Vestibular Functions and Parkinson's Disease

Paul F Smith, Paul F Smith

Abstract

For decades it has been speculated that Parkinson's Disease (PD) is associated with dysfunction of the vestibular system, especially given that postural instability is one of the major symptoms of the disorder. Nonetheless, clear evidence of such a connection has been slow to emerge. There are still relatively few studies of the vestibulo-ocular reflexes (VORs) in PD. However, substantial evidence of vestibulo-spinal reflex deficits, in the form of abnormal vestibular-evoked myogenic potentials (VEMPs), now exists. The evidence for abnormalities in the subjective visual vertical is less consistent. However, some studies suggest that the integration of visual and vestibular information may be abnormal in PD. In the last few years, a number of studies have been published which demonstrate that the neuropathology associated with PD, such as Lewy bodies, is present in the central vestibular system. Increasingly, stochastic or noisy galvanic vestibular stimulation (nGVS) is being investigated as a potential treatment for PD, and a number of studies have presented evidence in support of this idea. The aim of this review is to summarize and critically evaluate the human and animal evidence relating to the connection between the vestibular system and PD.

Keywords: Parkinson's disease; VEMPs; dopamine; striatum; vestibular system; vestibulo-ocular reflexes; vestibulo-spinal reflexes.

Figures

Figure 1
Figure 1
Possible neuronal pathways connecting the vestibular nucleus complex to the striatum. PFN, Parafascicular nucleus; PPT, pedunculopontine tegmental nucleus; SNc, Substantia nigra pars compacta; VNC, vestibular nucleus complex. Reproduced from Stiles et al. (59) with permission from the publisher.
Figure 2
Figure 2
Estimated number of c-Fos positive cells in the striatum following vestibular stimulation. ***P ≤ 0.0001 for the comparison of the higher current with both the sham groups and the lower current group. From Stiles et al. (59) with permission.
Figure 3
Figure 3
Examples of the firing patterns of the 6 single striatal neurons responding to electrical stimulation of the vestibular labyrinth in a phase-locked manner, (A) with examples of their action potential waveforms (averages of 200 action potentials (B); mean ± SD in red). From Stiles et al. (59) with permission.
Figure 4
Figure 4
Peri-stimulus histograms of neuronal responses to electrical vestibular stimulation. (A) Combined histogram of firing of all non-responsive neurons at 1 × (top) and 2 × (bottom) the threshold of nystagmus. (B) Combined firing of all 6 responsive neurons, at 3 × the threshold of nystagmus, phase-locked to the stimulus. Red bar represents the stimulation period. Spikes from the stimulus artifact have been removed for clarity. Data are presented as mean (black bars) and standard deviation (gray bars). From Stiles et al. (59) with permission.

References

    1. Williams-Gray CH, Mason SL, Evans JR, Foltynie T, Brayne C, Robbins TW, et al. . The CamPaIGN study of Parkinson's disease: 10-year outlook in an incident population-based cohort. J Neurol Neurosurg Psychiatry (2013) 84:1258–64. 10.1136/jnnp-2013-305277
    1. Van Den Eeden SK, Tanner CM, Bernstein AL, Fross RD, Leimpeter A, Bloch DA, et al. . Incidence of Parkinson's disease: variation by age, gender, and race/ethnicity. Am J Epidemiol. (2003) 157:1015–22. 10.1093/aje/kwg068
    1. Tysnes OB, Storstein A. Epidemiology of Parkinson's disease. J Neural Transm (Vienna). (2017) 124:901–5. 10.1007/s00702-017-1686-y
    1. Pastor MA, Day BL, Marsden CD. Vestibular induced postural responses in Parkinson's disease. Brain. (1993) 116(Pt 5):1177–90. 10.1093/brain/116.5.1177
    1. Cronin T, Arshad Q, Seemungal BM. Vestibular deficits in neurodegenerative disorders: balance, dizziness, and spatial disorientation. Front Neurol. (2017) 8:538. 10.3389/fneur.2017.00538
    1. Stiles L, Smith PF. The vestibular-basal ganglia connection: balancing motor control. Brain Res. (2015) 1597:180–8. 10.1016/j.brainres.2014.11.063
    1. Yamamoto Y, Struzik ZR, Soma R, Ohashi K, Kwak S. Noisy vestibular stimulation improves autonomic and motor responsiveness in central neurodegenerative disorders. Ann Neurol. (2005) 58:175–81. 10.1002/ana.20574
    1. Wilkinson D, Podlewska A, Sakel M. A durable gain in motor and non-motor symptoms of Parkinson's Disease following repeated caloric vestibular stimulation: a single-case study. NeuroRehabilitation. (2016) 38:179–82. 10.3233/NRE-161308
    1. Reichert WH, Doolittle J, McDowell FH. Vestibular dysfunction in Parkinson disease. Neurol. (1982) 32:1133–8. 10.1212/WNL.32.10.1133
    1. Cipparrone L, Ginanneschi A, Degl'Innocenti F, Porzio P, Pagnini P, Marini P. Electro- oculographic routine examination in Parkinson's disease. Acta Neurol Scand. (1988) 77:6–11. 10.1111/j.1600-0404.1988.tb06966.x
    1. Vitale C, Marcelli V, Furia T, Santangelo G, Cozzolino A, Longo K, et al. . Vestibular impairment and adaptive postural imbalance in Parkinsonian patients with lateral trunk flexion. Mov Disord. (2011) 26:1458–63. 10.1002/mds.23657
    1. Lv W, Guan Q, Hu X, Chen J, Jiang H, Zhang L, et al. . Vestibulo-ocular reflex abnormality in Parkinson's disease detected by video head impulse test. Neurosci Lett. (2017) 657:211–4. 10.1016/j.neulet.2017.08.021
    1. Pollak L, Prohorov T, Kushnir M, Rabey M. Vestibulo-cervical reflexes in idiopathic Parkinson's disease. Neurophysiol Clin. (2009) 39:235–40. 10.1016/j.neucli.2009.07.001
    1. Pötter-Nerger M, Reich MM, Colebatch JG, Deuschl G, Volkmann J. Differential effect of dopa and subthalamic stimulation on vestibular activity in Parkinson's disease. Mov Disord. (2012) 27:1268–75. 10.1002/mds.25061
    1. de Natale ER, Ginatempo F, Paulus KS. Paired neurophysiological and clinical study of the brainstem at different stages of Parkinson's disease. Clin Neurophysiol. (2015) 126:1871–8. 10.1016/j.clinph.2014.12.017
    1. de Natale ER, Ginatempo F, Paulus KS, Pes GM, Manca A, Tolu E, et al. . Abnormalities of vestibular-evoked myogenic potentials in idiopathic Parkinson's disease are associated with clinical evidence of brainstem involvement. Neurol Sci. (2015) 36:995–1001. 10.1007/s10072-014-2054-4
    1. Pötter-Nerger M, Govender S, Deuschl G, Volkmann J, Colebatch JG. Selective changes of ocular vestibular myogenic potentials in Parkinson's disease. Mov Disord. (2015) 30:584–9. 10.1002/mds.26114
    1. Venhovens J, Meulstee J, Bloem BR. Neurovestibular analysis and falls in Parkinson's disease and atypical Parkinsonism. Eur J Neurosci. (2016) 43:1636–46. 10.1111/ejn.13253
    1. Shalash AS, Hassan DM, Elrassas HH, Salama MM, Méndez-Hernández E, Salas-Pacheco JM, et al. . Auditory- and vestibular-evoked potentials correlate with motor and non-motor features of Parkinson's Disease. Front Neurol. (2017) 8:55. 10.3389/fneur.2017.00055
    1. Huh YE, Hwang S, Kim K, Chung WH, Youn J, Cho JW. Postural sensory correlates of freezing of gait in Parkinson's disease. Parkinsonism Relat Disord. (2016) 25:72–7. 10.1016/j.parkreldis.2016.02.004
    1. Vidal PP, Cullen K, Curthoys IS, Du Lac S, Holstein G, Idoux E, et al. The vestibular system. In Paxinos G., editor. The Rat Nervous System, 4th ed., Chapter 28, San Diego, CA: Academic Press; (2014). p. 805–64.
    1. Anderson TJ, MacAskill MR. Eye movements in patients with neurodegenerative disorders. Nat Rev Neurol. (2013) 9:74–85. 10.1038/nrneurol.2012.273
    1. Videnovic A. Disturbances of sleep and alertness in Parkinson's Disease. Curr Neurol Neurosci Rep. (2018) 18:29. 10.1007/s11910-018-0838-2
    1. Neikrug AB, Ancoli-Israel S. Diagnostic tools for REM sleep behavior disorder. Sleep Med Rev. (2012) 16:415–29. 10.1016/j.smrv.2011.08.004
    1. Bronstein AM, Yardley L, Moore AP, Cleeves L. Visually and posturally mediated tilt illusion in Parkinson's disease and in labyrinthine defective subjects. Neurol (1996) 47:651–6. 10.1212/WNL.47.3.651
    1. Scocco DH, Wagner JN, Racosta J, Chade A, Gershanik OS. Subjective visual vertical in Pisa syndrome. Parkinsonism Relat Disord. (2014) 20:878–83. 10.1016/j.parkreldis.2014.04.030
    1. Barnett-Cowan M, Dyde RT, Fox SH, Moro E, Hutchison WD, Harris LR. Multisensory determinants of orientation perception in Parkinson's disease. Neuroscience (2010) 167:1138–50. 10.1016/j.neuroscience.2010.02.065
    1. Bertolini G, Wicki A, Baumann CR. Impaired tilt perception in Parkinson's disease: a central vestibular integration failure. PLoS ONE (2015) 10:e0124253. 10.1371/journal.pone.0124253
    1. Gandor F, Basta D, Gruber D, Poewe W, Ebersbach G. Subjective visual vertical in PD patients with lateral trunk flexion. Parkinsons Dis. (2016) 2016:7489105. 10.1155/2016/7489105
    1. Montgomery P, Silverstein P, Wichmann R, Fleischaker K, Andberg M. Spatial updating in Parkinson's disease. Brain Cogn. (1993) 23:113–26. 10.1006/brcg.1993.1050
    1. Putcha D, Ross RS, Rosen ML, Norton DJ, Cronin-Golomb A, Somers DC, et al. . Functional correlates of optic flow motion processing in Parkinson's disease. Front Integr Neurosci. (2014) 8:57. 10.3389/fnint.2014.00057
    1. Dastgheib ZA, Lithgow B, Moussavi Z. Application of fractal dimension on vestibular response signals for diagnosis of Parkinson's disease. Conf Proc IEEE Eng Med Biol Soc. (2011) 2011:7892–5. 10.1109/IEMBS.2011.6091946
    1. Dastgheib ZA, Lithgow B, Moussavi Z. Vestibular spontaneous response as a potential signature for Parkinson's disease. Conf Proc IEEE Eng Med Biol Soc. (2012) 2012:3704–7. 10.1109/EMBC.2012.6346771
    1. Dastgheib ZA, Lithgow B, Moussavi Z. Diagnosis of Parkinson's disease using electrovestibulography. Med Biol Eng Comput. (2012) 50:483–91. 10.1007/s11517-012-0890-z
    1. Shoushtarian M, Lithgow B. The relationship between electrovestibulography and Parkinson's disease severity. Conf Proc IEEE Eng Med Biol Soc. (2007) 2007:2377–80. 10.1109/IEMBS.2007.4352805
    1. Lithgow BJ, Shoushtarian M. Parkinson's disease: disturbed vestibular function and levodopa. J Neurol Sci. (2015) 353:49–58. 10.1016/j.jns.2015.03.050
    1. Weinrich M, Bhatia R. Abnormal eye-head coordination in Parkinson's disease patients after administration of levodopa: a possible substrate of levodopa-induced dyskinesia. J Neurol Neurosurg Psychiatry (1986) 49:785–90. 10.1136/jnnp.49.7.785
    1. Hwang S, Agada P, Grill S, Kiemel T, Jeka JJ. A central processing sensory deficit with Parkinson's disease. Exp Brain Res. (2016) 234:2369–79. 10.1007/s00221-016-4642-4
    1. Seidel K, Mahlke J, Siswanto S, Krüger R, Heinsen H, Auburger G, et al. . The brainstem pathologies of Parkinson's Disease and Dementia with Lewy bodies. Brain Pathol. (2015) 25:121–35. 10.1111/bpa.12168
    1. Müller ML, Albin RL, Kotagal V, Koeppe RA, Scott PJ, Frey KA, et al. . Thalamic cholinergic innervation and postural sensory integration function in Parkinson's disease. Brain. (2013) 136(Pt 11):3282–9. 10.1093/brain/awt247
    1. Aravamuthan BR, Angelaki DE. Vestibular responses in the macaque pedunculopontine nucleus and central mesencephalic reticular formation. Neurosci. (2012) 223:183–99. 10.1016/j.neuroscience.2012.07.054
    1. Aitken P, Zheng Y, Smith PF. Effects of bilateral vestibular deafferentation in rat on hippocampal theta response to somatosensory stimulation, acetylcholine release and cholinergic neurons in the pedunculopontine tegmental nucleus. Brain Struct Funct. (2017) 222:3319–32. 10.1007/s00429-017-1407-1
    1. Cai J, Lee S, Ba F, Garg S, Kim LJ, Liu A, et al. . Galvanic vestibular stimulation (GVS) augments deficient pedunculopontine nucleus (PPN) connectivity in mild Parkinson's Disease: fMRI effects of different stimuli. Front Neurosci. (2018) 12:101. 10.3389/fnins.2018.00101
    1. Wellings TP, Brichta AM, Lim R. Altered neurofilament protein expression in the lateral vestibular nucleus in Parkinson's disease. Exp Brain Res. (2017) 235:3695–708. 10.1007/s00221-017-5092-3
    1. Smith PF. The vestibular system and cognition. Curr Opin Neurol. (2017) 30:84–9. 10.1097/WCO.0000000000000403
    1. Rancz EA, Moya J, Drawitsch F, Brichta AM, Canals S, Margie TW. Widespread vestibular activation of the rodent cortex. J Neurosci. (2015) 35:5926–34. 10.1523/JNEUROSCI.1869-14.2015
    1. Shepherd GM. Corticostriatal connectivity and its role in disease. Nat Rev Neurosci. (2013) 14:278–91. 10.1038/nrn3469
    1. Garcia-Rill E. The basal ganglia and the locomotor regions. Brain Res Rev. (1986) 11:47–63. 10.1016/0165-0173(86)90009-3
    1. Kelley A, Domesick V. The distribution of the projection from the hippocampal formation to the nucleus accumbens in the rat: an anterograde and retrograde-horseradish peroxidase study. Neuroscience (1982) 7:2321–35. 10.1016/0306-4522(82)90198-1
    1. Muskens L. An anatomico-physiological study of the posterior longitudinal bundle in its relation to forced movements. Brain (1914) 36:352–426. 10.1093/brain/36.3-4.352
    1. Muskens L. The central connections of the vestibular nuclei with the corpus striatum, and their significance for ocular movements and for locomotion. Brain (1922) 45:454–78. 10.1093/brain/45.3-4.454
    1. Potegal M, Copack P, de Jong JMBV, Krauthamer G, Gilman S. Vestibular input to the caudate nucleus. Exp Neurol. (1971) 32:448–65. 10.1016/0014-4886(71)90011-2
    1. Liedgren S, Schwarz D. Vestibular evoked potentials in thalamus and basal ganglia of the squirrel monkey (Saimiri sciureus). Acta Otolaryngol. (1976) 81:73–82. 10.3109/00016487609107480
    1. Spiegel EA, Szekely EG, Gildenberg PL. Vestibular responses in midbrain, thalamus, and basal ganglia. Arch Neurol. (1965) 12:258–69. 10.1001/archneur.1965.00460270034005
    1. Segundo J, Machne X. Unitary responses to afferent volleys in lenticular nucleus and claustrum. J Neurophysiol. (1956) 19:325–39. 10.1152/jn.1956.19.4.325
    1. Matsunami K, Cohen B. Afferent modulation of unit activity in globus pallidus and caudate nucleus: changes induced by vestibular nucleus and pyramidal tract stimulation. Brain Res. (1975) 91:140–6. 10.1016/0006-8993(75)90473-4
    1. Barter JW, Castro S, Sukharnikova T, Rossi MA, Yin HH. The role of the substantia nigra in posture control. Eur J Neurosci. (2014) 39:1465–73. 10.1111/ejn.12540
    1. Kim N, Barter JW, Sukharnikova T, Yin HH. Striatal firing rate reflects head movement velocity. Eur J Neurosci. (2014) 40:3481–90. 10.1111/ejn.12722
    1. Stiles L, Reynolds JN, Napper R, Zheng Y, Smith PF. Single neuron activity and c-Fos expression in the rat striatum following electrical stimulation of the peripheral vestibular system. Physiol Reps. (2018) 6:e13791. 10.14814/phy2.13791
    1. Stiles L, Zheng Y, Smith PF. The effects of electrical stimulation of the peripheral vestibular system on the release of neurochemicals in the rat striatum. PLoS ONE (2018) 13:e0205869 10.1371/journal.pone.0205869
    1. Lai H, Tsumori T, Shiroyama T, Yokota S, Nakano K, Yasui Y. Morphological evidence for a vestibulo-thalamo-striatal pathway via the parafascicular nucleus in the rat. Brain Res. (2000) 872:208–14. 10.1016/S0006-8993(00)02457-4
    1. Kim N, Choi MA, Koo H, Park BR, Han SW, Cheong C, et al. . Activation of the thalamic parafascicular nucleus by electrical stimulation of the peripheral vestibular nerve in rats. Exp Brain Res. (2017) 235:1617–25. 10.1007/s00221-016-4864-5
    1. Schulz JM, Redgrave P, Mehring C, Aertsen A, Clements KM, Wickens JR, et al. . Short-latency activation of striatal spiny neurons via subcortical visual pathways. J Neurosci. (2009) 29:6336–6347. 10.1523/JNEUROSCI.4815-08.2009
    1. Giardino L, Zanni M, Pignataro O. DA1 and DA2 receptor regulation in the striatum of young and old rats after peripheral vestibular lesion. Brain Res. (1996) 736:111–7. 10.1016/0006-8993(96)00692-0
    1. Stiles L, Zheng Y, Darlington CL, Smith PF. The D2 dopamine receptor and locomotor hyperactivity following bilateral vestibular deafferentation in the rat. Behav Brain Res. (2012) 227:150–8. 10.1016/j.bbr.2011.11.006
    1. Eugène D, Deforges S, Vibert N, Vidal PP. Vestibular critical period, maturation of central vestibular neurones and locomotor control. Ann NY Acad Sci. (2009) 1164:180–7. 10.1111/j.1749-6632.2008.03727.x
    1. Richter A, Ebert U, Nobrega J, Vallbacka JJ, Fedrowitz M, Löscher W. Immunohistochemical and neurochemical studies on nigral and striatal functions in the circling (ci) rat, a genetic animal model with spontaneous rotational behavior. Neuroscience (1999) 89:461–71. 10.1016/S0306-4522(98)00321-2
    1. Schirmer M, Lessenich A, Lindemann S, Löscher W. Marked differences in response to dopamine receptor antagonism in two rat mutants, ci2 and ci3, with lateralized rotational behavior. Behav Brain Res. (2007) 180:218–25. 10.1016/j.bbr.2007.03.013
    1. Antoine MW, Hubner CA, Arezzo JC, Hebert JM. A causative link between inner ear defects and long term striatal dysfunction. Science (2013) 341:1120–3. 10.1126/science.1240405
    1. Pan L, Qi R, Wang J, Zhou W, Liu J, Cai Y. Evidence for a role of orexin/hypocretin system in vestibular lesion-induced locomotor abnormalities in rats. Front Neurosci. (2016) 10:355. 10.3389/fnins.2016.00355
    1. Besnard S, Tighilet B, Chabert C, Hitier M, Toulouse J, Legall A, et al. . The balance of sleep: role of the vestibular sensory system. Sleep Med Revs. (2018) 42:220–8. 10.1016/j.smrv.2018.09.001
    1. Aitken P, Benoit A, Zheng Y, Philoxene B, Le Gall A, Denise P, et al. . Hippocampal and striatal M1-muscarinic acetylcholine receptors are down-regulated following bilateral vestibular loss in rats. Hippocampus (2016) 26:1509–14. 10.1002/hipo.22651
    1. Benoit A, Guillamin M, Aitken P, Smith PF, Philoxene B, Sola B, et al. . Flow cytometry for receptor analysis from ex-vivo brain tissue in adult rat. J Neurosci Meth. (2018) 304:11–23. 10.1016/j.jneumeth.2018.04.005
    1. Benoit A, Besnard S, Guillamin M, Philoxene B, Sola B, Le Gall A, et al. . Differential regulation of NMDA receptor-expressing neurons in the rat hippocampus and striatum following bilateral vestibular loss demonstrated using flow cytometry. Neurosci Lett. (2018) 683:43–7. 10.1016/j.neulet.2018.06.035
    1. Samoudi G, Nissbrandt H, Dutia MB, Bergquist F. Noisy galvanic vestibular stimulation promotes GABA release in the substantia nigra and improves locomotion in hemiparkinsonian rats. PLoS ONE (2012) 7:e29308. 10.1371/journal.pone.0029308
    1. Bottini G, Sterzi R, Paulesu E, Vallar G, Cappa SF, Erminio F, et al. . Identification of the central vestibular projections in man: a positron emission tomography activation study. Exp Brain Res. (1994) 99:164–9. 10.1007/BF00241421
    1. Lopez C, Blanke O, Mast FW. The human vestibular cortex revealed by coordinate-based activation likelihood estimation meta-analysis. Neuroscience (2012) 212:159–79. 10.1016/j.neuroscience.2012.03.028
    1. Bense S, Stephan T, Yousry TA, Brandt T, Dieterich M. Multisensory cortical signal increases and decreases during vestibular galvanic stimulation (fMRI). J Neurophysiol. (2001) 85:886–99. 10.1152/jn.2001.85.2.886
    1. Vitte E, Derosier C, Caritu Y, Berthoz A, Hasboun D, Soulie D. Activation of the hippocampal formation by vestibular stimulation: a functional magnetic resonance imaging study. Exp Brain Res. (1996) 112:523–6. 10.1007/BF00227958
    1. Emri M, Kisely M, Lengyel Z, Balkay L, Márián T, Mikó L, et al. . Cortical projection of peripheral vestibular signaling. J Neurophysiol. (2003) 89:2639–46. 10.1152/jn.00599.2002
    1. Stephane T, Deutschländer A, Nolte A, Schneider E, Wiesmann M, Brandt T, et al. Functional MRI of galvanic vestibular stimulation with alternating currents at different frequencies. Neuroimage (2005) 26:721–32. 10.1016/j.neuroimage.2005.02.049
    1. Della-Justina HM, Gamba HR, Lukasova K, Nucci-da-Silva MP, Winkler AM, Amaro E, Jr. Interaction of brain areas of visual and vestibular simultaneous activity with fMRI. Exp Brain Res. (2014) 233:1–16. 10.1007/s00221-014-4107-6
    1. Wurthmann S, Naegel S, Schulte Steinberg B, Theysohn N, Diener HC, Kleinschnitz C, et al. . Cerebral gray matter changes in persistent postural perceptual dizziness. J Psychosom Res. (2017) 103:95–101. 10.1016/j.jpsychores.2017.10.007
    1. Jansen NL, Feuerecker R, Becker-Bense S, Zwergal A, Wulff M, Xiong G, et al. Assessment of cerebral dopamine D2/3 formula- receptors in patients with bilateral vestibular failure. J Vest Res. (2014) 24:403–13. 10.3233/VES-140526
    1. Moss F, Ward LM, Sannita WG. Stochastic resonance and sensory information processing: a tutorial and review of application. Clin Neurophysiol. (2004) 115:267–81. 10.1016/j.clinph.2003.09.014
    1. Pal S, Rosengren SM, Colebatch JG. Stochastic galvanic vestibular stimulation produces a small reduction in sway in Parkinson's disease. J Vestib Res. (2009) 19:137–42. 10.3233/VES-2009-0360
    1. Kataoka H, Okada Y, Kiriyama T, Kita Y, Nakamura J, Morioka S, et al. . Can postural instability respond to galvanic vestibular stimulation in patients with Parkinson's Disease? J Mov Disord. (2016) 9:40–43. 10.14802/jmd.15030
    1. Okada Y, Kita Y, Nakamura J, Kataoka H, Kiriyama T, Ueno S, et al. . Galvanic vestibular stimulation may improve anterior bending posture in Parkinson's disease. Neuroreport (2015) 26:405–10. 10.1097/WNR.0000000000000360
    1. Lee S, Kim DJ, Svenkeson D, Parras G, Oishi MM, McKeown MJ. Multifaceted effects of noisy galvanic vestibular stimulation on manual tracking behavior in Parkinson's disease. Front Syst Neurosci. (2015) 9:5. 10.3389/fnsys.2015.00005
    1. Samoudi G, Jivegard M, Mulavara A, Bergquist F. Effects of stochastic vestibular galvanic stimulation and L-DOPA on balance and motor symptoms in patients with Parkinson's Disease. Brain Stimul. (2015) 8:474–80. 10.1016/j.brs.2014.11.019
    1. Khoshnam M, Häner DMC, Kuatsjah E, Zhang X, Menon C. Effects of galvanic vestibular stimulation on upper and lower extremities motor symptoms in Parkinson's Disease. Front Neurosci. (2018) 12:633. 10.3389/fnins.2018.00633
    1. Iwasaki S, Yamamoto Y, Togo F, Kinoshita M, Yoshifuji Y, Fujimoto C, et al. . Noisy vestibular stimulation improves body balance in bilateral vestibulopathy. Neurology (2014) 82:969–975. 10.1212/WNL.0000000000000215
    1. Schniepp R, Boerner JC, Decker J, Jahn K, Brandt T, Wuehr M. Noisy vestibular stimulation improves vestibulospinal function in patients with bilateral vestibulopathy. J Neurol. (2018) 265(Suppl. 1):57–62. 10.1007/s00415-018-8814-y
    1. Goel R, Kofman I, Jeevarajan J. Using Low levels of stochastic vestibular stimulation to improve balance function. PLoS ONE (2015) 10:e0136335. 10.1371/journal.pone.0136335
    1. Pan W, Soma R, Kwak S, Yamamoto Y. Improvement of motor functions by noisy vestibular stimulation in central neurodegenerative disorders. J Neurol. (2008) 255:1657–61. 10.1007/s00415-008-0950-3
    1. Kim DJ, Yogendrakumar V, Chiang J, Ty E, Wang ZJ, McKeown MJ. Noisy galvanic vestibular stimulation modulates the amplitude of EEG synchrony patterns. PLoS ONE (2013) 8:e69055. 10.1371/journal.pone.0069055
    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. (2003) 91:078101. 10.1103/PhysRevLett.91.078101
    1. Acarer A, Karapolat H, Celebisoy N, Ozgen G, Colakoglu Z. Is customized vestibular rehabilitation effective in patients with Parkinson's? NeuroRehabilitation (2015) 37:255–62. 10.3233/NRE-151258
    1. Yousif N, Bhatt H, Bain PG, Nandi D, Seemungal BM. The effect of pedunculopontine nucleus deep brain stimulation on postural sway and vestibular perception. Eur J Neurol. (2016) 23:668–70. 10.1111/ene.12947
    1. Hitier M, Sato G, Zhang Y, Zheng Y, Besnard S, Smith PF, et al. . Anatomy and surgical approach to rat's vestibular sensors and nerves. J Neurosci Meth. (2016) 270:1–8. 10.1016/j.jneumeth.2016.05.013
    1. Hitier M, Sato G, Zhang Y, Zheng Y, Besnard S, Smith PF. Vestibular-related eye movements in the rat following selective electrical stimulation of the vestibular sensors. J Comp Physiol A (2018) 204:835–47. 10.1007/s00359-018-1286-9

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