Volume 21, Issue 1 (Iranian South Medical Journal 2018)                   Iran South Med J 2018, 21(1): 40-53 | Back to browse issues page

XML Persian Abstract Print

Download citation:
BibTeX | RIS | EndNote | Medlars | ProCite | Reference Manager | RefWorks
Send citation to:

Tekieh E, Kazemi M, Tavakoli H, Saberi M, Ghanaati H, Hajinasrollah M, et al . The Effect of Extremely Low Frequency Electromagnetic Fields on Visual Learning, Memory and Anatomical Structures of the Brain in Male Rhesus Monkeys. Iran South Med J 2018; 21 (1) :40-53
URL: http://ismj.bpums.ac.ir/article-1-913-en.html
1- Neuroscience Research Center, Baqiyatallah University of Medical Sciences, Tehran, Iran
2- Department of Pharmacology & Toxicology, Faculty of pharmacy, Baqiyatallah University of Medical Sciences, Tehran, Iran
3- Department of Radiology Medical Imaging Center, Imam Khomeini Hospital, Tehran University of Medical Sciences, Tehran, Iran
4- Animal core facility, Reproductive Biomedicine Research Center, Royan Institute for Biotechnology, ACECR, Tehran, Iran
5- Department of Electrical, Biomedical and Mechatronics Engineering, Qazvin Branch, Islamic Azad University, Qazvin, Iran.
6- Neuroscience Research Center, Baqiyatallah University of Medical Sciences, Tehran, Iran , hsahrei1343@gmail.com
Abstract:   (6042 Views)
Background: Humans in modern societies are exposed to substantially elevated levels of electromagnetic field (EMF) emissions with different frequencies. The neurobiological effects of EMF have been the subject of debate and intensive research over the past few decades. Therefore, we evaluated the effects of EMF on visual learning and anatomical dimensions of the hippocampus and the prefrontal area (PFA) in male Rhesus monkeys.
Materials and Methods: In this study, four rhesus monkeys of Macaca mulatta species were irradiated by 0.7 microtesla ELF-EMF either at 5 or 30 Hz, 4 h a day, for 30 days. Alterations in visual learning and memory were assessed before and after irradiation phase by using a box designed for challenging animals for gaining rewards. Furthermore, the monkeys’ brains were scanned by MRI technique one week before and one week after irradiation. The monkeys were anesthetized by intramuscular injection of ketamine hydrochloride (10–20 mg/kg) and xylazine (0.2–0.4 mg/kg), and scanned with a 3-Tesla Magnetom, in axial, sagittal, and coronal planes using T2 weighted protocol with a slice thickness of 3 mm. The anatomical changes of hippocampus and the prefrontal area (PFA) were measured by volumetric study.
Results: Electromagnetic field exposure at a frequency of 30 Hz reduced the number of correct responses in the learning process and delayed memory formation in the two tested monkeys. Meanwhile, ELF-EMF at 5 Hz had no effect on the visual learning and memory changes. No anatomical changes were observed in the prefrontal area and the hippocampus at both frequencies. 
Conclusion: ELF-EMF irradiation at 30 Hz adversely affected visual learning and memory, probably through factors other than changes in brain structure and anatomy.
Full-Text [PDF 1109 kb]   (3310 Downloads)    
Type of Study: Original | Subject: Nervous System
Received: 2017/04/26 | Accepted: 2017/09/25 | Published: 2018/02/26

1. Repacholi MH, editor An overview of WHO's EMF project and the health effects of EMF exposure. Proceedings of the International Conference on Non-Ionizing Radiation at UNITEN (ICNIR 2003) Electromagnetic Fields and Our Health; October 2003: 20-22.
2. Lacy-Hulbert A, Metcalfe JC, Hesketh R. Biological responses to electromagnetic fields. FASE J. 1998;12(6):395-420. [DOI:10.1096/fasebj.12.6.395]
3. Legros A, Modolo J, Brown S, et al. Effects of a 60 Hz Magnetic Field Exposure Up to 3000 μT on Human Brain Activation as Measured by Functional Magnetic Resonance Imaging. PloS one. 2015;10(7):1-27. [DOI:10.1371/journal.pone.0132024]
4. Gajšek P, Ravazzani P, Grellier J, et al. Review of Studies Concerning Electromagnetic Field (EMF) Exposure Assessment in Europe: Low Frequency Fields (50 Hz-100 kHz). International Journal of Environmental Research and Public Health. 2016;13(9):875. [DOI:10.3390/ijerph13090875]
5. Hannay G, Leavesley D, Pearcy M. Timing of pulsed electromagnetic field stimulation does not affect the promotion of bone cell development. Bio electro magnetics. 2005;26(8):670-6. [DOI:10.1002/bem.20166]
6. De Mattei M, Caruso A, Traina GC, et al. Correlation between pulsed electromagnetic fields exposure time and cell proliferation increase in human osteosarcoma cell lines and human normal osteoblast cells in vitro. Bio electro magnetics. 1999;20(3):177-82. https://doi.org/10.1002/(SICI)1521-186X(1999)20:3<177::AID-BEM4>3.0.CO;2-# [DOI:10.1002/(SICI)1521-186X(1999)20:33.0.CO;2-#]
7. Baker LL, Chambers R, DeMuth SK, et al. Effects of electrical stimulation on wound healing in patients with diabetic ulcers. Diabetes care. 1997;20(3):405-12. [DOI:10.2337/diacare.20.3.405]
8. Trock DH, Bollet AJ, Dyer RH, et al. double-blind trial of the clinical effects of pulsed electromagnetic fields in osteoarthritis. Journal of rheumatol. 1993;20:456-60. [DOI:10.1097/00002508-199303000-00013]
9. Okano H, Ohkubo C. Modulatory effects of static magnetic fields on blood pressure in rabbits. Bio electro magnetics. 2001;22(6):408-18. [DOI:10.1002/bem.68]
10. Benzel EC, Hart BL, Ball PA, et al. Magnetic resonance imaging for the evaluation of patients with occult cervical spine injury. Journal of neurosurgery. 1996;85(5):824-9. [DOI:10.3171/jns.1996.85.5.0824]
11. Hardell L, Sage C. Biological effects from electromagnetic field exposure and public exposure standards. Biomedicine & pharmacotherapy. 2008;62(2):104-9. [DOI:10.1016/j.biopha.2007.12.004]
12. Mostafa RM, Mostafa YM, Ennaceur A. Effects of exposure to extremely low-frequency magnetic field of 2 G intensity on memory and corticosterone level in rats. Physiology & behavior. 2002;76(4-5):589-95. [DOI:10.1016/S0031-9384(02)00730-8]
13. Hao D, Yang L, Chen S, et al. Effects of long-term electromagnetic field exposure on spatial learning and memory in rats. Neurological Sciences. 2013; 34(2):157-64. [DOI:10.1007/s10072-012-0970-8]
14. Liu T, Wang S, He L, et al. Chronic exposure to low-intensity magnetic field improves acquisition and maintenance of memory. Neuroreport. 2008;19(5):549-52. [DOI:10.1097/WNR.0b013e3282f8b1a0]
15. Liu X, Zuo H, Wang D, Peng R, Song T, Wang S, et al. Improvement of spatial memory disorder and hippocampal damage by exposure to electromagnetic fields in an Alzheimer's disease rat model. PloS one. 2015;10(5):e0126963. [DOI:10.1371/journal.pone.0126963]
16. Akhtary Z, Rashidy-Pour A, Vafaei AA, et al. Effects of extremely low-frequency electromagnetic fields on learning and memory and anxiety-like behaviors in rats. Koomesh 2011;12(4):435-46. (Persian)
17. Delaney RC, Rosen AJ, Mattson RH, et al. Memory function in focal epilepsy: a comparison of non-surgical, unilateral temporal lobe and frontal lobe samples. Cortex 1980;16(1):103-17. [DOI:10.1016/S0010-9452(80)80026-8]
18. Wheeler MA, Stuss DT, Tulving E. Toward a theory of episodic memory: the frontal lobes and autonoetic consciousness. Psychological bulletin. 1997; 121(3): 331-54. [DOI:10.1037/0033-2909.121.3.331]
19. Prabhakaran V, Narayanan K, Zhao Z, et al. Integration of diverse information in working memory within the frontal lobe. Nature neuroscience. 2000; 3(1):85-90. [DOI:10.1038/71156]
20. Kolb B, Fantie B. Development of the child's brain and behavior. Handbook of clinical child neuropsychology: Springer; 1997; 17-41. [DOI:10.1007/978-1-4757-5351-6_2]
21. Rojas DC, Peterson E, Winterrowd E, et al. Regional gray matter volumetric changes in autism associated with social and repetitive behavior symptoms. BMC psychiatry. 2006; 6(1):56. [DOI:10.1186/1471-244X-6-56]
22. Hazlett HC, Poe M, Gerig G, et al. Magnetic resonance imaging and head circumference study of brain size in autism: birth through age 2 years. Archives of general psychiatry. 2005; 62(12): 1366-76. [DOI:10.1001/archpsyc.62.12.1366]
23. Koivisto M, Krause CM, Revonsuo A, et al. The effects of electromagnetic field emitted by GSM phones on working memory. Neuroreport. 2000;11(8): 1641-3. [DOI:10.1097/00001756-200006050-00009]
24. Rola R, Raber J, Rizk A, Otsuka S, VandenBerg SR, Morhardt DR, et al. Radiation-induced impairment of hippocampal neurogenesis is associated with cognitive deficits in young mice. Experimental neurology. 2004; 188(2): 316-30. [DOI:10.1016/j.expneurol.2004.05.005]
25. Lyons DM, Buckmaster PS, Lee AG, et al. Stress coping stimulates hippocampal neurogenesis in adult monkeys. Proceedings of the National Academy of Sciences. 2010; 107(33): 14823-7. [DOI:10.1073/pnas.0914568107]
26. Saleem KS, Logothetis NK. Atlas of the rhesus monkey brain in stereotaxic coordinates: a combined mri and histology: Academic Press; 2006.
27. Shanthi V, Singh D. Estimation of Hippocam-pus Volume from MRI Using ImageJ for Alz-heimer's Diagnosis. Atlas Journal of Medical & Biological Sciences 2011; 1 (1): 15-20. [DOI:10.5147/ajmbs.2011.0045]
28. Morey RA, Gold AL, LaBar KS, et al. Amygdala volume changes in posttraumatic stress disorder in a large case-controlled veterans group. Archives of general psychiatry. 2012; 69(11):1169-78. [DOI:10.1001/archgenpsychiatry.2012.50]
29. Shamy JL, Habeck Ch, Hof PR, et al. Volumetric correlates of spatiotemporal working and recognition memory impairment in aged rhesus monkeys. Cerebral cortex 2011; 21(7): 1559-73. [DOI:10.1093/cercor/bhq210]
30. Agarwal A, Desai NR, Makker K, et al. Effects of radiofrequency electromagnetic waves (RF-EMW) from cellular phones on human ejaculated semen: an in vitro pilot study. Fertility and sterility. 2009; 92(4): 1318-25. [DOI:10.1016/j.fertnstert.2008.08.022]
31. Atli E, Ünlü H. The effects of microwave frequency electromagnetic fields on the fecundity of Drosophila melanogaster. Turkish Journal of Biology. 2007; 31(1):1-5.
32. McKay BE, Persinger MA, Koren SA. Exposure to a theta-burst patterned magnetic field impairs memory acquisition and consolidation for contextual but not discrete conditioned fear in rats. Neuroscience Letters. 2000;292(2):99-102. [DOI:10.1016/S0304-3940(00)01437-3]
33. Chung YH, Lee YJ, Lee HS, et al. Extremely low frequency magnetic field modulates the level of neurotransmitters. The Korean journal of physiology & pharmacology. 2015;19(1): 15-20. [DOI:10.4196/kjpp.2015.19.1.15]
34. Davanipour Z, Sobel E. Long-term exposure to magnetic fields and the risks of Alzheimer's disease and breast cancer: Further biological research. Pathophysiology. 2009;16(2): 149-56. [DOI:10.1016/j.pathophys.2009.01.005]
35. J O. de LorgeJ. D. Grissett. Behavioral effects in monkeys exposed to extremely low frequency electromagnetic fields .International Journal of Biometeorology 1977; 21(4): 357- 65. [DOI:10.1007/BF01555197]
36. Nooshinfar E, Rezaei-Tavirani M, Khodakarim S. Long-term exposure to low frequency electro-magnetic fields of 50-and 217-Hz leads to learning and memory deficits in mice. Journal of Paramedical Sciences. 2012; 3(3): 30 -37
37. Foroozandeh E, Ahadi H, Askari P, et al. Effects of single, brief exposure to an 8 mT electromagnetic field on avoidance learning in male and female mice. Psychology & Neuroscience. 2011;4(1): 143-48 [DOI:10.3922/j.psns.2011.1.016]
38. Zhao QR, Lu JM, Yao JJ, et al. Neuritin reverses deficits in murine novel object associative recognition memory caused by exposure to extremely low-frequency (50 Hz) electromagnetic fields. Scientific reports. 2015; 5: 11768. [DOI:10.1038/srep11768]
39. He L, Shi H, Liu T, Xu Y, et al. Effects of extremely low frequency magnetic field on anxiety level and spatial memory of adult rats. Chinese medical journal. 2011;124(20): 3362-6.
40. Manikonda PK, Rajendra P, Devendranath D, et al. Influence of extremely low frequency magnetic fields on Ca 2+ signaling and NMDA receptor functions in rat hippocampus. Neuroscience letters. 2007; 413(2): 145-9. [DOI:10.1016/j.neulet.2006.11.048]
41. Liu X, Zuo H, Wang D, et al. Improvement of spatial memory disorder and hippocampal damage by exposure to electromagnetic fields in an Alzheimer's disease rat model. PloS one. 2015; 10(5): e0126963. [DOI:10.1371/journal.pone.0126963]
42. Zatorre RJ, Fields RD, Johansen-Berg H. Plasticity in gray and white: neuroimaging changes in brain structure during learning.Nature neuroscience. 2012; 15(4): 528-36. [DOI:10.1038/nn.3045]

Send email to the article author

Rights and Permissions
Creative Commons License This work is licensed under a Creative Commons Attribution-NonCommercial 4.0 International License.

© 2024 CC BY-NC 4.0 | Iranian South Medical Journal

Designed & Developed by: Yektaweb