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Neurobiological effects of repeated radiofrequency exposures in male senescent rats

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Abstract

The increasing use of mobile phones by aging people raises issues about the effects of radiofrequency electromagnetic fields (RF-EMF) on the aging central nervous system. Here, we tested if mobile phone RF-EMF exposures could exacerbate senescence-typical neurobiological deficits. Thus, aged (22–24 months) and young (4–6 months) adult male rats were subjected to head RF-EMF exposures (900 MHz, specific absorption rate (SAR) of 6 W/kg, 45 min/day for 1 month in restraint rockets). To assess senescence-typical neurobiological deficits, spatial memory, emotional memory, anxiety-related behavior, locomotor activity, interleukins (IL)-1β and 6, glial fibrillary acidic protein and corticosterone were measured. Aged rats presented deficits in spatial learning, exploration, anxiety-related behaviors, and increased hippocampal ILs and cortical IL-1β. Results showed that senescence-typical neurobiological deficits were not modified by RF-EMF exposures. RF-EMF-exposed rats (young and aged adults pooled) had decreased anxiety-related behaviors in the elevated plus maze. This study which is the first to assess RF-EMF exposures during late aging did not support the hypothesis of a specific cerebral vulnerability to RF-EMF during senescence. More investigations using longer RF-EMF exposures should be performed to conclude regarding the inoffensiveness of RF-EMF exposures.

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References

  • Ammari M, Brillaud E, Gamez C, Lecomte A, Sakly M, Abdelmelek H, de Seze R (2008a) Effect of a chronic GSM 900 MHz exposure on glia in the rat brain. Biomed Pharmacother 62:273–281

    Article  CAS  PubMed  Google Scholar 

  • Ammari M, Jacquet A, Lecomte A, Sakly M, Abdelmelek H, de Seze R (2008b) Effect of head-only sub-chronic and chronic exposure to 900-MHz GSM electromagnetic fields on spatial memory in rats. Brain Inj 22:1021–1029

    Article  PubMed  Google Scholar 

  • Ammari M, Gamez C, Lecomte A, Sakly M, Abdelmelek H, De Seze R (2010) GFAP expression in the rat brain following sub-chronic exposure to a 900 MHz electromagnetic field signal. Int J Radiat Biol 86:367–375

    Article  CAS  PubMed  Google Scholar 

  • Barrientos RM, Frank MG, Hein AM, Higgins EA, Watkins LR, Rudy JW, Maier SF (2009) Time course of hippocampal IL-1 beta and memory consolidation impairments in aging rats following peripheral infection. Brain Behav Immun 23:46–54

    Article  CAS  PubMed  Google Scholar 

  • Barth A, Ponocny I, Gnambs T, Winker R (2011) No effects of short-term exposure to mobile phone electromagnetic fields on human cognitive performance: a meta-analysis. Bioelectromagnetics 33:159–165

    Article  PubMed  Google Scholar 

  • Bekker AY, Weeks EJ (2003) Cognitive function after anaesthesia in the elderly. Best Pract Res 17:259–272

    Article  Google Scholar 

  • Besset A, Espa F, Dauvilliers Y, Billiard M, de Seze R (2005) No effect on cognitive function from daily mobile phone use. Bioelectromagnetics 26:102–108

    Article  PubMed  Google Scholar 

  • Bizon JL, LaSarge CL, Montgomery KS, McDermott AN, Setlow B, Griffith WH (2009) Spatial reference and working memory across the lifespan of male Fischer 344 rats. Neurobiol Aging 30:646–655

    Article  CAS  PubMed  Google Scholar 

  • Bouji M, Lecomte A, Hode Y, de Seze R, Villegier AS (2012) Effects of 900 MHz radiofrequency on corticosterone, emotional memory and neuroinflammation in middle-aged rats. Exp Gerontol 47:444–451

    Article  CAS  PubMed  Google Scholar 

  • Brenes GA (2006) Age differences in the presentation of anxiety. Aging Ment Health 10:298–302

    Article  CAS  PubMed  Google Scholar 

  • Brillaud E, Piotrowski A, de Seze R (2007) Effect of an acute 900 MHz GSM exposure on glia in the rat brain: a time-dependent study. Toxicology 238:23–33

    Article  CAS  PubMed  Google Scholar 

  • Carballo-Quintas M, Martinez-Silva I, Cadarso-Suarez C, Alvarez-Figueiras M, Ares-Pena FJ, Lopez-Martin E (2011) A study of neurotoxic biomarkers, c-fos and GFAP after acute exposure to GSM radiation at 900 MHz in the picrotoxin model of rat brains. Neurotoxicology 32:478–494

    Article  CAS  PubMed  Google Scholar 

  • Cordero MI, Kruyt ND, Sandi C (2003) Modulation of contextual fear conditioning by chronic stress in rats is related to individual differences in behavioral reactivity to novelty. Brain Res 970:242–245

    Article  CAS  PubMed  Google Scholar 

  • Court-Kowalski S, Finnie JW, Manavis J, Blumbergs PC, Helps SC, Vink R (2015) Effect of long-term (2 years) exposure of mouse brains to global system for mobile communication (GSM) radiofrequency fields on astrocytic immunoreactivity. Bioelectromagnetics 36:245–250

    Article  PubMed  Google Scholar 

  • Daniels WM, Pitout IL, Afullo TJ, Mabandla MV (2009) The effect of electromagnetic radiation in the mobile phone range on the behaviour of the rat. Metab Brain Dis 24:629–641

    Article  PubMed  Google Scholar 

  • Doyere V, Gisquet-Verrier P, de Marsanich B, Ammassari-Teule M (2000) Age-related modifications of contextual information processing in rats: role of emotional reactivity, arousal and testing procedure. Behav Brain Res 114:153–165

    Article  CAS  PubMed  Google Scholar 

  • Dubreuil D, Jay T, Edeline JM (2002) Does head-only exposure to GSM-900 electromagnetic fields affect the performance of rats in spatial learning tasks? Behav Brain Res 129:203–210

    Article  PubMed  Google Scholar 

  • Dubreuil D, Jay T, Edeline JM (2003) Head-only exposure to GSM 900-MHz electromagnetic fields does not alter rat’s memory in spatial and non-spatial tasks. Behav Brain Res 145:51–61

    Article  PubMed  Google Scholar 

  • Edelstyn N, Oldershaw A (2002) The acute effects of exposure to the electromagnetic field emitted by mobile phones on human attention. NeuroReport 13:119–121

    Article  PubMed  Google Scholar 

  • Eltiti S, Wallace D, Ridgewell A, Zougkou K, Russo R, Sepulveda F, Fox E (2009) Short-term exposure to mobile phone base station signals does not affect cognitive functioning or physiological measures in individuals who report sensitivity to electromagnetic fields and controls. Bioelectromagnetics 30:556–563

    Article  PubMed  Google Scholar 

  • El-Zein A, Tewtel-Salem M, Nehme G (2004) A time-series analysis of mortality and air temperature in Greater Beirut. Sci Total Environ 330:71–80

    Article  CAS  PubMed  Google Scholar 

  • Finnie JW, Cai Z, Manavis J, Helps S, Blumbergs PC (2010) Microglial activation as a measure of stress in mouse brains exposed acutely (60 minutes) and long-term (2 years) to mobile telephone radiofrequency fields. Pathology 42:151–154

    Article  CAS  PubMed  Google Scholar 

  • Fragopoulou AF, Miltiadous P, Stamatakis A, Stylianopoulou F, Koussoulakos SL, Margaritis LH (2010) Whole body exposure with GSM 900 MHz affects spatial memory in mice. Pathophysiology 17:179–187

    Article  CAS  PubMed  Google Scholar 

  • Fragopoulou AF et al (2012) Brain proteome response following whole body exposure of mice to mobile phone or wireless DECT base radiation. Electromagn Biol Med 31:250–274

    Article  CAS  PubMed  Google Scholar 

  • Frick KM, Baxter MG, Markowska AL, Olton DS, Price DL (1995) Age-related spatial reference and working memory deficits assessed in the water maze. Neurobiol Aging 16:149–160

    Article  CAS  PubMed  Google Scholar 

  • Garrido P, De Blas M, Gine E, Santos A, Mora F (2012) Aging impairs the control of prefrontal cortex on the release of corticosterone in response to stress and on memory consolidation. Neurobiol Aging 33:821–829

    Article  Google Scholar 

  • Gatta L et al (2003) Effects of in vivo exposure to GSM-modulated 900 MHz radiation on mouse peripheral lymphocytes. Radiat Res 160:600–605

    Article  CAS  PubMed  Google Scholar 

  • Grafstrom G, Nittby H, Brun A, Malmgren L, Persson BR, Salford LG, Eberhardt J (2008) Histopathological examinations of rat brains after long-term exposure to GSM-900 mobile phone radiation. Brain Res Bull 77:257–263

    Article  PubMed  Google Scholar 

  • Haarala C, Ek M, Bjornberg L, Laine M, Revonsuo A, Koivisto M, Hamalainen H (2004) 902 MHz mobile phone does not affect short term memory in humans. Bioelectromagnetics 25:452–456

    Article  PubMed  Google Scholar 

  • Haarala C, Takio F, Rintee T, Laine M, Koivisto M, Revonsuo A, Hamalainen H (2007) Pulsed and continuous wave mobile phone exposure over left versus right hemisphere: effects on human cognitive function. Bioelectromagnetics 28:289–295

    Article  PubMed  Google Scholar 

  • Hao D et al (2013) Effects of long-term electromagnetic field exposure on spatial learning and memory in rats. Neurol Sci 34:157–164

    Article  PubMed  Google Scholar 

  • Hewett JA (2009) Determinants of regional and local diversity within the astroglial lineage of the normal central nervous system. J Neurochem 110:1717–1736

    Article  CAS  PubMed  Google Scholar 

  • Hirose H, Sasaki A, Ishii N, Sekijima M, Iyama T, Nojima T, Ugawa Y (2012) 1950 MHz IMT-2000 field does not activate microglial cells in vitro. Bioelectromagnetics 31:104–112

    Google Scholar 

  • Ivancsits S, Diem E, Jahn O, Rudiger HW (2003) Intermittent extremely low frequency electromagnetic fields cause DNA damage in a dose-dependent way. Int Arch Occup Environ Health 76:431–436

    Article  CAS  PubMed  Google Scholar 

  • Jacobson L, Sapolsky R (1991) The role of the hippocampus in feedback regulation of the hypothalamic-pituitary-adrenocortical axis. Endocr Rev 12:118–134

    Article  CAS  PubMed  Google Scholar 

  • Jech R, Sonka K, Ruzicka E, Nebuzelsky A, Bohm J, Juklickova M, Nevsimalova S (2001) Electromagnetic field of mobile phones affects visual event related potential in patients with narcolepsy. Bioelectromagnetics 22:519–528

    Article  CAS  PubMed  Google Scholar 

  • Junior LC, Guimaraes Eda S, Musso CM, Stabler CT, Garcia RM, Mourao-Junior CA, Andreazzi AE (2014) Behavior and memory evaluation of Wistar rats exposed to 1.8 GHz radiofrequency electromagnetic radiation. Neurol Res 36:800–803

    Article  PubMed  Google Scholar 

  • Klose M, Grote K, Spathmann O, Streckert J, Clemens M, Hansen VW, Lerchl A (2014) Effects of early-onset radiofrequency electromagnetic field exposure (GSM 900 MHz) on behavior and memory in rats. Radiat Res 182:435–447

    Article  CAS  PubMed  Google Scholar 

  • Kohama SG, Goss JR, Finch CE, McNeill TH (1995) Increases of glial fibrillary acidic protein in the aging female mouse brain. Neurobiol Aging 16:59–67

    Article  CAS  PubMed  Google Scholar 

  • Koivisto M, Krause CM, Revonsuo A, Laine M, Hamalainen H (2000a) The effects of electromagnetic field emitted by GSM phones on working memory. NeuroReport 11:1641–1643

    Article  CAS  PubMed  Google Scholar 

  • Koivisto M, Revonsuo A, Krause C, Haarala C, Sillanmaki L, Laine M, Hamalainen H (2000b) Effects of 902 MHz electromagnetic field emitted by cellular telephones on response times in humans. NeuroReport 11:413–415

    Article  CAS  PubMed  Google Scholar 

  • Kumar RS, Sareesh NN, Nayak S, Mailankot M (2009) Hypoactivity of Wistar rats exposed to mobile phone on elevated plus maze. Indian J Physiol Pharmacol 53:283–286

    PubMed  Google Scholar 

  • Kumlin T et al (2007) Mobile phone radiation and the developing brain: behavioral and morphological effects in juvenile rats. Radiat Res 168:471–479

    Article  CAS  PubMed  Google Scholar 

  • Leung S et al (2011) Effects of 2G and 3G mobile phones on performance and electrophysiology in adolescents, young adults and older adults. Clin Neurophysiol 122:2203–2216

    Article  CAS  PubMed  Google Scholar 

  • Leveque P, Dali C, Veyret B, Wiart J (2004) Dosimetric analysis of a 900 MHz rat head exposure system. IEEE Trans Microw Theory Tech 52:2076–2083

    Article  Google Scholar 

  • Lu Y et al (2014) Differential pro-inflammatory responses of astrocytes and microglia involve STAT3 activation in response to 1800 MHz radiofrequency fields. PLoS ONE 9:e108318

    Article  PubMed  PubMed Central  Google Scholar 

  • Lynch MA (1998) Age-related impairment in long-term potentiation in hippocampus: a role for the cytokine, interleukin-1 beta? Prog Neurobiol 56:571–589

    Article  CAS  PubMed  Google Scholar 

  • Maaroufi K, Had-Aissouni L, Melon C, Sakly M, Abdelmelek H, Poucet B, Save E (2014) Spatial learning, monoamines and oxidative stress in rats exposed to 900 MHz electromagnetic field in combination with iron overload. Behav Brain Res 258:80–89

    Article  CAS  PubMed  Google Scholar 

  • Maskey D et al (2010) Chronic 835-MHz radiofrequency exposure to mice hippocampus alters the distribution of calbindin and GFAP immunoreactivity. Brain Res 1346:237–246

    Article  CAS  PubMed  Google Scholar 

  • Maskey D, Kim HJ, Kim HG, Kim MJ (2012) Calcium-binding proteins and GFAP immunoreactivity alterations in murine hippocampus after 1 month of exposure to 835 MHz radiofrequency at SAR values of 1.6 and 4.0 W/kg. Neurosci Lett 506:292–296

    Article  CAS  PubMed  Google Scholar 

  • Mausset-Bonnefont AL, Hirbec H, Bonnefont X, Privat A, Vignon J, de Seze R (2004) Acute exposure to GSM 900-MHz electromagnetic fields induces glial reactivity and biochemical modifications in the rat brain. Neurobiol Dis 17:445–454

    Article  CAS  PubMed  Google Scholar 

  • Moyer JR Jr, Brown TH (2006) Impaired trace and contextual fear conditioning in aged rats. Behav Neurosci 120:612–624

    Article  PubMed  Google Scholar 

  • Narayanan SN, Kumar RS, Potu BK, Nayak S, Mailankot M (2009) Spatial memory performance of Wistar rats exposed to mobile phone. Clinics (Sao Paulo, Brazil) 64:231–234

    Article  Google Scholar 

  • Narayanan SN, Kumar RS, Potu BK, Nayak S, Bhat PG, Mailankot M (2010) Effect of radio-frequency electromagnetic radiations (RF-EMR) on passive avoidance behaviour and hippocampal morphology in Wistar rats. Ups J Med Sci 115:91–96

    Article  PubMed  PubMed Central  Google Scholar 

  • Narayanan SN, Kumar RS, Karun KM, Nayak SB, Bhat PG (2015) Possible cause for altered spatial cognition of prepubescent rats exposed to chronic radiofrequency electromagnetic radiation. Metab Brain Dis 30:1193–1206

    Article  CAS  PubMed  Google Scholar 

  • Ng TP, Lim ML, Niti M, Collinson S (2012) Long-term digital mobile phone use and cognitive decline in the elderly. Bioelectromagnetics 33:176–185

    Article  PubMed  Google Scholar 

  • Nittby H et al (2008) Cognitive impairment in rats after long-term exposure to GSM-900 mobile phone radiation. Bioelectromagnetics 29:219–232

    Article  PubMed  Google Scholar 

  • Ntzouni MP, Stamatakis A, Stylianopoulou F, Margaritis LH (2011) Short-term memory in mice is affected by mobile phone radiation. Pathophysiology 18:193–199

    Article  CAS  PubMed  Google Scholar 

  • Oler JA, Markus EJ (1998) Age-related deficits on the radial maze and in fear conditioning: hippocampal processing and consolidation. Hippocampus 8:402–415

    Article  CAS  PubMed  Google Scholar 

  • Park DC, Hedden T (2002) Working memory and aging. In: Naveh-Benjamin M, Moscovitch M, Rodiger HL III (eds) Perspective on human memory and cognitive aging: essays in honor of Fergus Craick. Psychology Press, East Sussex

    Google Scholar 

  • Petitdant N, Lecomte A, Robidel F, Gamez C, Blazy K, Villégier AS (in press) Cerebral radiofrequency exposures during adolescence: impact on astrocytes and brain functions in healthy and pathologic rat models. Bioelectromagnetics

  • Prochnow N et al (2011) Electromagnetic field effect or simply stress? Effects of UMTS exposure on hippocampal longterm plasticity in the context of procedure related hormone release. PLoS ONE 6:e19437

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ronnlund M, Nyberg L, Backman L, Nilsson LG (2005) Stability, growth, and decline in adult life span development of declarative memory: cross-sectional and longitudinal data from a population-based study. Psychol Aging 20:3–18

    Article  PubMed  Google Scholar 

  • Russo R, Fox E, Cinel C, Boldini A, Defeyter MA, Mirshekar-Syahkal D, Mehta A (2006) Does acute exposure to mobile phones affect human attention? Bioelectromagnetics 27:215–220

    Article  PubMed  Google Scholar 

  • Saikhedkar N, Bhatnagar M, Jain A, Sukhwal P, Sharma C, Jaiswal N (2014) Effects of mobile phone radiation (900 MHz radiofrequency) on structure and functions of rat brain. Neurol Res 36:1072–1079

    Article  CAS  PubMed  Google Scholar 

  • Salthouse TA (2009) When does age-related cognitive decline begin? Neurobiol Aging 30:507–514

    Article  PubMed  PubMed Central  Google Scholar 

  • Schaie K (1996) Intellectual development in adulthood: the Seattle longitudinal study. Cambridge University Press, New York

    Google Scholar 

  • Segar TM, Kasckow JW, Welge JA, Herman JP (2009) Heterogeneity of neuroendocrine stress responses in aging rat strains. Physiol Behav 96:6–11

    Article  CAS  PubMed  Google Scholar 

  • Sofroniew MV (2015) Astrocyte barriers to neurotoxic inflammation. Nat Rev 16:249–263

    Article  CAS  Google Scholar 

  • Son Y et al (2015) The effect of sub-chronic whole-body exposure to a 1,950 MHz electromagnetic field on the hippocampus in the mouse brain. JEES 15:151–157

    Google Scholar 

  • Takahashi S et al (2012) Lack of adverse effects of whole-body exposure to a mobile telecommunication electromagnetic field on the rat fetus. Radiat Res 173:362–372

    Article  Google Scholar 

  • Tang J et al (2015) Exposure to 900 MHz electromagnetic fields activates the mkp-1/ERK pathway and causes blood-brain barrier damage and cognitive impairment in rats. Brain Res 1601:92–101

    Article  CAS  PubMed  Google Scholar 

  • Thorlin T et al (2006) Exposure of cultured astroglial and microglial brain cells to 900 MHz microwave radiation. Radiat Res 166:409–421

    Article  CAS  PubMed  Google Scholar 

  • Valentini E, Ferrara M, Presaghi F, De Gennaro L, Curcio G (2011) Systematic review and meta-analysis of psychomotor effects of mobile phone electromagnetic fields. Occup Environ Med 67:708–716

    Article  Google Scholar 

  • Vecchio F et al (2010) Mobile phone emission modulates inter-hemispheric functional coupling of EEG alpha rhythms in elderly compared to young subjects. Clin Neurophysiol 121:163–171

    Article  PubMed  Google Scholar 

  • Vozeh F, Donek A, Cendelin J, Korelusova I, Vrba J (2007) Study of high-frequency electromagnetic field effect on some somatic and neuro-behavioral characteristics in healthy and neurodefetive mice. Environmentalist 27:501–504

    Article  Google Scholar 

  • Watilliaux A, Edeline JM, Leveque P, Jay TM, Mallat M (2011) Effect of exposure to 1,800 MHz electromagnetic fields on heat shock proteins and glial cells in the brain of developing rats. Neurotoxicol Res 20:109–119

    Article  CAS  Google Scholar 

  • Woodson JC, Macintosh D, Fleshner M, Diamond DM (2003) Emotion-induced amnesia in rats: working memory-specific impairment, corticosterone-memory correlation, and fear versus arousal effects on memory. Learn Mem 10:326–336

    Article  PubMed  PubMed Central  Google Scholar 

  • Zhao W, Zhang J, Davis EG, Rebeck GW (2014) Aging reduces glial uptake and promotes extracellular accumulation of Abeta from a lentiviral vector. Front Aging Neurosci 6:210

    PubMed  PubMed Central  Google Scholar 

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Acknowledgments

We thank Mr. Franck Robidel for his technical help.

Funding

This work was funded by the PR 190 of French Ministry of Ecology (MEDDTL).

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Authors and Affiliations

  1. Unité de Toxicologie Expérimentale, Institut National de l’Environnement Industriel et des Risques (INERIS), Parc Technologique ALATA, BP no. 2, 60550, Verneuil-en-Halatte, France

    Marc Bouji, Anthony Lecomte, Christelle Gamez, Kelly Blazy & Anne-Sophie Villégier

  2. PERITOX EA 4285-UM INERIS 01 UFR de médecine, 3, rue des Louvels, 80036, Amiens, France

    Anthony Lecomte, Christelle Gamez, Kelly Blazy & Anne-Sophie Villégier

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  1. Marc Bouji
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  2. Anthony Lecomte
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Correspondence to Marc Bouji.

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Bouji, M., Lecomte, A., Gamez, C. et al. Neurobiological effects of repeated radiofrequency exposures in male senescent rats. Biogerontology 17, 841–857 (2016). https://doi.org/10.1007/s10522-016-9654-8

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