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Galvanic vestibular stimulation: a novel modulatory countermeasure for vestibular-associated movement disorders

Estimulação galvânica vestibular para corrigir transtornos neurológicos associados à disfunção vestibular

Abstracts

Motion sickness or kinetosis is the result of the abnormal neural output originated by visual, proprioceptive and vestibular mismatch, which reverses once the dysfunctional sensory information becomes coherent. The space adaptation syndrome or space sickness relates to motion sickness; it is considered to be due to yaw, pith, and roll coordinates mismatch. Several behavioural and pharmacological measures have been proposed to control these vestibular-associated movement disorders with no success. Galvanic vestibular stimulation has the potential of up-regulating disturbed sensory-motor mismatch originated by kinetosis and space sickness by modulating the GABA-related ion channels neural transmission in the inner ear. It improves the signal-to-noise ratio of the afferent proprioceptive volleys, which would ultimately modulate the motor output restoring the disordered gait, balance and human locomotion due to kinetosis, as well as the spatial disorientation generated by gravity transition.

kinetosis; spatial orientation; galvanic vestibular stimulation; movement disorders; space adaptation syndrome; GABA


A cinetose ou doença do movimento resulta de uma resposta neural anormal originada do desequilíbrio entre estímulos visuais, proprioceptivos e vestibulares, que melhora quando esse desequilíbrio é corrigido. A síndrome de adaptação espacial ou doença do espaço está relacionada à doença do movimento e é desencadeada por mudanças bruscas de direção, inclinação e rotação da cabeça. Têm sido propostas várias medidas comportamentais e farmacológicas para controlar esses transtornos do movimento associados com o sistema vestibular, mas sem sucesso. A estimulação galvânica vestibular pode regular o desequilíbrio sensitivo-motor causado pela cinetose e pela doença do espaço modulando os canais iônicos GABA, relacionados à transmissão de impulsos nervosos no ouvido interno. Essa estimulação melhora a relação sinal-ruído dos impulsos proprioceptivos que acabam modulando a resposta motora, restabelecendo o equilíbrio e a marcha, recuperando a desorientação espacial causada pelos diversos gradientes de gravidade.

enjoo de movimento; orientação aeroespacial; estimulação galvânica vestibular; distúrbios do movimento; síndrome de adaptação aeroespacial; GABA


Motion sickness (MS) or kinetosis is a sensory-motor dysfunction caused by a mismatch between the visually perceived movement and its neural integration with the proprioceptive and vestibular system 1. Shupak A, Gordon C. Motion sickness: advances in pathogenesis, prediction, prevention, and treatment. Aviat Space Environ Med 2006;77:1213-1223. , 2. Rainford D, Gradwell D. Ernsting’s Aviation Medicine, 3 rd Ed., London, Hodder Arnold, 2006. . As a result of this mismatch balance, gait and locomotion anomalies appear, which worsens the disabling dysautonomia that such mismatch originates 1. Shupak A, Gordon C. Motion sickness: advances in pathogenesis, prediction, prevention, and treatment. Aviat Space Environ Med 2006;77:1213-1223. , 3. National transportation safety board (NTSB). Annual Review of General Aviation Accident Data 2005, NTSB, Washington DC, 2009.

. Rizzo-Sierra CV, Leon-Sarmiento FE. Pathophysiology of movement disorders due to gravity transitions: The channelopathy linkage in human balance and locomotion. Med Hypoth 2011;77:97-100.
- 5. Valderrama C, Calderón A, Malpica D, Leon-Sarmiento FE. Non invasive autonomous evaluation: proven priciples and posible practices. Actual Enferm 2007;10:17-24. . These neural disorders debut during land, marine, and aerospace motion, among others conditions 1. Shupak A, Gordon C. Motion sickness: advances in pathogenesis, prediction, prevention, and treatment. Aviat Space Environ Med 2006;77:1213-1223. , 2. Rainford D, Gradwell D. Ernsting’s Aviation Medicine, 3 rd Ed., London, Hodder Arnold, 2006. . MS can be developed in up to 39% of airplane pilot students 6. Davis J, Johnson R, Stepanek J, Fogarty J. Fundamentals of Aerospace Medicine, 4 th Ed., Houston (TX), Lippincott Williams and Wilkins, 2008. , 7. Lucertini M, Lugli V, Casagrande M, Trivelloni P. Effects of airsickness in male and female student pilots: adaptation rates and 4-year outcomes. Aviat Space Environ Med 2008;79:677-684. . Of remark, kinetosis is present in up to 91% of the human factors involved in aerial accidents 3. National transportation safety board (NTSB). Annual Review of General Aviation Accident Data 2005, NTSB, Washington DC, 2009. . Despite repeated exposure to environmental conditions simulating kinetosis, MS appears in up to 70% of civilian and military airplane pilots while they are under training in flight simulators 2. Rainford D, Gradwell D. Ernsting’s Aviation Medicine, 3 rd Ed., London, Hodder Arnold, 2006. , 4. Rizzo-Sierra CV, Leon-Sarmiento FE. Pathophysiology of movement disorders due to gravity transitions: The channelopathy linkage in human balance and locomotion. Med Hypoth 2011;77:97-100. , 6. Davis J, Johnson R, Stepanek J, Fogarty J. Fundamentals of Aerospace Medicine, 4 th Ed., Houston (TX), Lippincott Williams and Wilkins, 2008. . Although a good number of investigations have been done 8. Lackner J, DiZio P. Space motion sickness. Exp Brain Res 2006;175:377-399. , the pathophysiology of MS is far from understood.

Space adaptation syndrome (SAS) or space sickness, on the other hand, is a disorder that relates to MS, which is experienced by almost 50% of people traveling out of the Earth 4. Rizzo-Sierra CV, Leon-Sarmiento FE. Pathophysiology of movement disorders due to gravity transitions: The channelopathy linkage in human balance and locomotion. Med Hypoth 2011;77:97-100. , 6. Davis J, Johnson R, Stepanek J, Fogarty J. Fundamentals of Aerospace Medicine, 4 th Ed., Houston (TX), Lippincott Williams and Wilkins, 2008. , 8. Lackner J, DiZio P. Space motion sickness. Exp Brain Res 2006;175:377-399. . It is believed that SAS is due to yaw, pith, and roll coordinates mismatch 6. Davis J, Johnson R, Stepanek J, Fogarty J. Fundamentals of Aerospace Medicine, 4 th Ed., Houston (TX), Lippincott Williams and Wilkins, 2008. , 8. Lackner J, DiZio P. Space motion sickness. Exp Brain Res 2006;175:377-399. . SAS accentuates with longer exposure to the stimulus that generates it, a situation that may lead to quit the career of the pilot at earlier times than planned 2. Rainford D, Gradwell D. Ernsting’s Aviation Medicine, 3 rd Ed., London, Hodder Arnold, 2006. , 4. Rizzo-Sierra CV, Leon-Sarmiento FE. Pathophysiology of movement disorders due to gravity transitions: The channelopathy linkage in human balance and locomotion. Med Hypoth 2011;77:97-100. , 6. Davis J, Johnson R, Stepanek J, Fogarty J. Fundamentals of Aerospace Medicine, 4 th Ed., Houston (TX), Lippincott Williams and Wilkins, 2008. . In addition, SAS possesses a risk of sudden disability in flight, as well as in the cabin of the plane 6. Davis J, Johnson R, Stepanek J, Fogarty J. Fundamentals of Aerospace Medicine, 4 th Ed., Houston (TX), Lippincott Williams and Wilkins, 2008. , 8. Lackner J, DiZio P. Space motion sickness. Exp Brain Res 2006;175:377-399.

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- 1515 . Valderrama C, Forster E. Coronary artery disease in airline transport pilots: part 2 of 2. Aviat Space Environ Med 2010;81:323. . Thus, SAS may endanger passengers, crew members and ground staff. In line with this, up to 29% of aerial accidents are considered to be due to the loss of control in aircrafts, most likely due to aerospace-related sickness 3. National transportation safety board (NTSB). Annual Review of General Aviation Accident Data 2005, NTSB, Washington DC, 2009. . Since not all airplanes’ pilot and astronauts experience SAS, it is presumed that very elaborated mechanisms have to play a role to produce it. Among them, inherited point mutations of ionic channel structures in the inner ear canal, and ethnic differences still under looked are good candidates to lead the ion channels to become dysfunctional whenever gravity changes appear 4. Rizzo-Sierra CV, Leon-Sarmiento FE. Pathophysiology of movement disorders due to gravity transitions: The channelopathy linkage in human balance and locomotion. Med Hypoth 2011;77:97-100. , 1616 . Leon-Sarmiento FE, Rizzo-Sierra CV, Gonzalez-Castaño A. Modeling the effects of gravity transitions in the vestibular system: Preliminary findings. Neurology 2012;78(Suppl):S6-S42. . Whether these channel disorders are responsible for abnormal spreading of neuronal waves following gravity transition remains to be clarified, but it is intuitively possible 1717 . Wiedemann M, Hanke W. Gravity sensing in the central nervous system. J Gravit Physiol 2002;9:43-44. . It is also quite likely that individuals with the highly sensitive neurobiological trait are more vulnerable to be affected by SAS 1818 . Rizzo-Sierra CV, Leon-S M, Leon-Sarmiento FE. Higher sensory processing sensitivity, introversion and ectomorphism: New biomarkers for human creativity in developing rural areas J Neurosci Rural Pract 2012;3:159-162. , 1919 . Rizzo-Sierra CV, Duran M, Leon-Sarmiento FE. Highly sensitive trait and ectomorphism: another link on creativity and psychopathology. Can J Psychiatry 2011;56:702-703. . Despite the aforementioned theories postulated in the etiology of SAS 4. Rizzo-Sierra CV, Leon-Sarmiento FE. Pathophysiology of movement disorders due to gravity transitions: The channelopathy linkage in human balance and locomotion. Med Hypoth 2011;77:97-100. , 8. Lackner J, DiZio P. Space motion sickness. Exp Brain Res 2006;175:377-399. , 1616 . Leon-Sarmiento FE, Rizzo-Sierra CV, Gonzalez-Castaño A. Modeling the effects of gravity transitions in the vestibular system: Preliminary findings. Neurology 2012;78(Suppl):S6-S42. , 2020 . Legner K. Humans in space & space biology, United Nations office for outer space affairs, Vienna, 2003. , the precise mechanism for this disorder – similarly as it has happened in kinetosis – is still unclear.

Current interventions in MS and SAS

When individuals develop MS they show self-consistent patterns of pathophysiological variations that constitute a personal signature, which remains unchanged across multiple provocative exposures 8. Lackner J, DiZio P. Space motion sickness. Exp Brain Res 2006;175:377-399. . Thus, autogenic feedback training has been proposed as a measure to prevent space and terrestrial MS 8. Lackner J, DiZio P. Space motion sickness. Exp Brain Res 2006;175:377-399. . Using this technique, individuals are trained to detect subtle changes in heart rate, respiration, and skin temperature among other parameters 8. Lackner J, DiZio P. Space motion sickness. Exp Brain Res 2006;175:377-399. , 2121 . Zajonc T, Roland P. Vertigo and motion sickness. Part I: vestibular anatomy and physiology. Ear Nose Throat J 2005; 58:1-4. , 2222 . Zajonc T, Roland P. Vertigo and motion sickness. Part II pharmacologic treatment. Ear Nose Throat J 2006;85:25-35. . People trained to keep in balance these physiological parameters are believed to become resistant to MS 8. Lackner J, DiZio P. Space motion sickness. Exp Brain Res 2006;175:377-399. , 2222 . Zajonc T, Roland P. Vertigo and motion sickness. Part II pharmacologic treatment. Ear Nose Throat J 2006;85:25-35. . In theory, motion abnormalities originated by kinetosis should revert when visual, proprioceptive and vestibular input becomes coherent, which is the main goal of this type of intervention 2020 . Legner K. Humans in space & space biology, United Nations office for outer space affairs, Vienna, 2003. , 2222 . Zajonc T, Roland P. Vertigo and motion sickness. Part II pharmacologic treatment. Ear Nose Throat J 2006;85:25-35. . However, current studies indicate that astronauts do not benefit from autogenic feedback training, thus providing little hope that SAS as well as MS could be prevented or attenuated by this type of intervention 8. Lackner J, DiZio P. Space motion sickness. Exp Brain Res 2006;175:377-399. .

Pharmacological approaches have also been undertaken to control kinetosis and SAS, without success. For example, medications prescribed to airplane pilots for short periods of time during commercial flights, and under strict medical supervision 2222 . Zajonc T, Roland P. Vertigo and motion sickness. Part II pharmacologic treatment. Ear Nose Throat J 2006;85:25-35. have impaired their flight performance. Promethazine, the most common medication used to treat space sickness 8. Lackner J, DiZio P. Space motion sickness. Exp Brain Res 2006;175:377-399. , prevents adaptation or hinders learning. Thus, there is still concern that medications would delay sensory-motor adaptation in people exposed to aerospace environments, among other side effects 8. Lackner J, DiZio P. Space motion sickness. Exp Brain Res 2006;175:377-399. .

Similarly, interventions proposed to improve the quality of life of people suffering SAS have fallen short to prevent it 6. Davis J, Johnson R, Stepanek J, Fogarty J. Fundamentals of Aerospace Medicine, 4 th Ed., Houston (TX), Lippincott Williams and Wilkins, 2008. , 2121 . Zajonc T, Roland P. Vertigo and motion sickness. Part I: vestibular anatomy and physiology. Ear Nose Throat J 2005; 58:1-4. ; further, they have also been inefficient to improve spatial disorientation and flight maneuverability 2. Rainford D, Gradwell D. Ernsting’s Aviation Medicine, 3 rd Ed., London, Hodder Arnold, 2006. , 6. Davis J, Johnson R, Stepanek J, Fogarty J. Fundamentals of Aerospace Medicine, 4 th Ed., Houston (TX), Lippincott Williams and Wilkins, 2008. . Else, they are expensive and may affect aviation safety 2. Rainford D, Gradwell D. Ernsting’s Aviation Medicine, 3 rd Ed., London, Hodder Arnold, 2006. , 6. Davis J, Johnson R, Stepanek J, Fogarty J. Fundamentals of Aerospace Medicine, 4 th Ed., Houston (TX), Lippincott Williams and Wilkins, 2008. , 8. Lackner J, DiZio P. Space motion sickness. Exp Brain Res 2006;175:377-399. . Of note, SAS re-appears on veteran astronauts during subsequent flights 2323 . Freeman M. Challenges of human space exploration, Chichester (West Sussex), Praxis Publishing, 2006. . It means that this condition is resistant to habituation procedures 2323 . Freeman M. Challenges of human space exploration, Chichester (West Sussex), Praxis Publishing, 2006. , which parallels kinetosis-resistant habituation 2. Rainford D, Gradwell D. Ernsting’s Aviation Medicine, 3 rd Ed., London, Hodder Arnold, 2006. , 6. Davis J, Johnson R, Stepanek J, Fogarty J. Fundamentals of Aerospace Medicine, 4 th Ed., Houston (TX), Lippincott Williams and Wilkins, 2008. .

Noteworthy, using a computational model, we recently demonstrated that gravity changes affect semicircular canals similarly as galvanic vestibular stimulation (GVS) does in humans, which in turn simulates SAS-like effects 1616 . Leon-Sarmiento FE, Rizzo-Sierra CV, Gonzalez-Castaño A. Modeling the effects of gravity transitions in the vestibular system: Preliminary findings. Neurology 2012;78(Suppl):S6-S42. . Of remark, the scientific literature is plenty of reports demonstrating the disordered motor output effects generated by GVS, and it is very scarce on the benefits that this non-invasive intervention may produce to humans. Interestingly, there is growing scientific evidence that supports the use of GVS as a novel and powerful neurorehabilitation measure in a number of movement disorders. Therefore, we anticipate that customized GVS can restore the abnormal human balance, gait and locomotion happening in the Earth, the moon, Mars and elsewhere.

Technical aspects of GVS

GVS is an non-invasive neural intervention developed since several centuries ago that is still overlooked in modern textbooks 2424 . Wassermann E, Epstein C, Ziemann U, Walsh V, Paus T, Lisanby S. The Oxford Handbook of Transcranial Stimulation, Oxford, Oxford University Press, 2008. , 2525 . Lisanby S. Brain stimulation in Psychiatry treatment, Arlington, American Psychiatric Publishing, 2004. . The galvanic stimulus is delivered by a controlled current source by means of a switch and a battery which usually does not exceed 9 V 2626 . Fitzpatrick R, Day B. Probing the human vestibular system with galvanic stimulation. J Appl Physiol 2004;96:2301-2316. . The current is delivered transcutaneously at levels of ~ 1mA, which reaches vestibular afferents, modulating neural firing 2626 . Fitzpatrick R, Day B. Probing the human vestibular system with galvanic stimulation. J Appl Physiol 2004;96:2301-2316. , 2727 . Pan W, Soma R, Kwak S, Yamamoto Y. Improvement of motor functions by noisy vestibular stimulation in central neurodegenerative disorders. J Neurol 2008;255:1657-1661. . Although the stimulators used to generate the GVS are essentially similar, the changes in body perception, movement and spatial location that GVS produces are based upon wave configuration, polarity, intensity, duration, timing and frequency of the stimulation, and number and placement of the stimulating electrodes 2828 . Ghanim Z, Lamy J, Lackmy A, et al. Effects of galvanic mastoid stimulation in seated human subjects. J Appl Physiol 2009;106:893-903.

29 . Kennedy P, Inglis T. Interaction effects of galvanic vestibular stimulation and head position on the soleus H reflex in humans. Clin Neurophysiol 2002;113:1709-1714.
- 3030 . Saj A, Honore J, Rousseaux M. Perception of the vertical in patients with right hemispheric lesion: Effect of galvanic vestibular stimulation. Neuropsychologia 2006;44:1509-1512. .

Briefly, bilateral bipolar GVS is the mode most commonly used ( Figure 1 ). In this case, the anode is placed on the mastoid process behind one ear, and the cathode behind the other ear 2727 . Pan W, Soma R, Kwak S, Yamamoto Y. Improvement of motor functions by noisy vestibular stimulation in central neurodegenerative disorders. J Neurol 2008;255:1657-1661. . The reference or ground signal is usually placed at the forehead. The signal originated from the semicircular canals during bilateral bipolar GVS mode originates a large roll and small yaw, both toward the cathodal side. Hence, the observed sway toward the anodal side appears to be the appropriate balance response. Another type of stimulation is called bilateral monopolar. In this case, electrodes with the same polarity are placed in both ears, and a distant reference electrode is used. This type of GVS mode produces a semicircular canal signal of a small backward pitch with no roll component. Thus, the subjects sway forward with cathodal GVS on both sides and backward with anodal GVS on both sides. Another stimulation mode is called unilateral GVS mode. In this instance, the stimulating electrode is placed in one mastoid and the nonstimulating electrode is placed on the forehead, or in more distant regions such as the arm 3131 . Tokita T, Ito Y, Miyata H, Koizumi H. Labyrinthine control of upright posture in humans. In: Tokita T, Ito Y, Miyata H, Koizumi H (Eds.). Progress in Brain Research. Amsterdam: Elsevier 1988:291–295. . This mode of GVS evokes sway responses with an oblique trajectory 3232 . Severac Cauquil A, Gervet MF, Ouaknine M. Body response to binaural monopolar galvanic vestibular stimulation in humans. Neurosci Lett 1998;245: 37–40. , 3333 . Severac Cauquil A, Martinez P, Ouaknine M, Tardy-Gervet MF. Orientation of the body response to galvanic stimulation as a function of the inter-vestibular imbalance. Exp Brain Res 2000;133: 501–505. . The lateral component of the oblique sway produced by unilateral GVS mode is either toward an anodal electrode or away from a cathodal electrode; however, the amount of sway is similar.

Figure 1
. Schematic representation of GVS. Left: bilateral bipolar mode with the anode (A) and the cathode (C) placed retromastoideally. Center: unilateral mode with the cathode placed on the forehead. Right: bilateral monopolar mode with the anode placed elsewhere in the body. A sinusoidal current waveform is shown for didactic purposes.

The galvanic current can also be modulated, with modifications owed to the aims of the study. In some cases, the stimulus is delivered in a continuous varying sinusoidal form 3434 . Coats A. The sinusoidal galvanic body-sway response. Acta Otolaryngol 1972;74:155–162. , 3535 . Petersen H, Magnusson M, Fransson PA, Johansson R. Vestibular disturbance at frequencies above 1 Hz affects human postural control. Acta Otolaryngol 1994;114:225–230. . In other occasions stochastic 3636 . Fitzpatrick R, Burke D, Gandevia SC. Loop gain of reflexes controlling human standing measured with the use of postural and vestibular disturbances. J Neurophysiol 1996;76:3994–4008. , 3737 . Pavlik AE, Inglis JT, Lauk M, Oddsson L, Collins JJ. The effects of stochastic galvanic vestibular stimulation on human postural sway. Exp Brain Res 1999;124:273–280. waveforms of alternating polarity have been used. These stimuli roughly modulate afferent firing similarly to the action exerted by the continuous tonic stimulus originated by the other modes of stimulation above mentioned.

Neurofunctional aspects of GVS

Very few or none adverse effects have been reported in humans; if any, they consist of mild sensations of transient retroauricular vibrations 3838 . Murofushi T, Iwasaki S, Ozeki H, Ushio M, Chihara Y. Tone burst–galvanic ratio of vestibular evoked myogenic potential amplitudes: a new parameter of vestibular evoked myogenic potential? Clin Neurophysiol 2007;118:1685-1690.

39 . Murofushi T, Takegoshi H, Ohki H, Ozeki H. Galvanic-evoked myogenic responses in patients with an absence of click-evoked vestibulo-collic reflexes. Clin Neurophysiol 2002;113:305-309.

40 . Rosengren S, Colebatch J. Cervical dystonia responsive to acoustic and galvanic vestibular stimulation. Mov Disord 2006;21:1495-1499.
- 4141 . Rorsman I, Magnusson M, Johansson B. Reduction of visuo-spatial neglect with vestibular galvanic stimulation. Scand J Rehab Med 1999;31:117-124. . This makes GVS unique, compared to other vestibular modulatory stimulations such as the caloric one 3838 . Murofushi T, Iwasaki S, Ozeki H, Ushio M, Chihara Y. Tone burst–galvanic ratio of vestibular evoked myogenic potential amplitudes: a new parameter of vestibular evoked myogenic potential? Clin Neurophysiol 2007;118:1685-1690.

39 . Murofushi T, Takegoshi H, Ohki H, Ozeki H. Galvanic-evoked myogenic responses in patients with an absence of click-evoked vestibulo-collic reflexes. Clin Neurophysiol 2002;113:305-309.
- 4040 . Rosengren S, Colebatch J. Cervical dystonia responsive to acoustic and galvanic vestibular stimulation. Mov Disord 2006;21:1495-1499. . GVS polarizes the vestibular nerves, which means that GVS separates and accumulate positive and negative electric charges in two distinct regions of the mentioned nerves. This process activates the semicircular canals, otolith organs, and the adjacent vestibular nerves 2626 . Fitzpatrick R, Day B. Probing the human vestibular system with galvanic stimulation. J Appl Physiol 2004;96:2301-2316. , 2727 . Pan W, Soma R, Kwak S, Yamamoto Y. Improvement of motor functions by noisy vestibular stimulation in central neurodegenerative disorders. J Neurol 2008;255:1657-1661. . Thus, GVS modulates posture and balance relationship 4242 . Orlov I, Stolbkov Y, Shuplyakov V. Effects of artificial feedback to the vestibular input on postural instability induced by asymmetric proprioceptive stimulation. Neurosci Behav Physiol 2008;38:195-201.

43 . Balter S, Castelijns M, Stokroos R, Kingma H. Galvanic-induced body sway in vestibular schwannoma patients: evidence for stimulation of the central vestibular system. Acta Otolaryngol 2004;124:1015-1021.
- 4444 . Monobe H, Murofushi T. Vestibular testing by electrical stimulation in patients with unilateral vestibular deafferentation: galvanic evoked myogenic responses testing versus galvanic body sway testing. Clin Neurophysiol 2004;11:807-811. , oculokinetic responses 9. Valderrama C, Álvarez C. Transmission of diseases in comercial flights: from myth to reality. Infectio 2009;13:203-216. , 3939 . Murofushi T, Takegoshi H, Ohki H, Ozeki H. Galvanic-evoked myogenic responses in patients with an absence of click-evoked vestibulo-collic reflexes. Clin Neurophysiol 2002;113:305-309. and spatial orientation 4545 . Moore S, MacDougall H, Peters B, Bloomberg J, Curthoys I, Cohen H. Modeling locomotor dysfunction following spaceflight with galvanic vestibular stimulation. Exp Brain Res 2006;174:647-659. . The action of GVS has been modeled using vector summation, following stimulation of the pars medialis, bilateral utricular macular and semicircular canals 3838 . Murofushi T, Iwasaki S, Ozeki H, Ushio M, Chihara Y. Tone burst–galvanic ratio of vestibular evoked myogenic potential amplitudes: a new parameter of vestibular evoked myogenic potential? Clin Neurophysiol 2007;118:1685-1690. . Such modeling has demonstrated that vector summation from utricular afferents does not explain the observed sway in people exposed to GVS. Therefore, new hypotheses have been proposed. Some of them have suggested that the otolithic component involved in the balance response originates only from the pars medialis of the utricular macula 2626 . Fitzpatrick R, Day B. Probing the human vestibular system with galvanic stimulation. J Appl Physiol 2004;96:2301-2316. . Further, functional neuroimaging studies have revealed the existence of a complex network of multisensory cortical areas activated by GVS in healthy and ill populations. Such areas include the insular and retroinsular regions, the superior temporal gyrus, temporo-parietal cortex, the basal ganglia and the anterior cingulate gyrus 4646 . Utz K, Dimova V, Oppenländer K, Kerkhoff G. Electrified minds: transcranial direct current stimulation (tDCS) and galvanic vestibular stimulation (GVS) as methods of non-invasive brain stimulation in neuropsychology, a review of current data and future implications. Neuropsychologia 2010;48:2789-2810. , 4747 . Lobel E, Kleine J.F, Bihan D.L, Leroy-Willig A, Berthoz A. Functional MRI of galvanic vestibular stimulation. J Neurophysiol 1998;80:2699–2709. . The parieto-insular vestibular cortex and the temporo-parietal junction area are activated as well in healthy subjects. Interestingly, bilateral activations of vestibular cortices are obtained by applying left-cathodal/right-anodal GVS, whereas unilateral, right-hemispheric activations are induced by right-cathodal/left-anoidal GVS 4646 . Utz K, Dimova V, Oppenländer K, Kerkhoff G. Electrified minds: transcranial direct current stimulation (tDCS) and galvanic vestibular stimulation (GVS) as methods of non-invasive brain stimulation in neuropsychology, a review of current data and future implications. Neuropsychologia 2010;48:2789-2810. , 4848 . Dieterich M, Bense S, Lutz S, et al. Dominance for vestibular cortical function in the non-dominant hemisphere. Cereb Cortex 2003;13:994–1007. .

Mechanisms of GVS

GVS applied at spaced intervals 2727 . Pan W, Soma R, Kwak S, Yamamoto Y. Improvement of motor functions by noisy vestibular stimulation in central neurodegenerative disorders. J Neurol 2008;255:1657-1661. may control abnormal movements secondary to MS, SAS and the like. This would be possible by modulating aberrant action potentials that happen in the sensory-motor mismatch 4. Rizzo-Sierra CV, Leon-Sarmiento FE. Pathophysiology of movement disorders due to gravity transitions: The channelopathy linkage in human balance and locomotion. Med Hypoth 2011;77:97-100. , 1616 . Leon-Sarmiento FE, Rizzo-Sierra CV, Gonzalez-Castaño A. Modeling the effects of gravity transitions in the vestibular system: Preliminary findings. Neurology 2012;78(Suppl):S6-S42. , which follows the abnormal neural re-firing originated by these disorders 4. Rizzo-Sierra CV, Leon-Sarmiento FE. Pathophysiology of movement disorders due to gravity transitions: The channelopathy linkage in human balance and locomotion. Med Hypoth 2011;77:97-100. , 4949 . Zheng H, Qin X, Fu Y. Detection of GABAA alpha 2 mRNA in rat vestibular end organ with in-situ hybridization. Zhonghua Er Bi Yan Hou Ke Za Zhi 2001;36:190-192. , 5050 . Leon-Sarmiento FE, Bayona-Prieto J, Gomez J. Neurophysiology of blepharospasm and multiple system atrophy: clues to its pathophysiology. Parkinsonism Relat Disord 2005;11:199–201. . The restorative action of GVS can be due to the time dependent electric field embedded system that has the potential of modulating GABA receptor signaling given its electromagnetic properties 5151 . Farrant M, Kaila K. The cellular, molecular and ionic basis of GABA (A) receptor signalling. Ptog Brain Res 2007;160:59-87. . As it is widely known, GABA is the main inhibitory neurotransmitter of the mammalian central nervous system that regulates neuronal excitability 5252 . Watanabe M, Maemura K, Kanbara K, Tamayama T, Hatasaki H. GABA and GABA receptors in the central nervous system and other organs. Int Rev Cytol 2002;213:1-47. . In the vestibular end organ, in particular, GABA modulates vestibular afferent nerve firing 5050 . Leon-Sarmiento FE, Bayona-Prieto J, Gomez J. Neurophysiology of blepharospasm and multiple system atrophy: clues to its pathophysiology. Parkinsonism Relat Disord 2005;11:199–201. , 5252 . Watanabe M, Maemura K, Kanbara K, Tamayama T, Hatasaki H. GABA and GABA receptors in the central nervous system and other organs. Int Rev Cytol 2002;213:1-47. . Recent research demonstrated that the GABAergic component of the olivocochlear system also contributes to the long-term homeostasis of key hair cells and related neuronsin the inner ear, which are needed to keep human balance in place 5353 . Maison S, Rosahl T, Homanics G, Liberman M. Functional role of GABAergic innervation of the cochlea: phenotypic analysis of mice lacking GABA receptor subunits. J Neurosci 2006;26:10315-10326. . Likewise, GVS modulates inhibitory activity recorded from the lateral vestibulo-spinal tract and from the spinal motor neuron activity, all of which is linked to GABAergic neural distribution 5454 . Okami K, Sekitani T, Ogata M, et al. GABA distribution in the central vestibular system after retroauricular galvanic stimulation. An immunohistochemical study. Acta Otolaryngol 1991;481(Suppl):S150-S152. . Furthermore, the GABAergic system found in the choclea and inner ear 4949 . Zheng H, Qin X, Fu Y. Detection of GABAA alpha 2 mRNA in rat vestibular end organ with in-situ hybridization. Zhonghua Er Bi Yan Hou Ke Za Zhi 2001;36:190-192. , 5555 . Kempf H, Brandle T, Wisden W, Zenner H, Marx A. Detection of GABA(A) receptor mRNA in cochlear tissue, an in situ hybridization study. HNO 1995;43:12-18. also plays an important role in the efferent modulation of balance and locomotion, postural stability and muscle tone 5252 . Watanabe M, Maemura K, Kanbara K, Tamayama T, Hatasaki H. GABA and GABA receptors in the central nervous system and other organs. Int Rev Cytol 2002;213:1-47. , 5353 . Maison S, Rosahl T, Homanics G, Liberman M. Functional role of GABAergic innervation of the cochlea: phenotypic analysis of mice lacking GABA receptor subunits. J Neurosci 2006;26:10315-10326. , 5656 . Tjernström F, Bagher A, Fransson P. Short and long-term postural learning to withstand galvanic vestibular perturbations. J Vestibular Research 2010;20:407–417. , which has been measured by different means including transcranial magnetic stimulation 5757 . Leon-Sarmiento FE, Granadillo E, Bayona EA. Present and future of the transcranial magnetic stimulation. Inv Clin 2013;54:74-89. , 5858 . Marsden J, Playford D, Day B. The vestibular control of balance after stroke. J Neurol Neurosurg Psychiatry 2005;76:670-678. .

Of remark, GVS would also help to restore balance, gait, equilibrium and locomotion in humans affected not only by MS or SAS, but also by the sensory and motor mismatch following neurodegenerative conditions 2727 . Pan W, Soma R, Kwak S, Yamamoto Y. Improvement of motor functions by noisy vestibular stimulation in central neurodegenerative disorders. J Neurol 2008;255:1657-1661. , 5656 . Tjernström F, Bagher A, Fransson P. Short and long-term postural learning to withstand galvanic vestibular perturbations. J Vestibular Research 2010;20:407–417. . The fact that GVS improves the disordered sensorimotor activity by modulating the abnormal sensoperceptual 2929 . Kennedy P, Inglis T. Interaction effects of galvanic vestibular stimulation and head position on the soleus H reflex in humans. Clin Neurophysiol 2002;113:1709-1714. , 3030 . Saj A, Honore J, Rousseaux M. Perception of the vertical in patients with right hemispheric lesion: Effect of galvanic vestibular stimulation. Neuropsychologia 2006;44:1509-1512. afferent information along with the disturbed motor output in patients with disabling neural disorders, including Parkinson’s disease 5959 . Samoudi G, Nissbrandt H, Dutia M, Bergquist F. Noisy galvanic vestibular stimulation promotes GABA release in the substantia nigra and improves locomotion in hemiparkinsonian rats. PloS One 2012;7:1. , 6060 . Leon-Sarmiento FE, Rizzo-Sierra CV, Bayona E, Bayona-Prieto J, Doty R, Bara-Jimenez W. Novel mechanisms underlying inhibitory and facilitatory transcranial magnetic stimulation abnormalities in Parkinson’s disease. Arch Med Res 2013;44:221-228. , normal pressure hydrocephalus 6161 . Leon-Sarmiento FE, Pradilla G, Zambrano M. Primary and reversible Pisa syndrome in juvenile normal pressure hydrocephalus. Acta Neuropsychiatry 2013;25:57-60. (Leon-Sarmiento et al., unpublished observations), and focal dystonia 4040 . Rosengren S, Colebatch J. Cervical dystonia responsive to acoustic and galvanic vestibular stimulation. Mov Disord 2006;21:1495-1499. , 6262 . Bohlhalter S, Leon-Sarmiento FE, Hallett M. Abnormality of motor cortex excitability in peripherally induced dystonia. Mov Disord 2007;22:1186-1189. supports this view. To prove more efficiently these assumptions, we re-analyzed the results of the effects of GVS in a patient with cervical dystonia 4040 . Rosengren S, Colebatch J. Cervical dystonia responsive to acoustic and galvanic vestibular stimulation. Mov Disord 2006;21:1495-1499. .

GVS and movement disorders

The effects of GVS in the neck muscles of a patient with focal dystonia were mathematically calculated. We measured the number of spikes of at least 50 μV of amplitude 6363 . Battaglia F, Ghilardi MF, Quartarone A, Bagnato S, Girlanda P, Hallett M. Impaired long-term potentiation-like plasticity of the trigeminal blink reflex circuit in Parkinson’s disease. Mov Disord 2006;21:2230-2233. before and after the application of GVS 4040 . Rosengren S, Colebatch J. Cervical dystonia responsive to acoustic and galvanic vestibular stimulation. Mov Disord 2006;21:1495-1499. . The galvanic stimuli were up to 2.5 mA square wave direct current steps of 20-msec duration. The stimuli were generated by an isolated stimulator (Model DS2A; Digitimer, Ltd., Hertfordshire, UK) and delivered to the mastoid processes at a rate of 3 Hz, by means of 20 cm 2. Rainford D, Gradwell D. Ernsting’s Aviation Medicine, 3 rd Ed., London, Hodder Arnold, 2006. self-adhesive electrodes, which were cut from electrosurgical plating (3M, St. Paul, MN) and coated with electrode gel 4040 . Rosengren S, Colebatch J. Cervical dystonia responsive to acoustic and galvanic vestibular stimulation. Mov Disord 2006;21:1495-1499. . The current was delivered with the cathode at the left mastoid and anode at the right, or vice-versa 4040 . Rosengren S, Colebatch J. Cervical dystonia responsive to acoustic and galvanic vestibular stimulation. Mov Disord 2006;21:1495-1499. . After GVS intervention, it was very impressive to observe that the muscle activity displayed by this patient before the intervention, which was 9.2 Hz, was significantly reduced to 1.4 Hz, after intervention (t test, p<0.05) ( Figure 2 ). The most likely explanation for such improvement seemed to be on the benefits exerted in the short latency afferents of the vestibule and trigeminal cervical pathways 6464 . Abrahams VC, Kori AA, Loeb GE, Richmond FJ, Rose PK, Keirstead SA. Facial input to neck motoneurons: trigemino-cervical reflexes in the conscious and anaesthetised cat. Exp Brain Res 1993;97:23-30.

65 . Ertekin C, Celebisoy N, Uludağ B. Trigemino-cervical reflexes in normal subjects. J Neurol Sci 1996;143:84-90.
- 6666 . Deriu F, Tolu E, Rothwell JC. A short latency vestibulomasseteric reflex evoked by electrical stimulation over the mastoid in healthy humans. J Physiol 2003;553:267-279. of this patient. Of remark, these neural pathways use GABA as one of their main neurotransmitters as well 6767 . Chana P, de Marinis A, Barrientos N. Gabapentin and motor fluctuations in Parkinson’s disease. Mov Disord 1997;12:608. .

Figure 2
. Electromyographic activity recorded in the right sternocleidomastoid muscle before (left) and after (right) intervention. Note the significant decrease of the muscle activity after applying GVS (modified from ref. 40).

Recently, limited studies also reported the benefits exerted by the application of GVS in patients with Parkinson’s disease. In one case, a patient who complained of camptocornia received a single session of GVS. Binaural monopolar GVS was applied for 20 minutes. In this stimulation mode, the cathode electrode was placed over each the mastoid process and the anode electrode over the trapezius muscle. Immediately after GVS application, the trunk flexion angle was reduced by 32.1% compared with the values obtained before GVS. This improvement lasted for a month 6868 .Okada Y, kita Y, Nakmura J, Tanizawa M, Morimoto S, Shomoto K. Galvanic vestibular stimulation for camptocormia in Parkinson’s disease. J Nov Physiother 2012:S1:1. . Another study 6969 . Pal S, Rosengren SM, Colebatch JG. Stochastic galvanic vestibular stimulation produces a small reduction in sway in Parkinson’s disease. J Vestib Res 2009;19:137-142. used bicathodal GVS in five patients with Parkinson’s disease. This GVS configuration employs two cathodal mastoid electrodes and one anodal electrode at the C7 vertebra. It was found that 0.1 mA stochastic current reduced the body sway of the patients. The aforementioned results are encouraging to implement novel GVS methodologies looking to improve balance and gait in Parkinson’s disease via modulation of the cholinergic system, without the side effects brought about by classical pharmacological interventions.

Concluding remarks

The easiness, low cost and portability makes GVS a novel countermeasure for restoring abnormal balance, gait and human locomotion in individuals living in different gravity conditions, including the Earth, the moon and elsewhere. In addition, given the encouraging results of GVS in improving motor function in humans 2525 . Lisanby S. Brain stimulation in Psychiatry treatment, Arlington, American Psychiatric Publishing, 2004. , 7070 . Scinicariello A, Eaton K, Inglis J, Collins J. Enhancing human balance control with galvanic vestibular stimulation. Biol Cybern 2001;84:475-480. , we stress out the potential of employing GVS in the rehabilitation of hypo- and hyperkinetic disorders, including those associated to brain and spinal cord injury as well as neurodegeneration that happens at different levels of the neuroaxis 7171 . Bayona-Prieto J, Bayona E, Leon-Sarmiento FE. Neuroplasticity, neuromodulation and neurorehabilitation: Three different concepts, one only true goal. Salud Uninorte 2011;27:95-107. , 7272 . Bayona-Prieto J, Bayona E, Leon-Sarmiento FE. Neurorehabilitation: from a rigid past to a plastic future. Gac Med Mex 2012;48:91-96. . We anticipate that novel vestibular neurorehabilitation and sensorimotor control of human balance, gait and locomotion would be at hand in a near future by customizing GVS interventions. Sooner than later, turning GVS devices ON will make a good number of disabling vestibular-associated neural disorders to turn OFF! ( Figure 3 ).

Figure 3
. Schematic representation of the proposed beneficial effects exerted by GVS in human gait and locomotion. The zig-zag gait recorded from a patient with gait disturbances, while the stimulator is OFF (A) turns to be straight when the stimulator is ON (B) (see text for details).

The authors would like to thank the assistance to an earlier version of this manuscript done by Carolina Valderrama, Melina Ariza, Evan Beals and Daniel S. Leon-Ariza. The guidance and support received from Dr. Richard L. Doty, Dr. Hongasandra R. Nagendra and Eng. Jaime Diaz are also greatly appreciated.

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Publication Dates

  • Publication in this collection
    Jan 2014

History

  • Received
    30 Mar 2013
  • Reviewed
    13 Aug 2013
  • Accepted
    21 Aug 2013
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