Abstract
Studies have found that extremely low-frequency (ELF, < 300 Hz) magnetic fields (MF) can modulate standing balance; however, the acute balance effects of high flux densities in this frequency range have not been systematically investigated yet. This study explores acute human standing balance responses of 22 participants exposed to magnetic induction at 50 and 100 mTrms (MF), and to 1.5 mA alternating currents (AC). The center of pressure displacement (COP) was collected and analyzed to investigate postural modulation. The path length, the area, the velocity, the power spectrum in low (< 0.5 Hz) and medium (0.5–2 Hz) bands have computed and showed the expected effect of the positive control direct current (DC) electric stimulation but failed to show any significant effect of the time-varying stimulations (AC and MF). However, we showed a significant biased stabilization effect on postural data from the custom experimental apparatus employed in this work, which might have neutralized the hypothesized results.
Similar content being viewed by others
Abbreviations
- AC:
-
Alternative current
- ANOVA:
-
Analysis of variance
- BPPV:
-
Benign paroxysmal positional vertigo
- COP:
-
Center of pressure
- DC:
-
Direct current
- E-fields:
-
Electric field
- ELF:
-
Extremely low-frequency
- GVS:
-
Galvanic vestibular stimulation
- HFB:
-
High frequency band
- ICES:
-
International Committee on Electromagnetic Safety
- ICNIRP:
-
International Commission for Non-Ionizing Radiation Protection
- IEEE:
-
Institute of Electrical and Electronics Engineers
- LFB:
-
Low frequency band
- MF:
-
Magnetic field
- MFB:
-
Medium frequency band
References
Antunes A, Glover PM, Li Y et al (2012) Magnetic field effects on the vestibular system: calculation of the pressure on the cupula due to ionic current-induced Lorentz force. Phys Med Biol 57:4477–4487. https://doi.org/10.1088/0031-9155/57/14/4477
Attwell D (2003) Interaction of low frequency electric fields with the nervous system: the retina as a model system. Radiat Prot Dosimetry 106:341–348
Aw ST, Todd MJ, Aw GE et al (2008) Gentamicin vestibulotoxicity impairs human electrically evoked vestibulo-ocular reflex. Neurology 71:1776–1782. https://doi.org/10.1212/01.wnl.0000335971.43443.d9
Barlow HB, Kohn HI, Walsh EG (1947) Visual sensations aroused by magnetic fields. Am J Physiol 148:372
Bracken TD, Rankin RF, Senior RS et al (2001) Magnetic-field exposures of cable splicers in electrical network distribution vaults. Appl Occup Environ Hyg 16:369–379. https://doi.org/10.1080/10473220118938
Bronstein AM, Guerraz M (1999) Visual-vestibular control of posture and gait: physiological mechanisms and disorders. Curr Opin Neurol 12:5–11. https://doi.org/10.1097/00019052-199902000-00002
Carriot J, Jamali M, Chacron MJ, Cullen KE (2014) Statistics of the vestibular input experienced during natural self-motion: implications for neural processing. J Neurosci 34:8347–8357. https://doi.org/10.1523/JNEUROSCI.0692-14.2014
Cullen KE (2012) The vestibular system: multimodal integration and encoding of self-motion for motor control. Trends Neurosci 35:185–196. https://doi.org/10.1016/j.tins.2011.12.001
Curthoys IS, MacDougall HG (2012) What galvanic vestibular stimulation actually activates. Front Neurol 3:1–5. https://doi.org/10.3389/fneur.2012.00117
Curthoys IS, Grant JW, Burgess AM et al (2018) Otolithic receptor mechanisms for vestibular-evoked myogenic potentials: A review. Front Neurol 9:1–15. https://doi.org/10.3389/fneur.2018.00366
d’Arsonval A (1896) Dispositifs pour la mesure des courants alternatifs de toutes fréquences. Socicété Biol 450–451
Day BL, Guerraz M (2007) Feedforward versus feedback modulation of human vestibular-evoked balance responses by visual self-motion information. J Physiol 582:153–161. https://doi.org/10.1113/jphysiol.2007.132092
Day BL, Steiger MJ, Thompson PD, Marsden CD (1993) Effect of vision and stance width on human body motion when standing: implications for afferent control of lateral sway. J Physiol 469:479–499
Day BL, Séverac Cauquil A, Bartolomei L et al (1997) Human body-segment tilts induced by galvanic stimulation: a vestibularly driven balance protection mechanism. J Physiol 500(Pt 3):661–672. https://doi.org/10.1113/jphysiol.1997.sp022051
Eatock RA (2006) Vertebrate hair cells. Springer, New York
Fitzpatrick RC, Day BL (2004) Probing the human vestibular system with galvanic stimulation. J Appl Physiol 96:2301–2316. https://doi.org/10.1152/japplphysiol.00008.2004
Fitzpatrick R, Burke D, Gandevia SC (1994) Task-dependent reflex responses and movement illusions evoked by galvanic vestibular stimulation in standing humans. J Physiol 478 (Pt 2):363–372. https://doi.org/10.1113/jphysiol.1994.sp020257
Forbes PA, Dakin CJ, Vardy AN et al (2013) Frequency response of vestibular reflexes in neck, back, and lower limb muscles. J Neurophysiol 110:1869–1881. https://doi.org/10.1152/jn.00196.2013
Forbes PA, Siegmund GP, Schouten AC, Blouin J-S (2014) Task, muscle and frequency dependent vestibular control of posture. Front Integr Neurosci 8:94. https://doi.org/10.3389/fnint.2014.00094
Forbes PA, Luu BL, Van der Loos HFM et al (2016) Transformation of vestibular signals for the control of standing in humans. J Neurosci 36:11510–11520. https://doi.org/10.1523/JNEUROSCI.1902-16.2016
Forbes PA, Fice JB, Siegmund GP, Blouin JS (2018) Electrical vestibular stimuli evoke robust muscle activity in deep and superficial neck muscles in humans. Front Neurol 9:1–8. https://doi.org/10.3389/fneur.2018.00535
Foster KR (2003) Mechanisms of interaction of extremely low frequency electric fields and biological systems. Radiat Prot Dosimetry 106:301–310
Gensberger KD, Kaufmann A-K, Dietrich H et al (2016) Galvanic vestibular stimulation: cellular substrates and response patterns of neurons in the vestibulo-ocular network. J Neurosci 36:9097–9110. https://doi.org/10.1523/JNEUROSCI.4239-15.2016
Glover PM, Cavin I, Qian W et al (2007) Magnetic-field-induced vertigo: a theoretical and experimental investigation. Bioelectromagnetics 28:349–361. https://doi.org/10.1002/bem.20316
Glover PM, Li Y, Antunes A et al (2014) A dynamic model of the eye nystagmus response to high magnetic fields. Phys Med Biol 59:631–645. https://doi.org/10.1088/0031-9155/59/3/631
Goldberg JM, Smith CE, Fernández C (1984) Relation between discharge regularity and responses to externally applied galvanic currents in vestibular nerve afferents of the squirrel monkey. J Neurophysiol 51:1236–1256
Goldberg JM, Wilson VJ, Cullen KE, Angelaki DE, Broussard DM, Buttner-Ennever J, Fukushima K, Minor LB (2012) The vestibular system: a sixth sense. Oxford University Press, New York. https://doi.org/10.1093/acprof:oso/9780195167085.001.0001
Hansson EE, Beckman A, Håkansson A (2010) Effect of vision, proprioception, and the position of the vestibular organ on postural sway. Acta Otolaryngol 130:1358–1363. https://doi.org/10.3109/00016489.2010.498024
Hirata A, Takano Y, Fujiwara O et al (2011) An electric field induced in the retina and brain at threshold magnetic flux density causing magnetophosphenes. Phys Med Biol 56:4091–4101. https://doi.org/10.1088/0031-9155/56/13/022
Hlavacka F, Njiokiktjien C (1985) Postural responses evoked by sinusoidal galvanic stimulation of the labyrinth. Acta Otolaryngol 99:107–112
IEEE (2002) C95.6. IEEE standard for safety levels with respect to human exposure to electromagnetic fields, 0–3 kHz. The institute of Electrical and Electronics Engineers, Inc., New York
Inglis JT, Shupert CL, Hlavacka F, Horak FB (1995) Effect of galvanic vestibular stimulation on human postural responses during support surface translations. J Neurophysiol 73:896–901
International Commission on Non-Ionizing Radiation Protection (2010) Guidelines for limiting exposure to time-varying electric and magnetic fields (1 Hz to 100 kHz). Health Phys 99:818–836. https://doi.org/10.1097/HP.0b013e3181f06c86
Jefferys JGR, Deans J, Bikson M, Fox J (2003) Effects of weak electric fields on the activity of neurons and neuronal networks. Radiat Prot Dosimetry 106:321–323
Laakso I, Hirata A (2012) Computational analysis of thresholds for magnetophosphenes. Phys Med Biol 57:6147–6165. https://doi.org/10.1088/0031-9155/57/19/6147
Laakso I, Hirata A (2013) Computational analysis shows why transcranial alternating current stimulation induces retinal phosphenes. J Neural Eng 10:046009. https://doi.org/10.1088/1741-2560/10/4/046009
Laakso I, Tanaka S, Koyama S et al (2015) Inter-subject variability in electric fields of motor cortical tDCS. Brain Stimul 8:906–913. https://doi.org/10.1016/j.brs.2015.05.002
Lang EE, McConn Walsh R (2010) Vestibular function testing. Ir J Med Sci 179:173–178. https://doi.org/10.1007/s11845-010-0465-7
Legros A, Corbacio M, Beuter A et al (2012) Neurophysiological and behavioral effects of a 60 Hz, 1,800 µT magnetic field in humans. Eur J Appl Physiol 112:1751–1762. https://doi.org/10.1007/s00421-011-2130-x
Lövsund P, Öberg P, Nilsson SEG (1980a) Magneto- and electrophosphenes: a comparative study. Med Biol Eng Comput 18:758–764. https://doi.org/10.1007/BF02441902
Lövsund P, Öberg P, Nilsson SEG, Reuter T (1980b) Magnetophosphenes: a quantitative analysis of thresholds. Med Biol Eng Comput 18:326–334. https://doi.org/10.1007/BF02443387
Magnusson M, Enbom H, Johansson R, Wiklund J (1990) Significance of pressor input from the human feet in lateral postural control. The effect of hypothermia on galvanically induced body-sway. Acta Otolaryngol 110:321–327. https://doi.org/10.3109/00016489009107450
Marcelli V, Esposito F, Aragri A et al (2009) Spatio-temporal pattern of vestibular information processing after brief caloric stimulation. Eur J Radiol 70:312–316. https://doi.org/10.1016/j.ejrad.2008.01.042
McIlroy WE, Maki BE (1997) Preferred placement of the feet during quiet stance: development of a standardized foot placement for balance testing. Clin Biomech (Bristol Avon) 12:66–70
Mezei G, Bracken TD, Senior R, Kavet R (2006) Analyses of magnetic-field peak-exposure summary measures. J Expo Sci Environ Epidemiol 16:477–485. https://doi.org/10.1038/sj.jea.7500457
Miranda PC, Lomarev M, Hallett M (2006) Modeling the current distribution during transcranial direct current stimulation. Clin Neurophysiol 117:1623–1629. https://doi.org/10.1016/j.clinph.2006.04.009
Norris CH, Miller AJ, Perin P et al (1998) Mechanisms and effects of transepithelial polarization in the isolated semicircular canal. Hear Res 123:31–40. https://doi.org/10.1016/S0378-5955(98)00096-3
Otero-Millan J, Zee DS, Schubert MC et al (2017) Three-dimensional eye movement recordings during magnetic vestibular stimulation. J Neurol 264:7–12. https://doi.org/10.1007/s00415-017-8420-4
Paillard T, Noé F (2015) Techniques and methods for testing the postural function in healthy and pathological subjects. Biomed Res Int 2015:1–15. https://doi.org/10.1155/2015/891390
Parazzini M, Fiocchi S, Rossi E et al (2011) Transcranial direct current stimulation: estimation of the electric field and of the current density in an anatomical human head model. IEEE Trans Biomed Eng 58:1773–1780. https://doi.org/10.1109/TBME.2011.2116019
Prato FS, Thomas AW, Cook CM (2001) Human standing balance is affected by exposure to pulsed ELF magnetic fields: light intensity-dependent effects. Neuroreport 12:1501–1505. https://doi.org/10.1097/00001756-200105250-00040
R Core Team (2016) R: a language and environment for statistical computing. R Found. Stat. Comput. Vienna Austria 0:{ISBN} 3-900051-07-0
Rankin RF, Bracken TD, Senior RS et al (2002) Results of a multisite study of U.S. residential magnetic fields. J Expo Anal Environ Epidemiol 12:9–20. https://doi.org/10.1038/sj/jea/7500196
Roberts DC, Marcelli V, Gillen JS et al (2011) MRI magnetic field stimulates rotational sensors of the brain. Curr Biol 21:1635–1640. https://doi.org/10.1016/j.cub.2011.08.029
Saunders RD, Jefferys JGR (2002) Weak electric field interactions in the central nervous system. Health Phys 83:366–375
Saunders RD, Jefferys JGR (2007) A neurobiological basis for ELF guidelines. Health Phys 92:596–603. https://doi.org/10.1097/01.HP.0000257856.83294.3e
Stål F, Fransson P, Magnusson M, Karlberg M (2003) Effects of hypothermic anesthesia of the feet on vibration-induced body sway and adaptation. J Vestib Res 13:39–52
Thomas AW, Drost DJ, Prato FS (2001a) Human subjects exposed to a specific pulsed (200 microT) magnetic field: effects on normal standing balance. Neurosci Lett 297:121–124
Thomas AW, White KP, Drost DJ et al (2001b) A comparison of rheumatoid arthritis and fibromyalgia patients and healthy controls exposed to a pulsed (200 microT) magnetic field: effects on normal standing balance. Neurosci Lett 309:17–20
Tinsley JN, Molodtsov MI, Prevedel R et al (2016) Direct detection of a single photon by humans. Nat Commun 7:12172. https://doi.org/10.1038/ncomms12172
Valberg P, Kavet R, Rafferty CN (1997) Can Low-Level 50/60 Hz Electric and Magnetic Fields Cause Biological Effects? Radiat Res 148:2. https://doi.org/10.2307/3579533
van Nierop LE (2015) The magnetized brain: working mechanisms for the effects of MRI-related magnetic fields on cognition, postural stability, and oculomotor function. Utrecht, Netherlands
van Nierop LE, Slottje P, Kingma H, Kromhout H (2013) MRI-related static magnetic stray fields and postural body sway: A double-blind randomized crossover study. Magn Reson Med 70:232–240. https://doi.org/10.1002/mrm.24454
Ward BK, Roberts DC, Della Santina CC et al (2015) Vestibular stimulation by magnetic fields. Ann N Y Acad Sci 1343:69–79. https://doi.org/10.1111/nyas.12702
World Health Organization (2007) Environmental health criteria 238 extremely low frequency fields. World Health Organization, Geneva, p 543
Yang Y, Pu F, Lv X et al (2015) Comparison of postural responses to galvanic vestibular stimulation between pilots and the general populace. Biomed Res Int. https://doi.org/10.1155/2015/567690
Zink R, Bucher SF, Weiss A et al (1998) Effects of galvanic vestibular stimulation on otolithic and semicircular canal eye movements and perceived vertical. Electroencephalogr Clin Neurophysiol 107:200–205. https://doi.org/10.1016/S0013-4694(98)00056-X
Acknowledgements
The authors thank Mr. Lynn Keenliside for his technical assistance and Mr. Rob Kavet for his expertise and assistance in the revision of this manuscript. This project was supported by: Hydro-Québec (Canada) EDF-RTE (France), NationalGrid and Energy Network Association (UK), Electric Power Research Institute (EPRI–USA) and Lawson Internal Research funding. This work was also supported by MITACS through the MITACS-Accelerate Program. The funders had no role in study design, data collection and analysis, decision to publish, study approvals, or preparation of the manuscript.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Villard, S., Allen, A., Bouisset, N. et al. Impact of extremely low-frequency magnetic fields on human postural control. Exp Brain Res 237, 611–623 (2019). https://doi.org/10.1007/s00221-018-5442-9
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00221-018-5442-9