Skip to main content
Top
Published in: Journal of Neurology 1/2019

Open Access 01-09-2019 | Bilateral Vestibulopathy | Orginial Communication

Cervical myogenic potentials and controlled postural responses elicited by a prototype vestibular implant

Authors: Angelica Perez Fornos, Raymond van de Berg, Stéphane Armand, Samuel Cavuscens, Maurizio Ranieri, Céline Crétallaz, Herman Kingma, Jean-Philippe Guyot, Nils Guinand

Published in: Journal of Neurology | Special Issue 1/2019

Login to get access

Abstract

Gaze stabilization and postural control are two key functions of the vestibular system. In consequence, oscillopsia and chronic imbalance are the two main complaints of patients presenting with a severe bilateral vestibular function loss. The vestibular implant is emerging as a promising treatment for this group of patients whose quality of life is significantly impaired. Although the final aim of the vestibular implant should be to restore vestibular function as a whole, until now the research has focused mainly on the restoration of the vestibulo-ocular reflex to improve gaze stabilization. In this study, we aimed to explore whether the vestibulo-collic and vestibulo-spinal pathways could be activated and controlled with the electrical stimuli provided by our vestibular implant prototype. This was first explored and demonstrated with recordings of electrically elicited cervical vestibular evoked myogenic potentials (ecVEMPs). ecVEMPs with characteristics similar to the classical acoustically elicited cervical vestibular evoked myogenic potentials (cVEMPs) were successfully evoked in five out of the eight tested patients. Amplitudes of the electrically elicited N–P complex varied, ranging from 44 to 120 µV. Mean latencies of the N and P waves were of 9.71(± 1.17) ms and 17.24 ms (± 1.74), respectively. We also evaluated the possibility of generating controlled postural responses using a stepping test. Here, we showed that controlled and consistent whole-body postural responses can be effectively obtained with rapid changes in the “baseline” (constant rate and amplitude) electrical activity delivered by the vestibular implant in two out of the three tested subjects. Furthermore, obtained amplitude of body rotations was significantly correlated with the intensity of stimulation and direction of body rotations correlated with the side of the delivered stimulus (implanted side). Altogether, these data suggest that the vestibular implant could also be used to improve postural control in patients with bilateral vestibulopathy.
Literature
1.
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):e78767CrossRef 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):e78767CrossRef
2.
go back to reference Goldberg JM, Cullen KE (2011) Vestibular control of the head: possible functions of the vestibulocollic reflex. Exp Brain Res 210(3–4):331–345CrossRef Goldberg JM, Cullen KE (2011) Vestibular control of the head: possible functions of the vestibulocollic reflex. Exp Brain Res 210(3–4):331–345CrossRef
3.
go back to reference Zingler VC, Weintz E, Jahn K, Mike A, Huppert D, Rettinger N et al (2008) Follow-up of vestibular function in bilateral vestibulopathy. J Neurol Neurosurg Psychiatry 79(3):284–288CrossRef Zingler VC, Weintz E, Jahn K, Mike A, Huppert D, Rettinger N et al (2008) Follow-up of vestibular function in bilateral vestibulopathy. J Neurol Neurosurg Psychiatry 79(3):284–288CrossRef
4.
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):471–477CrossRef Guinand N, Boselie F, Guyot JP, Kingma H (2012) Quality of life of patients with bilateral vestibulopathy. Ann Otol Rhinol Laryngol 121(7):471–477CrossRef
5.
go back to reference Sun D, Ward BK, Semenov Y, Carey J, Della Santina CC (2014) Bilateral vestibular deficiency: quality of life and economic implications. JAMA Otolaryngol Head Neck Surg 140(6):527–534CrossRef Sun D, Ward BK, Semenov Y, Carey J, Della Santina CC (2014) Bilateral vestibular deficiency: quality of life and economic implications. JAMA Otolaryngol Head Neck Surg 140(6):527–534CrossRef
6.
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):240–250CrossRef 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):240–250CrossRef
7.
go back to reference Herdman SJ, Hall CD, Schubert MC, Das VE, Tusa RJ (2007) Recovery of dynamic visual acuity in bilateral vestibular hypofunction. Arch Otolaryngol Head Neck Surg 133(4):383–389CrossRef Herdman SJ, Hall CD, Schubert MC, Das VE, Tusa RJ (2007) Recovery of dynamic visual acuity in bilateral vestibular hypofunction. Arch Otolaryngol Head Neck Surg 133(4):383–389CrossRef
9.
go back to reference Wuehr M, Nusser E, Decker J, Krafczyk S, Straube A, Brandt T et al (2016) Noisy vestibular stimulation improves dynamic walking stability in bilateral vestibulopathy. Neurology 86(23):2196–2202CrossRef Wuehr M, Nusser E, Decker J, Krafczyk S, Straube A, Brandt T et al (2016) Noisy vestibular stimulation improves dynamic walking stability in bilateral vestibulopathy. Neurology 86(23):2196–2202CrossRef
10.
go back to reference Iwasaki S, Yamamoto Y, Togo F, Kinoshita M, Yoshifuji Y, Fujimoto C et al (2014) Noisy vestibular stimulation improves body balance in bilateral vestibulopathy. Neurology 82(11):969–975CrossRef Iwasaki S, Yamamoto Y, Togo F, Kinoshita M, Yoshifuji Y, Fujimoto C et al (2014) Noisy vestibular stimulation improves body balance in bilateral vestibulopathy. Neurology 82(11):969–975CrossRef
11.
go back to reference Guyot JP, Perez Fornos A (2019) Milestones in the development of a vestibular implant. Curr Opin Neurol. 32(1):145–153CrossRef Guyot JP, Perez Fornos A (2019) Milestones in the development of a vestibular implant. Curr Opin Neurol. 32(1):145–153CrossRef
12.
go back to reference Guinand N, van de Berg R, Cavuscens S, Stokroos RJ, Ranieri M, Pelizzone M 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(4):227–240CrossRef Guinand N, van de Berg R, Cavuscens S, Stokroos RJ, Ranieri M, Pelizzone M 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(4):227–240CrossRef
13.
go back to reference Perez Fornos A, Guinand N, van de Berg R, Stokroos R, Micera S, Kingma H et al (2014) Artificial balance: restoration of the vestibulo-ocular reflex in humans with a prototype vestibular neuroprosthesis. Front Neurol 5:66CrossRef Perez Fornos A, Guinand N, van de Berg R, Stokroos R, Micera S, Kingma H et al (2014) Artificial balance: restoration of the vestibulo-ocular reflex in humans with a prototype vestibular neuroprosthesis. Front Neurol 5:66CrossRef
14.
go back to reference Guinand N, Van de Berg R, Cavuscens S, Ranieri M, Schneider E, Lucieer F, Kingma H, Guyot JP, Pérez Fornos A (2017) The video head impulse test to assess the efficacy of vestibular implants in humans. Front Neurol 8:600CrossRef Guinand N, Van de Berg R, Cavuscens S, Ranieri M, Schneider E, Lucieer F, Kingma H, Guyot JP, Pérez Fornos A (2017) The video head impulse test to assess the efficacy of vestibular implants in humans. Front Neurol 8:600CrossRef
15.
go back to reference Guinand N, Van de Berg R, Cavuscens S, Stokroos R, Ranieri M, Pelizzone M, Kingma H, Guyot JP, Pérez Fornos A (2016) Restoring visual acuity in dynamic conditions with a vestibular implant. Front Neurosci 10:577CrossRef Guinand N, Van de Berg R, Cavuscens S, Stokroos R, Ranieri M, Pelizzone M, Kingma H, Guyot JP, Pérez Fornos A (2016) Restoring visual acuity in dynamic conditions with a vestibular implant. Front Neurosci 10:577CrossRef
16.
go back to reference Phillips C, Defrancisci C, Ling L, Nie K, Nowack A, Phillips JO et al (2013) Postural responses to electrical stimulation of the vestibular end organs in human subjects. Exp Brain Res 229(2):181–195CrossRef Phillips C, Defrancisci C, Ling L, Nie K, Nowack A, Phillips JO et al (2013) Postural responses to electrical stimulation of the vestibular end organs in human subjects. Exp Brain Res 229(2):181–195CrossRef
17.
go back to reference Curthoys IS, Grant JW, Burgess AM, Pastras CJ, Brown DJ, Manzari L (2018) Otolithic receptor mechanisms for vestibular-evoked myogenic potentials: a review. Front Neurol 9:366CrossRef Curthoys IS, Grant JW, Burgess AM, Pastras CJ, Brown DJ, Manzari L (2018) Otolithic receptor mechanisms for vestibular-evoked myogenic potentials: a review. Front Neurol 9:366CrossRef
18.
go back to reference Grommes C, Conway D (2011) The stepping test: a step back in history. J Hist Neurosci 20(1):29–33CrossRef Grommes C, Conway D (2011) The stepping test: a step back in history. J Hist Neurosci 20(1):29–33CrossRef
19.
go back to reference Honaker JA, Shepard NT (2012) Performance of Fukuda stepping test as a function of the severity of caloric weakness in chronic dizzy patients. J Am Acad Audiol 23(8):616–622CrossRef Honaker JA, Shepard NT (2012) Performance of Fukuda stepping test as a function of the severity of caloric weakness in chronic dizzy patients. J Am Acad Audiol 23(8):616–622CrossRef
20.
go back to reference Strupp M, Magnusson M (2015) Acute unilateral vestibulopathy. Neurol Clin 33(3):669–685CrossRef Strupp M, Magnusson M (2015) Acute unilateral vestibulopathy. Neurol Clin 33(3):669–685CrossRef
21.
go back to reference Kos MI, Feigl G, Anderhuber F, Wall C, Fasel JH, Guyot JP (2006) Transcanal approach to the singular nerve. Otol Neurotol 27(4):542–546PubMed Kos MI, Feigl G, Anderhuber F, Wall C, Fasel JH, Guyot JP (2006) Transcanal approach to the singular nerve. Otol Neurotol 27(4):542–546PubMed
22.
go back to reference Feigl G, Kos I, Anderhuber F, Guyot JP, Fasel J (2008) Development of surgical skill with singular neurectomy using human cadaveric temporal bones. Ann Anat Anat Anz 190(4):316–323CrossRef Feigl G, Kos I, Anderhuber F, Guyot JP, Fasel J (2008) Development of surgical skill with singular neurectomy using human cadaveric temporal bones. Ann Anat Anat Anz 190(4):316–323CrossRef
23.
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 3:18CrossRef 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 3:18CrossRef
24.
go back to reference Guyot JP, Sigrist A, Pelizzone M, Kos MI (2011) Adaptation to steady-state electrical stimulation of the vestibular system in humans. Ann Otol Rhinol Laryngol 120(3):143–149CrossRef Guyot JP, Sigrist A, Pelizzone M, Kos MI (2011) Adaptation to steady-state electrical stimulation of the vestibular system in humans. Ann Otol Rhinol Laryngol 120(3):143–149CrossRef
25.
go back to reference Watson SR, Colebatch JG (1998) Vestibulocollic reflexes evoked by short-duration galvanic stimulation in man. J Physiol 513(Pt 2):587–597CrossRef Watson SR, Colebatch JG (1998) Vestibulocollic reflexes evoked by short-duration galvanic stimulation in man. J Physiol 513(Pt 2):587–597CrossRef
26.
go back to reference Shinoda Y, Sugiuchi Y, Futami T, Ando N, Kawasaki T (1994) Input patterns and pathways from the six semicircular canals to motoneurons of neck muscles. I. The multifidus muscle group. J Neurophysiol 72(6):2691–2702CrossRef Shinoda Y, Sugiuchi Y, Futami T, Ando N, Kawasaki T (1994) Input patterns and pathways from the six semicircular canals to motoneurons of neck muscles. I. The multifidus muscle group. J Neurophysiol 72(6):2691–2702CrossRef
27.
go back to reference Suzuki JI, Cohen B (1964) Head, eye, body and limb movements from semicircular canal nerves. Exp Neurol 10:393–405CrossRef Suzuki JI, Cohen B (1964) Head, eye, body and limb movements from semicircular canal nerves. Exp Neurol 10:393–405CrossRef
Metadata
Title
Cervical myogenic potentials and controlled postural responses elicited by a prototype vestibular implant
Authors
Angelica Perez Fornos
Raymond van de Berg
Stéphane Armand
Samuel Cavuscens
Maurizio Ranieri
Céline Crétallaz
Herman Kingma
Jean-Philippe Guyot
Nils Guinand
Publication date
01-09-2019
Publisher
Springer Berlin Heidelberg
Published in
Journal of Neurology / Issue Special Issue 1/2019
Print ISSN: 0340-5354
Electronic ISSN: 1432-1459
DOI
https://doi.org/10.1007/s00415-019-09491-x

Other articles of this Special Issue 1/2019

Journal of Neurology 1/2019 Go to the issue