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Effects of 3 Hz and 60 Hz Extremely Low Frequency Electromagnetic Fields on Anxiety-Like Behaviors, Memory Retention of Passive Avoidance and Electrophysiological Properties of Male Rats

Amin Rostami, Minoo Shahani, Mohammad Reza Zarrindast, Saeed Semnanian, Mohammad Rahmati Roudsari, Mostafa Rezaei Tavirani, Hadi Hasanzadeh




Introduction: The effects of electromagnetic fields on biological organisms have been a controversial and also interesting debate over the past few decades, despite the wide range of investigations, many aspects of extremely low frequency electromagnetic fields (ELF/EMFs) effects including mechanism of their interaction with live organisms and also their possible biological applications still remain ambiguous. In the present study, we investigated whether the exposures of ELF/EMF with frequencies of 3 Hz and 60 Hz can affect the memory, anxiety like behaviors, electrophysiological properties and brain’s proteome in rats.

Methods: Male rats were exposed to 3 Hz and 60 Hz ELF/EMFs in a protocol consisting of 2 cycles of 2 h/day exposure for 4 days separated with a 2-day interval. Short term memory and anxiety like behaviors were assessed immediately, 1 and 2 weeks after the exposures. Effects of short term exposure were also assessed using electrophysiological approach immediately after 2 hours exposure.

Results: Behavioral test revealed that immediately after the end of exposures, locomotor activity of both 3 Hz and 60 Hz exposed groups significantly decreased compared to sham group. This exposure protocol had no effect on anxiety like behavior during the 2 weeks after the treatment and also on short term memory. A significant reduction in firing rate of locus coeruleus (LC) was found after 2 hours of both 3 Hz and 60 Hz exposures. Proteome analysis also revealed global changes in whole brain proteome after treatment.

Conclusion: Here, some evidence regarding the fact that such exposures can alter locomotor activity and neurons firing rate in male rats were presented.


ELF/EMFs; Locomotion; Memory; Locus Coeruleus.


Cifra M, Fields JZ, Farhadi A. Electromagnetic cellular interactions. Prog Biophys Mol Biol. 2010;105(3):223-246.

Karasek M, Lerchl A. Melatonin magnetic fields. Neuro Endocrinol Lett. 2002;23:84-87.

Woldanska-Okonska M, Karasek M, Czernicki J. The influence of chronic exposure to low frequency pulsating magnetic fields on concentrations of FSH, LH, prolactin, testosterone and estradiol in men with back pain. Neuro Endocrinol Lett. 2004;25:201-206.

Woldanska-Okonska M, Czernicki J. Effects of low frequency pulsating magnetic fields used in magnetotherapy and magnetostimulation on cortisol secretion in humans. Med Pr. 2003;54(1):29-32.

Akerstedt T, Arnetz B, Ficca G, Paulsson LE, Kallner A. A 50 Hz electromagnetic field impair sleep. J Sleep Res. 1999; 8:77-81. doi:10.1046/j.1365-2869.1999.00100.x.

Selmaoui B, lambrozo J, Touito Y. Endocrine functions in young men exposed one night to 50 Hz magnetic field A circadian study of pituitary, thyroid and adrenocortical hormones. Life Sci. 1997;61:473-486.

Graham C, Cook MR, Cohen HD, Riffle DW, Hoffman S, Gerkovich MM. Human exposure to 60-Hz magnetic fields: neurophysiological effects. Int J Psychophysiol. 1999;33:169-175.

Graham C, Cook M R. Human sleep in 60 Hz magnetic fields. Bioelectromagnetics. 1999;20:277-283.

Bonhomme-Faivre L, Macé A, Bezie Y, et al. Alteration of biological parameters in mice chronically exposed to low-frequeny (50-Hz) electromagnetic fields. Life Sci. 1998;62: 1271-1280. doi:10.1016/s0024-3205(98)00057-5.

Zwirska-Korczala K, Jochem J, Adamczyk-Sowa M, et al. Effect of extremely low frequency electromagnetic fields on cell proliferation, antioxidative enzyme activities and lipid peroxidation in 3T3-L1 preadipocytes- an in vitro study. J Physiol Pharmacol. 2005;56:101-108.

Gerardi G, De Ninno A, Prosdocimi M, et al. Effects of electromagnetic fields of low frequency and low intensity on rat metabolism. Biomagn Res Technol. 2008;6:3.

Zecca L, Mantegazza C, Margonato V, et al. Biological effects of prolonged exposure to ELF electromagnetic fields in rats: III. 50 Hz electrommagnetic fields. Bioelectromagnetics. 1998;19(1):57-66.

Margonato V, Veicsteinas A, Conti R, Nicolini P, Cerretelli P. Biologic effects of prolonged exposure to ELF electromagnetic fields in rats. I. 50 Hz electric fields. Bioelectromagnetics. 1993;14:479-493. doi:10.1002/ bem.2250140508.

Wolf FI, Torsello A, Tedesco B, et al. 50-Hz extremely low frequency electromagnetic fields enhance cell proliferation and DNA damage: possible involvement of redox mechanism. Biochim Biophys Acta. 2005;1743:120-129. doi:10.1016/j.bbamcr.2004.09.005.

Ivancsits S, Pilger A, Diem E, Jahn O, Rüdiger HW. Cell type-specific genotoxic effects of intermittent extremely low-frequency electromagnetic fields. Mutat Res. 2005; 583:184-188. doi:10.1016/j.mrgentox.2005.03.011.

Pilger A, Ivancsits S, Diem E, Steffens M, Kolb HA, Rüdiger HW. No effects of intermittent 50 Hz EMF on cytoplasmic free calcium and on the mitochondrial membrane potential in human diploid fibroblasts. Radiat Environ Biophys. 2004;43:203-207. doi:10.1007/s00411-004-0252-9.

Cho YH, Chung HW. The effect of extremely low frequency electromagnetic fields (ELF/EMF) on the frequency of micronuclei and sister chromatid exchange in human lymphocytes induced by benzo (a) pyrene. Toxicol Lett. 2003;143:37-44. doi:10.1016/s0378-4274(03)00111-5.

Winker R, Ivancsits S, Pilger A, Adlkofer F, Rüdiger HW. Chromosomal damage in human diploid fibroblast by intermittent exposure to extremely low frequency electromagnetic fields. Mutat Res. 2005;585:43-9.

Erdal N, Gürgül S, Celik A. Cytogenetic effects of extremely low frequency magnetic field on Wistar rat bone marrow. Mutat Res. 2007; 630: 69–77.

Pourlis AF. Reproductive and developmental effects of EMF in vertebrate animal models. Pathophysiology. 2009;16:179- 189. doi:10.1016/j.pathophys.2009.01.010.

Narita K, Hanakawa K, Kasahara T, Hisamitsu T, Asano K. Induction of apoptotic cell death in human leukemic cell line, HL-60, by extremely low frequency electric magnetic fields: analysis of the possible mechanisms in vitro. In Vivo. 1997;11:329-336.

Hisamitsu T, Narita K, Kasahara T, Seto A, Yu Y, Asano K. Induction of apoptosis in human leukemic cells by magnetic fields. Jpn J Physiol. 1997;47:307–310.

Feychting M, Ahlbom A. Magnetic-fields, leukemia and central nervous-system tumors in Swedish adults residing near high-voltage power-lines. Epidemiology. 1994;5:501- 509. doi:10.1097/00001648-199807000-00008.

Vázquez-García M, Elías-Viñas D, Reyes-Guerrero G, Domínguez-González A, Verdugo-Díaz L, Guevara- Guzmán R. Exposure to low-frequency electromagnetic field improves social recognition in male rats. Physiol Behav. 2004;82:685-90. doi:10.1016/j.physbeh.2004.06.004.

Trimmel M, Schweiger E. Effect of an ELF 50 Hz, 1mT electromagnetic field on concentration in visual attention, perception and memory including effects of EMF sensitivity. Toxicol Lett. 1998;97:377-382.

Szemerszky R, Zelena D, Barna I, Bárdos G. Stress-related endocrinological and psychopathological effects of short-and long-term 50 Hz electromagnetic field exposure in rats. Brain Res Bull. 2010;81:92-99.

Falone S, Mirabilio A, Carbone MC, et al. Chronic exposure to 50Hz magnetic fields causes a significant weakening of antioxidant defence systems in aged rat brain. Int J Biochem Cell Biol. 2008;40:2762-2770.

Gulturk S, Demirkazik A, Kosar I, Cetin A, Dökmetas HS, Demir T. Effect of exposure to 50 Hz magnetic field with or without insulin on blood-brain barrier permeability in streptozotocin-induced diabetic rats. Bioelectromagnetics. 2010;31(4):262-269. doi:10.1002/bem.20557.

Marchionni I, Paffi A, Pellegrino M, et al. Comparison between low-level 50 Hz and 900 MHz electromagnetic stimulation on single channel ionic currents and on firing frequency in dorsal root ganglion isolated neurons Biochim Biophys Acta. 2006;1758:597-605. doi:10.1016/j. bbamem.2006.03.014.

Lai H, Carino M. 60 Hz magnetic fields and central cholinergic activity: effects of exposure intensity and duration. Bioelectromagnetics. 1999;20(5):284-289.

Cuccurazzu B, Leone L, Podda MV, et al. Exposure to extremely low-frequency (50 Hz) electromagnetic fields enhances adult hippocampal neurogenesis in C57BL/6 mice. Exp Neurol. 2010;226:173-182. doi:10.1016/j. expneurol.2010.08.022.

Choleris E, Thomas AW, Kavaliers M, Prato FS. A detailed ethological analysis of the mouse open field test: effects of diazepam, chlordiazepoxide and an extremely low frequency pulsed magnetic field. Neurosci Biobehav Rev. 2001;25:235-260. doi:10.1016/s0149-7634(01)00011-2.

Tamasidze AG. Influence of the chronic exposure to network frequency electromagnetic field on rats under interrupted and continuous action of EMF. Georgian Med News. 2006;140:91-93.

Rezayat M, Roohbakhsh A, Zarrindast MR, Massoudi R, Djahanguiri B. Cholecystokinin and GABA interaction in the dorsal hippocampus of rats in the elevated plus-maze test of anxiety. Physiol Behav. 2005;84:775-782. doi:10.1016/j.physbeh.2005.03.002.

Haghparast A, Semnanian S, Fathollahi Y. Morphine tolerance and dependence in the nucleus paragigantocellularis: single unit recording study in vivo. Brain Res. 1998;814:71-77. doi:10.1016/s0006- 8993(98)01029-4.

Lai H, Carino MA, Ushijima I. Acute exposure to 60 Hz magnetic field affects rats’ water-maze performance. Bioelectromagnetics. 1998;19:117-122.

Lai H, Carino M. Intracerebroventricular injections of mu-and delta-opiate receptor antagonists block 60 Hz magnetic field-induced decreases in cholinergic activity in the fronral cortex and hippocampus of the rat. Bioelectromagnetics. 1998;19:432-427.

Kavaliers M, Ossenkopp KP. Magnetic fields opioid systems and day–night rhythms of behavior. In: Moore-Ede MC, Campbell SS, Reiter RJ, eds. Electromagnetic Fields and Circadian Rhythmicity. Boston, MA: Birkhauser; 1992:93- 117.

Reyes-Guerrero G, Vázquez-García M, Elias-Viñas D, Donatti-Albarrán OA, Guevara-Guzmán R. Effects of 17 b-estradiol and extremely low-frequency electromagnetic fields on social recognition memory in female rats: a possible interaction? Brain Res. 2006;1095:131-138.

DOI: https://doi.org/10.22037/jlms.v7i2.8735