UDC

612.8:57.042

DOI

10.37482/2687-1491-Z256

Authors

Natalia I. Khorseva* ORCID: https://orcid.org/0000-0002-3444-0050
*Emanuel Institute of Biochemical Physics, Russian Academy of Sciences (Moscow, Russia)
**Sevastopol State University (Sevastopol, Russia)
***Sechenov Academic Research Institute of Physical Treatment Methods, Medical Climatology and Rehabilitation (Yalta, Republic of Crimea, Russia)

Abstract

This paper is a continuation of a series of reviews of research into the effect of radiofrequency electromagnetic fields (RF EMF) on the nervous system of young animals in vitro and in vivo. The first review considered changes in the action potential and permeability of the blood–brain barrier, transformations in cell and myelin sheath morphology, as well as materials presenting various approaches to studying the effects of RF EMF. The second review analysed the morphological and histological changes in the central nervous system, primarily in the hippocampus, which is involved in the formation of emotions and spatial memory (necessary for navigation) as well as in the consolidation of information from short-term memory to long-term memory. Since the identified changes in the hippocampus can affect cognitive processes and behaviour, this paper examines experimental data obtained using behavioural tests looking into the effects of RF EMF, Wi-Fi and 5G on the cognitive processes and psycho-emotional state of young animals (rats and mice). The article analyses methods for studying cognitive processes and psycho-emotional state in rodents, as well as changes in spatial memory, levels of anxiety-like behaviour, fear, stress and depressive-like behaviour when exposed to RF EMF of various frequency ranges (from 900 MHz to 10 GHz), Wi-Fi and 5G. The presented results allow us to consider the adverse impact of cellular electromagnetic fields produced by cellular networks on the nervous system of young animals proven and to give an indirect assessment of possible negative changes in children and adolescents as the cohort most vulnerable to any environmental factors. These data should be taken into account when developing specific regulations for the use of RF EMF among the young population and/or adjusting the existing standards in the context of ever-increasing electromagnetic pollution.

Keywords

radiofrequency electromagnetic field, Wi-Fi, 5G, spatial memory, anxiety, anxiety-like behaviour, depressive-like behaviour, young animals

References

1. Khorseva N.I., Grigoriev P.E. Effects of Radio Frequency Electromagnetic Fields on the Nervous System. In vivo Experiments (Review). J. Med. Biol. Res., 2024, vol. 12, no. 3, pp. 383–398. https://doi.org/10.37482/2687-1491-Z195
2. Amikishieva A.V. Povedencheskoe fenotipirovanie: sovremennye metody i oborudovanie [Behavioral Phenotyping: Up-to-Date Methods and Equipment]. Informatsionnyy vestnik VOGiS, 2009, vol. 13, no. 3, pp. 529–542.
3. Belyakov V.I., Gromova D.S., Popova N.R., Myakisheva Yu.V. Modern Methods for Studying Rodent Behavior in Model Biomedical Studies (Problem Review). Mod. Iss. Biomed., 2022, vol. 6, no. 4. Art. no. 1 (in Russ.). https://doi.org/10.51871/2588-0500_2022_06_04_1
4. Khorseva N.I., Grigoriev P.E. Electromagnetic Fields of Cellular Communication as a Health Risk Factor for Children and Adolescents (Review). Health Risk Anal., 2023, no. 2, pp. 186–193. https://doi.org/10.21668/health.risk/2023.2.18.eng
5. Khorseva N.I., Grigoriev P.E. Assessing the Risk of Negative Effects Produced by Electromagnetic Fields of Cellular Communication on the Central Nervous System of Children and Adolescents (Review). Part 2. Indicators of Cognitive Processes. Health Risk Anal., 2024, no. 3, pp. 146–154. https://doi.org/10.21668/health.risk/2024.3.15.eng
6. Lai Y.-F., Wang H.-Y., Peng R.-Y. Establishment of Injury Models in Studies of Biological Effects Induced by Microwave Radiation. Mil. Med. Res., 2021, vol. 8, no. 1. Art. no. 12. https://doi.org/10.1186/s40779-021-00303-w
7. Narayanan S.N., Kumar R.S., Potu B.K., Nayak S., Mailankot M. Spatial Memory Performance of Wistar Rats Exposed to Mobile Phone. Clinics (Sao Paulo), 2009, vol. 64, no. 3, pp. 231–234. https://doi.org/10.1590/s1807-59322009000300014
8. Fragopoulou A.F., Miltiadous P., Stamatakis A., Stylianopoulou F., Koussoulakos S.L., Margaritis L.H. Whole Body Exposure with GSM 900MHz Affects Spatial Memory in Mice. Pathophysiology, 2010, vol. 17, no. 3, pp. 179–187. https://doi.org/10.1016/j.pathophys.2009.11.002
9. Deshmukh P.S., Banerjee B.D., Abegaonkar M.P., Megha K., Ahmed R.S., Tripathi A.K., Mediratta P.K. Effect of Low Level Microwave Radiation Exposure on Cognitive Function and Oxidative Stress in Rats. Indian J. Biochem. Biophys., 2013, vol. 50, no. 2, pp. 114–119.
10. Wang H., Peng R., Zhou H., Wang S., Gao Y., Wang L., Yong Z., Zuo H., Zhao L., Dong J., Xu X., Su Z. Impairment of Long-Term Potentiation Induction Is Essential for the Disruption of Spatial Memory After Microwave Exposure. Int. J. Radiat. Biol., 2013, vol. 89, no. 12, pp. 1100–1107. https://doi.org/10.3109/09553002.2013.817701
11. Sharma A., Sisodia R., Bhatnagar D., Saxena V.K. Spatial Memory and Learning Performance and Its Relationship to Protein Synthesis of Swiss Albino Mice Exposed to 10 GHz Microwaves. Int. J. Radiat. Biol., 2014, vol. 90, no. 1, pp. 29–35. https://doi.org/10.3109/09553002.2013.835883
12. Qiao S., Peng R., Yan H., Gao Y., Wang C., Wang S., Zou Y., Xu X., Zhao L., Dong J., Su Z., Feng X., Wang L., Hu X. Reduction of Phosphorylated Synapsin I (ser-553) Leads to Spatial Memory Impairment by Attenuating GABA Release After Microwave Exposure in Wistar Rats. PLoS One, 2014, vol. 9, no. 4. Art. no. e95503. https://doi.org/10.1371/journal.pone.0095503
13. Saikhedkar N., Bhatnagar M., Jain A., Sukhwal P., Sharma C., Jaiswal N. Effects of Mobile Phone Radiation (900 MHz Radiofrequency) on Structure and Functions of Rat Brain. Neurol. Res., 2014, vol. 36, no. 12, pp. 1072–1079. https://doi.org/10.1179/1743132814y.0000000392
14. Li H.-J., Peng R.-Y., Wang C.-Z., Qiao S.-M., Yong Z., Gao Y.-B., Xu X.-P., Wang S.-X., Dong J., Zuo H.-Y., Li Z., Zhou H.-M., Wang L.-F., Hu X.-J. Alterations of Cognitive Function and 5-HT System in Rats After Long Term Microwave Exposure. Physiol. Behav., 2015, vol. 140, pp. 236–246. https://doi.org/10.1016/j.physbeh.2014.12.039
15. Narayanan S.N., Kumar R.S., Karun K.M., Nayak S.B., Bhat P.G. Possible Cause for Altered Spatial Cognition of Prepubescent Rats Exposed to Chronic Radiofrequency Electromagnetic Radiation. Metab. Brain Dis., 2015, vol. 30, no. 5, pp. 1193–1206. https://doi.org/10.1007/s11011-015-9689-6
16. Tang J., Zhang Y., Yang L., Chen Q., Tan L., Zuo S., Feng H., Chen Z., Zhu G. Exposure to 900 MHz Electromagnetic Fields Activates the mkp-1/ERK Pathway and Causes Blood-Brain Barrier Damage and Cognitive Impairment in Rats. Brain Res., 2015, vol. 1601, pp. 92–101. https://doi.org/10.1016/j.brainres.2015.01.019
17. Deshmukh P.S., Megha K., Nasare N., Banerjee B.D., Ahmed R.S., Abegaonkar M.P., Tripathi A.K., Mediratta P.K. Effect of Low Level Subchronic Microwave Radiation on Rat Brain. Biomed. Environ. Sci., 2016, vol. 29, no. 12, pp. 858–867. https://doi.org/10.3967/bes2016.115
18. Sharma A., Kesari K.K., Saxena V.K., Sisodia R. Ten Gigahertz Microwave Radiation Impairs Spatial Memory, Enzymes Activity, and Histopathology of Developing Mice Brain. Mol. Cell. Biochem., 2017, vol. 435, no. 1–2, pp. 1–13. https://doi.org/10.1007/s11010-017-3051-8
19. Zhang J.-P., Zhang K.-Y., Guo L., Chen Q.-L., Gao P., Wang T., Li J., Guo G.-Z., Ding G.-R. Effects of 1.8 GHz Radiofrequency Fields on the Emotional Behavior and Spatial Memory of Adolescent Mice. Int. J. Environ. Res. Public Health, 2017, vol. 14, no. 11. Art. no. 1344. https://doi.org/10.3390/ijerph14111344
20. Wang H., Tan S., Xu X., Zhao L., Zhang J., Yao B., Gao Y., Zhou H., Peng R. Long Term Impairment of Cognitive Functions and Alterations of NMDAR Subunits After Continuous Microwave Exposure. Physiol. Behav., 2017, vol. 181, pp. 1–9. https://doi.org/10.1016/j.physbeh.2017.08.022
21. Tan S., Wang H., Xu X., Zhao L., Zhang J., Dong J., Yao B., Wang H., Zhou H., Gao Y., Peng R. Study on Dose-Dependent, Frequency-Dependent, and Accumulative Effects of 1.5 GHz and 2.856 GHz Microwave on Cognitive Functions in Wistar Rats. Sci. Rep., 2017, vol. 7, no. 1. Art. no. 10781. https://doi.org/10.1038/s41598-017-11420-9
22. Zhi W.-J., Peng R.-Y., Li H.-J., Zou Y., Yao B.-W., Wang C.-Z., Liu Z.-H., Gao X.-H., Xu X.-P., Dong J., Zhao L., Zhou H.-M., Wang L.-F., Hu X.-J. Microwave Radiation Leading to Shrinkage of Dendritic Spines in Hippocampal Neurons Mediated by SNK–SPAR Pathway. Brain Res., 2018, vol. 1679, pp. 134–143. https://doi.org/10.1016/j.brainres.2017.11.020
23. Varghese R., Majumdar A., Kumar G., Shukla A. Rats Exposed to 2.45 GHz of Non-Ionizing Radiation Exhibit Behavioral Changes with Increased Brain Expression of Apoptotic Caspase 3. Pathophysiology, 2018, vol. 25, no. 1, pp. 19–30. https://doi.org/10.1016/j.pathophys.2017.11.001
24. Sharaf N.E., Galal A.F., El-Sawy M.S., Shalby A.B., Sayed A.H., Ahmed H.H. Role of Designed Bio-Geometrical Forms in Antagonizing Neurobehavioral Burden of Wi-Fi Radiation: Evidence-Based Experimental Study. Biomed. Pharmacol. J., 2019, vol. 12, no. 3. https://dx.doi.org/10.13005/bpj/1751
25. Tan S., Wang H., Xu X., Zhao L., Zhang J., Dong J., Yao B., Wang H., Hao Y., Zhou H., Gao Y., Peng R. Acute Effects of 2.856 GHz and 1.5 GHz Microwaves on Spatial Memory Abilities and CREB-Related Pathways. Sci. Rep., 2021, vol. 11, no. 1. Art. no. 12348. https://doi.org/10.1038/s41598-021-91622-4
26. Zhu R., Wang H., Xu X., Zhao L., Zhang J., Dong J., Yao B., Wang H., Zhou H., Gao Y., Peng R. Effects of 1.5 and 4.3 GHz Microwave Radiation on Cognitive Function and Hippocampal Tissue Structure in Wistar Rats. Sci. Rep., 2021, vol. 11, no. 1. Art. no. 10061. https://doi.org/10.1038/s41598-021-89348-4
27. Wang H., Liu Y., Sun Y., Zhao L., Dong J., Xu X., Wang H., Zhang J., Yao B., Zhao X., Liu S., Zhang K., Peng R. Changes in Rat Spatial Learning and Memory as Well as Serum Exosome Proteins After Simultaneous Exposure to 1.5 GHz and 4.3 GHz Microwaves. Ecotoxicol. Environ. Saf., 2022, vol. 243. Art. no. 113983. https://doi.org/10.1016/j.ecoenv.2022.113983
28. Zheng R., Zhang X., Gao Y., Gao D., Gong W., Zhang C., Dong G., Li Z. Biological Effects of Exposure to 2650 MHz Electromagnetic Radiation on the Behavior, Learning, and Memory of Mice. Brain Behav., 2023, vol. 13, no. 6. Art. no. e3004. https://doi.org/10.1002/brb3.3004
29. Wang H., Song L., Zhao L., Wang H., Xu X., Dong J., Zhang J., Yao B., Zhao X., Peng R. The Dose-Dependent Effect of 1.5-GHz Microwave Exposure on Spatial Memory and the NMDAR Pathway in Wistar Rats. Environ. Sci. Pollut. Res., 2023, vol. 30, no. 13, pp. 37427–37439. https://doi.org/10.1007/s11356-022-24850-4
30. Wang H., Liu Y., Sun Y., Dong J., Xu X., Wang H., Zhao X., Zhang J., Yao B., Zhao L., Liu S., Peng R. Changes in Cognitive Function, Synaptic Structure and Protein Expression After Long-Term Exposure to 2.856 and 9.375 GHz Microwaves. Cell Commun. Signal., 2023, vol. 21. Art. no. 34. https://doi.org/10.1186/s12964-022-01011-1
31. Krivova N.A., Kudabaeva M.S., Zaeva O.B., Borodina S.V., Lepekhina T.B., Pavlenko O.A., Makhmanazarov R.M., Kokin D.S., Shipilov S.E. The Effect of Exposure to RF-EMF from the Laboratory Simulator of 5G NR Base Station on Physiological Parameters and Cognitive Abilities of Male Wistar Rats of Different Ages. Sci. Rep., 2024, vol. 14, no. 1. Art. no. 10283. https://doi.org/10.1038/s41598-024-60862-5
32. Chernyuk D.P., Bol’shakova A.V., Vlasova O.L., Bezprozvanny I.B. Opportunities and Prospects of the Behavioral Test “Morris Water Maze”. Russ. J. Physiol., 2021, vol. 107, no. 3, pp. 267–287 (in Russ.). https://doi.org/10.31857/S0869813921030043
33. Iptyshev A.M., Gorina Ya.V., Lopatina O.L., Komleva Yu.K., Chernykh A.I., Belova O.A., Salmina A.B. Sravnenie testov “Vos’mirukavnyy radial’nyy labirint” i “Vodnyy labirint Morrisa” pri otsenke prostranstvennoy pamyati u eksperimental’nykh zhivotnykh v khode neyropovedencheskogo testirovaniya [Comparison of Radial Arm Maze and Morris Water Maze for Evaluation of Spatial Memory in Experimental Animals During Neurobehavioral Testing]. Fundamental’naya i klinicheskaya meditsina, 2017, vol. 2, no. 2, pp. 62–69.
34. Keleş A.İ., Yıldırım M., Gedikli Ö., Çolakoğlu S., Kaya H., Baş O., Sönmez O.F., Odacı E. 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., 2018, vol. 94, pp. 46–53. https://doi.org/10.1016/j.jchemneu.2018.08.006
35. Hao D., Yang L., Chen S., Tian Y., Wu S. 916 MHz Electromagnetic Field Exposure Affects Rat Behavior and Hippocampal Neuronal Discharge. Neural Regen. Res., 2012, vol. 7, no. 19, pp. 1488–1492. https://doi.org/10.3969/j.issn.1673-5374.2012.19.007
36. Hao D., Yang L., Chen S., Tong J., Tian Y., Su B., Wu S., Zeng Y. Effects of Long-Term Electromagnetic Field Exposure on Spatial Learning and Memory in Rats. Neurol. Sci., 2013, vol. 34, no. 2, pp. 157–164. https://doi.org/10.1007/s10072-012-0970-8
37. Gupta S.K., Patel S.K., Tomar M.S., Singh S.K., Mesharam M.K., Krishnamurthy S. Long-Term Exposure of 2450 MHz Electromagnetic Radiation Induces Stress and Anxiety Like Behavior in Rats. Neurochem. Int., 2019, vol. 128, pp. 1–13. https://doi.org/10.1016/j.neuint.2019.04.001
38. Gökçek-Saraç Ç., Akçay G., Karakurt S., Ateş K., Özen Ş., Derin N. Possible Effects of Different Doses of 2.1 GHz Electromagnetic Radiation on Learning, and Hippocampal Levels of Cholinergic Biomarkers in Wistar Rats. Electromagn. Biol. Med., 2021, vol. 40, no. 1, pp. 179–190. https://doi.org/10.1080/15368378.2020.1851251
39. Zibarev E.V., Afanasev A.S., Slusareva O.V., Bulavina I.D. Exploratory Studies of the Influence of Wireless Equipment on the Body of Laboratory Animals. Hyg. Sanitation, 2017, vol. 96, no. 7, pp. 661–664 (in Russ.). http://dx.doi.org/10.18821/0016-9900-2017-96-7-661-664
40. Sharma S., Shukla S. Effect of Electromagnetic Radiation on Redox Status, Acetylcholine Esterase Activity and Cellular Damage Contributing to the Diminution of the Brain Working Memory in Rats. J. Chem. Neuroanat., 2020, vol. 106. Art. no. 101784. https://doi.org/10.1016/j.jchemneu.2020.101784
41. Jiang S., Ma Y., Shi Y., Zou Y., Yang Z., Zhi W., Zhao Z., Shen W., Chen L., Wu Y., Wang L., Hu X., Wu H. Acute Exposure of Microwave Impairs Attention Process by Activating Microglial Inflammation. Cell Biosci., 2024, vol. 14, no. 1. Art. no. 2. https://doi.org/10.1186/s13578-023-01162-9
42. Qin T.-Z., Wang X., Du J.-Z., Lin J.-J., Xue Y.-Z., Guo L., Lai P.-P., Jing Y.-T., Zhang Z.-W., Ding G.-R. Effects of Radiofrequency Field from 5G Communications on the Spatial Memory and Emotionality in Mice. Int. J. Environ. Health Res., 2024, vol. 34, no. 1, pp. 316–327. https://doi.org/10.1080/09603123.2022.2149708
43. Narayanan S.N., Kumar R.S., Potu B.K., Nayak S., Bhat P.G., Mailankot M. Effect of Radio-Frequency Electromagnetic Radiations (RF-EMR) on Passive Avoidance Behaviour and Hippocampal Morphology in Wistar Rats. Ups. J. Med. Sci., 2010, vol. 115, no. 2, pp. 91–96. https://doi.org/10.3109/03009730903552661
44. Murai T., Okuda S., Tanaka T., Ohta H. Characteristics of Object Location Memory in Mice: Behavioral and Pharmacological Studies. Physiol. Behav., 2007, vol. 90, no. 1, pp. 116–124. https://doi.org/10.1016/j.physbeh.2006.09.013
45. Kim J.H., Chung K.H., Hwang Y.R., Park H.R., Kim H.J., Kim H.-G., Kim H.R. Exposure to RF-EMF Alters Postsynaptic Structure and Hinders Neurite Outgrowth in Developing Hippocampal Neurons of Early Postnatal Mice. Int. J. Mol. Sci., 2021, vol. 22, no. 10. Art. no. 5340. https://doi.org/10.3390/ijms22105340
46. Attah T.A., Ayantunji B., Adamu A., Omede A., Leleji J., Hussiani S., Enemali J.-P., Suleiman Z.I., Dumbiri C., Bwala I., Polok C. Biological Effects of High Radiofrequency Radiation on Wistar Rats: A Literature Review. J. Public Health Int., 2022, vol. 5, no. 2, pp. 1–31. https://doi.org/10.14302/issn.2641-4538.jphi-22-4197
47. Belyaev I., Blackman C., Chamberlin K., DeSalles A., Dasdag S., Fernández C., Hardell L., Héroux P., Kelley E., Kesari K., Maisch D., Mallery-Blythe E., Melnick R.L., Miller A., Moskowitz J.M., Sun W., Yakymenko I. Scientific Evidence Invalidates Health Assumptions Underlying the FCC and ICNIRP Exposure Limit Determinations for Radiofrequency Radiation: Implications for 5G. Environ. Health, 2022, vol. 21, no. 1. Art. no. 92. https://doi.org/10.1186/s12940-022-00900-9
48. Uche U.I., Naidenko O.V. Development of Health-Based Exposure Limits for Radiofrequency Radiation from Wireless Devices Using a Benchmark Dose Approach. Environ. Health, 2021, vol. 20, no. 1. Art. no. 84. https://doi.org/10.1186/s12940-021-00768-1