Human Postural Responses to High Vestibular Specific Extremely Low-Frequency Magnetic Stimulations

Background: International agencies recognize the lack of knowledge to further establish standards and guidelines to protect the workers and the public from extremely low-frequency magnetic fields (ELF-MF). In that regard, postural control has been proposed as a biomarker of potential adverse effects in humans. Considering its crucial role in postural control and its specific neurophysiological characteristics, the vestibular system emerges as an ELF-MF likely target. However, postural modulation to vestibular ELF-MF exposure remains inconclusive. Previous studies led us to investigate stimulation orientation and point of application to clarify the ELF-MF impact on balance in humans. Objectives: This research aimed to investigate the acute postural impact of lateral vestibular-specific ELF-MF stimulations. Methods: Postural control of thirty eight healthy participants was analyzed with lateral vestibular-specific ELF-MF stimulations ranging from 20 Hz to 160 Hz, up to 142 T/s and vestibular electrical stimulations at the same frequencies. Both spatial orientation and quantity of movement variables were used to investigate postural modulations. Results: Despite a conclusive positive control effect, no significant effects of ELF-MF and alternating current stimulation exposures were found regardless of frequency conditions. Conclusions: Although important electric fields were generated, no postural modulation was found. However, at these frequencies, the potential vestibular activation did not translate into functional postural sway but might be observed with reflexive vestibular outcomes.

[1]  T. Murofushi,et al.  Vestibular testing by electrical stimulation in patients with unilateral vestibular deafferentation: galvanic evoked myogenic responses testing versus galvanic body sway testing , 2004, Clinical Neurophysiology.

[2]  Ian S. Curthoys,et al.  What Galvanic Vestibular Stimulation Actually Activates , 2012, Front. Neur..

[3]  P. Å. Öberg,et al.  Magnetophosphenes: a quantitative analysis of thresholds , 1980, Medical and Biological Engineering and Computing.

[4]  Michael A. Gresty,et al.  CLINICAL NEUROPHYSIOLOGY OF THE VESTIBULAR SYSTEM, 3RD EDN , 2002 .

[5]  Gaps in Knowledge Relevant to the “Guidelines for Limiting Exposure to Time-Varying Electric and Magnetic Fields (1 Hz–100 kHz)” , 2020, Health physics.

[6]  Peter Dalgaard,et al.  R Development Core Team (2010): R: A language and environment for statistical computing , 2010 .

[7]  Satoshi Tanaka,et al.  Inter-subject Variability in Electric Fields of Motor Cortical tDCS , 2015, Brain Stimulation.

[8]  H P Zenner,et al.  Electrically evoked motile responses of mammalian type I vestibular hair cells. , 1992, Journal of vestibular research : equilibrium & orientation.

[9]  N. Isu,et al.  Cross‐Striolar and Commissural Inhibition in the Otolith System , 1999, Annals of the New York Academy of Sciences.

[10]  R Johansson,et al.  Vestibular stimulation perturbs human stance also at higher frequencies. , 1995, Acta oto-laryngologica. Supplementum.

[11]  G Michael Halmagyi,et al.  Latency and initiation of the human vestibuloocular reflex to pulsed galvanic stimulation. , 2006, Journal of neurophysiology.

[12]  Mohsen Jamali,et al.  Integration of Canal and Otolith Inputs by Central Vestibular Neurons Is Subadditive for Both Active and Passive Self-Motion: Implication for Perception , 2015, The Journal of Neuroscience.

[13]  Callum J. Osler,et al.  Galvanic Vestibular Stimulation Produces Sensations of Rotation Consistent with Activation of Semicircular Canal Afferents , 2012, Front. Neur..

[14]  Philipp Berens,et al.  CircStat: AMATLABToolbox for Circular Statistics , 2009, Journal of Statistical Software.

[15]  H. Wässle,et al.  Glutamate Receptors in the Rod Pathway of the Mammalian Retina , 2001, The Journal of Neuroscience.

[16]  Maurice Ouaknine,et al.  Orientation of the body response to galvanic stimulation as a function of the inter-vestibular imbalance , 2000, Experimental Brain Research.

[17]  J. Nadal,et al.  Calculation of area of stabilometric signals using principal component analysis , 1996, Physiological measurement.

[18]  Julia Dlugaiczyk,et al.  Galvanic vestibular stimulation: from basic concepts to clinical applications. , 2019, Journal of neurophysiology.

[19]  Kathleen E. Cullen,et al.  The vestibular system: multimodal integration and encoding of self-motion for motor control , 2012, Trends in Neurosciences.

[20]  M. Todd,et al.  Gentamicin vestibulotoxicity impairs human electrically evoked vestibulo-ocular reflex , 2008, Neurology.

[21]  Brian L Day,et al.  Probing the human vestibular system with galvanic stimulation. , 2004, Journal of applied physiology.

[22]  K. Jokela,et al.  Computational dosimetry of induced electric fields during realistic movements in the vicinity of a 3 T MRI scanner. , 2013, Physics in medicine and biology.

[23]  B. Day,et al.  Short-latency eye movements evoked by near-threshold galvanic vestibular stimulation , 2003, Experimental Brain Research.

[24]  H. Straka,et al.  Galvanic Vestibular Stimulation: Cellular Substrates and Response Patterns of Neurons in the Vestibulo-Ocular Network , 2016, The Journal of Neuroscience.

[25]  J. Birchall,et al.  Comparison of body sway analysis techniques. Assessment with subjects standing on a stable surface. , 1994, Acta oto-laryngologica.

[26]  M. Bikson,et al.  Role of cortical cell type and morphology in subthreshold and suprathreshold uniform electric field stimulation in vitro , 2009, Brain Stimulation.

[27]  David R. Wozny,et al.  The electrical conductivity of human cerebrospinal fluid at body temperature , 1997, IEEE Transactions on Biomedical Engineering.

[28]  Jen-Fang Yu,et al.  Anthropometry of external auditory canal by non-contactable measurement. , 2015, Applied ergonomics.

[29]  E. Glowatzki,et al.  Glutamatergic Signaling at the Vestibular Hair Cell Calyx Synapse , 2014, The Journal of Neuroscience.

[30]  Jorge M. Serrador,et al.  Head position modifies cerebrovascular response to orthostatic stress , 2003, Brain Research.

[31]  P. A. Forbes,et al.  Frequency response of vestibular reflexes in neck, back, and lower limb muscles. , 2013, Journal of neurophysiology.

[32]  John Timothy Inglis,et al.  Frequency-specific modulation of vestibular-evoked sway responses in humans. , 2010, Journal of neurophysiology.

[33]  A. Cappello,et al.  Feature selection of stabilometric parameters based on principal component analysis , 2006, Medical and Biological Engineering and Computing.

[34]  E. Hansson,et al.  Effect of vision, proprioception, and the position of the vestibular organ on postural sway , 2010, Acta oto-laryngologica.

[35]  B L Day,et al.  Magnetic field effects on the vestibular system: calculation of the pressure on the cupula due to ionic current-induced Lorentz force , 2012, Physics in medicine and biology.

[36]  K. Fukushima,et al.  The Vestibular System: A Sixth Sense , 2012 .

[37]  G. Michael Halmagyi,et al.  Galvanic ocular vestibular evoked myogenic potentials provide new insight into vestibulo-ocular reflexes and unilateral vestibular loss , 2009, Clinical Neurophysiology.

[38]  Jorge Otero-Millan,et al.  Knowing what the brain is seeing in three dimensions: A novel, noninvasive, sensitive, accurate, and low-noise technique for measuring ocular torsion. , 2015, Journal of vision.

[39]  William H Warren,et al.  A new measure of the CoP trajectory in postural sway: dynamics of heading change. , 2014, Medical engineering & physics.

[40]  I. Curthoys,et al.  The new vestibular stimuli: sound and vibration—anatomical, physiological and clinical evidence , 2017, Experimental Brain Research.

[41]  K. Jokela,et al.  ICNIRP Guidelines GUIDELINES FOR LIMITING EXPOSURE TO TIME-VARYING , 1998 .

[42]  Akimasa Hirata,et al.  An electric field induced in the retina and brain at threshold magnetic flux density causing magnetophosphenes , 2011, Physics in medicine and biology.

[43]  Geoffrey A. Manley.  Vertebrate Hair Cells , 2006 .

[44]  J. P. Reilly,et al.  Magnetic field excitation of peripheral nerves and the heart: a comparison of thresholds , 1991, Medical and Biological Engineering and Computing.

[46]  K. Cullen.  Vestibular processing during natural self-motion: implications for perception and action , 2019, Nature Reviews Neuroscience.

[47]  J. Songer,et al.  Vestibular hair cells and afferents: two channels for head motion signals. , 2011, Annual review of neuroscience.

[48]  Stephen Palmisano,et al.  Frequency‐dependent and montage‐based differences in phosphene perception thresholds via transcranial alternating current stimulation , 2019, Bioelectromagnetics.

[49]  D. Attwell,et al.  Interaction of low frequency electric fields with the nervous system: the retina as a model system. , 2003, Radiation protection dosimetry.

[50]  Christophe Bourdin,et al.  Vestibular signals contribute to the online control of goal-directed arm movements , 2002 .

[51]  Jing Li,et al.  Comparison of Postural Responses to Galvanic Vestibular Stimulation between Pilots and the General Populace , 2015, BioMed research international.

[52]  Nicolas Bouisset,et al.  Human Postural Control Under High Levels of Extremely Low Frequency Magnetic Fields , 2020, IEEE Access.

[53]  Gergely Nagymáté,et al.  Reliability analysis of a sensitive and independent stabilometry parameter set , 2018, PloS one.

[54]  Sarah Khan,et al.  Anatomy of the vestibular system: a review. , 2013, NeuroRehabilitation.

[55]  Alfred C. Schouten,et al.  Task, muscle and frequency dependent vestibular control of posture , 2015, Front. Integr. Neurosci..

[56]  Paola Perin,et al.  Mechanisms and effects of transepithelial polarization in the isolated semicircular canal , 1998, Hearing Research.

[57]  Patrik Raudaschl,et al.  Analysis of Vestibular Labyrinthine Geometry and Variation in the Human Temporal Bone , 2018, Front. Neurosci..

[58]  Nicolas Bouisset,et al.  Impact of extremely low-frequency magnetic fields on human postural control , 2018, Experimental Brain Research.

[59]  Stuart W. Mackenzie,et al.  Ocular torsion responses to sinusoidal electrical vestibular stimulation , 2018, Journal of Neuroscience Methods.

[60]  A. S. French,et al.  Information processing by graded-potential transmission through tonically active synapses , 1996, Trends in Neurosciences.

[61]  L. Parra,et al.  Measurements and models of electric fields in the in vivo human brain during transcranial electric stimulation , 2017, Brain Stimulation.

[62]  Angelo Cappello,et al.  Stabilometric parameters are affected by anthropometry and foot placement. , 2002, Clinical biomechanics.

[63]  Kathleen E. Cullen,et al.  Neural Mechanisms Underlying High-Frequency Vestibulocollic Reflexes In Humans And Monkeys , 2020, The Journal of Neuroscience.