Volume 9, Issue 3 (Issue in Progress 2018 2018)                   BCN 2018, 9(3): 167-176 | Back to browse issues page


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1- Neuroscience Research Center, Baqiyatallah University of Medical Sciences, Tehran, Iran.
2- Faculty of Electrical, Biomedical and Mechatronics Engineering, Qazvin Branch, Islamic Azad University, Qazvin, Iran.
3- Department of Pharmacology, School of Medicine, Baqiyatallah University of Medical Sciences, Tehran, Iran.
4- PhD Neuroscience Research Center, Baqiyatallah University of Medical Sciences, Tehran, Iran.
5- Medical Imaging Centre, Imam Khomeini University Hospital, Tehran, Iran.
6- Reproductive Biomedicine Research Center, Royan Institute for Biotechnology, Academic Center for Education, Culture and Research (ACECR), Tehran, Iran.
Abstract:  
Introduction: The present research aimed to examine Visual Working Memory (VWM) test scores, as well as hormonal, genomic, and brain anatomic changes in the male rhesus macaques exposed to Extremely Low Frequency Magnetic Field (ELF-MF).
Methods: Four monkeys were exposed to two different ELF-MF frequencies: 1 Hz (control) and 12 Hz (experiment) with 0.7 µT (magnitude) 4 h/d for 30 consecutive days. Before and after the exposure, VWM test was conducted using a coated devise on a movable stand. About 10 mL of the animals’ blood was obtained from their femoral vain and used to evaluate their melatonin concentration. Blood lymphocytes were used for assaying the expressions of N-Methyl-D-aspartate NMDA-receptor genes expression before and after ELF exposure. Anatomical changes of hippocampus size were also assessed using MRI images.
Results: Results indicated that VWM scores in primates exposed to 12 Hz frequency ELF increased significantly. Plasma melatonin level was also increased in these animals. However, these variables did not change in the animals exposed to 1 Hz ELF. At last, expression of the NMDA receptors increased at exposure to 12 Hz frequency. However, hippocampal volume did not increase significantly in the animals exposed to both frequencies. 
Conclusion: In short, these results indicate that ELF (12 Hz) may have a beneficial value for memory enhancement (indicated by the increase in VWM scores). This may be due to an increase in plasma melatonin and or expression of NMDA glutamate receptors. However, direct involvement of the hippocampus in this process needs more research.
Type of Study: Original | Subject: Computational Neuroscience
Received: 2017/07/23 | Accepted: 2018/01/1 | Published: 2018/05/1

References
1. Al-Akhras, M. A., Darmani, H., & Elbetieha, A. (2006). Influence of 50 Hz magnetic field on sex hormones and other fertility parameters of adult male rats. Bioelectromagnetics, 27(2), 127–131. [DOI:10.1002/bem.20186] [DOI:10.1002/bem.20186]
2. Alkadhi, K. (2013). Brain Physiology and Pathophysiology in Mental Stress. ISRN Physiology, 2013, 1–23. [DOI:10.1155/2013/806104] [DOI:10.1155/2013/806104]
3. An, G. Z., Xu, H., Zhou, Y., Du, L., Miao, X., Jiang, D. P., et al. (2015). Effects of Long-Term 50Hz Power-Line Frequency Electromagnetic Field on Cell Behavior in Balb/c 3T3 Cells. PLOS ONE, 10(2), e0117672. [DOI:10.1371/journal.pone.0117672] [DOI:10.1371/journal.pone.0117672]
4. Baharara. J., Zahedifar, Z. (2015). The effect of low-frequency electromagnetic fields on some biological activities of animals. Arak Medical University Journal, 15(7), 80-93.
5. Baydas, G., Özer, M., Yasar, A., Tuzcu, M., & Koz, S. T. (2005). Melatonin improves learning and memory performances impaired by hyperhomocysteinemia in rats. Brain Research, 1046(1-2), 187–194. [DOI:10.1016/j.brainres.2005.04.011] [DOI:10.1016/j.brainres.2005.04.011]
6. Casile, A. (2013). Mirror neurons (and beyond) in the macaque brain: An overview of 20 years of research. Neuroscience Letters, 540, 3–14. [DOI:10.1016/j.neulet.2012.11.003] [DOI:10.1016/j.neulet.2012.11.003]
7. Constantinidis, C., & Procyk, E. (2004). The primate working memory networks. Cognitive, Affective, & Behavioral Neuroscience, 4(4), 444–465. [DOI:10.3758/CABN.4.4.444] [DOI:10.3758/CABN.4.4.444]
8. Cook, C. M., Thomas, A. W., & Prato, F. S. (2002). Human electrophysiological and cognitive effects of exposure to ELF magnetic and ELF modulated RF and microwave fields: A review of recent studies. Bioelectromagnetics, 23(2), 144–157. [DOI:10.1002/bem.107] [DOI:10.1002/bem.107]
9. Cvetkovic, D., & Cosic, I. (2009). Alterations of human electroencephalographic activity caused by multiple extremely low frequency magnetic field exposures. Medical & Biological Engineering & Computing, 47(10), 1063–1073. [DOI:10.1007/s11517-009-0525-1] [DOI:10.1007/s11517-009-0525-1]
10. Cvetkovic, D., Fang, Q., & Cosic, I. (2008). Multiple human electrophysiological responses to extremely low-frequency pulsed electromagnetic field exposures: a pilot study. Estonian Journal of Engineering 14(2), 138-153. [DOI:10.3176/eng.2008.2.04] [DOI:10.3176/eng.2008.2.04]
11. D'Angelo, C., Costantini, E., Kamal, M. A., & Reale, M. (2015). Experimental model for ELF-EMF exposure: Concern for human health. Saudi Journal of Biological Sciences, 22(1), 75–84. [DOI:10.1016/j.sjbs.2014.07.006] [DOI:10.1016/j.sjbs.2014.07.006]
12. De Lorge, J. O., & Grissett, J. D. (1977). Behavioral effects in monkeys exposed to extremely low frequency electromagnetic fields. International Journal of Biometeorology, 21(4), 357–365. [DOI:10.1007/BF01555197] [DOI:10.1007/BF01555197]
13. Fabbri-Destro, M., & Rizzolatti, G. (2008). Mirror Neurons and Mirror Systems in Monkeys and Humans. Physiology, 23(3), 171–179. [DOI:10.1152/physiol.00004.2008] [DOI:10.1152/physiol.00004.2008]
14. Fang, X., Zhang, Y., Zhang, R., Yang, L., Li, M., Ye, K., et al. (2011). Genome sequence and global sequence variation map with 5.5 million SNPs in Chinese rhesus macaque. Genome Biology, 12(7), R63. [DOI:10.1186/gb-2011-12-7-r63] [DOI:10.1186/gb-2011-12-7-r63]
15. Fukunaga, K., Horikawa, K., Shibata, S., Takeuchi, Y., & Miyamoto, E. (2002). Ca2+/calmodulin-dependent protein kinase II-dependent long-term potentiation in the rat suprachiasmatic nucleus and its inhibition by melatonin. Journal of Neuroscience Research, 70(6), 799–807. [DOI:10.1002/jnr.10400] [DOI:10.1002/jnr.10400]
16. Hampton, R. R., Hampstead, B. M., & Murray, E. A. (2005). Rhesus monkeys (Macaca mulatta) demonstrate robust memory for what and where, but not when, in an open-field test of memory. Learning and Motivation, 36(2), 245–259. [DOI:10.1016/j.lmot.2005.02.004] [DOI:10.1016/j.lmot.2005.02.004]
17. Hillmann, A. G., Ramdas, J., Multanen, K., Norman, M. R., & Harmon, J. M. (2000). Glucocorticoid receptor gene mutations in leukemic cells acquired in vitro and in vivo. Cancer Research 60(7), 2056-62. [PMID] [PMID]
18. Jaba, L., Shanthi, V., & Singh, D. (2011). Estimation of Hippocampus Volume from MRI Using ImageJ for Alzheimer's Diagnosis. Atlas Journal of Medical and Biological Sciences, 15–20. [DOI:10.5147/ajmbs.2011.0045] [DOI:10.5147/ajmbs.2011.0045]
19. Kanthaswamy, S., Ng, J., Ross, C. T., Trask, J. S., Smith, D. G., Buffalo, V. S., et al. (2013). Identifying human-rhesus macaque gene orthologs using heterospecific SNP probes. Genomics, 101(1), 30–37. [DOI:10.1016/j.ygeno.2012.09.001] [DOI:10.1016/j.ygeno.2012.09.001]
20. Keller, S. S., & Roberts, N. (2009). Measurement of brain volume using MRI: software, techniques, choices and prerequisites. Journal of Anthropological Sciences. 87, 127-151. [PMID] [PMID]
21. Kula, B., Sobczak, A., & Kuska, R. (2002). Effects of Electromagnetic Field on Free-Radical Processes in Steelworkers. Part I: Magnetic Field Influence on the Antioxidant Activity in Red Blood Cells and Plasma. Journal of Occupational Health, 44(4), 226–229. [DOI:10.1539/joh.44.226] [DOI:10.1539/joh.44.226]
22. Lingnau, A., Gesierich, B., & Caramazza, A. (2009). Asymmetric fMRI adaptation reveals no evidence for mirror neurons in humans. Proceedings of the National Academy of Sciences, 106(24), 9925–9930. [DOI:10.1073/pnas.0902262106] [DOI:10.1073/pnas.0902262106]
23. Lucassen, P. J., Pruessner, J., Sousa, N., Almeida, O. F. X., Van Dam, A. M., Rajkowska, G., et al. (2013). Neuropathology of stress. Acta Neuropathologica, 127(1), 109–135. [DOI:10.1007/s00401-013-1223-5] [DOI:10.1007/s00401-013-1223-5]
24. Lynch, M. (2004). Long-Term Potentiation and Memory. Physiological Reviews, 84(1), 87–136. [DOI:10.1152/physrev.00014.2003] [DOI:10.1152/physrev.00014.2003]
25. Mahmoodzadeh Hosseini, H. M., Soleimanirad, J., Mehdizadeh Aghdam, E. M., Amin, M., & Fooladi, A. A. (2015). Texosome-anchored superantigen triggers apoptosis in original ovarian cancer cells. Medical Oncology, 32(1), 409. [DOI:10.1007/s12032-014-0409-6] [DOI:10.1007/s12032-014-0409-6]
26. Marino, A. A., & Becker, R. O. (1977). Biological effects of extremely low-frequency electric and magnetic fields: a review. Physiological Chemistry and Physics, 9(2), 131-147. [PMID] [PMID]
27. McEwen, B. S., Nasca, C., & Gray, J. D. (2015). Stress Effects on Neuronal Structure: Hippocampus, Amygdala and Prefrontal Cortex. Neuropsychopharmacology, 41(1), 3–23. [DOI:10.1038/npp.2015.171] [DOI:10.1038/npp.2015.171]
28. Mitchell, J. F., & Leopold, D. A. (2015). The marmoset monkey as a model for visual neuroscience. Neuroscience Research, 93, 20–46. [DOI:10.1016/j.neures.2015.01.008] [DOI:10.1016/j.neures.2015.01.008]
29. Morris, R. G. M. (2013). NMDA receptors and memory encoding. Neuropharmacology, 74, 32–40. [DOI:10.1016/j.neuropharm.2013.04.014] [DOI:10.1016/j.neuropharm.2013.04.014]
30. Nakazawa, K., McHugh, T. J., Wilson, M. A., & Tonegawa, S. (2004). NMDA receptors, place cells and hippocampal spatial memory. Nature Reviews Neuroscience, 5(5), 361–372. [DOI:10.1038/nrn1385] [DOI:10.1038/nrn1385]
31. Newcomer, J. W., Farber, N. B., & Olney, J. W. (2000). NMDA receptor function, memory, and brain aging. Dialogues in Clinical Neuroscience, 2(3), 219-32. [PMID] [PMCID] [PMID] [PMCID]
32. Ozdemir, D., Tugyan, K., Uysal, N., Sonmez, U., Sonmez, A., Acikgoz, O., et al. (2005). Protective effect of melatonin against head trauma-induced hippocampal damage and spatial memory deficits in immature rats. Neuroscience Letters, 385(3), 234–239. [DOI:10.1016/j.neulet.2005.05.055] [DOI:10.1016/j.neulet.2005.05.055]
33. Pandiperumal, S. R., Trakht, I., Srinivasan, V., Spence, D. W., Maestroni, G. J., Zisapel, N., et al. (2008). Physiological effects of melatonin: Role of melatonin receptors and signal transduction pathways. Progress in Neurobiology, 85(3), 335–353. [DOI:10.1016/j.pneurobio.2008.04.001] [DOI:10.1016/j.pneurobio.2008.04.001]
34. Richter-Levin, G., & Akirav, I. (2000). Amygdala-Hippocampus Dynamic Interaction in Relation to Memory. Molecular Neurobiology, 22(1-3), 11–20. [DOI:10.1385/MN:22:1-3:011] [DOI:10.1385/MN:22:1-3:011]
35. Rimbach, R., Link, A., Montes-Rojas, A., Di Fiore, A., Heistermann, M., & Heymann, E. W. (2014). Behavioral and physiological responses to fruit availability of spider monkeys ranging in a small forest fragment. American Journal of Primatology, 76(11), 1049–1061. [DOI:10.1002/ajp.22292] [DOI:10.1002/ajp.22292]
36. Ross, C. L., Siriwardane, M., Almeida-Porada, G., Porada, C. D., Brink, P., Christ, G. J., & Harrison, B. S. (2015). The effect of low-frequency electromagnetic field on human bone marrow stem/progenitor cell differentiation. Stem Cell Research, 15(1), 96–108. [DOI:10.1016/j.scr.2015.04.009] [DOI:10.1016/j.scr.2015.04.009]
37. Rostami, A., Shahani, M., Zarrindast, M. R., Semnanian, S., Rahmati Roudsari, M., Rezaei Tavirani, M., & Hasanzadeh, H. (2016). 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. Journal of Lasers in Medical Sciences, 7(2), 120–125. [DOI:10.15171/jlms.2016.20] [DOI:10.15171/jlms.2016.20]
38. Sakhnini, L., Al-Ghareeb, S., Khalil, S., Ahmed, R., Ameer, A. A., & Kamal, A. (2014). Effects of exposure to 50 Hz electromagnetic fields on Morris water-maze performance of prenatal and neonatal mice. Journal of the Association of Arab Universities for Basic and Applied Sciences, 15(1), 1–5. [DOI:10.1016/j.jaubas.2013.05.004] [DOI:10.1016/j.jaubas.2013.05.004]
39. Salford, L. G., & Nittby, H. (2012). Effects of Electromagnetic Fields From Wireless Communication upon the Blood-Brain Barrier. Paper presented in: BioInitiative Working Group: "A Rationale for Biologically-Based Exposure Standards for Low-Intensity Electromagnetic Radiation. Amsterdam: Bioinitiative.
40. Shahrivar, T., Moazedi, A. A., Rasekh, A. R., Almasi-Turk, S., & Roozbehi, A. (2014). [The effects of intrahippocampus injection of progesterone on passive avoidance learning and memory in adult male rats (Persian)]. Iranian South Medical Journal, 17(4), 524-532.
41. Sobczak, A., Kula, B., & Danch, A. (2002). Effects of Electromagnetic Field on Free-Radical Processes in Steelworkers. Part II: Magnetic Field Influence on Vitamin A, E and Selenium Concentrations in Plasma. Journal of Occupational Health, 44(4), 230–233. [DOI:10.1539/joh.44.230] [DOI:10.1539/joh.44.230]
42. Tae, W. S., Kim, S. S., Lee, K. U., Nam, E. C., & Kim, K. W. (2008). Validation of hippocampal volumes measured using a manual method and two automated methods (FreeSurfer and IBASPM) in chronic major depressive disorder. Neuroradiology, 50(7), 569–581. [DOI:10.1007/s00234-008-0383-9] [DOI:10.1007/s00234-008-0383-9]
43. Tekieh, E., Riahi, E., Kazemi, M., Sahraei, H., Tavakoli, H., Aliyary, H., et al. (2017). Role of basal stress hormones and amygdala dimensions in stress coping strategies of male rhesus monkeys in response to a hazard-reward conflict. Iranian Journal of Basic Medical Sciences 20(8), 951-957. doi: 10.22038/ijbms.2017.9120
44. Touitou, Y., & Selmaoui, B. (2012). The effects of extremely low-frequency magnetic fields on melatonin and cortisol, two marker rhythms of the circadian system. Dialogues in Clinical Neuroscience, 14(4), 381-399. [PMID] [PMCID] [PMID] [PMCID]
45. Zare, S., Hayatgeibi, H., Alivandi, S., & Ebadi, A. (2005). Effects of Whole-body Magnetic Field on Changes of Glucose and Cortisol Hormone in Guinea Pigs. American Journal of Biochemistry and Biotechnology, 1(4), 217–219. [DOI:10.3844/ajbbsp.2005.217.219] [DOI:10.3844/ajbbsp.2005.217.219]
46. Zhu, K., Lv, Y., Cheng, Q., Hua, J., & Zeng, Q. (2016). Extremely low frequency magnetic fields do not induce DNA damage in human lens epithelial cells in vitro. The Anatomical Record, 299(5), 688–697. [DOI:10.1002/ar.23312] [DOI:10.1002/ar.23312]