Effects of exposure to a 50 Hz sinusoidal magnetic field during the early adolescent period on spatial memory in mice

Adolescence is a critical developmental stage during which substantial remodeling occurs in brain areas involved in emotional and learning processes. Although a robust literature on the biological effects of extremely low frequency magnetic fields (ELF-MFs) has been documented, data on the effects of ELF-MF exposure during this period on cognitive functions remain scarce. In this study, early adolescent male mice were exposed from postnatal day (P) 23-35 to a 50 Hz MF at 2 mT for 60 min/day. On P36-45, the potential effects of the MF exposure on spatial memory performance were examined using the Y-maze and Morris water maze tasks. The results showed that the MF exposure did not affect Y-maze performance but improved spatial learning acquisition and memory retention in the water maze task under the present experimental conditions.

[1]  T. Zeng,et al.  Effects of morphine and its withdrawal on Y-maze spatial recognition memory in mice , 2007, Neuroscience.

[2]  Z. Sienkiewicz,et al.  Prenatal exposure to a 50 Hz magnetic field has no effect on spatial learning in adult mice. , 1996, Bioelectromagnetics.

[3]  Majid Jadidi,et al.  Acute exposure to a 50Hz magnetic field impairs consolidation of spatial memory in rats , 2007, Neurobiology of Learning and Memory.

[4]  H. Lai,et al.  Spatial learning deficit in the rat after exposure to a 60 Hz magnetic field. , 1996, Bioelectromagnetics.

[5]  R. Guevara-Guzmán,et al.  Exposure to extremely low-frequency electromagnetic fields improves social recognition in male rats , 2004, Physiology & Behavior.

[6]  Yuanye Ma,et al.  Effects of prenatal exposure to a 50‐Hz magnetic field on one‐trial passive avoidance learning in 1‐day‐old chicks , 2009, Bioelectromagnetics.

[7]  Z. Sienkiewicz,et al.  Neurobehavioural effects of electromagnetic fields , 2005, Bioelectromagnetics.

[8]  Abdelkader Ennaceur,et al.  Effects of exposure to extremely low-frequency magnetic field of 2 G intensity on memory and corticosterone level in rats , 2002, Physiology & Behavior.

[9]  G. Koob,et al.  Genetic Differences in Response to Novelty and Spatial Memory Using a Two-Trial Recognition Task in Mice , 2000, Neurobiology of Learning and Memory.

[10]  M. van den Buuse,et al.  Impaired spatial reference memory in aromatase-deficient (ArKO) mice , 2003, Neuroreport.

[11]  I. Whishaw,et al.  Dopamine depletion, stimulation or blockade in the rat disrupts spatial navigation and locomotion dependent upon beacon or distal cues , 1985, Behavioural Brain Research.

[12]  A. Wieraszko,et al.  Modulation of learning and hippocampal, neuronal plasticity by repetitive transcranial magnetic stimulation (rTMS) , 2006, Bioelectromagnetics.

[13]  A. Dellarole,et al.  Acquisition, retention, and recall of memory after injection of RS67333, a 5-HT(4) receptor agonist, into the nucleus basalis magnocellularis of the rat. , 2003, Learning & memory.

[14]  Martin H. Teicher,et al.  Delayed Effects of Early Stress on Hippocampal Development , 2004, Neuropsychopharmacology.

[15]  Jiang-Ning Zhou,et al.  Age-related learning and memory impairments in adult-onset hypothyroidism in Kunming mice , 2007, Physiology & Behavior.

[16]  Lihua He,et al.  Effects of extremely low frequency magnetic field on anxiety level and spatial memory of adult rats. , 2011, Chinese medical journal.

[17]  M. Le Moal,et al.  Extension of a New Two-Trial Memory Task in the Rat: Influence of Environmental Context on Recognition Processes , 1997, Neurobiology of Learning and Memory.

[18]  M. Gallagher,et al.  Opiate antagonists improve spatial memory. , 1983, Science.

[19]  I. Izquierdo,et al.  The role of opioid peptides in memory and learning , 1980, Behavioural Brain Research.

[20]  R. D'Hooge,et al.  Applications of the Morris water maze in the study of learning and memory , 2001, Brain Research Reviews.

[21]  J. Roder,et al.  Differential involvement of the Mu and Kappa opioid receptors in spatial learning , 2003, Genes, brain, and behavior.

[22]  F. Prato,et al.  Evidence for the involvement of nitric oxide and nitric oxide synthase in the modulation of opioid-induced antinociception and the inhibitory effects of exposure to 60-Hz magnetic fields in the land snail , 1998, Brain Research.

[23]  Judy Reilly,et al.  Cognitive efficiency on a match to sample task decreases at the onset of puberty in children , 2002, Brain and Cognition.

[24]  W. Beatty Opiate antagonists, morphine and spatial memory in rats , 1983, Pharmacology Biochemistry and Behavior.

[25]  G. Richter-Levin,et al.  Juvenile stress induces a predisposition to either anxiety or depressive-like symptoms following stress in adulthood , 2007, European Neuropsychopharmacology.

[26]  E. Kandel The Molecular Biology of Memory Storage: A Dialogue Between Genes and Synapses , 2001, Science.

[27]  C. McCormick,et al.  HPA function in adolescence: Role of sex hormones in its regulation and the enduring consequences of exposure to stressors , 2007, Pharmacology Biochemistry and Behavior.

[28]  Tongtong Liu,et al.  Chronic exposure to low-intensity magnetic field improves acquisition and maintenance of memory , 2008, Neuroreport.

[29]  Yuanye Ma,et al.  Effects of extremely low-frequency electromagnetic fields on morphine-induced conditioned place preferences in rats , 2005, Neuroscience Letters.

[30]  R. Sandyk Alzheimer's disease: improvement of visual memory and visuoconstructive performance by treatment with picotesla range magnetic fields. , 1994, The International journal of neuroscience.

[31]  M. Kavaliers,et al.  Brief exposure to 60 Hz magnetic fields improves sexually dimorphic spatial learning performance in the meadow vole, Microtus pennsylvanicus , 1993, Journal of Comparative Physiology A.

[32]  Z. Azizi,et al.  Involvement of hippocampal nitric oxide in spatial learning in the rat , 2008, Neurobiology of Learning and Memory.

[33]  P Cerretelli,et al.  Biological effects of prolonged exposure to ELF electromagnetic fields in rats: III. 50 Hz electromagnetic fields. , 1998, Bioelectromagnetics.

[34]  R. Schwarting,et al.  Animal models of human psychopathology based on individual differences in novelty-seeking and anxiety , 2008, Neuroscience & Biobehavioral Reviews.

[35]  M. Carino,et al.  Acute exposure to a 60 Hz magnetic field affects rats' water-maze performance. , 1998, Bioelectromagnetics.

[36]  T. Insel,et al.  The ontogeny of excitatory amino acid receptors in rat forebrain—I.N-methyl-d-aspartate and quisqualate receptors , 1990, Neuroscience.

[37]  R. Sandyk Brief communication: electromagnetic fields improve visuospatial performance and reverse agraphia in a parkinsonian patient. , 1996, The International journal of neuroscience.

[38]  F. Prato,et al.  Spatial learning in deer mice: sex differences and the effects of endogenous opioids and 60 Hz magnetic fields , 1996, Journal of Comparative Physiology A.

[39]  J. S. Johnson,et al.  Critical period effects in second language learning: The influence of maturational state on the acquisition of English as a second language , 1989, Cognitive Psychology.

[40]  Leeka Kheifets,et al.  The Sensitivity of Children to Electromagnetic Fields , 2005, Pediatrics.

[41]  L. Spear The adolescent brain and age-related behavioral manifestations , 2000, Neuroscience & Biobehavioral Reviews.

[42]  Maria Toledo-Rodriguez,et al.  Stress before Puberty Exerts a Sex- and Age-Related Impact on Auditory and Contextual Fear Conditioning in the Rat , 2007, Neural plasticity.

[43]  F. Schenk,et al.  Spaced training facilitates long-term retention of place navigation in adult but not in adolescent rats , 2002, Behavioural Brain Research.

[44]  M. Persinger,et al.  BEHAVIORAL EFFECTS OF COMBINED PERINATAL L-NAME AND 0.5 Hz MAGNETIC FIELD TREATMENTS , 2003, The International journal of neuroscience.

[45]  Yuanye Ma,et al.  LONG‐TERM EXPOSURE TO EXTREMELY LOW‐FREQUENCY MAGNETIC FIELDS IMPAIRS SPATIAL RECOGNITION MEMORY IN MICE , 2008, Clinical and experimental pharmacology & physiology.

[46]  Jong-Choon Kim,et al.  Lack of adverse effects in pregnant/lactating female rats and their offspring following pre‐ and postnatal exposure to ELF magnetic fields , 2004, Bioelectromagnetics.

[47]  Fulton Crews,et al.  Adolescent cortical development: A critical period of vulnerability for addiction , 2007, Pharmacology Biochemistry and Behavior.

[48]  M. Kavaliers,et al.  Brief exposure of mice to 60 Hz magnetic fields reduces the analgesic effects of the neuroactive steroid, 3α-hydroxy-4-pregnen-20-one , 1998, Neuroscience Letters.

[49]  A. Sieroń,et al.  Alternating extremely low frequency magnetic field increases turnover of dopamine and serotonin in rat frontal cortex , 2004, Bioelectromagnetics.

[50]  Z. Sienkiewicz,et al.  50 Hz magnetic field effects on the performance of a spatial learning task by mice. , 1998, Bioelectromagnetics.

[51]  B. Veyret,et al.  ELF magnetic fields: animal studies, mechanisms of action. , 2011, Progress in biophysics and molecular biology.

[52]  Leeka Kheifets,et al.  EMF and health. , 2005, Annual review of public health.

[53]  Wendy K. Adams,et al.  Serotonin depletion in the dorsal and ventral hippocampus: Effects on locomotor hyperactivity, prepulse inhibition and learning and memory , 2008, Neuropharmacology.

[54]  C. McCormick,et al.  Adolescent development, hypothalamic-pituitary-adrenal function, and programming of adult learning and memory , 2010, Progress in Neuro-Psychopharmacology and Biological Psychiatry.

[55]  Yuanye Ma,et al.  Extremely low-frequency electromagnetic field exposure during chronic morphine treatment strengthens downregulation of dopamine D2 receptors in rat dorsal hippocampus after morphine withdrawal , 2008, Neuroscience Letters.

[56]  M. Kavaliers,et al.  Pain perception and electromagnetic fields , 2007, Neuroscience & Biobehavioral Reviews.

[57]  A. Małecki,et al.  Behavioral effects of long-term exposure to magnetic fields in rats. , 1993, Bioelectromagnetics.

[58]  R. D. Saunders,et al.  Acute exposure to power-frequency magnetic fields has no effect on the acquisition of a spatial learning task by adult male mice , 1996 .

[59]  S. Łopuch A magnetic field effect on learning in male golden hamsters , 2009, Behavioural Processes.

[60]  S. Harvey,et al.  Role of Hippocampal CA3 μ-Opioid Receptors in Spatial Learning and Memory , 2004, The Journal of Neuroscience.

[61]  M. Kavaliers,et al.  Evidence for the involvement of protein kinase C in the modulation of morphine-induced ‘analgesia’ and the inhibitory effects of exposure to 60-Hz magnetic fields in the snail,Cepaea nemoralis , 1991, Brain Research.

[62]  Xiaoyan Chen,et al.  Chronic Morphine Treatment Impaired Hippocampal Long-Term Potentiation and Spatial Memory via Accumulation of Extracellular Adenosine Acting on Adenosine A1 Receptors , 2010, The Journal of Neuroscience.

[63]  Z. Sienkiewicz,et al.  Single, brief exposure to a 50 Hz magnetic field does not affect the performance of an object recognition task in adult mice. , 2001, Bioelectromagnetics.

[64]  M. Otto,et al.  Electromagnetic fields (EMF): do they play a role in children's environmental health (CEH)? , 2007, International journal of hygiene and environmental health.

[65]  Debby Van Dam,et al.  Effect of Morris water maze diameter on visual-spatial learning in different mouse strains , 2006, Neurobiology of Learning and Memory.

[66]  M. Repacholi,et al.  Guest editors' introduction: Is EMF a potential environmental risk for children? , 2005, Bioelectromagnetics.

[67]  A. Fenton,et al.  A Critical Role for α4βδ GABAA Receptors in Shaping Learning Deficits at Puberty in Mice , 2010, Science.

[68]  L. Sher The role of the endogenous opioid system in the effects of acupuncture on mood, behavior, learning, and memory. , 1998, Medical hypotheses.

[69]  S. Blakemore The social brain in adolescence , 2008, Nature Reviews Neuroscience.