Electrical stimulation of the peripheral and central vestibular system.


Journal

Current opinion in neurology
ISSN: 1473-6551
Titre abrégé: Curr Opin Neurol
Pays: England
ID NLM: 9319162

Informations de publication

Date de publication:
26 Oct 2023
Historique:
pubmed: 27 10 2023
medline: 27 10 2023
entrez: 27 10 2023
Statut: aheadofprint

Résumé

Electrical stimulation of the peripheral and central vestibular system using noninvasive (galvanic vestibular stimulation, GVS) or invasive (intracranial electrical brain stimulation, iEBS) approaches have a long history of use in studying self-motion perception and balance control. The aim of this review is to summarize recent electrophysiological studies of the effects of GVS, and functional mapping of the central vestibular system using iEBS in awake patients. The use of GVS has become increasingly common in the assessment and treatment of a wide range of clinical disorders including vestibulopathy and Parkinson's disease. The results of recent single unit recording studies have provided new insight into the neural mechanisms underlying GVS-evoked improvements in perceptual and motor responses. Furthermore, the application of iEBS in patients with epilepsy or during awake brain surgery has provided causal evidence of vestibular information processing in mostly the middle cingulate cortex, posterior insula, inferior parietal lobule, amygdala, precuneus, and superior temporal gyrus. Recent studies have established that GVS evokes robust and parallel activation of both canal and otolith afferents that is significantly different from that evoked by natural head motion stimulation. Furthermore, there is evidence that GVS can induce beneficial neural plasticity in the central pathways of patients with vestibular loss. In addition, iEBS studies highlighted an underestimated contribution of areas in the medial part of the cerebral hemispheres to the cortical vestibular network.

Identifiants

pubmed: 37889571
doi: 10.1097/WCO.0000000000001228
pii: 00019052-990000000-00122
doi:

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Subventions

Organisme : NIDCD NIH HHS
ID : R01 DC018304
Pays : United States

Informations de copyright

Copyright © 2023 Wolters Kluwer Health, Inc. All rights reserved.

Références

Fitzpatrick RC, Day BL. Probing the human vestibular system with galvanic stimulation. J Appl Physiol (1985) 2004; 96:2301–2316.
Tarnutzer AA, Ward BK, Shaikh AG. Novel ways to modulate the vestibular system: magnetic vestibular stimulation, deep brain stimulation and transcranial magnetic stimulation/transcranial direct current stimulation. J Neurol Sci 2023; 445:120544.
Lopez C. The vestibular system: balancing more than just the body. Curr Opin Neurol 2016; 29:74–83.
Utz KS, Dimova V, Oppenländer K, Kerkhoff G. Electrified minds: transcranial direct current stimulation (tDCS) and galvanic vestibular stimulation (GVS) as methods of noninvasive brain stimulation in neuropsychology--a review of current data and future implications. Neuropsychologia 2010; 48:2789–2810.
Lobel E, Kleine JF, Le Bihan D, et al. Functional MRI of galvanic vestibular stimulation. J Neurophysiol 1998; 80:2699–2709.
Bense S, Stephan T, Yousry TA, et al. Multisensory cortical signal increases and decreases during vestibular galvanic stimulation (fMRI). J Neurophysiol 2001; 85:886–899.
Ruehl RM, Flanagin VL, Ophey L, et al. The human egomotion network. NeuroImage 2022; 264:119715.
Siddiqi SH, Kording KP, Parvizi J, Fox MD. Causal mapping of human brain function. Nat Rev Neurosci 2022; 23:361–375.
Penfield W. Vestibular sensation and the cerebral cortex. Ann Otol Rhinol Laryngol 1957; 66:691–698.
Sluydts M, Curthoys I, Vanspauwen R, et al. Electrical vestibular stimulation in humans: a narrative review. Audiol Neurootol 2020; 25 (1–2):6–24.
Wuehr M, Boerner JC, Pradhan C, et al. Stochastic resonance in the human vestibular system - noise-induced facilitation of vestibulospinal reflexes. Brain Stimulat 2018; 11:261–263.
Shaikh AG, Antoniades C, Fitzgerald J, Ghasia FF. Effects of deep brain stimulation on eye movements and vestibular function. Front Neurol 2018; 9:444.
Dlugaiczyk J, Gensberger KD, Straka H. Galvanic vestibular stimulation: from basic concepts to clinical applications. J Neurophysiol 2019; 121:2237–2255.
Lee S, Liu A, McKeown MJ. Current perspectives on galvanic vestibular stimulation in the treatment of Parkinson's disease. Expert Rev Neurother 2021; 21:405–418.
Forbes PA, Siegmund GP, Schouten AC, Blouin JS. Task, muscle and frequency dependent vestibular control of posture. Front Integr Neurosci 2014; 8:94.
Khosravi-Hashemi N, Forbes PA, Dakin CJ, Blouin JS. Virtual signals of head rotation induce gravity-dependent inferences of linear acceleration. J Physiol 2019; 597:5231–5246.
St George RJ, Day BL, Fitzpatrick RC. Adaptation of vestibular signals for self-motion perception. J Physiol 2011; 589 (Pt 4):843–853.
Peters RM, Rasman BG, Inglis JT, Blouin JS. Gain and phase of perceived virtual rotation evoked by electrical vestibular stimuli. J Neurophysiol 2015; 114:264–273.
Schneider E, Glasauer S, Dieterich M. Comparison of human ocular torsion patterns during natural and galvanic vestibular stimulation. J Neurophysiol 2002; 87:2064–2073.
Forbes PA, Kwan A, Mitchell DE, et al. The neural basis for biased behavioral responses evoked by galvanic vestibular stimulation in primates. J Neurosci 2023; 43:1905–1919.
Forbes PA, Luu BL, Van der Loos HFM, et al. Transformation of vestibular signals for the control of standing in humans. J Neurosci 2016; 36:11510–11520.
Mian OS, Day BL. Violation of the craniocentricity principle for vestibularly evoked balance responses under conditions of anisotropic stability. J Neurosci 2014; 34:7696–7703.
Tisserand R, Dakin CJ, Van der Loos MH, et al. Down regulation of vestibular balance stabilizing mechanisms to enable transition between motor states. eLife 2018; 7:e36123.
Dakin CJ, Inglis JT, Chua R, Blouin JS. Muscle-specific modulation of vestibular reflexes with increased locomotor velocity and cadence. J Neurophysiol 2013; 110:86–94.
Forbes PA, Vlutters M, Dakin CJ, et al. Rapid limb-specific modulation of vestibular contributions to ankle muscle activity during locomotion. J Physiol 2017; 595:2175–2195.
Forbes PA, Kwan A, Rasman BG, et al. Neural mechanisms underlying high-frequency vestibulocollic reflexes in humans and monkeys. J Neurosci 2020; 40:1874–1887.
Keywan A, Jahn K, Wuehr M. Noisy galvanic vestibular stimulation primarily affects otolith-mediated motion perception. Neuroscience 2019; 399:161–166.
Wuehr M, Eder J, Keywan A, Jahn K. Noisy galvanic vestibular stimulation improves vestibular perception in bilateral vestibulopathy. J Neurol 2023; 270:938–943.
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.
Gensberger KD, Kaufmann AK, Dietrich H, et al. Galvanic vestibular stimulation: cellular substrates and response patterns of neurons in the vestibulo-ocular network. J Neurosci 2016; 36:9097–9110.
Lajoie K, Marigold DS, Valdés BA, Menon C. The potential of noisy galvanic vestibular stimulation for optimizing and assisting human performance. Neuropsychologia 2021; 152:107751.
Assländer L, Giboin LS, Gruber M, et al. No evidence for stochastic resonance effects on standing balance when applying noisy galvanic vestibular stimulation in young healthy adults. Sci Rep 2021; 11:12327.
Piccolo C, Bakkum A, Marigold DS. Subthreshold stochastic vestibular stimulation affects balance-challenged standing and walking. PLoS One 2020; 15:e0231334.
Stefani SP, Serrador JM, Breen PP, Camp AJ. Impact of galvanic vestibular stimulation-induced stochastic resonance on the output of the vestibular system: a systematic review. Brain Stimulat 2020; 13:533–535.
McLaren R, Smith PF, Taylor RL, et al. Efficacy of nGVS to improve postural stability in people with bilateral vestibulopathy: a systematic review and meta-analysis. Front Neurosci 2022; 16:1010239.
McLaren R, Smith PF, Taylor RL, et al. Scoping out noisy galvanic vestibular stimulation: a review of the parameters used to improve postural control. Front Neurosci 2023; 17:1156796.
Kwan A, Forbes PA, Mitchell DE, et al. Neural substrates, dynamics and thresholds of galvanic vestibular stimulation in the behaving primate. Nat Commun 2019; 10:1904.
Kim KS, Minor LB, Della Santina CC, Lasker DM. Variation in response dynamics of regular and irregular vestibular-nerve afferents during sinusoidal head rotations and currents in the chinchilla. Exp. Brain Res 2011; 210:643–649.
Goldberg JM, Fernández C, Smith CE. Responses of vestibular-nerve afferents in the squirrel monkey to externally applied galvanic currents. Brain Res 1982; 252:156–160.
Smith CE, Goldberg JM. A stochastic afterhyperpolarization model of repetitive activity in vestibular afferents. Biol Cybern 1986; 54:41–51.
Govindaraju AC, Quraishi IH, Lysakowski A, et al. Nonquantal transmission at the vestibular hair cell-calyx synapse: KLV currents modulate fast electrical and slow K+ potentials. Proc Natl Acad Sci U S A 2023; 120:e2207466120.
Mildren RL, Cullen KE. Vestibular contributions to primate neck postural muscle activity during natural motion. J Neurosci 2023; 43:2326–2337.
Cullen KE. Vestibular processing during natural self-motion: implications for perception and action. Nat Rev Neurosci 2019; 20:346–363.
Eugène D, Idoux E, Beraneck M, et al. Intrinsic membrane properties of central vestibular neurons in rodents. Exp Brain Res 2011; 210:423–436.
Kim G, Lee S, Kim KS. Repeated galvanic vestibular stimulation modified the neuronal potential in the vestibular nucleus. Neural Plast 2020; 2020:5743972.
Carriot J, Jamali M, Brooks JX, Cullen KE. Integration of canal and otolith inputs by central vestibular neurons is subadditive for both active and passive self-motion: implication for perception. J Neurosci 2015; 35:3555–3565.
Zheng Y, Geddes L, Sato G, et al. Galvanic vestibular stimulation impairs cell proliferation and neurogenesis in the rat hippocampus but not spatial memory. Hippocampus 2014; 24:541–552.
Stephan T, Deutschländer A, Nolte A, et al. Functional MRI of galvanic vestibular stimulation with alternating currents at different frequencies. Neuroimage 2005; 26:721–732.
Stephan T, Hüfner K, Brandt T. Stimulus profile and modeling of continuous galvanic vestibular stimulation in functional magnetic resonance imaging. Ann N Y Acad Sci 2009; 1164:472–475.
Rühl M, Kimmel R, Ertl M, et al. In Vivo localization of the human velocity storage mechanism and its core cerebellar networks by means of galvanic-vestibular afternystagmus and fMRI. Cerebellum 2023; 22:194–205.
Hernández-Román J, Montero-Hernández S, Vega R, et al. Galvanic vestibular stimulation activates the parietal and temporal cortex in humans: a functional near-infrared spectroscopy (fNIRS) study. Eur J Neurosci 2023; 58:2267–2277.
Habig K, Krämer HH, Lautenschläger G, et al. Processing of sensory, painful and vestibular stimuli in the thalamus. Brain Struct Funct 2023; 228:433–447.
Huber J, Ruehl M, Flanagin V, Zu Eulenburg P. Delineating neural responses and functional connectivity changes during vestibular and nociceptive stimulation reveal the uniqueness of cortical vestibular processing. Brain Struct Funct 2022; 227:779–791.
Helmchen C, Rother M, Spliethoff P, Sprenger A. Increased brain responsivity to galvanic vestibular stimulation in bilateral vestibular failure. NeuroImage Clin 2019; 24:101942.
Helmchen C, Machner B, Rother M, et al. Effects of galvanic vestibular stimulation on resting state brain activity in patients with bilateral vestibulopathy. Hum Brain Mapp 2020; 41:2527–2547.
Mitsutake T, Sakamoto M, Horikawa E. Comparing activated brain regions between noisy and conventional galvanic vestibular stimulation using functional magnetic resonance imaging. Neuroreport 2021; 32:583–587.
Guldin WO, Grüsser OJ. Is there a vestibular cortex? Trends Neurosci 1998; 21:254–259.
Liu S, Dickman JD, Angelaki DE. Response dynamics and tilt versus translation discrimination in parietoinsular vestibular cortex. Cereb Cortex 2011; 21:563–573.
Chen A, DeAngelis GC, Angelaki DE. Macaque parieto-insular vestibular cortex: responses to self-motion and optic flow. J Neurosci 2010; 30:3022–3042.
Penfield W, Faulk MEJ. The insula: further observations on its functions. Brain 1955; 78:445–470.
Mazzola L, Lopez C, Faillenot I, et al. Vestibular responses to direct stimulation of the human insular cortex. Ann Neurol 2014; 76:609–619.
Yu K, Yu T, Qiao L, et al. Electrical stimulation of the insulo-opercular region: visual phenomena and altered body-ownership symptoms. Epilepsy Res 2018; 148:96–106.
Mazzola L, Mauguière F, Isnard J. Functional mapping of the human insula: data from electrical stimulations. Rev Neurol (Paris) 2019; 175:150–156.
Lopez C, Blanke O. The thalamocortical vestibular system in animals and humans. Brain Res Rev 2011; 67:119–146.
Kahane P, Hoffmann D, Minotti L, Berthoz A. Reappraisal of the human vestibular cortex by cortical electrical stimulation study. Ann Neurol 2003; 54:615–624.
Li Y, Qi L, Schaper FLWVJ, et al. A vertigo network derived from human brain lesions and brain stimulation. Brain Commun 2023; 5:fcad071.
Eickhoff SB, Weiss PH, Amunts K, et al. Identifying human parieto-insular vestibular cortex using fMRI and cytoarchitectonic mapping. Hum Brain Mapp 2006; 27:611–621.
Ibitoye RT, Mallas EJ, Bourke NJ, et al. The human vestibular cortex: functional anatomy of OP2, its connectivity and the effect of vestibular disease. Cereb Cortex 2023; 33:567–582.
Raiser TM, Flanagin VL, Duering M, et al. The human corticocortical vestibular network. NeuroImage 2020; 223:117362.
Balestrini S, Francione S, Mai R, et al. Multimodal responses induced by cortical stimulation of the parietal lobe: a stereo-electroencephalography study. Brain 2015; 138 (Pt 9):2596–2607.
Sun F, Zhang G, Yu T, et al. Functional characteristics of the human primary somatosensory cortex: an electrostimulation study. Epilepsy Behav 2021; 118:107920.
Sun F, Zhang G, Ren L, et al. Functional organization of the human primary somatosensory cortex: a stereo-electroencephalography study. Clin Neurophysiol 2021; 132:487–497.
Schwarz DWF, Fredrickson JM. Rhesus monkey vestibular cortex: a bimodal primary projection field. Science 1971; 172:280–281.
Rancz EA, Moya J, Drawitsch F, et al. Widespread vestibular activation of the rodent cortex. J Neurosci 2015; 35:5926–5934.
Lyu D, Stieger JR, Xin C, et al. Causal evidence for the processing of bodily self in the anterior precuneus. Neuron 2023; 111:2502.e4–2512.e4.
Beer AL, Becker M, Frank SM, Greenlee MW. Vestibular and visual brain areas in the medial cortex of the human brain. J Neurophysiol 2023; 129:948–962.
Guldin WO, Akbarian S, Grüsser OJ. Cortico-cortical connections and cytoarchitectonics of the primate vestibular cortex: a study in squirrel monkeys (Saimiri sciureus). J Comp Neurol 1992; 326:375–401.
Liu B, Tian Q, Gu Y. Robust vestibular self-motion signals in macaque posterior cingulate region. eLife 2021; 10:e64569.
Leong ATL, Gu Y, Chan YS, et al. Optogenetic fMRI interrogation of brain-wide central vestibular pathways. Proc Natl Acad Sci U S A 2019; 116:10122–10129.
Smith AT, Wall MB, Thilo KV. Vestibular inputs to human motion-sensitive visual cortex. Cereb Cortex N Y N 19912012; 22:1068–1077.
Caruana F, Gerbella M, Avanzini P, et al. Motor and emotional behaviours elicited by electrical stimulation of the human cingulate cortex. Brain 2018; 141:3035–3051.
Oane I, Barborica A, Chetan F, et al. Cingulate cortex function and multimodal connectivity mapped using intracranial stimulation. NeuroImage 2020; 220:117059.
Xue Y, Yan H, Hao G, et al. Symptomatic responses elicited by electrical stimulation of the cingulate cortex: study of a cohort of epileptic patients and literature review. Hum Brain Mapp 2023; 44:4498–4511.
Ertl M, Zu Eulenburg P, Woller M, et al. Vestibular mapping of the naturalistic head-centered motion spectrum. J Vestib Res 2023; 33:299–312.
Dary Z, Lenggenhager B, Lagarde S, et al. Neural bases of the bodily self as revealed by electrical brain stimulation: a systematic review. Hum Brain Mapp 2023; 44:2936–2959.
Dieterich M, Kirsch V, Brandt T. Right-sided dominance of the bilateral vestibular system in the upper brainstem and thalamus. J Neurol 2017; 264: (Suppl 1): 55–62.
Qi L, Xu C, Wang X, et al. Intracranial direct electrical mapping reveals the functional architecture of the human basal ganglia. Commun Biol 2022; 5:1123.
Zhang H, Wang D, Wei P, et al. Integrative roles of human amygdala subdivisions: insight from direct intracerebral stimulations via stereotactic EEG. Hum Brain Mapp 2023; 44:3610–3623.
Beylergil SB, Noecker AM, Petersen M, et al. Subthalamic deep brain stimulation affects heading perception in Parkinson's disease. J Neurol 2022; 269:253–268.
Stiles L, Smith PF. The vestibular-basal ganglia connection: balancing motor control. Brain Res 2015; 1597:180–188.
Stiles L, Reynolds JN, Napper R, et al. Single neuron activity and c-Fos expression in the rat striatum following electrical stimulation of the peripheral vestibular system. Physiol Rep 2018; 6:e13791.
Sabzevar FT, Vautrelle N, Zheng Y, Smith PF. Vestibular modulation of the tail of the rat striatum. Sci Rep 2023; 13:4443.
Stiles L, Zheng Y, Smith PF. The effects of electrical stimulation of the peripheral vestibular system on neurochemical release in the rat striatum. PloS One 2018; 13:e0205869.
Balaban CD. Projections from the parabrachial nucleus to the vestibular nuclei: potential substrates for autonomic and limbic influences on vestibular responses. Brain Res 2004; 996:126–137.
Chow MR, Ayiotis AI, Schoo DP, et al. Posture, gait, quality of life, and hearing with a vestibular implant. N Engl J Med 2021; 384:521–532.
Boutros PJ, Schoo DP, Rahman M, et al. Continuous vestibular implant stimulation partially restores eye-stabilizing reflexes. JCI Insight 2019; 4:e128397 128397.
Wiboonsaksakul KP, Roberts DC, Della Santina CC, Cullen KE. A prosthesis utilizing natural vestibular encoding strategies improves sensorimotor performance in monkeys. PLoS Biol 2022; 20:e3001798.
Mitchell DE, Della Santina CC, Cullen KE. Plasticity within noncerebellar pathways rapidly shapes motor performance in vivo. Nat Commun 2016; 7:11238.
Mitchell DE, Della Santina CC, Cullen KE. Plasticity within excitatory and inhibitory pathways of the vestibulo-spinal circuitry guides changes in motor performance. Sci Rep 2017; 7:853.
Tarnutzer AA, Lee SH, Robinson KA, et al. Clinical and electrographic findings in epileptic vertigo and dizziness: a systematic review. Neurology 2015; 84:1595–1604.
Pelliccia V, Avanzini P, Rizzi M, et al. Association between semiology and anatomo-functional localization in patients with cingulate epilepsy: a cohort study. Neurology 2022; 98:e2211–e2223.
Harroud A, Boucher O, Tran TPY, et al. Precuneal epilepsy: clinical features and surgical outcome. Epilepsy Behav 2017; 73:77–82.

Auteurs

Christophe Lopez (C)

Laboratory of Cognitive Neuroscience (LNC), CNRS, Aix Marseille Univ, FR3C, Marseille, France.

Kathleen E Cullen (KE)

Department of Biomedical Engineering.
Department of Otolaryngology-Head and Neck Surgery.
Department of Neuroscience.
Kavli Neuroscience Discovery Institute, Johns Hopkins University, Baltimore, Maryland, USA.

Classifications MeSH