Restoring Visual Acuity in Dynamic Conditions with a Vestibular Implant

Nils Guinand, Raymond Van de Berg, Samuel Cavuscens, Robert Stokroos, Maurizio Ranieri, Marco Pelizzone, Herman Kingma, Jean-Philippe Guyot, Angélica Pérez Fornos, Nils Guinand, Raymond Van de Berg, Samuel Cavuscens, Robert Stokroos, Maurizio Ranieri, Marco Pelizzone, Herman Kingma, Jean-Philippe Guyot, Angélica Pérez Fornos

Abstract

Vestibular implants are devices designed to rehabilitate patients with a bilateral vestibular loss (BVL). These patients lack a properly functioning vestibulo-ocular reflex (VOR), which impairs gaze stabilization abilities and results in an abnormal loss of visual acuity (VA) in dynamic situations (i.e., severely limiting the patient's ability to read signs or recognize faces while walking). We previously demonstrated that the VOR can be artificially restored in a group of BVL patients fitted with a prototype vestibular implant. This study was designed to investigate whether these promising results could be translated to a close-to-reality task, significantly improving VA abilities while walking. Six BVL patients previously implanted with a vestibular implant prototype participated in the experiments. VA was determined using Sloan letters displayed on a computer screen, in four conditions: (1) with the patient standing still without moving (static), (2) while the patient was walking on a treadmill at constant speed with the vestibular implant prototype turned off (systemOFF), (3) while the patient was walking on a treadmill at constant speed with the vestibular implant prototype turned on providing coherent motion information (systemONmotion), and (4) a "placebo" condition where the patient was walking on a treadmill at constant speed with the vestibular implant prototype turned on providing reversed motion information (systemONsham). The analysis (one-way repeated measures analysis of variance) revealed a statistically significant effect of the test condition [F(3, 12) = 30.5, p < 0.001]. Significant decreases in VA were observed with the systemOFF condition when compared to the static condition (Tukey post-hoc p < 0.001). When the vestibular implant was turned on, delivering pertinent motion information (systemONmotion) the VA improved to close to normal values. The improvement disappeared in the placebo condition (systemONsham) and VA-values also dropped significantly in this condition (Tukey post-hoc p < 0.001). These results are a significant step forward in the field, demonstrating for the first time in humans that gaze stabilization abilities can be restored with a vestibular implant prototype. The vestibular implant shows considerable promise of being the first-ever effective therapeutic alternative for patients with a BVL in the near future.

Keywords: bilateral vestibular loss; cochlear implant; dynamic visual acuity; electrical stimulation; vestibular implant; vestibulo-ocular reflex.

Figures

Figure 1
Figure 1
Normalized visual acuity results. (A) Individual results obtained in the dynamic conditions (colored bars; red—systemOFF, blue—systemONmotion, green—systemONsham) for the six participating subjects, normalized to results obtained in the static condition (black bar). (B) Average normalized results (± standard error of the mean, SEM). ***Indicates significant differences between conditions in the post-hoc tests (Tukey). Dotted gray lines indicate theoretical performance of “normal” subjects (i.e., no loss of visual acuity in dynamic situations).

References

    1. Brainard D. H. (1997). The psychophysics toolbox. Spat. Vis. 10, 433–436.
    1. Cushing S. L., Pothier D., Hughes C., Hubbard B. J., Gordon K. A., Papsin B. C. (2012). Providing auditory cues to improve stability in children who are deaf. Laryngoscope 122, S101–S102. 10.1002/lary.23807
    1. Dai C., Fridman G. Y., Davidovics N. S., Chiang B., Ahn J. H., Della Santina C. C. (2011). Restoration of 3D vestibular sensation in rhesus monkeys using a multichannel vestibular prosthesis. Hear. Res. 281, 74–83. 10.1016/j.heares.2011.08.008
    1. Gong W., Merfeld D. M. (2002). System design and performance of a unilateral horizontal semicircular canal prosthesis. IEEE Trans. Biomed. Eng. 49, 175–181. 10.1109/10.979358
    1. Grossman G. E., Leigh R. J., Bruce E. N., Huebner W. P., Lanska D. J. (1989). Performance of the human vestibuloocular reflex during locomotion. J. Neurophysiol. 62, 264–272.
    1. Guinand N., Boselie F., Guyot J. P., Kingma H. (2012a). Quality of life of patients with bilateral vestibulopathy. Ann. Otol. Rhinol. Laryngol. 121, 471–477. 10.1177/000348941212100708
    1. Guinand N., Pijnenburg M., Janssen M., Kingma H. (2012b). Visual acuity while walking and oscillopsia severity in healthy subjects and patients with unilateral and bilateral vestibular function loss. Arch. Otolaryngol. Head Neck Surg. 138, 301–306. 10.1001/archoto.2012.4
    1. Guinand N., Van de Berg R., Cavuscens S., Stokroos R. J., 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 J. Otorhinolaryngol. Relat. Spec. 77, 227–240. 10.1159/000433554
    1. Guyot J. P., Sigrist A., Pelizzone M., Kos M. I. (2011). Adaptation to steady-state electrical stimulation of the vestibular system in humans. Ann. Otol. Rhinol. Laryngol. 120, 143–149. 10.1177/000348941112000301
    1. Hillman E. J., Bloomberg J. J., McDonald P. V., Cohen H. S. (1999). Dynamic visual acuity while walking in normals and labyrinthine-deficient patients. J. Vestib. Res. 9, 49–57.
    1. Holladay J. T. (1997). Proper method for calculating average visual acuity. J. Refract. Surg. 13, 388–391.
    1. Kleiner M., Brainard D. H., Pelli D. G. (2007). What's new in Psychtoolbox-3? Perception 36, 1–65. ECVP Abstract Supplement.
    1. Kos M. I., Feigl G., Anderhuber F., Wall C., Fasel J. H., Guyot J. P. (2006). Transcanal approach to the singular nerve. Otol. Neurotol. 27, 542–546. 10.1097/01.mao.0000217349.09796.d1
    1. Lambert S., Sigrist A., Delaspre O., Pelizzone M., Guyot J. P. (2010). Measurement of dynamic visual acuity in patients with vestibular areflexia. Acta Otolaryngol. 130, 820–823. 10.3109/00016480903426592
    1. Lewis R. F., Haburcakova C., Gong W., Makary C., Merfeld D. M. (2010). Vestibuloocular reflex adaptation investigated with chronic motion-modulated electrical stimulation of semicircular canal afferents. J. Neurophysiol. 103, 1066–1079. 10.1152/jn.00241.2009
    1. Merfeld D. M., Haburcakova C., Gong W., Lewis R. F. (2007). Chronic vestibulo-ocular reflexes evoked by a vestibular prosthesis. IEEE Trans. Biomed. Eng. 54(6 Pt 1), 1005–1015. 10.1109/TBME.2007.891943
    1. Parkes W. J., Gnanasegaram J. J., Cushing S. L., McKnight C. L., Papsin B. C., Gordon K. A. (2016). Vestibular evoked myogenic potential testing as an objective measure of vestibular stimulation with cochlear implants. Laryngoscope.. [Epub ahead of print]. 10.1002/lary.26037
    1. Pelizzone M., Perez Fornos A., Ranieri M., Cavuscens S. (2013). Device and Method for Electrical Stimulation of Neural or Muscular Tissue. EP12153300.x-1652, Geneva.
    1. Pelli D. G. (1997). The VideoToolbox software for visual psychophysics: transforming numbers into movies. Spat. Vis. 10, 437–442.
    1. 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. 5:66. 10.3389/fneur.2014.00066
    1. Phillips C., Defrancisci C., Ling L., Nie K., Nowack A., Phillips J. O., et al. . (2013). Postural responses to electrical stimulation of the vestibular end organs in human subjects. Exp. Brain Res. 229, 181–195. 10.1007/s00221-013-3604-3
    1. Schubert M. C., Migliaccio A. A., Della Santina C. C. (2006). Dynamic visual acuity during passive head thrusts in canal planes. J. Assoc. Res. Otolaryngol. 7, 329–338. 10.1007/s10162-006-0047-6
    1. Sun D. Q., Ward B. K., Semenov Y. R., Carey J. P., Della Santina C. C. (2014). Bilateral vestibular deficiency: quality of life and economic implications. JAMA Otolaryngol. Head Neck Surg. 140, 527–534. 10.1001/jamaoto.2014.490
    1. Suzuki J. I., Cohen B., Bender M. B. (1964). Compensatory eye movements induced by vertical semicircular canal stimulation. Exp. Neurol. 9, 137–160.
    1. Van de Berg R., Guinand N., Guyot J. P., Kingma H., Stokroos R. J. (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. 3:18. 10.3389/fneur.2012.00018
    1. Van de Berg R., Guinand N., Nguyen K., Ranieri M., Cavuscens S., GUYOT J.-P., et al. . (2015). The vestibular implant: frequency-dependency of the electrically evoked vestibulo-ocular reflex in humans. Front. Syst. Neurosci. 8:255. 10.3389/fnsys.2014.00255
    1. Vital D., Hegemann S. C., Straumann D., Bergamin O., Bockisch C. J., Angehrn D., et al. . (2010). A new dynamic visual acuity test to assess peripheral vestibular function. Arch. Otolaryngol. Head Neck Surg. 136, 686–691. 10.1001/archoto.2010.99

Source: PubMed

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