Effects of 50 Hz electromagnetic field on rat working memory and investigation of neural mechanisms_Journal of Biomedical Engineering

Authors：

WANG Longlong ^1,2 ,  LI Shuangyan ^1,2 , LI Tianxiang ^1,2 , ZHENG Weiran ^1,2 , LI Yang ³ ,  XU Guizhi ^1,2

1. State Key Laboratory of Reliability and Intelligence of Electrical Equipment, Hebei University of Technology, Tianjin 300130, P. R. China;
2. Key Laboratory of Bioelectromagnetics and Neuroengineering of Hebei Province, Hebei University of Technology, Tianjin 300130, P. R. China;
3. School of Pharmacy, North China University of Science and Technology, Tangshan, Hebei 063210, P. R. China;

Corresponding?author：

LI Shuangyan, Email: lishuangyan@hebut.edu.cn; XU Guizhi, Email: gzxu@hebut.edu.cn

Keywords：

Electromagnetic field; Working memory; Media prefrontal cortex; Local field potential; Phase-amplitude coupling

DOI：

10.7507/1001-5515.202303032

Video：

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With the widespread use of electrical equipment, cognitive functions such as working memory (WM) could be severely affected when people are exposed to 50 Hz electromagnetic fields (EMF) for long term. However, the effects of EMF exposure on WM and its neural mechanism remain unclear. In the present paper, 15 rats were randomly assigned to three groups, and exposed to an EMF environment at 50 Hz and 2 mT for a different duration: 0 days (control group), 24 days (experimental group I), and 48 days (experimental group II). Then, their WM function was assessed by the T-maze task. Besides, their local field potential (LFP) in the media prefrontal cortex (mPFC) was recorded by the in vivo multichannel electrophysiological recording system to study the power spectral density (PSD) of θ and γ oscillations and the phase-amplitude coupling (PAC) intensity of θ-γ oscillations during the T-maze task. The results showed that the PSD of θ and γ oscillations decreased in experimental groups I and II, and the PAC intensity between θ and high-frequency γ (hγ) decreased significantly compared to the control group. The number of days needed to meet the task criterion was more in experimental groups I and II than that of control group. The results indicate that long-term exposure to EMF could impair WM function. The possible reason may be the impaired communication between different rhythmic oscillations caused by a decrease in θ-hγ PAC intensity. This paper demonstrates the negative effects of EMF on WM and reveals the potential neural mechanisms from the changes of PAC intensity, which provides important support for further investigation of the biological effects of EMF and its mechanisms.

Citation： WANG Longlong, LI Shuangyan, LI Tianxiang, ZHENG Weiran, LI Yang, XU Guizhi. Effects of 50 Hz electromagnetic field on rat working memory and investigation of neural mechanisms. Journal of Biomedical Engineering, 2023, 40(6): 1135-1141. doi: 10.7507/1001-5515.202303032 Copy

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2.	邊洪英, 郝建梅, 陳永青, 等. 極低頻電磁場致職業暴露人群神經行為損傷的研究. 疾病監測, 2019, 34(4): 365-370.
3.	Baaken D, Dechent D, Blettner M, et al. Occupational exposure to extremely low-frequency magnetic fields and risk of amyotrophic lateral sclerosis: results of a feasibility study for a pooled analysis of original data. Bioelectromagnetics, 2021, 42(4): 271-283.
4.	Bagheri H M, Khanjani N, Ebrahimi M H, et al. The effect of chronic exposure to extremely low-frequency electromagnetic fields on sleep quality, stress, depression and anxiety. Electromagn Biol Med, 2019, 38(1): 96-101.
5.	Jalilian H, Teshnizi S H, R??sli M, et al. Occupational exposure to extremely low frequency magnetic fields and risk of Alzheimer disease: a systematic review and meta-analysis. Neurotoxicology, 2018, 69: 242-252.
6.	Bernal-Mondragón C, Arriaga-Avila V, Martínez-Abundis E, et al. Effects of repeated 9 and 30-day exposure to extremely low-frequency electromagnetic fields on social recognition behavior and estrogen receptors expression in olfactory bulb of Wistar female rats. Neuro Res, 2017, 39(2): 165-175.
7.	International Commission on Non-Ionizing Radiation Protection (ICNIRP). ICNIRP statement-Protection of workers against ultraviolet radiation. Health Phys, 2010, 99(1): 66-87.
8.	Chung Y H, Lee Y J, Lee H S, et al. Extremely low frequency magnetic field modulates the level of neurotransmitters. Korean J Physiol Pharmacol, 2015, 19(1): 15-20.
9.	Afrasiabi A, Riazi G H, Abbasi S, et al. Synaptosomal acetylcholinesterase activity variation pattern in the presence of electromagnetic fields. Int J Bio Macromol, 2014, 65: 8-15.,.
10.	鄭秀秀, 包家立, 朱朝陽. 電磁場擾動下的細胞系統魯棒性. 高電壓技術, 2014, 40(12): 3837-3845.
11.	Merla C, Liberti M, Consales C, et al. Evidences of plasma membrane-mediated ROS generation upon ELF exposure in neuroblastoma cells supported by a computational multiscale approach. Biochim Biophys Acta Biomembr, 2019, 1861(8): 1446-1457.
12.	Zheng Y, Cheng J, Dong L, et al. Effects of exposure to extremely low frequency electromagnetic fields on hippocampal long-term potentiation in hippocampal CA1 region. Biochem Biophys Res Commun, 2019, 517(3): 513-519.
13.	Prakash S S, Mayo J P, Ray S. Decoding of attentional state using local field potentials. Curr Opin Neurobiol, 2022, 76: 102589.
14.	郭苗苗, 王中豪, 張天恒, 等. 經顱磁刺激模式差異性對大鼠工作記憶神經網絡關聯特性的影響研究. 電工技術學報, 2021, 36(18): 3809-3820.
15.	McLaughlin A E, Diehl G W, Redish A D. Potential roles of the rodent medial prefrontal cortex in conflict resolution between multiple decision-making systems. Int Rev Neurobiol, 2021, 158: 249-281.
16.	Jobson D D, Hase Y, Clarkson A N, et al. The role of the medial prefrontal cortex in cognition, ageing and dementia. Nat Commun, 2021, 3(3): fcab125.
17.	Jaffe R J, Constantinidis C. Working memory: from neural activity to the sentient mind. Compr Physiol, 2021, 11(4): 2547-2587.
18.	Miller E K, Lundqvist M, Bastos A M. Working memory 2. 0. Neuron, 2018, 100(2): 463-475.
19.	Wang J, Zhang S, Liu T, et al. Directional prefrontal-thalamic information flow is selectively required during spatial working memory retrieval. Front Neurosci, 2022, 16: 1055986.
20.	Guan A, Wang S, Huang A, et al. The role of gamma oscillations in central nervous system diseases: mechanism and treatment. Front Cell Neurosci, 2022, 16: 962957.
21.	Abubaker M, Al Qasem W, Kva?ňák E. Working memory and cross-frequency coupling of neuronal oscillations. Front Psychol, 2021, 12: 756661.
22.	Zhang Y, Zhang Y, Yu H, et al. Theta-gamma coupling in hippocampus during working memory deficits induced by low frequency electromagnetic field exposure. Physiol Behav, 2017, 179: 135-142.
23.	National Research Council (US) Committee for the Update of the Guide for the Care and Use of Laboratory Animals. Guide for the Care and Use of Laboratory Animals. 8th ed. Washington (DC): National Academies Press (US), 2011.
24.	Sengupta P. The laboratory rat: relating its age with human’s. Int J Prev Med, 2013, 4(6): 624-630.
25.	Thomson D J. Spectrum estimation and harmonic analysis. Proc IEEE, 1982, 70(9): 1055-1096.
26.	徐桂芝, 王寧, 郭苗苗, 等. 高頻重復經顱磁刺激后大鼠工作記憶局部場電位時頻特征與相干性差異分析. 生物醫學工程學雜志, 2020, 37(5): 756-764.
27.	López-Madrona V J, Pérez-Montoyo E, álvarez-Salvado E, et al. Different theta frameworks coexist in the rat hippocampus and are coordinated during memory-guided and novelty tasks. Elife, 2020, 9: e57313.
28.	Zhong W, Ciatipis M, Wolfenstetter T, et al. Selective entrainment of gamma subbands by different slow network oscillations. Proc Natl Acad Sci USA, 2017, 114(17): 4519-4524.

1. Pang Xiaofeng. Investigation of influences of environment electromagnetic field irradiated by high-voltage transmission on the health of human and animals. Environ Sci Indian J, 2017, 13(4): 140.
2. 邊洪英, 郝建梅, 陳永青, 等. 極低頻電磁場致職業暴露人群神經行為損傷的研究. 疾病監測, 2019, 34(4): 365-370.
3. Baaken D, Dechent D, Blettner M, et al. Occupational exposure to extremely low-frequency magnetic fields and risk of amyotrophic lateral sclerosis: results of a feasibility study for a pooled analysis of original data. Bioelectromagnetics, 2021, 42(4): 271-283.
4. Bagheri H M, Khanjani N, Ebrahimi M H, et al. The effect of chronic exposure to extremely low-frequency electromagnetic fields on sleep quality, stress, depression and anxiety. Electromagn Biol Med, 2019, 38(1): 96-101.
5. Jalilian H, Teshnizi S H, R??sli M, et al. Occupational exposure to extremely low frequency magnetic fields and risk of Alzheimer disease: a systematic review and meta-analysis. Neurotoxicology, 2018, 69: 242-252.
6. Bernal-Mondragón C, Arriaga-Avila V, Martínez-Abundis E, et al. Effects of repeated 9 and 30-day exposure to extremely low-frequency electromagnetic fields on social recognition behavior and estrogen receptors expression in olfactory bulb of Wistar female rats. Neuro Res, 2017, 39(2): 165-175.
7. International Commission on Non-Ionizing Radiation Protection (ICNIRP). ICNIRP statement-Protection of workers against ultraviolet radiation. Health Phys, 2010, 99(1): 66-87.
8. Chung Y H, Lee Y J, Lee H S, et al. Extremely low frequency magnetic field modulates the level of neurotransmitters. Korean J Physiol Pharmacol, 2015, 19(1): 15-20.
9. Afrasiabi A, Riazi G H, Abbasi S, et al. Synaptosomal acetylcholinesterase activity variation pattern in the presence of electromagnetic fields. Int J Bio Macromol, 2014, 65: 8-15.,.
10. 鄭秀秀, 包家立, 朱朝陽. 電磁場擾動下的細胞系統魯棒性. 高電壓技術, 2014, 40(12): 3837-3845.
11. Merla C, Liberti M, Consales C, et al. Evidences of plasma membrane-mediated ROS generation upon ELF exposure in neuroblastoma cells supported by a computational multiscale approach. Biochim Biophys Acta Biomembr, 2019, 1861(8): 1446-1457.
12. Zheng Y, Cheng J, Dong L, et al. Effects of exposure to extremely low frequency electromagnetic fields on hippocampal long-term potentiation in hippocampal CA1 region. Biochem Biophys Res Commun, 2019, 517(3): 513-519.
13. Prakash S S, Mayo J P, Ray S. Decoding of attentional state using local field potentials. Curr Opin Neurobiol, 2022, 76: 102589.
14. 郭苗苗, 王中豪, 張天恒, 等. 經顱磁刺激模式差異性對大鼠工作記憶神經網絡關聯特性的影響研究. 電工技術學報, 2021, 36(18): 3809-3820.
15. McLaughlin A E, Diehl G W, Redish A D. Potential roles of the rodent medial prefrontal cortex in conflict resolution between multiple decision-making systems. Int Rev Neurobiol, 2021, 158: 249-281.
16. Jobson D D, Hase Y, Clarkson A N, et al. The role of the medial prefrontal cortex in cognition, ageing and dementia. Nat Commun, 2021, 3(3): fcab125.
17. Jaffe R J, Constantinidis C. Working memory: from neural activity to the sentient mind. Compr Physiol, 2021, 11(4): 2547-2587.
18. Miller E K, Lundqvist M, Bastos A M. Working memory 2. 0. Neuron, 2018, 100(2): 463-475.
19. Wang J, Zhang S, Liu T, et al. Directional prefrontal-thalamic information flow is selectively required during spatial working memory retrieval. Front Neurosci, 2022, 16: 1055986.
20. Guan A, Wang S, Huang A, et al. The role of gamma oscillations in central nervous system diseases: mechanism and treatment. Front Cell Neurosci, 2022, 16: 962957.
21. Abubaker M, Al Qasem W, Kva?ňák E. Working memory and cross-frequency coupling of neuronal oscillations. Front Psychol, 2021, 12: 756661.
22. Zhang Y, Zhang Y, Yu H, et al. Theta-gamma coupling in hippocampus during working memory deficits induced by low frequency electromagnetic field exposure. Physiol Behav, 2017, 179: 135-142.
23. National Research Council (US) Committee for the Update of the Guide for the Care and Use of Laboratory Animals. Guide for the Care and Use of Laboratory Animals. 8th ed. Washington (DC): National Academies Press (US), 2011.
24. Sengupta P. The laboratory rat: relating its age with human’s. Int J Prev Med, 2013, 4(6): 624-630.
25. Thomson D J. Spectrum estimation and harmonic analysis. Proc IEEE, 1982, 70(9): 1055-1096.
26. 徐桂芝, 王寧, 郭苗苗, 等. 高頻重復經顱磁刺激后大鼠工作記憶局部場電位時頻特征與相干性差異分析. 生物醫學工程學雜志, 2020, 37(5): 756-764.
27. López-Madrona V J, Pérez-Montoyo E, álvarez-Salvado E, et al. Different theta frameworks coexist in the rat hippocampus and are coordinated during memory-guided and novelty tasks. Elife, 2020, 9: e57313.
28. Zhong W, Ciatipis M, Wolfenstetter T, et al. Selective entrainment of gamma subbands by different slow network oscillations. Proc Natl Acad Sci USA, 2017, 114(17): 4519-4524.

Journal of Biomedical Engineering

Effects of 50 Hz electromagnetic field on rat working memory and investigation of neural mechanisms

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