Milestones in the development of a vestibular implant

Jean-Philippe Guyot, Angelica Perez Fornos, Jean-Philippe Guyot, Angelica Perez Fornos

Abstract

Purpose of review: Bilateral vestibular deficits exist and their prevalence is more important than believed by the medical community. Their severe impact has inspired several teams to develop technical solutions in an attempt to rehabilitate patients. A particularly promising pathway is the vestibular implant. This article describes the main milestones in this field, mainly focusing on work conducted in human patients.

Recent findings: There have been substantial research efforts, first in animals and more recently in humans, toward the development of vestibular implants. Humans have demonstrated surprising adaptation capabilities to the artificial vestibular signal. Today, the possibility of restoring vestibular reflexes, particularly the vestibulo-ocular reflex, and even achieving useful function in close-to-reality tasks (i.e. improving visual abilities while walking) have been demonstrated in humans.

Summary: The vestibular implant opens new perspectives, not only as an effective therapeutic tool, but also pushes us to go beyond current knowledge and well-established clinical concepts.

Figures

Box 1
Box 1
no caption available
FIGURE 1
FIGURE 1
Cochleo-vestibular implant prototype. Scheme of the vestibulo-cochlear prototype developed by the Geneva – Maastricht group in collaboration with Med El (Innsbruck, Austria). One to three electrodes are removed from the cochlear array and placed in the vicinity of the vestibular nerve branches innervating the semicircular canals.
FIGURE 2
FIGURE 2
Restoration of the vestibulo-ocular reflex with a vestibular implant [32]. Patients suffering from a BVD and equipped of a vestibular implant were submitted to horizontal whole-body rotations. The vestibulo-ocular reflex is absent with the device turned OFF (left) and normalized when the device was turned ON (right). From [41].
FIGURE 3
FIGURE 3
Vestibulo-ocular response to the head impulse test in a patient equipped with a vestibular implant [35]. In this case, the response replicates the normal behavior of the normal reflex. From [▪▪].
FIGURE 4
FIGURE 4
Comparison of visual acuity scores measured in six BVD patients equipped with the vestibular implant [38]. The visual acuity was measured using Sloan letters displayed on a computer screen in static (at rest) and dynamic (while walking at controlled velocity) conditions. Values were normalized to those obtained in static conditions. The visual acuity decreased in dynamic condition and normalized when the vestibular implant was turned ON. This finding was reinforced by the fact that visual acuity decreased again when the prosthesis provided random information instead of motion information, ruling out a ‘placebo’ effect. Modified from [▪▪].

References

    1. Ward BK, Agrawal Y, Hoffman HJ, et al. Prevalence and impact of bilateral vestibular hypofunction: results from the 2008 US national health interview survey. JAMA Otolaryngol Head Neck Surg 2013; 139:803–810.
    1. Dandy WE. The surgical treatment of Meniere's disease. Surg Gynecol Obstet 1941; 72:421–425.
    1. Miffon M, Guyot JPh. Difficulties faced by patients suffering from a total, bilateral vestibular loss. ORL 2015; 77:241–247.
    1. Vibert D, Liard P, Häusler R. Bilateral idiopathic loss of peripheral vestibular function with normal hearing. Acta Otolaryngol (Stockh) 1995; 115:611–615.
    1. Guinand N, Boselie F, Guyot JPh, Kingma H. Quality of life of patients with bilateral vestibulopathy: necessity to treat? Ann Otol Rhinol Laryngol 2012; 121:471–477.
    1. Zingler VC, Cnyrim C, Jahn K, et al. Causative factors and epidemiology of bilateral vestibulopathy in 255 patients. Ann Neurol 2007; 61:524–532.
    1. Wall C, 3rd, Oddsson LE, Horak FB, et al. Applications of vibrotactile display of body tilt for rehabilitation. Conf Proc IEEE Eng Med Biol Soc 2004; 7:4763–4765.
    1. Honegger F, Hillebrandt IM, van den Elzen NG, et al. The effect of prosthetic feedback on the strategies and synergies used by vestibular loss subjects to control stance. J Neuroeng Rehabil 2013; 10:115.
    1. Sienko KH, Balkwill MD, Oddsson LI, Wall C., 3rd The effect of vibrotactile feedback on postural sway during locomotor activities. J Neuroeng Rehabil 2013; 10:93.
    1. Janssen M, Pas R, Aarts J, et al. Clinical observational gait analysis to evaluate improvement of balance during gait with vibrotactile feed back.with vibrotactile biofeedback. Physiother Res Int 2012; 17:4–11.
    1. Iwasaki S, Yamamoto Y, Togo F, et al. Noisy vestibular stimulation improves body balance in bilateral vestibulopathy. Neurology 2014; 82:969–975.
    1. Iwasaki S, Karino S, Kamogashira T, et al. Effect of noisy galvanic vestibular stimulation on ocular vestibular-evoked myogenic potentials to bone-conducted vibration. Front Neurol 2017; 8:26.
    1. Mulavara AP, Kofman IS, De Dios YE, et al. Using low levels of stochastic vestibular stimulation to improve locomotor stability. Front Syst Neurosci 2015; 9:117.
    1. Schniepp R, Boerner JC, Decker J, et al. Noisy vestibular stimulation improves vestibulospinal function in patients with bilateral vestibulopathy. J Neurol 2018; 265 Suppl 1:57–62.
    1. Wuehr M, Nusser E, Decker J, et al. Noisy vestibular stimulation improves dynamic walking stability in bilateral vestibulopathy. Neurology 2016; 86:2196–2202.
    1. Wuehr M, Nusser E, Krafczyk S, et al. Noise-enhanced vestibular input improves dynamic walking stability in healthy subjects. Brain Stimul 2016; 9:109–116.
    1. Fujimoto C, Yamamoto Y, Kamogashira T, et al. Noisy galvanic vestibular stimulation induces a sustained improvement in body balance in elderly adults. Sci Rep 2016; 6:37575.
    1. Moss F, Ward LM, Sannita WG. Stochastic resonance and sensory information processing: a tutorial and review of application. Clin Neurophysiol 2004; 115:267–281.
    1. Wuehr M, Boerner JC, Pradhan C, et al. Stochastic resonance in the human vestibular system: noise-induced facilitation of vestibulospinal reflexes. Brain Stimul 2018; 11:261–263.
    1. Cohen B, Suzuki JI. Eye movements induced by ampullary nerve stimulation. Am J Physiol 1963; 204:347–351.
    1. Cohen B, Suzuki JI, Bender MB. Eye movements from semicircular canal nerve stimulation in the cat. Ann Otol Rhinol Laryngol 1964; 73:153–169.
    1. Suzuki JI, Goto K, Tokumasu K, Cohen B. Implantation of electrodes near individual vestibular nerve branches in mammals. Ann Otol Rhinol Laryngol 1969; 78:815–826.
    1. Cohen B. Kornhuber HH. The vestibulo-ocular reflex arc. Vestibular system, part 1, Basic mechanisms. Berlin, Heidelberg, New York: Sringer Verlag; 1974. 477–540.
    1. Goldberg JM, Fernandez C. Physiology of peripheral neurons innervating semicircular canals of the squirrel monkey. I. Resting discharge and response to constant angular accelerations. J Neurophysiol 1971; 34:635–660.
    1. Fernandez C, Goldberg JM. Physiology of peripheral neurons innervating semicircular canals of the squirrel monkey. II. Response to sinusoidal stimulation and dynamics of peripheral vestibular system. J Neurophysiol 1971; 34:661–675.
    1. Goldberg JM, Fernandez C. Physiology of peripheral neurons innervating semicircular canals of the squirrel monkey. III. Variations among units in their discharge properties. J Neurophysiol 1971; 34:676–684.
    1. Gong W, Merfeld DM. Prototype neural semicircular canal prosthesis using patterned electrical stimulation. Ann Biomed Engineer 2000; 28:572–581.
    1. Gong W, Merfeld DM. System design and performance of a unilateral horizontal semicircular canal prosthesis. IEEE Trans Biomed Eng 2002; 49:175–181.
    1. Lewis RF, Gong W, Ramsey M, et al. Vestibular adaptation studied with a prosthetic semicircular canal. J Vestib Res 2002; 12:87–94.
    1. Merfeld DM, Gong W, Morrissey J, et al. Acclimation to chronic constant-rate peripheral stimulation provided by a vestibular prosthesis. IEEE Trans Biomed Eng 2006; 53:2362–2372.
    1. Merfeld DM, Haburcakova C, Gong W, Lewis RF. Chronic vestibulo-ocular reflexes evoked by a vestibular prosthesis. IEEE Trans Biomed Eng 2007; 54:1005–1015.
    1. Kós MI, Feigl G, Anderhuber F, et al. Transcanal approach to the singular nerve. Otol Neurotol 2006; 27:542–546.
    1. Feigl GC, Fasel JH, Anderhuber F, et al. Superior vestibular neurectomy : a novel transmeatal approach for a denervation of the superior and lateral semicircular canals. Otol Neurotol 2009; 30:586–591.
    1. van de Berg R, Guinand N, Guyot JP, et al. The modified ampullar approach for vestibular implant surgery: feasibility and its first application in a human with a long-term vestibular loss. Front Neurol 2012; 20:18.
    1. Wall C, 3rd, Guyot JPh, Kos MI, et al. Electrical stimulation of the posterior ampularis nerve in an alert patient: preliminary results. Barany Society, XXIII International Congress. Paris, July 2004.
    1. Wall C, 3rd, Kos MI, Guyot JPh. Eye movements in response to electric stimulation of the human posterior ampullary nerve. Ann Otol Rhinol Laryngol 2007; 116:369–374.
    1. Guyot JPh, Sigrist A, Pelizzone M, et al. Eye movements in response to electric stimulation of the lateral and superior ampullary nerves. Ann Otol Rhinol Laryngol 2011; 120:81–87.
    1. Guyot JPh, Sigrist A, Pelizzone M, Kos MI. Adaptation to steady-state electrical stimulation of the vestibular system in the human. Ann Otol Rhinol Laryngol 2011; 120:143–149.
    1. Guyot JPh, Gay A, Kos MI, Pelizzone M. Ethical, anatomical and physiological issues in developing vestibular implants for human use. J Vest Res 2012; 22:3–9.
    1. Geneva University Hospitals and University of Geneva: Device and method for electrical stimulation of neural or muscular tissue. Patent EP2762196B1 /US9511226B2 /CN104968391B /WO2014118094A1WO2014118094A1. 2013-01-30.
    1. Pérez Fornos A, Guinand N, Van De Berg R, et al. Artificial balance: restoration of the vestibulo-ocular reflex in humans with a prototype vestibular neuroprosthesis. Front Neuro-Otol 2014; 10:3389.
    1. Barnes GR. Visual-vestibular interaction in the control of head and eye movement: the role of visual feedback and predictive mechanisms. Prog Neurobiol 1993; 41:435–472.
    1. van de Berg R, Guinand N, Nguyen TAK, et al. The vestibular implant: frequency dependency of the electrically evoked vestibulo-ocular reflex in humans. Front Syst Neurosci 2015; 8:255.
    1. Guinand N, van de Berg, Cavuscens S, et al. The video head impulse test (vHIT) to assess the efficacy of vestibular implants in humans. Front Neurol 2017; 8:600.

    2. In this experiment, authors show that their vestibular implant prototype allows restoring efficiently high-frequency vestibulo-ocular reflexes in the plane of the three semicircular canals.

    1. Lambert S, Sigrist A, Delaspre O, et al. Measurement of dynamic visual acuity in patients with vestibular areflexia. Acta Otolaryngol 2010; 130:820–823.
    1. Guinand N, Pijnenburg M, Janssen M, Kingma H. Visual acuity while walking and oscillopsia severity in healthy subjects and patients with unilateral and bilateral vestibular function loss. Arch Otolaryngol Head Neck Surg 2012; 138:301–306.
    1. Guinand N, van de Berg R, Cavuscens S, et al. Restoring visual acuity in dynamic conditions with a vestibular implant. Front Neurosci 2016; 10:1–6. Article ID: 577.

    2. This article provides the first demonstration of useful rehabilitation in recipients of early vestibular implant prototypes: the restoration of visual abilities in dynamic conditions via the motion modulated electrical stimulation delivered by the device.

    1. Pérez Fornos A, Cavuscens S, Ranieri M, et al. The vestibular implant: a probe in orbit around the human balance system. J Vest Res 2017; 27:51–61.

    2. Authors show here that, in addition to the vestibuloocular reflex, the vestibulocollic reflexes are also activated by the vestibular implant.

    1. Rubinstein JT, Della Santina CC. Development of a biophysical model for vestibular prosthesis research. J Vestib Res 2002; 12:69–76.
    1. Della Santina CC, Migliaccio AA, Patel AH. A multichannel semicircular canal neural prosthesis using electrical stimulation to restore 3-d vestibular sensation. IEEE Trans Biomed Eng 2007; 54:1016–1030.
    1. Hayden R, Sawyer S, Frey E, et al. Virtual labyrinth model of vestibular afferent excitation via implanted electrodes: validation and application to design of a multichannel vestibular prosthesis. Exp Brain Res 2011; 210:623–640.
    1. Tang S, Melvin TA, Della Santina CC. Effects of semicircular canal electrode implantation on hearing in chinchillas. Acta Otolaryngol 2009; 129:481–486.
    1. Rubinstein JT, Bierer S, Kaneko C, et al. Implantation of the semicircular canals with preservation of hearing and rotational sensitivity: a vestibular neurostimulator suitable for clinical research. Otol Neurotol 2012; 33:789–796.
    1. Phillips JO, Ling L, Nie K, et al. Vestibular implantation and longitudinal electrical stimulation of the semicircular canal afferents in human subjects. J Neurophysiol 2015; 113:3866–3892.
    1. Kattah JC, Talkad AV, Wang DZ, et al. HINTS to diagnose stroke in the acute vestibular syndrome: three-step bedside oculomotor examination more sensitive than early MRI diffusion-weighted imaging. Stroke 2009; 40:3504–3510.
    1. Todic J, Guyot JPh, Perez Fornos A, et al. Vestibular and visual stimulation: simultaneous perception or not? Rev Méd Suisse 2016; 12:1650–1652.
    1. Guinand N, Todic J, Guyot JPh, et al. Cochleovestibular simultaneity. J Vest Research 2016; 26:100.

Source: PubMed

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