Environmental Science and Pollution Research

, Volume 24, Issue 27, pp 21693–21699 | Cite as

Anxiety-like behavioural effects of extremely low-frequency electromagnetic field in rats

  • Natasa Z. DjordjevicEmail author
  • Milica G. Paunović
  • Aleksandar S. Peulić
Research Article


In recent years, extremely low-frequency electromagnetic field (ELF-EMF) has received considerable attention for its potential biological effects. Numerous studies have shown the role of ELF-EMF in behaviour modulation. The aim of this study was to investigate the effect of short-term ELF-EMF (50 Hz) in the development of anxiety-like behaviour in rats through change hypothalamic oxidative stress and NO. Ten adult male rats (Wistar albino) were divided in two groups: control group—without exposure to ELF-EMF and experimental group—exposed to ELF-EMF during 7 days. After the exposure, time open field test and elevated plus maze were used to evaluate the anxiety-like behaviour of rats. Upon completion of the behavioural tests, concentrations of superoxide anion (O2·), nitrite (NO2 , as an indicator of NO) and peroxynitrite (ONOO) were determined in the hypothalamus of the animals. Obtained results show that ELF-EMF both induces anxiety-like behaviour and increases concentrations of O2· and NO, whereas it did not effect on ONOO concentration in hypothalamus of rats. In conclusion, the development of anxiety-like behaviour is mediated by oxidative stress and increased NO concentration in hypothalamus of rats exposed to ELF-EMF during 7 days.


Electromagnetic field Anxiety Nitric oxide Oxidative stress Hypothalamus 



This study was supported by the Ministry of Education, Science and Technological Development of Republic of Serbia, Grant No. 173041. Authors are grateful to Jovan Vukovic (MSc in biology) and Vojkan Cvetković (MSc in biology) for technical assistance during the experiment.

Compliance with ethical standards

All experimental procedures were approved by the Faculty Ethics Committee, University of Kragujevac.

Conflict of interest

The authors declare that they have no conflicts of interest.


  1. Auclair C, Voisin E (1985) Nitroblue tetrazolium reduction. In: Greenwald RA (ed) Handbook of methods for oxygen radical research. CRC Press, Boca Raton, pp 123–132Google Scholar
  2. Barth A, Ponocny I, Ponocny-Seliger E, Vana N, Winker R (2010) Effects of extremely low-frequency magnetic field exposure on cognitive functions: results of a meta-analysis. Bioelectromagnetics 31:173–179Google Scholar
  3. Beckman JS, Beckman TW, Chem J, Marshall PA, Freeman BA (1990) Apparent hydroxyl radical production by peroxynitrite: implications for endothelial injury from nitric oxide and superoxide. Proc Nati Acad Sci USA 87:1620–1624CrossRefGoogle Scholar
  4. Carola V, D'Olimpio F, Brunamonti E, Mangia F, Renzi P (2002) Evaluation of the elevated plus-maze and open-field tests for the assessment of anxiety-related behaviour in inbred mice. Behav Brain Res 134:49–57CrossRefGoogle Scholar
  5. Ceylan MF, Guney E, Alisik M, Ergin M, Dinc GS, Goker Z, Eker S, Kizilgun M, Erel O (2014) Lipid peroxidation markers in children with anxiety disorders and their diagnostic implications. Redox Rep 19:92–96CrossRefGoogle Scholar
  6. Cho SI, Nam YS, Chu LY, Lee JH, Bang JS, Kim HR, Kim HC, Lee YJ, Kim HD, Sul JD, Kim D, Chung YH, Jeong JH (2012) Extremely low-frequency magnetic fields modulate nitric oxide signaling in rat brain. Bioelectromagnetics 33:568–574CrossRefGoogle Scholar
  7. Chu SC, Yu CH, Chen PN, Hsieh YS, Kuo DY (2016) Role of oxidative stress in disrupting the function of negative glucocorticoid response element in daily amphetamine-treated rats. Psychoneuroendocrinology 71:1–11CrossRefGoogle Scholar
  8. Consales C, Merla C, Marino C, Benassi B (2012) Electromagnetic fields, oxidative stress, and neurodegeneration. Int J Cell Biol 2012:683897CrossRefGoogle Scholar
  9. Dhir A, Kulkarni SK (2011) Nitric oxide and major depression. Nitric Oxide 24:125–131CrossRefGoogle Scholar
  10. Filipović D, Todorović N, Bernardi RE, Gass P (2016) Oxidative and nitrosative stress pathways in the brain of socially isolated adult male rats demonstrating depressive- and anxiety-like symptoms. Brain Struct Funct. doi: 10.1007/s00429-016-1218-9
  11. Foroozandeh E, Derakhshan-Barjoei P, Jadidi M (2013) Toxic effects of 50 Hz electromagnetic field on memory consolidation in male and female mice. Toxicol Ind Health 29:293–299CrossRefGoogle Scholar
  12. Förstermann U, Sessa WC (2012) Nitric oxide synthases: regulation and function. Eurt Heart J 33:829–837CrossRefGoogle Scholar
  13. Golbach LA, Scheer MH, Cuppen JJ, Savelkoul H, Verburg-van Kemenade BM (2015) Low-frequency electromagnetic field exposure enhances extracellular trap formation by human neutrophils through the NADPH pathway. J Innate Immun 7:459–465CrossRefGoogle Scholar
  14. Green LC, Wagner DA, Glogowski J, Skipper PL, Wishnok JS, Tannenbaum SR (1982) Analysis of nitrate, nitrite, and [15N] nitrate in biological fluids. Anal Biochem 126:131–138CrossRefGoogle Scholar
  15. Halliwel B, Gutteridge JMC (2007) Free radicals in biology and medicine. Oxford University Press, New YorkGoogle Scholar
  16. Herce-Pagliai C, Kotecha S, Shuker D (1998) Analytical methods for 3-nitrotyrosine as a marker of exposure to reactive nitrogen species. Nitric Oxide 2:324–336CrossRefGoogle Scholar
  17. Herman JP, Figueiredo H, Mueller NK, Ulrich-Lai Y, Ostrander MM, Choi DC, Cullinan WE (2003) Central mechanisms of stress integration: hierarchical circuitry controlling hypothalamo-pituitary-adrenocortical responsiveness. Front Neuroendocrinol 24:151–180CrossRefGoogle Scholar
  18. Herrero AI, Sandi C, Venero C (2006) Individual differences in anxiety trait are related to spatial learning abilities and hippocampal expression of mineralocorticoid receptors. Neurobiol Learn Mem 86:150–159CrossRefGoogle Scholar
  19. Joung HY, Jung EY, Kim K, Lee MS, Her S, Shim I (2012) The differential role of NOS inhibitors on stress-induced anxiety and neuroendocrine alterations in the rat. Behav Brain Research 235:176–181CrossRefGoogle Scholar
  20. Kovacic P, Somanathan R (2010) Electromagnetic fields: mechanism, cell signaling, other bioprocesses, toxicity, radicals, antioxidants and beneficial effects. J Recept Signal Transduct Res 30:214–226CrossRefGoogle Scholar
  21. Lai J, Zhang Y, Liu X, Zhang J, Ruan G, Chaugai S, Chen C, Wang DW (2016) Effects of extremely low frequency electromagnetic fields (100μT) on behaviors in rats. Neurotoxicology 52:104–113CrossRefGoogle Scholar
  22. Markov MS (2007) Expanding use of pulsed electromagnetic field therapies. Electromagn Biol Med 26:257–274CrossRefGoogle Scholar
  23. Martínez-Sámano J, Torres-Durán PV, Juárez-Oropeza MA, Elías-Viñas D, Verdugo-Díaz L (2010) Effects of acute electromagnetic field exposure and movement restraint on antioxidant system in liver, heart, kidney and plasma of Wistar rats: a preliminary report. Int J Radiat Biol 86:1088–1094CrossRefGoogle Scholar
  24. Martínez-Sámano J, Torres-Durán PV, Juárez-Oropeza MA, Verdugo-Díaz L (2012) Effect of acute extremely low frequency electromagnetic field exposure on the antioxidant status and lipid levels in rat brain. Arch Med Res 43:183–189CrossRefGoogle Scholar
  25. Rauš Balind S, Manojlović-Stojanoski M, Milošević V, Todorović D, Nikolić L, Petković B (2016) Short- and long-term exposure to alternating magnetic field (50 Hz, 0.5 mT) affects rat pituitary ACTH cells: stereological study. Environ Toxicol 31:461–468CrossRefGoogle Scholar
  26. Riordan JF, Vallee BL (1972) Nitration with tetranitromethane. In: Hirs CHW, Timasheff SN (eds) Methods in enzymology. Academic Press, New York, pp 515–521Google Scholar
  27. Santini MT, Rainaldi G, Indovina PL (2009) Cellular effects of extremely low frequency (ELF) electromagnetic fields. Int J Radiat Biol 85:294–313CrossRefGoogle Scholar
  28. Sena LA, Chandel NS (2012) Physiological roles of mitochondrial reactive oxygen species. Mol Cell 48:158–167CrossRefGoogle Scholar
  29. Sestakova N, Puzserova A, Kluknavsky M, Bernatova I (2013) Determination of motor activity and anxiety-related behaviour in rodents: methodological aspects and role of nitric oxide. Interdiscip Toxicol 6:126–135CrossRefGoogle Scholar
  30. Shehu A, Mohammed A, Magaji RA, Muhammad MS (2016) Exposure to mobile phone electromagnetic field radiation, ringtone and vibration affects anxiety-like behaviour and oxidative stress biomarkers in albino wistar rats. Metab Brain Dis 31:355–362CrossRefGoogle Scholar
  31. Shiva S (2013) Nitrite: a physiological store of nitric oxide and modulator of mitochondrial function. Redox Biol 1:40–44CrossRefGoogle Scholar
  32. The ELF Working Group (2005) Health effects and exposure guidelines related to extremely low frequency (ELF) 50/60 Hz electric and magnetic fields - an overview. The Federal-Provincial-Territorial Radiation Protection Committee (FPTRPC), CanadaGoogle Scholar
  33. Walton JC, Selvakumar B, Weil ZM, Snyder SH, Nelson RJ (2013) Neural nitric oxide synthase and NADPH oxidase interact to affect cognitive, affective and social behaviors in mice. Behav Brain Res 256:320–327CrossRefGoogle Scholar
  34. Zhang R, Asai M, Mahoney CE, Joachim M, Shen Y, Gunner G, Majzoub JA (2016) Loss of hypothalamic corticotropin-releasing hormone markedly reduces anxiety behaviors in mice. Mol Psychiatry. doi: 10.1038/mp.2016.136
  35. Zhou QG, Zhu LJ, Chen C, Wu HY, Luo CX, Chang L, Zhu DY (2011) Hippocampal neuronal nitric oxide synthase mediates the stress-related depressive behaviors of glucocorticoids by downregulating glucocorticoid receptor. J Neurosci 31:7579–7590CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany 2017

Authors and Affiliations

  • Natasa Z. Djordjevic
    • 1
    Email author
  • Milica G. Paunović
    • 2
  • Aleksandar S. Peulić
    • 3
  1. 1.Department of Biomedical SciencesState University of Novi PazarNovi PazarSerbia
  2. 2.Institute of Biology and Ecology, Faculty of ScienceUniversity of KragujevacKragujevacSerbia
  3. 3.Faculty of engineeringUniversity of KragujevacKragujevacSerbia

Personalised recommendations