 203:499–515PubMedCrossRef Fridman GY, Blair HT, Blaisdell AP, Judy JW (2010b) A quantitative model for the perceived intensity of cortical electrical stimulation. Exp Brain Res 203:499–515PubMedCrossRef
go back to reference Gong WS, Merfeld DM (2000) Prototype neural semicircular canal prosthesis using patterned electrical stimulation. Ann Biomed Eng 28:572–581PubMedCrossRef Gong WS, Merfeld DM (2000) Prototype neural semicircular canal prosthesis using patterned electrical stimulation. Ann Biomed Eng 28:572–581PubMedCrossRef
go back to reference Gong WS, Merfeld DM (2002) System design and performance of a unilateral horizontal semicircular canal prosthesis. IEEE Trans Biomed Eng 49:175–181PubMedCrossRef Gong WS, Merfeld DM (2002) System design and performance of a unilateral horizontal semicircular canal prosthesis. IEEE Trans Biomed Eng 49:175–181PubMedCrossRef
go back to reference Gong WS, Haburcakova C, Merfeld DM (2008) Vestibulo-ocular responses evoked via bilateral electrical stimulation of the lateral semicircular canals. IEEE Trans Biomed Eng 55:2608–2619PubMedCrossRef Gong WS, Haburcakova C, Merfeld DM (2008) Vestibulo-ocular responses evoked via bilateral electrical stimulation of the lateral semicircular canals. IEEE Trans Biomed Eng 55:2608–2619PubMedCrossRef
go back to reference Grossman GE, Leigh RJ, Abel LA, Lanska DJ, Thurston SE (1988) Frequency and velocity of rotational head perturbations during locomotion. Exp Brain Res 70:470–476PubMedCrossRef Grossman GE, Leigh RJ, Abel LA, Lanska DJ, Thurston SE (1988) Frequency and velocity of rotational head perturbations during locomotion. Exp Brain Res 70:470–476PubMedCrossRef
go back to reference Hirvonen TP, Minor LB, Hullar TE, Carey JP (2005) Effects of intratympanic gentamicin on vestibular afferents and hair cells in the chinchilla. J Neurophysiol 93:643–655PubMedCrossRef Hirvonen TP, Minor LB, Hullar TE, Carey JP (2005) Effects of intratympanic gentamicin on vestibular afferents and hair cells in the chinchilla. J Neurophysiol 93:643–655PubMedCrossRef
go back to reference Kesar T, Chou L-W, Binder-Macleod SA (2008) Effects of stimulation frequency versus pulse duration modulation on muscle fatigue. J Electromyogr Kinesiol 18:662–671PubMedCrossRef Kesar T, Chou L-W, Binder-Macleod SA (2008) Effects of stimulation frequency versus pulse duration modulation on muscle fatigue. J Electromyogr Kinesiol 18:662–671PubMedCrossRef
go back to reference Lewis RF, Merfeld DM, Gong WS (2001) Cross-axis vestibular adaptation produced by patterned electrical stimulation. Neurology 56:A18 Lewis RF, Merfeld DM, Gong WS (2001) Cross-axis vestibular adaptation produced by patterned electrical stimulation. Neurology 56:A18
go back to reference Lewis RF, Gong WS, Ramsey M, Minor L, Boyle R, Merfeld DM (2002) Vestibular adaptation studied with a prosthetic semicircular canal. J Vestib Res Equilib Orientat 12:87–94 Lewis RF, Gong WS, Ramsey M, Minor L, Boyle R, Merfeld DM (2002) Vestibular adaptation studied with a prosthetic semicircular canal. J Vestib Res Equilib Orientat 12:87–94
go back to reference Lewis R, Haburcakova C, Gong W, Makary C, Merfeld D (2010) Vestibuloocular reflex adaptation investigated with chronic motion-modulated electrical stimulation of semicircular canal afferents. J Neurophysiol 103:1066–1079PubMedCrossRef Lewis R, Haburcakova C, Gong W, Makary C, Merfeld D (2010) Vestibuloocular reflex adaptation investigated with chronic motion-modulated electrical stimulation of semicircular canal afferents. J Neurophysiol 103:1066–1079PubMedCrossRef
go back to reference Mamoto Y, Yamamoto K, Imai T, Tamura M, Kubo T (2002) Three-dimensional analysis of human locomotion in normal subjects and patients with vestibular deficiency. Acta Otolaryngol 122:495–500PubMedCrossRef Mamoto Y, Yamamoto K, Imai T, Tamura M, Kubo T (2002) Three-dimensional analysis of human locomotion in normal subjects and patients with vestibular deficiency. Acta Otolaryngol 122:495–500PubMedCrossRef
go back to reference Merfeld DM, Gong WS, Morrissey J, Saginaw M, Haburcakova C, Lewis RF (2006) Acclimation to chronic constant-rate peripheral stimulation provided by a vestibular prosthesis. IEEE Trans Biomed Eng 53:2362–2372PubMedCrossRef Merfeld DM, Gong WS, Morrissey J, Saginaw M, Haburcakova C, Lewis RF (2006) Acclimation to chronic constant-rate peripheral stimulation provided by a vestibular prosthesis. IEEE Trans Biomed Eng 53:2362–2372PubMedCrossRef
go back to reference Merfeld DM, Haburcakova C, Gong W, Lewis RF (2007) Chronic vestibulo-ocular reflexes evoked by a vestibular prosthesis. IEEE Trans Biomed Eng 54:1005–1015PubMedCrossRef Merfeld DM, Haburcakova C, Gong W, Lewis RF (2007) Chronic vestibulo-ocular reflexes evoked by a vestibular prosthesis. IEEE Trans Biomed Eng 54:1005–1015PubMedCrossRef
go back to reference Migliaccio AA, Della Santina CC, Carey JP, Niparko JK, Minor LB (2005) The vestibulo-ocular reflex response to head impulses rarely decreases after cochlear implantation. Otol Neurotol 26:655–660PubMedCrossRef Migliaccio AA, Della Santina CC, Carey JP, Niparko JK, Minor LB (2005) The vestibulo-ocular reflex response to head impulses rarely decreases after cochlear implantation. Otol Neurotol 26:655–660PubMedCrossRef
go back to reference Minor LB (1998) Gentamicin-induced bilateral vestibular hypofunction. Jama-J Am Med Assoc 279:541–544CrossRef Minor LB (1998) Gentamicin-induced bilateral vestibular hypofunction. Jama-J Am Med Assoc 279:541–544CrossRef
go back to reference Rinne T, Bronstein AM, Rudge P, Gresty MA, Luxon LM (1998) Bilateral loss of vestibular function: clinical findings in 53 patients. J Neurol 245:314–321PubMedCrossRef Rinne T, Bronstein AM, Rudge P, Gresty MA, Luxon LM (1998) Bilateral loss of vestibular function: clinical findings in 53 patients. J Neurol 245:314–321PubMedCrossRef
go back to reference Suzuki JI, Cohen B (1964) Head eye body and limb movements from semicircular canal nerves. Exp Neurol 10:393–405PubMedCrossRef Suzuki JI, Cohen B (1964) Head eye body and limb movements from semicircular canal nerves. Exp Neurol 10:393–405PubMedCrossRef
go back to reference Suzuki J, Cohen B, Bender MB (1964) Compensatory eye movements induced by vertical semicircular canal stimulation. Exp Neurol 9:137–160PubMedCrossRef Suzuki J, Cohen B, Bender MB (1964) Compensatory eye movements induced by vertical semicircular canal stimulation. Exp Neurol 9:137–160PubMedCrossRef
go back to reference Suzuki JI, Goto K, Tokumasu K, Cohen B (1969) Implantation of electrodes near individual vestibular nerve branches in mammals. Ann Otol Rhinol Laryngol 78:815–826PubMed Suzuki JI, Goto K, Tokumasu K, Cohen B (1969) Implantation of electrodes near individual vestibular nerve branches in mammals. Ann Otol Rhinol Laryngol 78:815–826PubMed
go back to reference Telgkamp PRI (2002) Depression of inhibitory synaptic transmission between Purkinje cells and neurons of the cerebellar nuclei. J Neurosci 22:8447–8457PubMed Telgkamp PRI (2002) Depression of inhibitory synaptic transmission between Purkinje cells and neurons of the cerebellar nuclei. J Neurosci 22:8447–8457PubMed
Metadata
Title
Co-modulation of stimulus rate and current from elevated baselines expands head motion encoding range of the vestibular prosthesis
Authors
Natan S. Davidovics
Gene Y. Fridman
Charles C. Della Santina
Publication date
01-05-2012
Publisher
Springer-Verlag
Published in
Experimental Brain Research / Issue 3/2012
Print ISSN: 0014-4819
Electronic ISSN: 1432-1106
DOI
https://doi.org/10.1007/s00221-012-3025-8

Other articles of this Issue 3/2012

Experimental Brain Research 3/2012 Go to the issue