Comparing the Effects of Long-term Exposure to Extremely Low-frequency Electromagnetic Fields With Different Values on Learning, Memory, Anxiety, and β-amyloid Deposition in Adult Rats

doi:10.32598/bcn.2021.1204.2

. 2021 Nov-Dec;12(6):849-860.

doi: 10.32598/bcn.2021.1204.2. Epub 2021 Nov 1.

Comparing the Effects of Long-term Exposure to Extremely Low-frequency Electromagnetic Fields With Different Values on Learning, Memory, Anxiety, and β-amyloid Deposition in Adult Rats

Nafiseh Faraji¹, Iraj Salehi¹, Akram Alizadeh^{2

3}, Arash Pourgholaminejad⁴, Alireza Komaki¹, Masoumeh Taheri Azandaryani¹, Reihaneh Sadeghian^{5

6}, Zoleikha Golipoor^{1

7}

Affiliations

¹ Neurophysiology Research Center, Hamadan University of Medical Sciences, Hamadan, Iran.
² Nervous System Stem Cells Research Center, Semnan University of Medical Sciences, Semnan, Iran.
³ Department of Tissue Engineering and Applied Cell Sciences, School of Medicine, Semnan University of Medical Sciences, Semnan, Iran.
⁴ Department of Immunology, School of Medicine, Guilan University of Medical Sciences, Rasht, Iran.
⁵ Medical Plants Research Center, Basic Health Sciences Institute, Shahrekord University of Medical Sciences, Shahrekord, Iran.
⁶ Department of Pharmacy, School of Medicine, Mashhad University of Medical Sciences, Mashhad, Iran.
⁷ Cellular and Molecular Research Center, School of Medicine, Guilan University of Medical Sciences, Rasht, Iran.

PMID: 35693151
PMCID: PMC9168822
DOI: 10.32598/bcn.2021.1204.2

Comparing the Effects of Long-term Exposure to Extremely Low-frequency Electromagnetic Fields With Different Values on Learning, Memory, Anxiety, and β-amyloid Deposition in Adult Rats

Nafiseh Faraji et al. Basic Clin Neurosci. 2021 Nov-Dec.

. 2021 Nov-Dec;12(6):849-860.

doi: 10.32598/bcn.2021.1204.2. Epub 2021 Nov 1.

Authors

Nafiseh Faraji¹, Iraj Salehi¹, Akram Alizadeh^{2

3}, Arash Pourgholaminejad⁴, Alireza Komaki¹, Masoumeh Taheri Azandaryani¹, Reihaneh Sadeghian^{5

6}, Zoleikha Golipoor^{1

7}

Affiliations

¹ Neurophysiology Research Center, Hamadan University of Medical Sciences, Hamadan, Iran.
² Nervous System Stem Cells Research Center, Semnan University of Medical Sciences, Semnan, Iran.
³ Department of Tissue Engineering and Applied Cell Sciences, School of Medicine, Semnan University of Medical Sciences, Semnan, Iran.
⁴ Department of Immunology, School of Medicine, Guilan University of Medical Sciences, Rasht, Iran.
⁵ Medical Plants Research Center, Basic Health Sciences Institute, Shahrekord University of Medical Sciences, Shahrekord, Iran.
⁶ Department of Pharmacy, School of Medicine, Mashhad University of Medical Sciences, Mashhad, Iran.
⁷ Cellular and Molecular Research Center, School of Medicine, Guilan University of Medical Sciences, Rasht, Iran.

PMID: 35693151
PMCID: PMC9168822
DOI: 10.32598/bcn.2021.1204.2

Abstract

Introduction: Extremely Low-Frequency Electromagnetic Fields (ELF-EMFs) have gathered significant consideration for their possible pathogenicity. However, their effects on the nervous system's functions were not fully clarified. This study aimed to assay the impact of ELF-EMFs with different intensities on memory, anxiety, antioxidant activity, β-amyloid (Aβ) deposition, and microglia population in rats.

Methods: Fifty male adult rats were randomly separated into 5 groups; 4 were exposed to a flux density of 1, 100, 500, and 2000 microtesla (μT), 50 Hz frequency for one h/day for two months, and one group as a control group. The control group was without ELF-EMF stimulation. After 8 weeks, passive avoidance and Elevated Plus Maze (EPM) tests were performed to assess memory formation and anxiety-like behavior, respectively. Total free thiol groups and the index of lipid peroxidation were evaluated. Additionally, for detection of Aβ deposition and stained microglia in the brain, anti-β-amyloid and anti-Iba1 antibodies were used.

Results: The step-through latency in the retention test in ELF-EMF exposure groups (100500 & 2000 μT) was significantly greater than the control group (P<0.05). Furthermore, the frequency of the entries into the open arms in ELF-EMF exposure groups (especially 2000 μT) decreased than the control group (P<0.05). No Aβ depositions were detected in the hippocampus of different groups. An increase in microglia numbers in the 100, 500, and 2000 μT groups was observed compared to the control and one μT group.

Conclusion: Exposure to ELF-EMF had an anxiogenic effect on rats, promoted memory, and induced oxidative stress. No Aβ depositions were detected in the brain. Moreover, the positive impact of ELF-EMF was observed on the microglia population in the brain.

Highlights: ELF-EMFs have gathered significant consideration for their possible pathogenicity.ELF-EMFs' effects on the nervous system's functions were not clarified yet.Positive impact of ELF-EMF was observed on the microglia population in the brain.

Plain language summary: ELF-EMFs effects on human health are a considerable concern. Studies revealed the adverse effects of ELF-EMF in neurological disorders such as Alzheimer's Disease (AD). Anxiety could be an early manifestation of AD. There is a correlation between occupational exposure to ELF-EMF and AD. Recently the researchers interested in the study of the effects of ELF-EMFs on the human body. Some studies examined the molecular mechanisms and the influence of ELF-EMFs on the biologic mechanisms in the body. Also, Microglia act in the Central Nervous system (CNS) immune responses; over-activated microglia can be responsible for devastating and progressive neurotoxic consequences in neurodegenerative disorders. This study aimed to evaluate the memory, anxiety, antioxidant activity, β-amyloid deposition, and frequency of the microglial cells exposed to microtesla (μT) and 2000 (μT) ELF-EMFs.

Keywords: Anxiety; Magnetic field; Memory; Microglial cell; Oxidative stress; β-amyloid.

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Conflict of interest statement

Conflict of interest The authors declared no conflict of interest.

Figures

**Figure 1**
The effect of exposure to magnetic fields on the delay in entering the dark area at the reminder stage (A) and on the presence in the dark area at the reminder stage (B). Con: Control group, 1μT: exposure group with magnetic field 1μT, 100μT: exposure groups with 100μT magnetic field, 500μT: exposure group with 500μT magnetic field, 2000μT: exposure group with magnetic field 2000μT (^*Significant when compared with the control group).

**Figure 2**
The effect of exposure to magnetic fields on the percentage of open arms entries A: The Elevated plus-maze; and B: On the percentage of time spent in open arms in the Elevated plus-maze. Con: Control group; 1μT: exposure group with magnetic field 1μT; 100μT: exposure groups with 100μT magnetic field; 500μT: exposure group with 500μT magnetic field; 2000μT: exposure group with magnetic field 2000μT. ^*Significant when compared with the control group.

**Figure 3**
The effects of magnetic fields exposure on TAC A: The effect of exposure to magnetic fields on serum levels of TAC (total antioxidant capacity); B: The effect of exposure to magnetic fields on serum levels of TOS (total oxidant status); C: The effect of exposure to magnetic fields on serum levels of thiol groups; D: Effect of exposure to magnetic fields on serum levels of Malondialdehyde (MDA). Con: Control group, 1 μT: exposure group with magnetic field 1 μT, 100 μT: exposure groups with 100 μT magnetic field, 500 μT: exposure group with 500 μT magnetic fields, 2000 μT: exposure group with magnetic field 2000 μT (^* significant when compared with the control group).

**Figure 4**
Immunohistochemistry images of β-amyloid staining using anti-beta amyloid antibody A: Control group; B: 1 μT group; C: 100 μT group; D: 500μT group; E: 2000 μT group; F: positive control group of β-amyloid.

**Figure 5**
Immunohistochemistry staining of microglial cells using anti-Iba1 antibody A-M: Nuclei staining by DAPI; B-N: Iba1 antibody staining using an anti-Iba1 antibody; C-O: Merge.

**Figure 6**
Column chart of the expression of Iba-1 in different groups A: Compared to control group; B: Compared to100 μT and 500μT groups.

See this image and copyright information in PMC

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References

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[1] Alizadeh R., Hassanzadeh G., Soleimani M., Joghataei M. T., Siavashi V., Khorgami Z. (2015). Gender and age related changes in number of dopaminergic neurons in adult human olfactory bulb. Journal of Chemical Neuroanatomy 69, 1–6. [DOI:10.1016/j.jchemneu.2015.07.003] [PMID ] - DOI - PubMed

[2] Alizadeh R., Hassanzadeh G., Soleimani M., Joghataei M. T., Siavashi V., Khorgami Z. (2015). Gender and age related changes in number of dopaminergic neurons in adult human olfactory bulb. Journal of Chemical Neuroanatomy 69, 1–6. [DOI:10.1016/j.jchemneu.2015.07.003] [PMID ] - DOI - PubMed

[3] Asadbegi M., Komaki A., Salehi I., Yaghmaei P., Ebrahim Habibi A., Shahidi S., et al. (2018). Effects of thymol on amyloid-β-induced impairments in hippocampal synaptic plasticity in rats fed a high-fat diet. Brain Research Bulletin, 137, 338–50. [DOI:10.1016/j.brainresbull.2018.01.008] [PMID ] - DOI - PubMed

[4] Asadbegi M., Komaki A., Salehi I., Yaghmaei P., Ebrahim Habibi A., Shahidi S., et al. (2018). Effects of thymol on amyloid-β-induced impairments in hippocampal synaptic plasticity in rats fed a high-fat diet. Brain Research Bulletin, 137, 338–50. [DOI:10.1016/j.brainresbull.2018.01.008] [PMID ] - DOI - PubMed

[5] Cho H., Seo Y. K., Yoon H. H., Kim S. C., Kim S. M., Song K. Y., et al. (2012). Neural stimulation on human bone marrow-derived mesenchymal stem cells by extremely low frequency electromagnetic fields. Biotechnol Progress, 28(5), 1329–35. [DOI:10.1002/btpr.1607] [PMID ] - DOI - PubMed

[6] Cho H., Seo Y. K., Yoon H. H., Kim S. C., Kim S. M., Song K. Y., et al. (2012). Neural stimulation on human bone marrow-derived mesenchymal stem cells by extremely low frequency electromagnetic fields. Biotechnol Progress, 28(5), 1329–35. [DOI:10.1002/btpr.1607] [PMID ] - DOI - PubMed

[7] Chu L. Y., Lee J. H., Nam Y. S., Lee Y. J., Park W. H., Lee B. C., et al. (2011). Extremely low frequency magnetic field induces oxidative stress in mouse cerebellum. General Physiology and Biophysics, 30(4), 415–21. [DOI:10.4149/gpb_2011_04_415] [PMID ] - DOI - PubMed

[8] Chu L. Y., Lee J. H., Nam Y. S., Lee Y. J., Park W. H., Lee B. C., et al. (2011). Extremely low frequency magnetic field induces oxidative stress in mouse cerebellum. General Physiology and Biophysics, 30(4), 415–21. [DOI:10.4149/gpb_2011_04_415] [PMID ] - DOI - PubMed

[9] Cichoń N., Bijak M., Miller E., Saluk J. (2017). Extremely low frequency electromagnetic field (ELF-EMF) reduces oxidative stress and improves functional and psychological status in ischemic stroke patients. Bioelectromagnetics, 38(5), 386–96. [DOI:10.1002/bem.22055] [PMID ] - DOI - PubMed

[10] Cichoń N., Bijak M., Miller E., Saluk J. (2017). Extremely low frequency electromagnetic field (ELF-EMF) reduces oxidative stress and improves functional and psychological status in ischemic stroke patients. Bioelectromagnetics, 38(5), 386–96. [DOI:10.1002/bem.22055] [PMID ] - DOI - PubMed

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Comparing the Effects of Long-term Exposure to Extremely Low-frequency Electromagnetic Fields With Different Values on Learning, Memory, Anxiety, and β-amyloid Deposition in Adult Rats

Affiliations

Comparing the Effects of Long-term Exposure to Extremely Low-frequency Electromagnetic Fields With Different Values on Learning, Memory, Anxiety, and β-amyloid Deposition in Adult Rats

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