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      Galvanic Vestibular Stimulation: Cellular Substrates and Response Patterns of Neurons in the Vestibulo-Ocular Network

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          Abstract

          Galvanic vestibular stimulation (GVS) uses modulated currents to evoke neuronal activity in vestibular endorgans in the absence of head motion. GVS is typically used for a characterization of vestibular pathologies; for studies on the vestibular influence of gaze, posture, and locomotion; and for deciphering the sensory–motor transformation underlying these behaviors. At variance with the widespread use of this method, basic aspects such as the activated cellular substrate at the sensory periphery or the comparability to motion-induced neuronal activity patterns are still disputed. Using semi-intact preparations of Xenopus laevis tadpoles, we determined the cellular substrate and the spatiotemporal specificity of GVS-evoked responses and compared sinusoidal GVS-induced activity patterns with motion-induced responses in all neuronal elements along the vestibulo-ocular pathway. As main result, we found that, despite the pharmacological block of glutamatergic hair cell transmission by combined bath-application of NMDA (7-chloro-kynurenic acid) and AMPA (CNQX) receptor blockers, GVS-induced afferent spike activity persisted. However, the amplitude modulation was reduced by ∼30%, suggesting that both hair cells and vestibular afferent fibers are normally recruited by GVS. Systematic alterations of electrode placement with respect to bilateral semicircular canal pairs or alterations of the bipolar stimulus phase timing yielded unique activity patterns in extraocular motor nerves, compatible with a spatially and temporally specific activation of vestibulo-ocular reflexes in distinct planes. Despite the different GVS electrode placement in semi-intact X. laevis preparations and humans and the more global activation of vestibular endorgans by the latter approach, this method is suitable to imitate head/body motion in both circumstances.

          SIGNIFICANCE STATEMENT Galvanic vestibular stimulation is used frequently in clinical practice to test the functionality of the sense of balance. The outcome of the test that relies on the activation of eye movements by electrical stimulation of vestibular organs in the inner ear helps to dissociate vestibular impairments that cause vertigo and imbalance in patients. This study uses an amphibian model to investigate at the cellular level the underlying mechanism on which this method depends. The outcome of this translational research unequivocally revealed the cellular substrate at the vestibular sensory periphery that is activated by electrical currents, as well as the spatiotemporal specificity of the evoked eye movements, thus facilitating the interpretation of clinical test results.

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          Author and article information

          Journal
          J Neurosci
          J. Neurosci
          jneuro
          jneurosci
          J. Neurosci
          The Journal of Neuroscience
          Society for Neuroscience
          0270-6474
          1529-2401
          31 August 2016
          : 36
          : 35
          : 9097-9110
          Affiliations
          [1] 1Department Biology II,
          [2] 2Graduate School of Systemic Neurosciences, and
          [3] 3German Center for Vertigo and Balance Disorders, Ludwig-Maximilians-University Munich, 82152 Planegg, Germany
          Author notes
          Correspondence should be addressed to Hans Straka, Department Biology II, Ludwig-Maximilians-Universität Munich, Grosshaderner Str. 2, 82152 Planegg, Germany. straka@ 123456lmu.de .

          Author contributions: H.S. designed research; K.D.G., A.-K.K., H.D., F.B., R.B., B.P.C., and H.S. performed research; K.D.G., A.-K.K., H.D., F.B., R.B., B.P.C., and H.S. analyzed data; K.D.G., A.-K.K., H.D., F.B., R.B., B.P.C., and H.S. wrote the paper.

          *K.D.G. and A.K.K. contributed equally to this work.

          Author information
          http://orcid.org/0000-0002-6084-418X
          http://orcid.org/0000-0001-5659-2787
          Article
          PMC6601907 PMC6601907 6601907 4239-15
          10.1523/JNEUROSCI.4239-15.2016
          6601907
          27581452
          dbeafc42-6ed4-4ea5-bfec-3a0aff3b0185
          Copyright © 2016 the authors 0270-6474/16/369097-14$15.00/0
          History
          : 25 November 2015
          : 12 July 2016
          : 14 July 2016
          Categories
          Articles
          Systems/Circuits

          hair cells,inner ear, Xenopus laevis ,vestibular,galvanic stimulation,extraocular motor

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