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Published in: Journal of Neurology 1/2020

01-12-2020 | Bilateral Vestibulopathy | Original Communication

Simultaneous activation of multiple vestibular pathways upon electrical stimulation of semicircular canal afferents

Authors: Anissa Boutabla, Samuel Cavuscens, Maurizio Ranieri, Céline Crétallaz, Herman Kingma, Raymond van de Berg, Nils Guinand, Angélica Pérez Fornos

Published in: Journal of Neurology | Special Issue 1/2020

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Abstract

Background and purpose

Vestibular implants seem to be a promising treatment for patients suffering from severe bilateral vestibulopathy. To optimize outcomes, we need to investigate how, and to which extent, the different vestibular pathways are activated. Here we characterized the simultaneous responses to electrical stimuli of three different vestibular pathways.

Methods

Three vestibular implant recipients were included. First, activation thresholds and amplitude growth functions of electrically evoked vestibulo-ocular reflexes (eVOR), cervical myogenic potentials (ecVEMPs) and vestibular percepts (vestibulo-thalamo-cortical, VTC) were recorded upon stimulation with single, biphasic current pulses (200 µs/phase) delivered through five different vestibular electrodes. Latencies of eVOR and ecVEMPs were also characterized. Then we compared the amplitude growth functions of the three pathways using different stimulation profiles (1-pulse, 200 µs/phase; 1-pulse, 50 µs/phase; 4-pulses, 50 µs/phase, 1600 pulses-per-second) in one patient (two electrodes).

Results

The median latencies of the eVOR and ecVEMPs were 8 ms (8–9 ms) and 10.2 ms (9.6–11.8 ms), respectively. While the amplitude of eVOR and ecVEMP responses increased with increasing stimulation current, the VTC pathway showed a different, step-like behavior. In this study, the 200 µs/phase paradigm appeared to give the best balance to enhance responses at lower stimulation currents.

Conclusions

This study is a first attempt to evaluate the simultaneous activation of different vestibular pathways. However, this issue deserves further and more detailed investigation to determine the actual possibility of selective stimulation of a given pathway, as well as the functional impact of the contribution of each pathway to the overall rehabilitation process.
Literature
1.
go back to reference Ward BK, Agrawal Y, Hoffman HJ, Carey JP (2013) Prevalence and impact of Bilateral Vestibular Deficiency (BVD): results from the 2008 United States National Health Interview Survey. JAMA Otolaryngol Head Neck Surg 139(August 1):803–810PubMedPubMedCentralCrossRef Ward BK, Agrawal Y, Hoffman HJ, Carey JP (2013) Prevalence and impact of Bilateral Vestibular Deficiency (BVD): results from the 2008 United States National Health Interview Survey. JAMA Otolaryngol Head Neck Surg 139(August 1):803–810PubMedPubMedCentralCrossRef
2.
go back to reference Guinand N, Boselie F, Guyot JP, Kingma H (2012) Quality of life of patients with bilateral vestibulopathy. Ann Otol Rhinol Laryngol 121(7):471–477PubMedCrossRef Guinand N, Boselie F, Guyot JP, Kingma H (2012) Quality of life of patients with bilateral vestibulopathy. Ann Otol Rhinol Laryngol 121(7):471–477PubMedCrossRef
3.
go back to reference Krebs DE, Gill-Body KM, Parker SW, Ramirez JV, Wernick-Robinson M (2003) Vestibular rehabilitation: useful but not universally so. Otolaryngol Head Neck Surg 128(2):240–250PubMedCrossRef Krebs DE, Gill-Body KM, Parker SW, Ramirez JV, Wernick-Robinson M (2003) Vestibular rehabilitation: useful but not universally so. Otolaryngol Head Neck Surg 128(2):240–250PubMedCrossRef
4.
go back to reference Zingler VC et al (2008) Follow-up of vestibular function in bilateral vestibulopathy. J Neurol Neurosurg Psychiatry 79(3):284–288PubMedCrossRef Zingler VC et al (2008) Follow-up of vestibular function in bilateral vestibulopathy. J Neurol Neurosurg Psychiatry 79(3):284–288PubMedCrossRef
5.
go back to reference Guyot JP, Perez Fornos A (2019) Milestones in the development of a vestibular implant. Curr Opin Neurol 32(1):145–153PubMedCrossRef Guyot JP, Perez Fornos A (2019) Milestones in the development of a vestibular implant. Curr Opin Neurol 32(1):145–153PubMedCrossRef
6.
go back to reference Merfeld DM, Lewis RF (2012) Replacing semicircular canal function with a vestibular implant. Curr Opin Otolaryngol Head Neck Surg 20(5):386–392PubMedCrossRef Merfeld DM, Lewis RF (2012) Replacing semicircular canal function with a vestibular implant. Curr Opin Otolaryngol Head Neck Surg 20(5):386–392PubMedCrossRef
7.
go back to reference Guinand N et al (2015) Vestibular implants: 8 years of experience with electrical stimulation of the vestibular nerve in 11 patients with bilateral vestibular loss. Orl 77:227–240PubMedCrossRef Guinand N et al (2015) Vestibular implants: 8 years of experience with electrical stimulation of the vestibular nerve in 11 patients with bilateral vestibular loss. Orl 77:227–240PubMedCrossRef
8.
go back to reference Cohen B, Suzuki J-I (1963) Eye movements induced by ampullary nerve stimulation’ difficult because of its position in the temporal. Am J Physiol 204(2):347–351PubMedCrossRef Cohen B, Suzuki J-I (1963) Eye movements induced by ampullary nerve stimulation’ difficult because of its position in the temporal. Am J Physiol 204(2):347–351PubMedCrossRef
9.
go back to reference Suzuki JI, Cohen B (1964) Head, eye, body and limb movements from semicircular canal nerves. Exp Neurol 10(5):393–405PubMedCrossRef Suzuki JI, Cohen B (1964) Head, eye, body and limb movements from semicircular canal nerves. Exp Neurol 10(5):393–405PubMedCrossRef
10.
go back to reference Sierra H, Cordova M, Chen CSJ, Rajadhyaksha M (2015) Confocal imaging-guided laser ablation of basal cell carcinomas: an ex vivo study. J Invest Dermatol 135(2):612–615PubMedCrossRef Sierra H, Cordova M, Chen CSJ, Rajadhyaksha M (2015) Confocal imaging-guided laser ablation of basal cell carcinomas: an ex vivo study. J Invest Dermatol 135(2):612–615PubMedCrossRef
11.
go back to reference Davidovics NS, Fridman GY, Della Santina CC (2012) Co-modulation of stimulus rate and current from elevated baselines expands head motion encoding range of the vestibular prosthesis. Exp Brain Res 218(3):389–400PubMedCrossRef Davidovics NS, Fridman GY, Della Santina CC (2012) Co-modulation of stimulus rate and current from elevated baselines expands head motion encoding range of the vestibular prosthesis. Exp Brain Res 218(3):389–400PubMedCrossRef
12.
go back to reference Dai C et al (2013) Directional plasticity rapidly improves 3D vestibulo-ocular reflex alignment in monkeys using a multichannel vestibular prosthesis. JARO J Assoc Res Otolaryngol 14(6):863–877PubMedCrossRef Dai C et al (2013) Directional plasticity rapidly improves 3D vestibulo-ocular reflex alignment in monkeys using a multichannel vestibular prosthesis. JARO J Assoc Res Otolaryngol 14(6):863–877PubMedCrossRef
13.
go back to reference Davidovics NS, Rahman MA, Dai C, Ahn J, Fridman GY, Della Santina CC (2013) Multichannel vestibular prosthesis employing modulation of pulse rate and current with alignment precompensation elicits improved vor performance in monkeys. JARO J Assoc Res Otolaryngol 14(2):233–248PubMedCrossRef Davidovics NS, Rahman MA, Dai C, Ahn J, Fridman GY, Della Santina CC (2013) Multichannel vestibular prosthesis employing modulation of pulse rate and current with alignment precompensation elicits improved vor performance in monkeys. JARO J Assoc Res Otolaryngol 14(2):233–248PubMedCrossRef
14.
go back to reference Lewis RF, Haburcakova C, Gong W, Makary C, Merfeld DM (2010) Vestibuloocular reflex adaptation investigated with chronic motion-modulated electrical stimulation of semicircular canal afferents. J Neurophysiol 103(2):1066–1079PubMedCrossRef Lewis RF, Haburcakova C, Gong W, Makary C, Merfeld DM (2010) Vestibuloocular reflex adaptation investigated with chronic motion-modulated electrical stimulation of semicircular canal afferents. J Neurophysiol 103(2):1066–1079PubMedCrossRef
15.
go back to reference Mitchell DE, Della Santina CC, Cullen KE (2016) Plasticity within non-cerebellar pathways rapidly shapes motor performance in vivo. Nat Commun 7(May):1–13 Mitchell DE, Della Santina CC, Cullen KE (2016) Plasticity within non-cerebellar pathways rapidly shapes motor performance in vivo. Nat Commun 7(May):1–13
16.
go back to reference Mitchell DE, Dai C, Rahman MA, Ahn JH, Della Santina CC, Cullen KE (2013) Head movements evoked in alert rhesus monkey by vestibular prosthesis stimulation: implications for postural and gaze stabilization. PLoS ONE 8(10):1–12 Mitchell DE, Dai C, Rahman MA, Ahn JH, Della Santina CC, Cullen KE (2013) Head movements evoked in alert rhesus monkey by vestibular prosthesis stimulation: implications for postural and gaze stabilization. PLoS ONE 8(10):1–12
17.
go back to reference Macias AR, De Miguel AR, Montesdeoca IR, Barreiro SB, González JCF (2020) Chronic electrical stimulation of the otolith organ: preliminary results in humans with bilateral vestibulopathy and sensorineural hearing loss. Audiol Neurotol 25(1–2):79–90 Macias AR, De Miguel AR, Montesdeoca IR, Barreiro SB, González JCF (2020) Chronic electrical stimulation of the otolith organ: preliminary results in humans with bilateral vestibulopathy and sensorineural hearing loss. Audiol Neurotol 25(1–2):79–90
18.
go back to reference Hageman KN et al (2020) Binocular 3D otolith-ocular reflexes: responses of chinchillas to prosthetic electrical stimulation targeting the utricle and saccule. J Neurophysiol 123(1):259–276PubMedCrossRef Hageman KN et al (2020) Binocular 3D otolith-ocular reflexes: responses of chinchillas to prosthetic electrical stimulation targeting the utricle and saccule. J Neurophysiol 123(1):259–276PubMedCrossRef
19.
go back to reference Della Santina CC, Migliaccio AA, Patel AH (2007) A multi-channel semicircular canal neural prosthesis using electrical stimulation to restore 3D vestibular sensation. IEEE Trans Biomed Eng 54(6):1016–1030PubMedPubMedCentralCrossRef Della Santina CC, Migliaccio AA, Patel AH (2007) A multi-channel semicircular canal neural prosthesis using electrical stimulation to restore 3D vestibular sensation. IEEE Trans Biomed Eng 54(6):1016–1030PubMedPubMedCentralCrossRef
20.
go back to reference van de Berg R, Guinand N, Guyot JP, Kingma H, Stokroos RJ (2012) The modified ampullar approach for vestibular implant surgery: Feasibility and its first application in a human with a long-term vestibular loss. Front Neurol FEB(February):1–7 van de Berg R, Guinand N, Guyot JP, Kingma H, Stokroos RJ (2012) The modified ampullar approach for vestibular implant surgery: Feasibility and its first application in a human with a long-term vestibular loss. Front Neurol FEB(February):1–7
21.
go back to reference van de Berg R et al (2017) The vestibular implant: hearing preservation during intralabyrinthine electrode insertion—a case report. Front Neurol 8(APR):1–7 van de Berg R et al (2017) The vestibular implant: hearing preservation during intralabyrinthine electrode insertion—a case report. Front Neurol 8(APR):1–7
22.
go back to reference Stultiens JJA, Postma AA, Guinand N, Pérez Fornos A, Kingma H, van de Berg R (2020) Vestibular implantation and the feasibility of fluoroscopy-guided electrode insertion. Otolaryngol Clin North Am 53(1):115–126PubMedCrossRef Stultiens JJA, Postma AA, Guinand N, Pérez Fornos A, Kingma H, van de Berg R (2020) Vestibular implantation and the feasibility of fluoroscopy-guided electrode insertion. Otolaryngol Clin North Am 53(1):115–126PubMedCrossRef
23.
go back to reference Kos MI, Feigl G, Anderhuber F, Wall C, Fasel JHD, Guyot JP (2006) Transcanal approach to the singular nerve. Otol Neurotol 27(4):542–546PubMedCrossRef Kos MI, Feigl G, Anderhuber F, Wall C, Fasel JHD, Guyot JP (2006) Transcanal approach to the singular nerve. Otol Neurotol 27(4):542–546PubMedCrossRef
24.
go back to reference Fornos AP et al (2014) Artificial balance: restoration of the vestibulo-ocular reflex in humans with a prototype vestibular neuroprosthesis. Front Neurol 5APR(April):1–11 Fornos AP et al (2014) Artificial balance: restoration of the vestibulo-ocular reflex in humans with a prototype vestibular neuroprosthesis. Front Neurol 5APR(April):1–11
25.
go back to reference Fornos AP et al (2019) Cervical myogenic potentials and controlled postural responses elicited by a prototype vestibular implant. J Neurol 266(1):33–41PubMedPubMedCentralCrossRef Fornos AP et al (2019) Cervical myogenic potentials and controlled postural responses elicited by a prototype vestibular implant. J Neurol 266(1):33–41PubMedPubMedCentralCrossRef
27.
go back to reference Boutros PJ et al (2019) Continuous vestibular implant stimulation partially restores eye-stabilizing reflexes. JCI Insight 4(22):1–19CrossRef Boutros PJ et al (2019) Continuous vestibular implant stimulation partially restores eye-stabilizing reflexes. JCI Insight 4(22):1–19CrossRef
28.
go back to reference van de Berg R et al (2015) The vestibular implant: frequency-dependency of the electrically evoked vestibulo-ocular reflex in humans. Front Syst Neurosci 8(JAN):1–12 van de Berg R et al (2015) The vestibular implant: frequency-dependency of the electrically evoked vestibulo-ocular reflex in humans. Front Syst Neurosci 8(JAN):1–12
29.
go back to reference Guinand N et al (2016) Restoring visual acuity in dynamic conditions with a vestibular implant. Front Neurosci 10(DEC):1–6 Guinand N et al (2016) Restoring visual acuity in dynamic conditions with a vestibular implant. Front Neurosci 10(DEC):1–6
30.
go back to reference Phillips C et al (2013) Postural responses to electrical stimulation of the vestibular end organs in human subjects. Exp Brain Res 229(2):181–195PubMedCrossRef Phillips C et al (2013) Postural responses to electrical stimulation of the vestibular end organs in human subjects. Exp Brain Res 229(2):181–195PubMedCrossRef
31.
go back to reference Fornos AP et al (2019) Cervical myogenic potentials and controlled postural responses elicited by a prototype vestibular implant. J Neurol 266(s1):33–41PubMedPubMedCentralCrossRef Fornos AP et al (2019) Cervical myogenic potentials and controlled postural responses elicited by a prototype vestibular implant. J Neurol 266(s1):33–41PubMedPubMedCentralCrossRef
32.
go back to reference Rubinstein JT, Ling L, Nowack A, Nie K, Phillips JO (2020) Results from a second-generation vestibular implant in human subjects. Otol Neurotol 41(1):68–77PubMedCrossRef Rubinstein JT, Ling L, Nowack A, Nie K, Phillips JO (2020) Results from a second-generation vestibular implant in human subjects. Otol Neurotol 41(1):68–77PubMedCrossRef
33.
go back to reference Straka H, Dieringer N (2004) Basic organization principles of the VOR: lessons from frogs. Prog Neurobiol 73(4):259–309PubMedCrossRef Straka H, Dieringer N (2004) Basic organization principles of the VOR: lessons from frogs. Prog Neurobiol 73(4):259–309PubMedCrossRef
34.
go back to reference Cullen KE (2016) Physiology of central pathways, 1st edn. In: Handbook of Clinical Neurology, vol 137, Elsevier B.V. Cullen KE (2016) Physiology of central pathways, 1st edn. In: Handbook of Clinical Neurology, vol 137, Elsevier B.V.
35.
go back to reference Goldberg J, Peterson BW (1986) Reflex and mechanical contributions to head stabilization in alert cats. J Neurophysiol 56(3):857–875PubMedCrossRef Goldberg J, Peterson BW (1986) Reflex and mechanical contributions to head stabilization in alert cats. J Neurophysiol 56(3):857–875PubMedCrossRef
36.
go back to reference Ezure K, Sasaki S (1978) Frequency-response analysis of vestibular-induced neck reflex in cat. I. Characteristics of neural transmission from horizontal semicircular canal to neck motoneurons. J Neurophysiol 41(2):445–458PubMedCrossRef Ezure K, Sasaki S (1978) Frequency-response analysis of vestibular-induced neck reflex in cat. I. Characteristics of neural transmission from horizontal semicircular canal to neck motoneurons. J Neurophysiol 41(2):445–458PubMedCrossRef
37.
go back to reference Crétallaz C et al (2020) Influence of systematic variations of the stimulation profile on responses evoked with a vestibular implant prototype in humans. J Neural Eng 17:1–14CrossRef Crétallaz C et al (2020) Influence of systematic variations of the stimulation profile on responses evoked with a vestibular implant prototype in humans. J Neural Eng 17:1–14CrossRef
38.
go back to reference Feigl GC et al (2009) Superior vestibular neurectomy: a novel transmeatal approach for a denervation of the superior and lateral semicircular canals. Otol Neurotol 30(5):586–591PubMedCrossRef Feigl GC et al (2009) Superior vestibular neurectomy: a novel transmeatal approach for a denervation of the superior and lateral semicircular canals. Otol Neurotol 30(5):586–591PubMedCrossRef
39.
go back to reference Huterer M, Cullen KE (2002) Vestibuloocular reflex dynamics during high-frequency and high-acceleration rotations of the head on body in Rhesus monkey. J Neurophysiol 88(1):13–28PubMedCrossRef Huterer M, Cullen KE (2002) Vestibuloocular reflex dynamics during high-frequency and high-acceleration rotations of the head on body in Rhesus monkey. J Neurophysiol 88(1):13–28PubMedCrossRef
40.
go back to reference Collewijn H, Smeets JBJ (2000) Early components of the human vestibulo-ocular response to head rotation: latency and gain. J Neurophysiol 84(1):376–389PubMedCrossRef Collewijn H, Smeets JBJ (2000) Early components of the human vestibulo-ocular response to head rotation: latency and gain. J Neurophysiol 84(1):376–389PubMedCrossRef
41.
go back to reference Watson SRD, Colebatch JG (1998) Vestibular-evoked electromyographic responses in soleus: a comparison between click and galvanic stimulation. Exp Brain Res 119(4):504–510PubMedCrossRef Watson SRD, Colebatch JG (1998) Vestibular-evoked electromyographic responses in soleus: a comparison between click and galvanic stimulation. Exp Brain Res 119(4):504–510PubMedCrossRef
43.
go back to reference Baird RA, Desmadryl G, Fernandez C (1988) The vestibular nerve of the chinchilla. II. Relation between afferent response properties and peripheral innervation patterns in the semicircular canals. J Neurophysiol 60(1):182–203PubMedCrossRef Baird RA, Desmadryl G, Fernandez C (1988) The vestibular nerve of the chinchilla. II. Relation between afferent response properties and peripheral innervation patterns in the semicircular canals. J Neurophysiol 60(1):182–203PubMedCrossRef
45.
go back to reference Goldberg JM, Lysakowski A, Fernández C (1990) Morphophysiological and ultrastructural studies in the mammalian cristae ampullares. 49:89–102 Goldberg JM, Lysakowski A, Fernández C (1990) Morphophysiological and ultrastructural studies in the mammalian cristae ampullares. 49:89–102
46.
go back to reference Boyle R, Goldberg JM, Highstein SM (1992) Inputs from regularly and irregularly discharging vestibular nerve afferents to secondary neurons in squirrel monkey vestibular nuclei. III. Correlation with vestibulospinal and vestibuloocular output pathways. J Neurophysiol 68(2):471–484PubMedCrossRef Boyle R, Goldberg JM, Highstein SM (1992) Inputs from regularly and irregularly discharging vestibular nerve afferents to secondary neurons in squirrel monkey vestibular nuclei. III. Correlation with vestibulospinal and vestibuloocular output pathways. J Neurophysiol 68(2):471–484PubMedCrossRef
48.
go back to reference De Fabrizio Gabbiani SJC (2010) Mathematics for neuroscientists, 2nd edn. REFRACTORY PERIOD, Academic Press, p 15.2 De Fabrizio Gabbiani SJC (2010) Mathematics for neuroscientists, 2nd edn. REFRACTORY PERIOD, Academic Press, p 15.2
Metadata
Title
Simultaneous activation of multiple vestibular pathways upon electrical stimulation of semicircular canal afferents
Authors
Anissa Boutabla
Samuel Cavuscens
Maurizio Ranieri
Céline Crétallaz
Herman Kingma
Raymond van de Berg
Nils Guinand
Angélica Pérez Fornos
Publication date
01-12-2020
Publisher
Springer Berlin Heidelberg
Published in
Journal of Neurology / Issue Special Issue 1/2020
Print ISSN: 0340-5354
Electronic ISSN: 1432-1459
DOI
https://doi.org/10.1007/s00415-020-10120-1

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