Effects of Head-Only Exposure to 900 MHz GSM Electromagnetic Fields in Rats: Changes in Neuronal Activity as Revealed by c-Fos Imaging without Concomitant Cognitive Impairments
Abstract
:1. Introduction
2. Materials and Methods
2.1. Animals
2.2. Electromagnetic Field Exposure System
2.3. Habituation to Restrained Conditions
2.4. Experiment 1
2.5. Experiment 2
2.5.1. Aim and Groups
2.5.2. Spatial Working Memory Task
2.5.3. Spatial Reference Memory Task
2.6. c-Fos Immunocytochemistry
2.7. Image Analysis and Cell Counting
2.8. Statistical Analyses
3. Results
3.1. Experiment 1: Effect of EMF Exposure on Neuronal Activity as Revealed by c-Fos Imaging
3.2. Experiment 2: Effect of EMF Exposure on Learning and Memory Performance and Associated Neuronal Activity
3.2.1. Behavioral Data
Working Memory Task
Reference Memory Task
3.2.2. c-Fos Mapping
Working Memory Task
Reference Memory Task
3.3. Relations between Dosimetric Analysis and Changes in c-Fos Expression
4. Discussion
4.1. Relation with Previous Studies Evaluating the Effects of Acute Exposure to EMFs
4.2. Relationship with Previous Studies Evaluating the Effects of Subchronic Exposure to EMFs
5. Conclusions and Open Questions
Supplementary Materials
Author Contributions
Funding
Institutional Review Board Statement
Data Availability Statement
Acknowledgments
Conflicts of Interest
References
- Ahlbom, I.C.; Cardis, E.; Green, A.; Linet, M.; Savitz, D.; Swerdlow, A.; ICNIRP (International Commission for Non-Ionizing Radiation Protection) Standing Committee on Epidemiology. Review of the epidemiologic literature on EMF and Health. Environ. Health Perspect. 2001, 109, 911–933. [Google Scholar] [CrossRef] [PubMed]
- Hermann, D.M.; Hossmann, K.-A. Neurological effects of microwave exposure related to mobile communication. J. Neurol. Sci. 1997, 152, 1–14. [Google Scholar] [CrossRef]
- Hossmann, K.; Hermann, D. Effects of electromagnetic radiation of mobile phones on the central nervous system. Bioelectromagnetics 2002, 24, 49–62. [Google Scholar] [CrossRef] [PubMed]
- Caplan, L.S.; Schoenfeld, E.R.; O’Leary, E.S.; Leske, M. Breast Cancer and Electromagnetic Fields—A Review. Ann. Epidemiol. 2000, 10, 31–44. [Google Scholar] [CrossRef] [PubMed]
- Hardell, L.; Mild, K.H.; Carlberg, M. Case-control study on the use of cellular and cordless phones and the risk for malignant brain tumours. Int. J. Radiat. Biol. 2002, 78, 931–936. [Google Scholar] [CrossRef]
- Richter, E.D.; Berman, T.; Levy, O. Brain Cancer with Induction Periods of Less Than 10 Years in Young Military Radar Workers. Arch. Environ. Health Int. J. 2002, 57, 270–272. [Google Scholar] [CrossRef]
- Juutilainen, J.; Pukkala, E.; Läärä, E. Incidence of leukaemia and brain tumours in Finnish workers exposed to ELF magnetic fields. Int. Arch. Occup. Environ. Health 1990, 62, 289–293. [Google Scholar] [CrossRef]
- Rothman, K.J.; Chou, C.-K.; Morgan, R.; Balzano, Q.; Guy, A.W.; Funch, D.P.; Preston-Martin, S.; Mandel, J.; Steffens, R.; Carlo, G. Assessment of Cellular Telephone and Other Radio Frequency Exposure for Epidemiologic Research. Epidemiology 1996, 7, 291–298. [Google Scholar] [CrossRef]
- Preece, A.W. Effect of a 915-MHz simulated mobile phone signal on cognitive function in man. Int. J. Radiat. Biol. 1999, 75, 447–456. [Google Scholar] [CrossRef]
- Koivisto, M.; Krause, C.M.; Revonsuo, A.; Laine, M.; Hämäläinen, H. The effects of electromagnetic field emitted by GSM phones on working memory. NeuroReport 2000, 11, 1641–1643. [Google Scholar] [CrossRef]
- A Borbély, A.; Huber, R.; Graf, T.; Fuchs, B.; Gallmann, E.; Achermann, P. Pulsed high-frequency electromagnetic field affects human sleep and sleep electroencephalogram. Neurosci. Lett. 1999, 275, 207–210. [Google Scholar] [CrossRef]
- Croft, R. Acute mobile phone operation affects neural function in humans. Clin. Neurophysiol. 2002, 113, 1623–1632. [Google Scholar] [CrossRef]
- Krause, L.S.C.M. Effects of electromagnetic fields emitted by cellular phones on the electroencephalogram during a visual working memory task. Int. J. Radiat. Biol. 2000, 76, 1659–1667. [Google Scholar] [CrossRef]
- Krause, C.M.; Sillanmäki, L.; Koivisto, M.; Häggqvist, A.; Saarela, C.; Revonsuo, A.; Laine, M.; Hämäläinen, H. Effects of electromagnetic field emitted by cellular phones on the EEG during a memory task. NeuroReport 2000, 11, 761–764. [Google Scholar] [CrossRef] [PubMed]
- Huber, R.; Treyer, V.; Borbély, A.A.; Schuderer, J.; Gottselig, J.M.; Landolt, H.; Werth, E.; Berthold, T.; Kuster, N.; Buck, A.; et al. Electromagnetic fields, such as those from mobile phones, alter regional cerebral blood flow and sleep and waking EEG. J. Sleep Res. 2002, 11, 289–295. [Google Scholar] [CrossRef] [PubMed]
- Huber, R.; Graf, T.; Cote, K.A.; Wittmann, L.; Gallmann, E.; Matter, D.; Schuderer, J.; Kuster, N.; Borbély, A.A.; Achermann, P. Exposure to pulsed high-frequency electromagnetic field during waking affects human sleep EEG. NeuroReport 2000, 11, 3321–3325. [Google Scholar] [CrossRef] [PubMed]
- Frey, A.H. Headaches from cellular telephones: Are they real and what are the implications? Environ. Health Perspect. 1998, 106, 101–103. [Google Scholar] [CrossRef] [PubMed]
- Hocking, B.; Westerman, R. Neurological abnormalities associated with CDMA exposure. Occup. Med. 2001, 51, 410–413. [Google Scholar] [CrossRef]
- Beason, R.C.; Semm, P. Responses of neurons to an amplitude modulated microwave stimulus. Neurosci. Lett. 2002, 333, 175–178. [Google Scholar] [CrossRef]
- Chance, W.; Grossman, C.; Newrock, R.; Bovin, G.; Yerian, S.; Schmitt, G.; Mendenhall, C. Effects of electromagnetic fields and gender on neurotransmitters and amino acids in rats. Physiol. Behav. 1995, 58, 743–748. [Google Scholar] [CrossRef]
- Lai, H.; Carino, M.A.; Wen, Y.F.; Horita, A.; Guy, A.W. Naltrexone pretreatment blocks microwave–induced changes in central cholinergic receptors. Bioelectromagnetics 1991, 12, 27–33. [Google Scholar] [CrossRef]
- Lai, H.; Carino, M.A.; Horita, A.; Guy, A.W. Single vs. Repeated microwave exposure: Effects on benzodiazepine receptors in the brain of the rat. Bioelectromagnetics 1992, 13, 57–66. [Google Scholar] [CrossRef] [PubMed]
- Lai, H.; Carino, M.A.; Horita, A.; Guy, A.W. Effects of a 60 Hz magnetic field on central cholinergic systems of the rat. Bioelectromagnetics 1993, 14, 5–15. [Google Scholar] [CrossRef] [PubMed]
- Mausset, A.-L.; de Seze, R.; Montpeyroux, F.; Privat, A. Effects of radiofrequency exposure on the GABAergic system in the rat cerebellum: Clues from semi-quantitative immunohistochemistry. Brain Res. 2001, 912, 33–46. [Google Scholar] [CrossRef] [PubMed]
- Ammari, M.; Brillaud, E.; Gamez, C.; Lecomte, A.; Sakly, M.; Abdelmelek, H.; de Seze, R. Effect of a chronic GSM 900MHz exposure on glia in the rat brain. Biomed. Pharmacother. 2008, 62, 273–281. [Google Scholar] [CrossRef] [PubMed]
- Brillaud, E.; Piotrowski, A.; de Seze, R. Effect of an acute 900MHz GSM exposure on glia in the rat brain: A time-dependent study. Toxicology 2007, 238, 23–33. [Google Scholar] [CrossRef]
- Maussetbonnefont, A.; Hirbec, H.; Bonnefont, X.; Privat, A.; Vignon, J.; Deseze, R. Acute exposure to GSM 900-MHz electromagnetic fields induces glial reactivity and biochemical modifications in the rat brain. Neurobiol. Dis. 2004, 17, 445–454. [Google Scholar] [CrossRef]
- Fritze, K.; Wiessner, C.; Kuster, N.; Sommer, C.; Gass, P.; Hermann, D.; Kiessling, M.; Hossmann, K.-A. Effect of global system for mobile communication microwave exposure on the genomic response of the rat brain. Neuroscience 1997, 81, 627–639. [Google Scholar] [CrossRef]
- Watilliaux, A.; Edeline, J.-M.; Lévêque, P.; Jay, T.M.; Mallat, M. Effect of Exposure to 1,800 MHz Electromagnetic Fields on Heat Shock Proteins and Glial Cells in the Brain of Developing Rats. Neurotox. Res. 2010, 20, 109–119. [Google Scholar] [CrossRef]
- Finnie, J.W.; Blumbergs, P.C.; Manavis, J.; Utteridge, T.D.; Gebski, V.; Davies, R.A.; Vernon-Roberts, B.; Kuchel, T.R. Effect of long-term mobile communication microwave exposure on vascular permeability in mouse brain. Pathology 2002, 34, 344–347. [Google Scholar] [CrossRef]
- de Gannes, F.P.; Billaudel, B.; Taxile, M.; Haro, E.; Ruffié, G.; Lévêque, P.; Veyret, B.; Lagroye, I. Effects of Head-Only Exposure of Rats to GSM-900 on Blood-Brain Barrier Permeability and Neuronal Degeneration. Radiat. Res. 2009, 172, 359–367. [Google Scholar] [CrossRef] [PubMed]
- Salford, L.G.; Brun, A.; Sturesson, K.; Eberhardt, J.L.; Persson, B.R.R. Permeability of the blood–brain barrier induced by 915 MHz electromagnetic radiation, continuous wave and modulated at 8, 16, 50, and 200 Hz. Microsc. Res. Tech. 1994, 27, 535–542. [Google Scholar] [CrossRef] [PubMed]
- Salford, L.G.; Brun, A.; Eberhardt, J.L.; Persson, R.R. Permeability of the blood–brain barrier induced by 915 MHz electromagnetic permeability of the blood–brain barrier induced by 915 MHz electromagnetic radiation, continuous wave and modulated at 8, 16, 50, and 200 Hz. Bioelectrochem. Bioenerg. 1993, 30, 293–301. [Google Scholar] [CrossRef]
- Nittby, H.; Brun, A.; Eberhardt, J.; Malmgren, L.; Persson, B.R.; Salford, L.G. Increased blood–brain barrier permeability in mammalian brain 7 days after exposure to the radiation from a GSM-900 mobile phone. Pathophysiology 2009, 16, 103–112. [Google Scholar] [CrossRef]
- Stam, R. Electromagnetic fields and the blood–brain barrier. Brain Res. Rev. 2010, 65, 80–97. [Google Scholar] [CrossRef] [PubMed]
- Lai, H. Spatial learning deficit in the rat after exposure to a 60 Hz magnetic field. Bioelectromagnetics 1996, 17, 494–496. [Google Scholar] [CrossRef]
- Lai, H.; Horita, A.; Guy, A.W. Microwave irradiation affects radial–arm maze performance in the rat. Bioelectromagnetics 1994, 15, 95–104. [Google Scholar] [CrossRef]
- Lai, H.; A Carino, M.; Ushijima, I. Acute exposure to a 60 Hz magnetic field affects rats’ water-maze performance. Bioelectromagnetics 1998, 19, 117–122. [Google Scholar] [CrossRef]
- Cassel, J.-C.; Cosquer, B.; Galani, R.; Kuster, N. Whole-body exposure to 2.45 GHz electromagnetic fields does not alter radial-maze performance in rats. Behav. Brain Res. 2004, 155, 37–43. [Google Scholar] [CrossRef]
- Cobb, B.L.; Jauchem, J.R.; Adair, E.R. Radial arm maze performance of rats following repeated low level microwave radiation exposure. Bioelectromagnetics 2003, 25, 49–57. [Google Scholar] [CrossRef]
- Davis, H.P.; Mizumori, S.J.Y.; Allen, H.; Rosenzweig, M.R.; Bennett, E.L.; Tenforde, T.S. Behavioral studies with mice exposed to DC and 60-Hz magnetic fields. Bioelectromagnetics 1984, 5, 147–164. [Google Scholar] [CrossRef]
- Dubreuil, D.; Jay, T.; Edeline, J.-M. Head-only exposure to GSM 900-MHz electromagnetic fields does not alter rat’s memory in spatial and non-spatial tasks. Behav. Brain Res. 2003, 145, 51–61. [Google Scholar] [CrossRef]
- Dubreuil, D.; Jay, T.; Edeline, J.-M. Does head-only exposure to GSM-900 electromagnetic fields affect the performance of rats in spatial learning tasks? Behav. Brain Res. 2002, 129, 203–210. [Google Scholar] [CrossRef] [PubMed]
- Hong, C.; Huestis, P.; Thompson, R.; Yu, J. Learning ability of young rats is unaffected by repeated exposure to a static electromagnetic field in early life. Bioelectromagnetics 1988, 9, 269–273. [Google Scholar] [CrossRef]
- Sienkiewicz, Z.J.; Blackwell, R.P.; Haylock, R.G.; Saunders, R.D.; Cobb, B.L. Low-level exposure to pulsed 900 MHz microwave radiation does not cause deficits in the performance of a spatial learning task in mice. Bioelectromagnetics 2000, 21, 151–158. [Google Scholar] [CrossRef]
- Sienkiewicz, Z.J.; Haylock, R.G.; Saunders, R.D. Acute exposure to power–frequency magnetic fields has no effect on the acquisition of a spatial learning task by adult male mice. Bioelectromagnetics 1996, 17, 180–186. [Google Scholar] [CrossRef]
- Sienkiewicz, Z.J.; Bartram, R.; Haylock, R.G.; Saunders, R.D. Single, brief exposure to a 50 Hz magnetic field does not affect the performance of an object recognition task in adult mice. Bioelectromagnetics 2000, 22, 19–26. [Google Scholar] [CrossRef]
- Kumlin, T.; Iivonen, H.; Miettinen, P.; Juvonen, A.; van Groen, T.; Puranen, L.; Pitkäaho, R.; Juutilainen, J.; Tanila, H. Mobile Phone Radiation and the Developing Brain: Behavioral and Morphological Effects in Juvenile Rats. Radiat. Res. 2007, 168, 471–479. [Google Scholar] [CrossRef]
- Arendash, G.W.; Sanchez-Ramos, J.; Mori, T.; Mamcarz, M.; Lin, X.; Runfeldt, M.; Wang, L.; Zhang, G.; Sava, V.; Tan, J.; et al. Electromagnetic Field Treatment Protects Against and Reverses Cognitive Impairment in Alzheimer’s Disease Mice. J. Alzheimer’s Dis. 2010, 19, 191–210. [Google Scholar] [CrossRef]
- Dragicevic, N.; Bradshaw, P.; Mamcarz, M.; Lin, X.; Wang, L.; Cao, C.; Arendash, G. Long-term electromagnetic field treatment enhances brain mitochondrial function of both Alzheimer’s transgenic mice and normal mice: A mechanism for electromagnetic field-induced cognitive benefit? Neuroscience 2011, 185, 135–149. [Google Scholar] [CrossRef]
- Leveque, P.; Dale, C.; Veyret, B.; Wiart, J. Dosimetric analysis of a 900-MHz rat head exposure system. IEEE Trans. Microw. Theory Tech. 2004, 52, 2076–2083. [Google Scholar] [CrossRef]
- Dubreuil, D.; Tixier, C.; Dutrieux, G.; Edeline, J.-M. Does the radial-arm maze necessarily test spatial memory? Neuro-Biol. Learn. Mem. 2003, 79, 109–117. [Google Scholar] [CrossRef] [PubMed]
- Delatour, B.; Gisquet-Verrier, P. Functional role of rat prelimbic-infralimbic cortices in spatial memory: Evidence for their involvement in attention and behavioural flexibility. Behav. Brain Res. 2000, 109, 113–128. [Google Scholar] [CrossRef] [PubMed]
- Lavenex, P.; Schenk, F. Influence of local environmental olfactory cues on place learning in rats. Physiol. Behav. 1995, 58, 1059–1066. [Google Scholar] [CrossRef]
- Paxinos, G.; Watson, C. The Rat Brain in Stereotaxic Coordinates; Academic Press, Inc.: San Diego, CA, USA, 1998. [Google Scholar]
- Sharp, F.; Sagar, S.; Hicks, K.; Lowenstein, D.; Hisanaga, K. c-fos mRNA, Fos, and Fos-related antigen induction by hypertonic saline and stress. J. Neurosci. 1991, 11, 2321–2331. [Google Scholar] [CrossRef]
- Armario, A.; Vallès, A.; Dal-Zotto, S.; Márquez, C.; Belda, X. A Single Exposure to Severe Stressors Causes Long-term Desensitisation of the Physiological Response to the Homotypic Stressor. Stress 2004, 7, 157–172. [Google Scholar] [CrossRef]
- Mickley, G.; Cobb, B.L.; Mason, P.A.; Farrell, S. Disruption of a putative working memory task and selective expression of brain c-fos following microwave-induced hyperthermia. Physiol. Behav. 1994, 55, 1029–1038. [Google Scholar] [CrossRef]
- Zhang, J.; Zhang, D.; McQuade, J.S.; Behbehani, M.; Tsien, J.Z.; Xu, M. c-fos regulates neuronal excitability and survival. Nat. Genet. 2002, 30, 416–420. [Google Scholar] [CrossRef]
- Blackman, C.F.; Benane, S.G.; Elder, J.A.; House, D.E.; Lampe, J.A.; Faulk, J.M. Induction of calcium-ion efflux from brain tissue by radiofrequency radiation: Effect of sample number and modulation frequency on the power-density window. Bioelectromagnetics 1980, 1, 35–43. [Google Scholar] [CrossRef]
- Gandhi, C.R.; Ross, D.H. Microwave induced stimulation of32Pi incorporation into phosphoinositides of rat brain synaptosomes. Radiat. Environ. Biophys. 1989, 28, 223–234. [Google Scholar] [CrossRef] [PubMed]
- McNamee, J.P.; Bellier, P.V.; Konkle, A.T.; Thomas, R.; Wasoontarajaroen, S.; Lemay, E.; Gajda, G.B. Analysis of gene expression in mouse brain regions after exposure to 1.9 GHz radiofrequency fields. Int. J. Radiat Biol. 2016, 92, 338–350. [Google Scholar] [CrossRef]
- Bektas, H.; Algul, S.; Altindag, F.; Yegin, K.; Akdag, M.Z.; Dasdag, S. Effects of 3.5 GHz radiofrequency radiation on ghrelin, nesfatin-1, and irisin level in diabetic and healthy brains. J. Chem. Neuroanat. 2022, 126, 102168. [Google Scholar] [CrossRef]
- Dasgupta, S.; Leong, C.; Simonich, M.T.; Truong, L.; Liu, H.; Tanguay, R.L. Transcriptomic and Long-Term Behavioral Deficits Associated with Developmental 3.5 GHz Radiofrequency Radiation Exposures in Zebrafish. Environ. Sci. Technol. Lett. 2022, 12, 327–332. [Google Scholar] [CrossRef]
- Wang, Y.; Zhang, H.; Zhang, Z.; Sun, B.; Tang, C.; Zhang, L.; Jiang, Z.; Ding, B.; Liao, Y.; Cai, P. Simulated mobile communication frequencies (3.5 GHz) emitted by a signal generator affects the sleep of Drosophila melanogaster. Environ. Pollut. 2021, 283, 117087. [Google Scholar] [CrossRef] [PubMed]
- Lameth, J.; Arnaud-Cormos, D.; Lévêque, P.; Boillée, S.; Edeline, J.-M.; Mallat, M. Effects of a Single Head Exposure to GSM-1800 MHz Signals on the Transcriptome Profile in the Rat Cerebral Cortex: Enhanced Gene Responses Under Proinflammatory Conditions. Neurotox. Res. 2020, 38, 105–123. [Google Scholar] [CrossRef] [PubMed]
- Aparicio, S.Y.L.; Fierro, D.J.L.; Abreu, G.E.A.; Cárdenas, R.T.; Hernández, L.I.G.; Ávila, G.A.C.; Durán, F.R.; Aguilar, M.E.H.; Denes, J.M.; Chi-Castañeda, L.D.; et al. Current Opinion on the Use of c-Fos in Neuroscience. NeuroSci 2022, 3, 687–702. [Google Scholar] [CrossRef]
- Lagroye, I.; Laclau, M.; Leveque, P.; De Gannes, F.P.; Billaudel, B.; Haro, E.; Taxile, M.; Ruffie, G.; Veyret, B. Exposure to Radiofrequency Fields and Heat Shock Protein (Hsp) Expression in the Rat Brain. Radioprotection 2008, 43, 066. [Google Scholar] [CrossRef]
- El Khoueiry, C.; Moretti, D.; Renom, R.; Camera, F.; Orlacchio, R.; Garenne, A.; De Gannes, F.P.; Poque-Haro, E.; Lagroye, I.; Veyret, B.; et al. Decreased spontaneous electrical activity in neuronal networks exposed to radiofrequency 1,800 MHz signals. J. Neurophysiol. 2018, 120, 2719–2729. [Google Scholar] [CrossRef]
- Canovi, A.; Orlacchio, R.; de Gannes, F.P.; Lévêque, P.; Arnaud-Cormos, D.; Lagroye, I.; Garenne, A.; Percherancier, Y.; Lewis, N. In vitro exposure of neuronal networks to the 5G-3.5 GHz signal. Front. Public Health 2023, 11, 1231360. [Google Scholar] [CrossRef]
- Occelli, F.; Lameth, J.; Adenis, V.; Huetz, C.; Lévêque, P.; Jay, T.M.; Edeline, J.-M.; Mallat, M. A Single Exposure to GSM-1800 MHz Signals in the Course of an Acute Neuroinflammatory Reaction can Alter Neuronal Responses and Microglial Morphology in the Rat Primary Auditory Cortex. Neuroscience 2018, 385, 11–24. [Google Scholar] [CrossRef]
- Souffi, S.; Lameth, J.; Gaucher, Q.; Arnaud-Cormos, D.; Lévêque, P.; Edeline, J.-M.; Mallat, M. Exposure to 1800 MHz LTE electromagnetic fields under proinflammatory conditions decreases the response strength and increases the acoustic threshold of auditory cortical neurons. Sci. Rep. 2022, 12, 1–14. [Google Scholar] [CrossRef]
- Di Carlo, A.; Mullins, J.; Litovitz, T. Electromagnetic field-induced protection of chick embryos against hypoxia exhibits characteristics of temporal sensing. Bioelectrochemistry 2000, 52, 17–21. [Google Scholar] [CrossRef]
- Di Carlo, A.; White, N.; Litovitz, T. Mechanical and electromagnetic induction of protection against oxidative stress. Bioelectrochemistry 2001, 53, 87–95. [Google Scholar] [CrossRef] [PubMed]
- Sagar, S.M.; Sharp, F.R.; Curran, T. Expression of c- fos Protein in Brain: Metabolic Mapping at the Cellular Level. Science 1988, 240, 1328–1331. [Google Scholar] [CrossRef] [PubMed]
- Nittby, H.; Grafström, G.; Tian, D.P.; Malmgren, L.; Brun, A.; Persson, B.R.; Salford, L.G.; Eberhardt, J. Cognitive impairment in rats after long-term exposure to GSM-900 mobile phone radiation. Bioelectromagnetics 2008, 29, 219–232. [Google Scholar] [CrossRef]
- Fragopoulou, A.; Miltiadous, P.; Stamatakis, A.; Stylianopoulou, F.; Koussoulakos, S.; Margaritis, L. Whole body exposure with GSM 900MHz affects spatial memory in mice. Pathophysiology 2010, 17, 179–187. [Google Scholar] [CrossRef]
- 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. Upsala J. Med Sci. 2010, 115, 91–96. [Google Scholar] [CrossRef] [PubMed]
- Narayanan, S.N.; Kumar, R.S.; Potu, B.K.; Nayak, S.; Mailankot, M. Spatial memory performance of Wistar rats exposed to mobile phone. Clinics 2009, 64, 231–234. [Google Scholar] [CrossRef]
- Ammari, M.; Lecomte, A.; Sakly, M.; Abdelmelek, H.; De-Seze, R. Exposure to GSM 900MHz electromagnetic fields affects cerebral cytochrome c oxidase activity. Toxicology 2008, 250, 70–74. [Google Scholar] [CrossRef]
- Ammari, M.; Jacquet, A.; Lecomte, A.; Sakly, M.; Abdelmelek, H.; de Seze, R. Effect of head-only sub-chronic and chronic exposure to 900-MHz GSM electromagnetic fields on spatial memory in rats. Brain Inj. 2008, 22, 1021–1029. [Google Scholar] [CrossRef]
- Adair, R. Hypothetical Biophysical Mechanisms for the Action of Weak Low Frequency Electromagnetic Fields at the Cellular Level. Radiat. Prot. Dosim. 1997, 72, 271–278. [Google Scholar] [CrossRef]
- Adey, W.R. Biological effects of electromagnetic fields. J. Cell. Biochem. 1993, 51, 410–416. [Google Scholar] [CrossRef] [PubMed]
- Berg, H. Problems of weak electromagnetic field effects in cell biology. Bioelectrochem. Bioenerg. 1999, 48, 355–360. [Google Scholar] [CrossRef] [PubMed]
- Anane, R.; Dulou, P.-E.; Taxile, M.; Geffard, M.; Crespeau, F.-L.; Veyret, B. Effects of GSM-900 Microwaves on DMBA-Induced Mammary Gland Tumors in Female Sprague-Dawley Rats. Radiat. Res. 2003, 160, 492–497. [Google Scholar] [CrossRef] [PubMed]
- Francis, J.T.; Gluckman, B.J.; Schiff, S.J. Sensitivity of Neurons to Weak Electric Fields. J. Neurosci. 2003, 23, 7255–7261. [Google Scholar] [CrossRef] [PubMed]
- Bertagna, F.; Lewis, R.; Silva, S.R.P.; McFadden, J.; Jeevaratnam, K. Effects of electromagnetic fields on neuronal ion channels: A systematic review. Ann. N. Y. Acad. Sci. 2021, 1499, 82–103. [Google Scholar] [CrossRef]
- Tattersall, J.E.; Scott, I.R.; Wood, S.J.; Nettell, J.J.; Bevir, M.K.; Wang, Z.; Somasiri, N.P.; Chen, X. Effects of low intensity radiofrequency electromagnetic fields on electrical activity in rat hippocampal slices. Brain Res. 2001, 904, 43–53. [Google Scholar] [CrossRef]
- Gündel, H.; Valet, M.; Sorg, C.; Huber, D.; Zimmer, C.; Sprenger, T.; Tölle, T.R. Altered cerebral response to noxious heat stimulation in patients with somatoform pain disorder. Pain 2008, 137, 413–421. [Google Scholar] [CrossRef]
- Kwan, C.L.; Crawley, A.P.; Mikulis, D.J.; Davis, K.D. An fMRI study of the anterior cingulate cortex and surrounding medial wall activations evoked by noxious cutaneous heat and cold stimuli. Pain 2000, 85, 359–374. [Google Scholar] [CrossRef]
- Moulton, E.A.; Keaser, M.L.; Gullapalli, R.P.; Greenspan, J.D. Regional Intensive and Temporal Patterns of Functional MRI Activation Distinguishing Noxious and Innocuous Contact Heat. J. Neurophysiol. 2005, 93, 2183–2193. [Google Scholar] [CrossRef] [PubMed]
- Seifert, F.; Jungfer, I.; Schmelz, M.; Maihöfner, C. Representation of UV-B-induced thermal and mechanical hyperalgesia in the human brain: A functional MRI study. Hum. Brain Mapp. 2007, 29, 1327–1342. [Google Scholar] [CrossRef]
- Huber, R.; Treyer, V.; Schuderer, J.; Berthold, T.; Buck, A.; Kuster, N.; Landolt, H.P.; Achermann, P. Exposure to pulse-modulated radio frequency electromagnetic fields affects regional cerebral blood flow. Eur. J. Neurosci. 2005, 21, 1000–1006. [Google Scholar] [CrossRef] [PubMed]
- Volkow, N.D.; Tomasi, D.; Wang, G.-J.; Fowler, J.S.; Telang, F.; Wang, R.; Alexoff, D.; Logan, J.; Wong, C.; Pradhan, K.; et al. Effects of low-field magnetic stimulation on brain glucose metabolism. NeuroImage 2010, 51, 623–628. [Google Scholar] [CrossRef] [PubMed]
- Sienkiewicz, Z.; van Rongen, E. Can Low-Level Exposure to Radiofrequency Fields Effect Cognitive Behaviour in Laboratory Animals? A Systematic Review of the Literature Related to Spatial Learning and Place Memory. Int. J. Environ. Res. Public Health 2019, 16, 1607. [Google Scholar] [CrossRef] [PubMed]
- Narayanan, S.N.; Jetti, R.; Kesari, K.K.; Kumar, R.S.; Nayak, S.B.; Bhat, P.G. Radiofrequency electromagnetic radiation-induced behavioral changes and their possible basis. Environ. Sci. Pollut. Res. 2019, 26, 30693–30710. [Google Scholar] [CrossRef] [PubMed]
Disclaimer/Publisher’s Note: The statements, opinions and data contained in all publications are solely those of the individual author(s) and contributor(s) and not of MDPI and/or the editor(s). MDPI and/or the editor(s) disclaim responsibility for any injury to people or property resulting from any ideas, methods, instructions or products referred to in the content. |
© 2024 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).
Share and Cite
Bontempi, B.; Lévêque, P.; Dubreuil, D.; Jay, T.M.; Edeline, J.-M. Effects of Head-Only Exposure to 900 MHz GSM Electromagnetic Fields in Rats: Changes in Neuronal Activity as Revealed by c-Fos Imaging without Concomitant Cognitive Impairments. Biomedicines 2024, 12, 1954. https://doi.org/10.3390/biomedicines12091954
Bontempi B, Lévêque P, Dubreuil D, Jay TM, Edeline J-M. Effects of Head-Only Exposure to 900 MHz GSM Electromagnetic Fields in Rats: Changes in Neuronal Activity as Revealed by c-Fos Imaging without Concomitant Cognitive Impairments. Biomedicines. 2024; 12(9):1954. https://doi.org/10.3390/biomedicines12091954
Chicago/Turabian StyleBontempi, Bruno, Philippe Lévêque, Diane Dubreuil, Thérèse M. Jay, and Jean-Marc Edeline. 2024. "Effects of Head-Only Exposure to 900 MHz GSM Electromagnetic Fields in Rats: Changes in Neuronal Activity as Revealed by c-Fos Imaging without Concomitant Cognitive Impairments" Biomedicines 12, no. 9: 1954. https://doi.org/10.3390/biomedicines12091954