Environmental Science and Pollution Research

, Volume 26, Issue 30, pp 30693–30710 | Cite as

Radiofrequency electromagnetic radiation-induced behavioral changes and their possible basis

  • Sareesh Naduvil NarayananEmail author
  • Raghu Jetti
  • Kavindra Kumar Kesari
  • Raju Suresh Kumar
  • Satheesha B. Nayak
  • P. Gopalakrishna Bhat
Review Article


The primary objective of mobile phone technology is to achieve communication with any person at any place and time. In the modern era, it is impossible to ignore the usefulness of mobile phone technology in cases of emergency as many lives have been saved. However, the biological effects they may have on humans and other animals have been largely ignored and not been evaluated comprehensively. One of the reasons for this is the speedy uncontrollable growth of this technology which has surpassed our researching ability. Initiated with the first generation, the mobile telephony currently reaches to its fifth generation without being screened extensively for any biological effects that they may have on humans or on other animals. Mounting evidences suggest possible non-thermal biological effects of radiofrequency electromagnetic radiation (RF-EMR) on brain and behavior. Behavioral studies have particularly concentrated on the effects of RF-EMR on learning, memory, anxiety, and locomotion. The literature analysis on behavioral effects of RF-EMR demonstrates complex picture with conflicting observations. Nonetheless, numerous reports suggest a possible behavioral effect of RF-EMR. The scientific findings about this issue are presented in the current review. The possible neural and molecular mechanisms for the behavioral effects have been proposed in the light of available evidences from the literature.


Mobile phone Radiofrequency electromagnetic radiation Brain Behavior Anxiety Locomotion Learning and memory Blood-brain barrier 



Radiofrequency electromagnetic radiation


International Agency for Research on Cancer


World Health Organization


Specific absorption rate




Global System for Mobile communication


Blood-brain barrier


Morris water maze

Amyloid beta


Elevated plus maze


Open field test


Spartic acid


Electromagnetic radiation


Cornu Ammonis 1


Cornu Ammonis 2


Cornu Ammonis 3




Glial fibrillary acidic protein






Parkinson’s disease


Alzheimer’s disease


Radiofrequency radiation


Electromagnetic fields


Electromagnetic radiation


Glial fibrillary acidic protein


Second generation


Radiomagnetic field


Radio frequency


Superoxide dismutase


Nitric oxide








Apoptosis-inducing factor


Deoxyribonucleic acid


Reactive oxygen species


Extremely low frequency


Code Division Multiple Access

HPA axis

Hypothalamic-pituitary-adrenal axis


Transient receptor potential vanilloid 1 channel


Digital Enhanced Cordless Telecommunications


Amyloid precursor protein



The authors are grateful to Dr. Sampath Kumar, Chief Librarian & other library staff of RAK Medical & Health Sciences University for their support.


  1. Adey WR (1981) Ionic nonequilibrium phenomena in tissue interactions with electromagnetic fields. In: Illinger KH (ed) Biological effects of nonionizing radiation Washington. American Chemical Society, DCGoogle Scholar
  2. Ahmadi S, Alavi SS, Jadidi M, Ardjmand A (2018) Exposure to GSM 900-MHz mobile radiation impaired inhibitory avoidance memory consolidation in rat: involvements of opioidergic and nitrergic systems. Brain Res 1701:36–45. Google Scholar
  3. Ahmed NA, AboulEzz HS, Khadrawy YA, Radwan NM (2007) Changes of amino acid neurotransmitter concentrations in striatum and thalamus inducedby exposure of young and adult rats to electromagnetic radiation. Med J Cairo Univ 75(suppl):73–84Google Scholar
  4. Aitken RJ, Bennetts LE, Sawyer D, Wiklendt AM, King BV (2005) Impact of radio frequency electromagnetic rad iation on DNA integrity in the male germline. Int J Androl 28:171–9.38Google Scholar
  5. Aksoy U, Sahin S, Ozkoc S, Ergor G (2005) The effect of electromagnetic waves on the growth of Entamoeba histolytica and Entamoeba dispar. Saudi Med J 26(9):1388–1390Google Scholar
  6. Albert EN, Sherif MF, Papadopoulos NJ, Slaby FJ, Monahan J (1981) Effect of nonionizing radiation on the Purkinje cells of the rat cerebellum. Bioelectromagnetics 2(3):247–257Google Scholar
  7. Aldad TS, Gan G, Gao XB, Taylor HS (2012) Fetal radiofrequency radiation exposure from 800-1900 mhz-rated cellular telephones affects neurodevelopment and behavior in mice. Sci Rep 2:312. CrossRefGoogle Scholar
  8. Alkis ME, Bilgin HM, Akpolat V, Dasdag S, Yegin K, Yavas MC, Akdag MZ (2019) Effect of 900-, 1800-, and 2100-MHz radiofrequency radiation on DNA and oxidative stress in brain. Electromagn Biol Med 2019;38(1):32-47. Google Scholar
  9. Altun G, Kaplan S, Deniz OG, Kocacan SE, Canan S, Davis D, Marangoz C (2017) Protective effects of melatonin and omega-3 on the hippocampus and the cerebellum of adult Wistar albino rats exposed to electromagnetic fields. J Microsc Ultrastruct 5(4):230–241Google Scholar
  10. Alzoubi KH, Khabour OF, Salah HA, Abu Rashid BE (2013) The combined effect of sleep deprivation and Western diet on spatial learning and memory: role of BDNF and oxidative stress. J Mol Neurosci 50(1):124–133Google Scholar
  11. Amal A, Tolba MA, Omayma K, Afifi A (2013) Histological and Immunohistochemical study onthe effect of mobile phone radiation on the hipocampus of adult and newborn albino rats. Nat Sci 11(8):98–113Google Scholar
  12. Ammari M, Brillaud E, Gamez C, Lecomte A, Sakly M, Abdelmelek H, de Seze R (2008a) Effect of a chronic GSM 900 MHz exposure on glia in the rat brain. Biomed Pharmacother 62(4):273–281Google Scholar
  13. Ammari M, Jacquet A, Lecomte A, Sakly M, Abdelmelek H, de Seze R (2008b) Effect of head-only sub-chronic and chronic exposure to 900-MHz GSM electromagnetic fields on spatial memory in rats. Brain Inj 22(13–14):1021–1029Google Scholar
  14. Aravalli RN, Cressman EN, Steer CJ (2013) Cellular and molecular mechanisms of hepatocellular carcinoma: an update. Arch Toxicol 87(2):227–247Google Scholar
  15. Aslan A, İkinci A, Baş O, Sönmez OF, Kaya H, Odacı E (2017) Long-term exposure to a continuous 900 MHz electromagnetic field disrupts cerebellar morphology in young adult male rats. Biotech Histochem 92(5):324–330Google Scholar
  16. Awad SM, Hassan NS (2008) Health risks of electromagnetic radiation from mobile phone on brain of rats. J Appl Sci Res 4(12):1994–1900Google Scholar
  17. Bas O, Odaci E, Mollaoglu H, Ucok K, Kaplan S (2009) Chronic prenatal exposure to the 900 megahertz electromagnetic field induces pyramidal cell loss in the hippocampus of newborn rats. Toxicol Ind Health 25(6):377–384Google Scholar
  18. Bas O, Sönmez OF, Aslan A, Ikinci A, Hanci H, Yildirim M, Kaya H, Akça M, Odaci E (2013) Pyramidal cell loss in the cornuammonis of 32-day-old female rats following exposure to a 900 megahertz electromagnetic field during prenatal days 13-21. Neuro Quantology 11(4):591–599Google Scholar
  19. Baureus Koch CL, Sommarin M, Persson BR, Salford LG, Eberhardt JL (2003) Interaction between weak low frequency magnetic fields and cell membranes. Bioelectromagnetics 24(6):395–402Google Scholar
  20. Black MM, Cochran JM, Kurdyla JT (1984) Solubility properties of neuronal tubulin: evidence for labile and stable microtubules. Brain Res 295(2):255–263Google Scholar
  21. Bolbanabad M, Kaffashian MR, Fatehi D, Rostamzadeh A (2014) Effects of cell phone radiation on migration of granule cells in rat cerebellum. J Bas Res Med Sci 2:15–22Google Scholar
  22. Bornhausen M, Scheingraber H (2000) Prenatal exposure to 900 MHz, cell-phone electromagnetic fields had no effect on operant-behavior performances of adult rats. Bioelectromagnetics 21(8):566–574Google Scholar
  23. Bouji M, Lecomte A, Gamez C, Blazy K, Villégier AS (2016) Neurobiological effects of repeated radiofrequency exposures in male senescent rats. Biogerontology 17(5-6):841-857Google Scholar
  24. Bouji M, Lecomte A, Hode Y, de Seze R, Villégier AS (2012) Effects of 900 MHz radiofrequency on corticosterone, emotional memory and neuroinflammation in middle-aged rats. Exp Gerontol 47(6):444–451Google Scholar
  25. Brillaud E, Piotrowski A, de Seze R (2007) Effect of an acute 900MHz GSM exposure on glia in the rat brain: a time dependent study. Toxicology 238:23–33Google Scholar
  26. Cam ST, Seyhan N (2012) Single-strand DNA breaks in human hair root cells exposed to mobile phone radiation. Int J Radiat Biol 88(5):420–424Google Scholar
  27. Cammaerts MC, Rachidi Z, Bellens F, De Doncker P (2013) Food collection and response to pheromones in an ant species exposed to electromagnetic radiation. Electromagn Biol Med 32(3):315–332Google Scholar
  28. Carlberg M, Hardell L (2017). Evaluation of Mobile phone and cordless phone use and glioma risk using the Bradford Hill viewpoints from 1965 on association or causation. Biomed Res Int 9218486. Google Scholar
  29. Chavdoula ED, Panagopoulos DJ, Margaritis LH (2010) Comparison of biological effects between continuous and intermittent exposure to GSM-900-MHz mobile phone radiation: detection of apoptotic cell-death features. Mutat Res 700(1–2):51–61Google Scholar
  30. Cleveland RF, Ulcek JJL (1999). Questions and answers about biological effects and potential hazards of radiofrequency electromagnetic fields, OET BULLETIN 56, 4th edition, Office of Engineering and Technology Federal Communications Commission; Washington D.C:
  31. Court-Kowalski S, Finnie JW, Manavis J, Blumbergs PC, Helps SC, Vink R (2015) Effect of long-term (2 years) exposure of mouse brains to global system for mobile communication (GSM) radiofrequency fields on astrocytic immunoreactivity. Bioelectromagnetics 36(3):245–250. CrossRefGoogle Scholar
  32. Daniels WM, Pitout IL, Afullo TJ, Mabandla MV (2009) The effect of electromagnetic radiation in the mobile phone range on the behaviour of the rat. Metab Brain Dis 24(4):629–641Google Scholar
  33. DeIullis GN, Newey RJ, King BV, Aitken RJ (2009) Mobile phone radiation induces reactive oxygen species production and DNA damage in human spermatozoa in vitro. PLoS One 4:e6446Google Scholar
  34. Eberhardt JL, Persson BR, Brun AE, Salford LG, Malmgren LO (2008) Blood-brain barrier permeability and nerve cell damage in rat brain 14 and 28 days after exposure to microwaves from GSM mobile phones. Electromagn Biol Med 27(3):215–229Google Scholar
  35. Elsawy N, Elkholy S, Azmy R, Maher EA, Shamloul R (2019) Electrophysiological assessment of the impact of Mobile phone radiation on cognition in persons with epilepsy. J Clin Neurophysiol 36(2):112–118. CrossRefGoogle Scholar
  36. Eris AH, Kiziltan HS, Meral I, Genc H, Trabzon M, Seyithanoglu H, Yagci B, Uysal O (2015) Effect of short-term 900 MHz low level electromagnetic radiation exposure on blood serotonin and glutamate levels. Bratisl Lek Listy 116(2):101–103Google Scholar
  37. Ertilav K, Uslusoy F, Ataizi S, Nazıroğlu M (2018) Long term exposure to cell phone frequencies (900 and 1800 MHz) induces apoptosis, mitochondrial oxidative stress and TRPV1 channel activation in the hippocampus and dorsal root ganglion of rats. Metab Brain Dis 33(3):753–763. CrossRefGoogle Scholar
  38. Eser O, Songur A, Aktas C, Karavelioglu E, Caglar V, Aylak F, Ozguner F, Kanter M (2013) The effect of electromagnetic radiation on the rat brain: an experimental study. Turk Neurosurg 23(6):707–715Google Scholar
  39. Faridi K, Khan AA (2013) Effects of radiofrequency electromagnetic radiations (RF-EMR) on sector CA3 of hippocampus in albino rats-a light and electron-microscopic study. Current Neurobiology 4(1&2):13–18Google Scholar
  40. Ferreri F, Curcio G, Pasqualetti P, De Gennaro L, Fini R, Rossini PM (2006) Mobile phone emissions and human brain excitability. Ann Neurol 60(2):188–196Google Scholar
  41. Fragopoulou AF, Margaritis LH (2010). Is cognitive function affected by mobile phone radiation exposure? In: Giuliani, L., Soffritti, M. European J. oncology-library, vol. 5 non-thermal effects and mechanisms of interaction between electromagnetic fields and living matter. An ICEMS monograph, (pp. 261–272) Bologna, Italy: Ramazzini instituteGoogle Scholar
  42. Fragopoulou AF, Miltiadous P, Stamatakis A, Stylianopoulou F, Koussoulakos SL, Margaritis LH (2010) Whole body exposure with GSM 900MHz affects spatial memory in mice. Pathophysiology 17(3):179–187Google Scholar
  43. Fragopoulou AF, Samara A, Antonelou MH, Xanthopoulou A, Papadopoulou A, Vougas K, Koutsogiannopoulou E, Anastasiadou E, Stravopodis DJ, Tsangaris GT, Margaritis LH (2012) Brain proteome response following whole body exposure of mice to mobile phone or wireless DECT base radiation. Electromagn Biol Med 31(4):250–274Google Scholar
  44. Fridovich I (1999) Fundamental aspects of reactive oxygen species, or what's the matter with oxygen? Ann N Y Acad Sci 893:13-8Google Scholar
  45. Gao X, Luo R, Ma B, Wang H, Liu T, Zhang J, Lian Z, Cui X (2013) Interference of vitamin E on the brain tissue damage by electromagnetic radiation of cell phone in pregnant and fetal rats. Wei Sheng Yan Jiu 42(4):642–646Google Scholar
  46. Gos E, Kohli J, Heyer WD (2000) No mutagenic or recombinogenic effects of mobile phone fields at 900 MHz detected in the yeast saccharomyces cerevisiae. Bioelectromagnetics 21(7):515–523Google Scholar
  47. Hao D, Yang L, Chen S, Tong J, Tian Y, Su B, Wu S, Zeng Y (2013) Effects of long-term electromagnetic field exposure on spatial learning and memory in rats. Neurol Sci 34(2):157–164. CrossRefGoogle Scholar
  48. Henz D, Schöllhorn WI, Poeggeler B (2018) Mobile phone chips reduce increases in EEG brain activity induced by Mobile phone-emitted electromagnetic fields. Front Neurosci 12:190. eCollection 2018CrossRefGoogle Scholar
  49. Hossmann KA, Hermann DM (2003) Effects of electromagnetic radiation of mobile phones on the central nervous system. Bioelectromagnetics 24:49–62Google Scholar
  50. Hovatta I, Tennant RS, Helton R, Marr RA, Singer O, Redwine JM, Ellison JA, Schadt EE, Verma IM, Lockhart DJ, Barlow C (2005) Glyoxalase 1 and glutathione reductase 1 regulate anxiety in mice. Nature 438:662–666Google Scholar
  51. Hussein S, El-Saba AA, Galal MK (2016) Biochemical and histological studies on adverse effects of mobile phone radiation on rat’s brain. J Chem Neuroanat 78:10–19Google Scholar
  52. IARC (International Agency for Research on Cancer) of World Health Organization (2011). “IARC classifies radiofrequency electromagnetic fields as possibly carcinogenic to humans”, press release no 208, 31 May.
  53. Irmak MK, Fadillioglu E, Guleç M, Erdogan H, Yagmurca M, Akyol O (2002) Effects of electromagnetic radiation from a cellular telephone on the oxidant and antioxidant levels in rabbits. Cell Biochem Funct 20(4):279–283Google Scholar
  54. IRWIN FRIDOVICH, (1999) Fundamental Aspects of Reactive Oxygen Species, or What's the Matter with Oxygen?. Annals of the New York Academy of Sciences 893 (1 OXIDATIVE/ENE):13-18Google Scholar
  55. Jing J, Yuhua Z, Xiao-qian Y, Rongping J, Dong-mei G, Xi C (2012) The influence of microwave radiation from cellular phone on fetal rat brain. Electromagn Biol Med 31(1):57–66Google Scholar
  56. Joubert V, Bourthoumieu S, Leveque P, Yardin C (2008) Apoptosis is induced by radiofrequency fields through the caspase-independent mitochondrial pathway in cortical neurons. Radiat Res 169(1):38–45Google Scholar
  57. Junior LC, Guimaraes Eda S, Musso CM, Stabler CT, Garcia RM, Mourao-Junior CA, Andreazzi AE (2014) Behavior and memory evaluation of Wistar rats exposed to 1·8 GHz radiofrequency electromagnetic radiation. Neurol Res 36:800–803Google Scholar
  58. Kai Wang, Jun-Mei Lu, Zhen-He Xing, Qian-Ru Zhao, Lin-Qi Hu, Lei Xue, Jie Zhang, Yan-Ai Mei, (2017) Effect of 1.8 GHz radiofrequency electromagnetic radiation on novel object associative recognition memory in mice. Scientific Reports 7 (1)Google Scholar
  59. Kamendulis LM, Jiang J, Xu Y, Klaunig JE (1999) Induction of oxidative stress and oxidative damage in rat glial cells by acrylonitrile. Carcinogenesis 20(8):1555–1560Google Scholar
  60. Keleş Aİ, Yıldırım M, Gedikli Ö, Çolakoğlu S, Kaya H, Baş O, Sönmez OF, Odacı E (2018) The effects of a continuous 1-h a day 900-MHz electromagnetic field applied throughout early and mid-adolescence on hippocampus morphology and learning behavior in late adolescent male rats. J Chem Neuroanat 94:46–53. CrossRefGoogle Scholar
  61. Kesari KK, Behari J, Kumar S (2010) Mutagenic response of 2.45 GHz radiation exposure on rat brain. Int J Radiat Biol 86:334–343Google Scholar
  62. Kesari KK, Kumar S, Behari J (2012) Evidence for mobile phone radiation exposure effects on reproductive pattern of male rats: role of ROS. Electromagn Biol Med 31:213–222Google Scholar
  63. Khadrawy YA, Ahmed NA, AboulEzz HS, Radwan NM (2009) Effect of electromagnetic radiation from mobile phone on the levels of cortical amino acid neurotransmitters in adult and young rats. Romanian J Biophs 19:295–305Google Scholar
  64. Khalil A, Al-Adhammi M, Al-shara B, Gagaa M, Rawshdeh A, Alshamli A (2012) Histological and ultra-structural analyses of male mice exposed to mobile phone radiation. J of Toxicology Review 1(1):1–6Google Scholar
  65. Kim JH, Yu DH, Huh YH, Lee EH, Kim HG, Kim HR (2017) Long-term exposure to 835 MHz RF-EMF induces hyperactivity, autophagy and demyelination in the cortical neurons of mice. Sci Rep 7:41129. CrossRefGoogle Scholar
  66. Kumar RS, Sareesh NN, Nayak S, Mailankot M (2009) Hypoactivity of Wistar rats exposed to mobile phone on elevated plus maze. Indian J Physiol Pharmacol 53:283–286Google Scholar
  67. Kumlin T, Iivonen H, Miettinen P, Juvonen A, van Groen T, Puranen L, Pitkaaho R, Juutilainen J, Tanila H (2007) Mobile phone radiation and the developing brain: behavioral and morphological effects in juvenile rats. Radiat Res 168(4):471–479Google Scholar
  68. Kuribayashi M, Wang J, Fujiwara O, Nabae K, Tamano S, Ogiso T, Asamoto M, Shirai T (2005) Lack of effects of 1439 MHz electromagnetic near field exposure on the blood–brain barrier in immature and young rats. Bioelectromagnetics 26(7):578–588Google Scholar
  69. Lai H (2014) Neurological effects of non-ionizing electromagnetic fields. Supplement for BioInitiative Working GroupGoogle Scholar
  70. Lai H, Singh NP (1995) Acute low-intensity microwave exposure increases DNA single-strand breaks in rat brain cells. Bioelectromagnetics 16(3):207–210Google Scholar
  71. Laming PR (1989) Do glia contribute to behaviour? A neuromodulatory review. Comp Biochem Physiol A 94:555–568Google Scholar
  72. Laming PR, Kimelberg H, Robinson S, Salm A, Hawrylak N, Müller C et al (2000) Neuronal-glial interactions and behaviour. Neurosci Biobehav Rev 24:295–340Google Scholar
  73. Li M, Wang Y, Zhang Y, Zhou Z, Yu Z (2008) Elevation of plasma corticosterone levels and hippocampal glucocorticoid receptor translocation in rats: a potential mechanism for cognition impairment following chronic low power density microwave exposure. J Radiat Res 49:163–170Google Scholar
  74. Li Y, Shi C, Lu G, Xu Q, Liu S (2012) Effects of electromagnetic radiation on spatial memory and synapses in rat hippocampal CA1. Neural Regen Res 7(16):1248–1255. CrossRefGoogle Scholar
  75. Liu B, Jian Z, Li Q, Li K, Wang Z, Liu L, Tang L, Yi X, Wang H, Li C, Gao T (2012) Baicalein protects human melanocytes from H2O2 induced apoptosis via inhibiting mitochondria-dependent caspase activation and the p38 MAPK pathway. Free Radical Bio Med 53:183–193Google Scholar
  76. Markkanen A, Penttinen P, Naarala J, Pelkonen J, Sihvonen AP, Juutilainen J (2004) Apoptosis induced by ultraviolet radiation is enhanced by amplitude modulated radiofrequency radiation in mutant yeast cells. Bioelectromagnetics 25(2):127–133Google Scholar
  77. Maskey D, Kim M, Aryal B, Pradhan J, Choi IY, Park KS, Son T, Hong SY, Kim SB, Kim HG, Kim MJ (2010a) Effect of 835 MHz radiofrequency radiation exposure on calcium binding proteins in the hippocampus of the mouse brain. Brain Res 1313:232–241Google Scholar
  78. Maskey D, Pradhan J, Aryal B, Lee CM, Choi IY, Park KS, Kim SB, Kim HG, Kim MJ (2010b) Chronic 835-MHz radiofrequency exposure to mice hippocampus alters the distribution of calbindin and GFAP immunoreactivity. Brain Res 1346:237–246Google Scholar
  79. Masuda H, Hirot S, Ushiyama A, Hirata A, Arima T, Kawai H, Wake K, Watanabe S, Taki M, Nagai A, Ohkubo C (2015) No dynamic changes in blood-brain barrier permeability occur in developing rats during local cortex exposure to microwaves. Vivo 9(3):351–357Google Scholar
  80. Mehmet Esref Alkis, Hakki Murat Bilgin, Veysi Akpolat, Suleyman Dasdag, Korkut Yegin, Mehmet Cihan Yavas, Mehmet Zulkuf Akdag, (2018) Effect of 900-, 1800-, and 2100-MHz radiofrequency radiation on DNA and oxidative stress in brain. Electromagn Biol Med 38 (1):32-47Google Scholar
  81. Meral I, Mert H, Mert N, Deger Y, Yoruk I, Yetkin A, Keskin S (2007) Effects of 900-MHz electromagnetic field emitted from cellular phone on brain oxidative stress and some vitamin levels of Guinea pigs. Brain Res 1169:120–124Google Scholar
  82. Mohsenzadegan M, Mirshafiey A (2012) The immunopathogenic role of reactive oxygen species in Alzheimer disease. Iran J Allergy Asthma Immunol 11(3):203–216Google Scholar
  83. Mokarram P, Sheikhi M, Mortazavi SMJ, Saeb S, Shokrpour N (2017) Effect of Exposure to 900 MHz GSM Mobile Phone Radiofrequency Radiation on Estrogen Receptor Methylation Status in Colon Cells of Male Sprague Dawley Rats. J Biomed Phys Eng 7(1):79-86Google Scholar
  84. de Moura MB, dos Santos LS, Van Houten B (2010) Mitochondrial dysfunction in neurodegenerative diseases and cancer. Environ Mol Mutagen 51(5):391–405Google Scholar
  85. Mugunthan N, Shanmugasamy K, Anbalagan J, Rajanarayanan S, Meenachi S (2016) Effects of long term exposure of 900-1800 MHz radiation emitted from 2G Mobile phone on mice Hippocampus-a Histomorphometric study. J Clin Diagn Res 10(8):AF01–AF06Google Scholar
  86. Narayanan SN, Kumar RS, Potu BK, Nayak S, Mailankot M (2009) Spatial memory performance of Wistar rats exposed to mobile phone. Clinics (Sao Paulo) 64(3):231–234Google Scholar
  87. Narayanan SN, Kumar RS, Potu BK, Nayak S, Bhat PG, Mailankot M (2010) Effect of radio-frequency electromagnetic radiations (RF-EMR) on passive avoidance behaviour and hippocampal morphology in Wistar rats. Upsala J Med Sci 115(2):91–96Google Scholar
  88. Narayanan SN, Kumar RS, Paval J, Kedage V, Bhat MS, Nayak S, Bhat PG (2013) Analysis of emotionality and locomotion in radio-frequency electromagnetic radiation exposed rats. Neurol Sci 34:1117–1124Google Scholar
  89. Narayanan SN, Kumar RS, Kedage V, Nalini K, Nayak S, Bhat PG (2014) Evaluation of oxidant stress and antioxidant defense in discrete brain regions of rats exposed to 900 MHz radiation. Bratisl Lek Listy 115(5):260–266Google Scholar
  90. Narayanan SN, Kumar RS, Karun KM, Nayak SB, Bhat PG (2015) Possible cause for altered spatial cognition of prepubescent rats exposed to chronic radiofrequency electromagnetic radiation. Metab Brain Dis 30(5):1193–1206. CrossRefGoogle Scholar
  91. Narayanan SN, Mohapatra N, John P, K N, Kumar RS, Nayak SB, Bhat PG (2018). Radiofrequency electromagnetic radiation exposure effects on amygdala morphology, place preference behavior and brain caspase-3 activity in rats. Environ Toxicol Pharmacol 58:220–229Google Scholar
  92. Nittby H, Grafström G, Tian DP, Malmgren L, Brun A, Persson BR, Salford LG, Eberhardt J (2008) Cognitive impairment in rats after long-term exposure to GSM-900 mobile phone radiation. Bioelectromagnetics 29(3):219–232Google Scholar
  93. Nittby H, Brun A, Eberhardt J, Malmgren L, Persson BR, Salford LG (2009) Increased blood–brain barrier permeability in mammalian brain 7 days after exposure to the radiation from a GSM-900 mobile phone. Pathophysiology 16(2):103–112Google Scholar
  94. Noor NA, Mohammed HS, Ahmed NA, Radwan NM (2011) Variations in amino acid neurotransmitters in some brain areas of adult and young male albino rats due to exposure to mobile phone radiation. Eur Rev Med PharmacolSci 15(7):729–742Google Scholar
  95. Ntzouni MP, Stamatakis A, Stylianopoulou F, Margaritis LH (2011) Short-term memory in mice is affected by mobile phone radiation. Pathophysiology 18(3):193–199Google Scholar
  96. Obajuluwa AO, Akinyemi AJ, Afolabi OB, Adekoya K, Sanya JO, Ishola AO (2017). Exposure to radio-frequency electromagnetic waves alters acetylcholinesterase gene expression, exploratory and motor coordination-linked behaviour in male rats Toxicol rep 4:30-534Google Scholar
  97. Occelli F, Lameth J, Adenis V, Huetz C, Lévêque P, Jay TM, Edeline JM, Mallat M (2018) A single exposure to GSM-1800 MHz signals in the course of an acute Neuroinflammatory reaction can Alter neuronal responses and microglial morphology in the rat primary auditory cortex. Neuroscience 385:11–24. CrossRefGoogle Scholar
  98. Odacı E, İkinci A, Yıldırım M, Kaya H, Akça M, Hancı H, Sönmez O.F, Aslan A, Okuyan M, Baş O (2013). The effects of 900 megahertz electromagnetic field applied in the prenatal period on spinal cord morphology and motor behavior in female rat pups. Neuroquantology 4:573–581Google Scholar
  99. Odaci E, Hanci H, İkinci A, Sönmez OF, Aslan A, Şahin A, Kaya H, Çolakoğlu S, Bas O (2016) Maternal exposure to a continuous 900-MHz electromagnetic field provokes neuronal loss and pathological changes in cerebellum of 32-day-old female rat offspring. J Chem Neuroanat 75:105–110Google Scholar
  100. Ohl F (2005) Animal models of anxiety. Handb Exp Pharmacol 169:35–69Google Scholar
  101. Oscar KJ, Hawkins TD (1977) Microwave alteration of the blood-brain barrier system of rats. Brain Res 126(2):281–293Google Scholar
  102. Phillips RG, LeDoux JE (1992) Differential contribution of amygdala and hippocampus to cued and contextual fear-conditioning. Behav Neurosci 106:274–285Google Scholar
  103. Radwan NM, Ahmed NA, AboulEzz HS (2007) Disturbances in amino acid neurotransmitters induced by mobile phone radiation in the hypothalamus of young and adult albino rats. J Union Arab Biol Cairo 27(A):73–91Google Scholar
  104. Ragbetli MC, Aydinlioglu A, Koyun N, Ragbetli C, Bektas S, Ozdemir S (2010) The effect of mobile phone on the number of Purkinje cells: a stereological study. Int J Radiat Biol 86(7):548–554Google Scholar
  105. Razavinasab M, Moazzami K, Shabani M (2016) Maternal mobile phone exposure alters intrinsic electrophysiological properties of CA1 pyramidal neurons in rat offspring. Toxicol Ind Health 32(6):968–979. CrossRefGoogle Scholar
  106. Saikhedkar N, Bhatnagar M, Jain A, Sukhwal P, Sharma C, Jaiswal N (2014) Effects of mobile phone radiation (900 MHz radiofrequency) on structure and functions of rat brain. Neurol Res 36(12):1072–1079. CrossRefGoogle Scholar
  107. Salford LG, Brun A, Sturesson K, Eberhardt JL, Persson BR (1994) Permeability of the blood-brain barrier induced by 915 MHz electromagnetic radiation, continuous wave and modulated at 8, 16, 50, and 200 Hz. Microsc Res Techniq 27(6):535–542Google Scholar
  108. Salford LG, Bru AE, Eberhardt JL, Malmgren L, Persson BR (2003) Nerve cell damage in mammalian brain after exposure to microwaves from GSM mobile phones. Environ Health Perspect 111(7):881–883Google Scholar
  109. Shahin S, Singh VP, Shukla RK (2013) 2.45 GHz microwave irradiation-induced oxidative stress affects implantation or pregnancy in mice, Mus musculus. Appl Biochem Biotechnol 169:1727–1751Google Scholar
  110. Shankaranarayana Rao BS, Govindaiah LTR, Meti BL, Raju TR (2001) Subicular lesions cause dendritic atrophy in CA1 and CA3 pyramidal neurons of the rat hippocampus. Neuroscience 102(2):319–327Google Scholar
  111. Sharma A, Sisodia R, Bhatnagar D, Saxena VK (2014) Spatial memory and learning performance and its relationship to protein synthesis of Swiss albino mice exposed to 10 GHz microwaves. Int J Radiat Biol 90(1):29–35Google Scholar
  112. Sharma A, Kesari KK, Saxena VK, Sisodia R (2017) The influence of prenatal 10 GHz microwave radiation exposure on a developing mice brain. Gen Physiol Biophys 36(1):41-51Google Scholar
  113. 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 31:355–362Google Scholar
  114. Sienkiewicz Z, van Rongen E (2019) Can low-level exposure to radiofrequency fields effect cognitive behaviour in laboratory animals? A systematic review of the literature related to spatial learning and place memory. Int J environ res public health. 8:16(9). Pii: E1607. Google Scholar
  115. Sirav B, Seyhan N (2009) Blood-brain barrier disruption by continuous-wave radio frequency radiation. Electromagn Biol Med 28(2):215–222Google Scholar
  116. Sloviter RS (1989) Calcium-binding protein (calbindin-D28k) and parvalbumin immunocytochemistry: localization in the rat hippocampus with specific reference to the selective vulnerability of hippocampal neurons to seizure activity. J Comp Neurol 280(2):183–196Google Scholar
  117. Sokolovic D, Djordjevic B, Kocic G, Babovic P, Ristic G, Stanojkovic Z, Sokolovic DM, Veljkovic A, Jankovic A, Radovanovic Z (2012) The effect of melatonin on body mass and behaviour of rats during an exposure to microwave radiation from mobile phone. Bratisl Lek Listy 113(5):265–269Google Scholar
  118. Son Y, Jeong YJ, Kwon JH, Choi HD, Pack JK, Kim N, Lee YS, Lee HJ (2016) 1950 MHz radiofrequency electromagnetic fields do not aggravate memory deficits in 5xFAD mice. Bioelectromagnetics 37(6):391–399. CrossRefGoogle Scholar
  119. Sonmez OF, Odaci E, Bas O, Kaplan S (2010) Purkinje cell number decreases in the adult female rat cerebellum following exposure to 900MHz electromagnetic field. Brain Res 1356:95–01Google Scholar
  120. Stam R (2010) Electromagnetic fields and the blood–brain barrier. Brain Res Rev 65(1):80–97Google Scholar
  121. Stefi AL, Margaritis LH, Skouroliakou AS, Vassilacopoulou D (2019) Mobile phone electromagnetic radiation affects amyloid precursor protein and α-synuclein metabolism in SH-SY5Y cells. Pathophysiology pii S0928-4680(18):30352–30353. [Epub ahead of print] CrossRefGoogle Scholar
  122. Steimer T (2002) The biology of fear- and anxiety-related behaviors dialogues. Clin Neurosci 4:231–249Google Scholar
  123. Tahvanainen K, Nino J, Halonen P, Kuusela T, Alanko T, Laitinen T, Lansimies E, Hietanen M, Lindholm H (2007) Effects of cellular phone use on ear canal temperature measured by NTC thermistors. Clin Physiol Funct Imaging 27(3):162–172Google Scholar
  124. Tang J, Zhang Y, Yang L, Chen Q, Tan L, Zuo S, Feng H, Chen Z, Zhu G (2015) Exposure to 900MHz electromagnetic fields activates the mkp-1/ERK pathway and causes blood-brain barrier damage and cognitive impairment in rats. Brain Res 1601:92–101Google Scholar
  125. Tice RR, Hook GG and Donner M (2002) Genotoxicity of radio frequency signals. Investigation of DNA damage and micronuclei induction in cultured human blood cells. Bioelectromagnetics. 23,113-126Google Scholar
  126. Tsybulin O, Sidorik E, Brieieva O, Buchynska L, Kyrylenko S, Henshel D, Yakymenko I (2013) GSM 900 MHz cellular phone radiation can either stimulate or depress early embryogenesis in Japanese quails depending on the duration of exposure. Int J Radiat Biol 89(9):756–763Google Scholar
  127. Walleczek J (1992) Electromagnetic field effects on cells of the immune system: the role of calcium signaling. FASEB J 6:3177–3185Google Scholar
  128. Wang K, Lu JM, Xing ZH, Zhao QR, Hu LQ, Xue L, Zhang J, Mei YA (2017) Effect of 1.8 GHz radiofrequency electromagnetic radiation on novel object associative recognition memory in mice. Sci Rep 7:44521. CrossRefGoogle Scholar
  129. WHO (World Health Organization) (2000). Office of Information.Electromagnetic field and public health: cautionary policies Geneva:World Health Organization
  130. WHO (World Health Organization) (2011), “Electromagnetic fields and public health: mobile phones”, Fact sheet No193,
  131. Yu-Hong Z, Yong Z, Tong-Jun Z, Ying-Rong H, Hui L (2007). Mechanism of permeation in calcium channels activation by applied magnetic fields. Conf proc IEEE Eng med biol Soc. 1391-3Google Scholar
  132. Zhang JP, Zhang KY, Guo L, Che QL, Gao P, Wang T, Li J, Guo GZ, Ding GR (2017) Effects of 1.8 GHz radiofrequency fields on the emotional behavior and spatial memory of adolescent mice. Int J Environ Res Public Health 14:1344Google Scholar
  133. Zhao TY, Zou SP, Knapp PE (2007) Exposure to cell phone radiation up-regulates apoptosis genes in primary cultures of neurons and astrocytes. Neurosci Lett 412:34–38Google Scholar
  134. Zhao YL, Yang JC, Zhang YH (2008). Effects of magnetic fields on intracellular calcium oscillations. Conf Proc IEEE Eng Med Biol Soc. 2124-7Google Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  1. 1.Department of Physiology, RAK College of Medical SciencesRAK Medical & Health Sciences UniversityRas Al KhaimahUAE
  2. 2.Department of Basic Medical Sciences, College of Applied Medical SciencesKing Khalid UniversityAbhaKingdom of Saudi Arabia
  3. 3.Department of Applied PhysicsAalto UniversityEspooFinland
  4. 4.Department of Basic SciencesCollege of Science and Health Professions–Jeddah, King Saud Bin Abdulaziz University for Health Sciences, National Guard Health AffairsJeddahKingdom of Saudi Arabia
  5. 5.Department of Anatomy, Melaka Manipal Medical College (Manipal Campus)Manipal Academy of Higher EducationManipalIndia
  6. 6.Division of Biotechnology, School of Life SciencesManipal Academy of Higher EducationManipalIndia

Personalised recommendations