Noisy galvanic vestibular stimulation induces a sustained improvement in body balance in elderly adults

Chisato Fujimoto, Yoshiharu Yamamoto, Teru Kamogashira, Makoto Kinoshita, Naoya Egami, Yukari Uemura, Fumiharu Togo, Tatsuya Yamasoba, Shinichi Iwasaki, Chisato Fujimoto, Yoshiharu Yamamoto, Teru Kamogashira, Makoto Kinoshita, Naoya Egami, Yukari Uemura, Fumiharu Togo, Tatsuya Yamasoba, Shinichi Iwasaki

Abstract

Vestibular dysfunction causes postural instability, which is prevalent in the elderly. We previously showed that an imperceptible level of noisy galvanic vestibular stimulation (nGVS) can improve postural stability in patients with bilateral vestibulopathy during the stimulus, presumably by enhancing vestibular information processing. In this study, we investigated the after-effects of an imperceptible long-duration nGVS on body balance in elderly adults. Thirty elderly participants underwent two nGVS sessions in a randomised order. In Session 1, participants received nGVS for 30 min twice with a 4-h interval. In Session 2, participants received nGVS for 3 h. Two-legged stance tasks were performed with eyes closed while participants stood on a foam rubber surface, with and without nGVS, and parameters related to postural stability were measured using posturography. In both sessions, the postural stability was markedly improved for more than 2 h after the cessation of the stimulus and tended to decrease thereafter. The second stimulation in Session 1 caused a moderate additional improvement in body balance and promoted the sustainability of the improvement. These results suggest that nGVS can lead to a postural stability improvement in elderly adults that lasts for several hours after the cessation of the stimulus, probably via vestibular neuroplasticity.

Figures

Figure 1. Experimental setup.
Figure 1. Experimental setup.
(a) Noisy galvanic vestibular stimulation (nGVS) was applied with electrodes on the right and left mastoids by a portable stimulator. Two-legged stance tasks were performed with eyes closed while participants stood on foam rubber with and without nGVS. (b) Waveforms of nGVS are shown. (c) A frequency spectrum of nGVS is shown.
Figure 2. Consolidated Standards of Reporting Trials…
Figure 2. Consolidated Standards of Reporting Trials diagram for the flow of participants through the study and protocols.
(a) We recruited 30 healthy elderly participants. Among them, 20 participants who had the optimal stimulus before both sessions were finally included in the analyses. (b) Two experimental sessions were performed in a randomised order. Arrowheads indicate the measurement time point of posturography. ST = stimulation period, PST = post-stimulation period.
Figure 3. Statokinesigrams and changes in the…
Figure 3. Statokinesigrams and changes in the normalised ratios (NRs) of the velocity, area, and RMS for a representative 67-year-old male participant in the first nGVS session (Session 1).
(a) Statokinesigrams are shown. (b) nGVS for 30 min improved the NRs of all three parameters in the PST. Dashed line indicates NR = 1.0.
Figure 4. Mean NRs at the measurement…
Figure 4. Mean NRs at the measurement time points in Session 1 and Session 2.
(a) Mean NRs of the velocity, area, and RMS in Session 1 are shown. (b) Mean NRs of the velocity, area, and RMS in Session 2 are shown. Dashed line indicates NR = 1.0. NR = normalised ratio, RMS = root mean square, ST = stimulation period, PST = post-stimulation period. *P < 0.05, **P < 0.01, ***P < 0.001, ****P < 0.0001, *****P < 0.00001.

References

    1. Rossignol S., Dubuc R. & Gossard J. P. Dynamic sensorimotor interactions in locomotion. Physiol Rev 86, 89–154, doi: 10.1152/physrev.00028.2005 (2006).
    1. Iwasaki S. & Yamasoba T. Dizziness and Imbalance in the Elderly: Age-related Decline in the Vestibular System. Aging and disease 6, 38–47, doi: 10.14336/AD.2014.0128 (2015).
    1. Aw S. T., Todd M. J., Aw G. E., Weber K. P. & Halmagyi G. M. Gentamicin vestibulotoxicity impairs human electrically evoked vestibulo-ocular reflex. Neurology 71, 1776–1782, doi: 10.1212/01.wnl.0000335971.43443.d9 (2008).
    1. Fitzpatrick R. C. & Day B. L. Probing the human vestibular system with galvanic stimulation. J Appl Physiol (1985) 96, 2301–2316, doi: 10.1152/japplphysiol.00008.2004 (2004).
    1. Pan W., Soma R., Kwak S. & Yamamoto Y. Improvement of motor functions by noisy vestibular stimulation in central neurodegenerative disorders. J Neurol 255, 1657–1661, doi: 10.1007/s00415-008-0950-3 (2008).
    1. Soma R., Nozaki D., Kwak S. & Yamamoto Y. 1/f noise outperforms white noise in sensitizing baroreflex function in the human brain. Phys Rev Lett 91, 078101 (2003).
    1. Yamamoto Y., Struzik Z. R., Soma R., Ohashi K. & Kwak S. Noisy vestibular stimulation improves autonomic and motor responsiveness in central neurodegenerative disorders. Ann Neurol 58, 175–181, doi: 10.1002/ana.20574 (2005).
    1. Iwasaki S. et al.. Noisy vestibular stimulation improves body balance in bilateral vestibulopathy. Neurology 82, 969–975, doi: 10.1212/WNL.0000000000000215 (2014).
    1. Mulavara A. P. et al.. Using low levels of stochastic vestibular stimulation to improve locomotor stability. Frontiers in systems neuroscience 9, 117, doi: 10.3389/fnsys.2015.00117 (2015).
    1. Wuehr M. et al.. Noisy vestibular stimulation improves dynamic walking stability in bilateral vestibulopathy. Neurology 86, 2196–2202, doi: 10.1212/WNL.0000000000002748 (2016).
    1. Wuehr M. et al.. Noise-Enhanced Vestibular Input Improves Dynamic Walking Stability in Healthy Subjects. Brain stimulation 9, 109–116, doi: 10.1016/j.brs.2015.08.017 (2016).
    1. McDonnell M. D. & Ward L. M. The benefits of noise in neural systems: bridging theory and experiment. Nat Rev Neurosci 12, 415–426, doi: 10.1038/nrn3061 (2011).
    1. Gittis A. H. & du Lac S. Intrinsic and synaptic plasticity in the vestibular system. Curr Opin Neurobiol 16, 385–390, doi: 10.1016/j.conb.2006.06.012 (2006).
    1. Straka H., Vibert N., Vidal P. P., Moore L. E. & Dutia M. B. Intrinsic membrane properties of vertebrate vestibular neurons: function, development and plasticity. Prog Neurobiol 76, 349–392, doi: 10.1016/j.pneurobio.2005.10.002 (2005).
    1. Curthoys I. S. Vestibular compensation and substitution. Curr Opin Neurol 13, 27–30 (2000).
    1. Smith P. F. & Curthoys I. S. Mechanisms of recovery following unilateral labyrinthectomy: a review. Brain Res Brain Res Rev 14, 155–180 (1989).
    1. Vidal P. P., de Waele C., Vibert N. & Muhlethaler M. Vestibular compensation revisited. Otolaryngol Head Neck Surg 119, 34–42 (1998).
    1. Johns G. M. In Disorders of the vestibular system (eds Baloh R. W. & Halmagyi G. M.) Ch. 7, 85–92 (Oxford University Press, 1996).
    1. Grassi S. & Pettorossi V. E. Synaptic plasticity in the medial vestibular nuclei: role of glutamate receptors and retrograde messengers in rat brainstem slices. Prog Neurobiol 64, 527–553 (2001).
    1. Kim D. J. et al.. Noisy galvanic vestibular stimulation modulates the amplitude of EEG synchrony patterns. PLoS One 8, e69055, doi: 10.1371/journal.pone.0069055 (2013).
    1. Martin P. & Hudspeth A. J. Compressive nonlinearity in the hair bundle’s active response to mechanical stimulation. Proc Natl Acad Sci USA 98, 14386–14391, doi: 10.1073/pnas.251530498 (2001).
    1. Minor L. B., Lasker D. M., Backous D. D. & Hullar T. E. Horizontal vestibuloocular reflex evoked by high-acceleration rotations in the squirrel monkey. I. Normal responses. J Neurophysiol 82, 1254–1270 (1999).
    1. Richardson K. A., Imhoff T. T., Grigg P. & Collins J. J. Using electrical noise to enhance the ability of humans to detect subthreshold mechanical cutaneous stimuli. Chaos 8, 599–603, doi: 10.1063/1.166341 (1998).
    1. Sasaki H. et al.. Suprathreshold stochastic resonance in visual signal detection. Behav Brain Res 193, 152–155, doi: 10.1016/j.bbr.2008.05.003 (2008).
    1. Zeng F. G., Fu Q. J. & Morse R. Human hearing enhanced by noise. Brain Res 869, 251–255 (2000).
    1. Markham C. H. Vestibular control of muscular tone and posture. The Canadian journal of neurological sciences. Le journal canadien des sciences neurologiques 14, 493–496 (1987).
    1. Manzoni D., Andre P. & Pompeiano O. Changes in gain and spatiotemporal properties of the vestibulospinal reflex after injection of a GABA-A agonist in the cerebellar anterior vermis. Journal of vestibular research: equilibrium & orientation 7, 7–20 (1997).
    1. Grassi S., Dieni C., Frondaroli A. & Pettorossi V. E. Influence of visual experience on developmental shift from long-term depression to long-term potentiation in the rat medial vestibular nuclei. The Journal of physiology 560, 767–777, doi: 10.1113/jphysiol.2004.069658 (2004).
    1. Puyal J. et al.. Developmental shift from long-term depression to long-term potentiation in the rat medial vestibular nuclei: role of group I metabotropic glutamate receptors. The Journal of physiology 553, 427–443, doi: 10.1113/jphysiol.2003.051995 (2003).
    1. Hille B. Ion Channels of Excitable Membranes (ed. Hille B.) (Sinauer Associates, Inc, 2001).
    1. Monte-Silva K., Kuo M. F., Liebetanz D., Paulus W. & Nitsche M. A. Shaping the optimal repetition interval for cathodal transcranial direct current stimulation (tDCS). J Neurophysiol 103, 1735–1740, doi: 10.1152/jn.00924.2009 (2010).
    1. Zingler V. C. et al.. Causative factors and epidemiology of bilateral vestibulopathy in 255 patients. Ann Neurol 61, 524–532 (2007).
    1. Baloh R. W., Jacobson K. & Honrubia V. Idiopathic bilateral vestibulopathy. Neurology 39, 272–275 (1989).
    1. Guinand N., Guyot J. P., Kingma H., Kos I. & Pelizzone M. Vestibular implants: the first steps in humans. Conf Proc IEEE Eng Med Biol Soc 2011, 2262–2264, doi: 10.1109/IEMBS.2011.6090569 (2011).
    1. Guyot J. P., Gay A., Kos M. I. & Pelizzone M. Ethical, anatomical and physiological issues in developing vestibular implants for human use. Journal of vestibular research: equilibrium & orientation 22, 3–9, doi: 10.3233/VES-2012-0446 (2012).
    1. Merfeld D. M. & Lewis R. F. Replacing semicircular canal function with a vestibular implant. Curr Opin Otolaryngol Head Neck Surg 20, 386–392, doi: 10.1097/MOO.0b013e328357630f (2012).

Source: PubMed

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