Complex magnetic fields enable static magnetic field cue use for rats in radial maze tasks

International Journal of Neuroscience

Volumn 115, Issue 5, 2005, Pages 625-648

  McKay, B E ^a   Persinger, M A ^a  

^a LAURENTIAN UNIVERSITY   (Canada)

Author keywords

Complex magnetic fields; Cues; Magnetic field; Rat; Spatial navigation

Indexed keywords

ANIMAL EXPERIMENT; ARTICLE; LEARNING TEST; MAGNETIC FIELD; MAGNETIC STIMULATION; MAGNETISM; MALE; MAZE TEST; NONHUMAN; RAT; SPATIAL MEMORY; TASK PERFORMANCE; THETA RHYTHM; WAVEFORM;

ANIMALS; BEHAVIOR, ANIMAL; CUES; ELECTROMAGNETIC FIELDS; HIPPOCAMPUS; MALE; MAZE LEARNING; MEMORY; RATS; RATS, WISTAR; SMELL;

EID: 18644379817     PISSN: 00207454     EISSN: None     Source Type: Journal    
DOI: 10.1080/00207450590523945     Document Type: Article

References (82)

1. Bawin, S. M., Satmary, W. M., Jones, R. A., Adey, W. R., & Zimmerman, G. (1996). Extremely-low frequency magnetic fields disrupt rhythmic slow activity in rat hippocampal slices. Bioelectromagnetics, 17, 388-395.
2. Beason, R. C., & Nichols, J. E. (1984). Magnetic orientation and magnetically sensitive material in a transequatorial migratory bird. Nature, 309, 151-153.
3. Blakemore, R. (1975). Magnetotactic bacteria. Science, 190, 377-379.
4. Bramham, C. R., & Sarvey, J. M. (1996). Endogenous activation of mu and delta-1 opioid receptors is required for long-term potentiation induction in the lateral perforant path: Dependence on GABAergic inhibition. Journal of Neuroscience, 16, 8123-8131.
5. Brassart, J., Kirschvink, J. L., Phillips, J. B., & Borland, S. C. (1999). Ferromagnetic material in the eastern red-spotted newt Notophthalmus viridescens. Journal of Experimental Biology, 202, 3155-3160.
6. Burda, H., Marhold, S., Westenberger, T., Wiltschko, R., & Wiltschko, W. (1990). Magnetic compass orientation in the subterranean rodent Cryptomys hottentotus (Bathyergidae). Experientia, 46, 528-530.
7. Deutschlander, M. E., Borland, S. C., & Phillips, J. B. (1999). Extraocular magnetic compass in newts. Nature, 400, 324-325.
8. Deutschlander, M. E., Phillips, J. B., & Borland, S. C. (1999). The case for light-dependent magnetic orientation in animals. Journal of Experimental Biology, 202, 891-908.
9. Diebel, C. E., Proksch, R., Green, C. R., Neilson, P., & Walker, M. M. (2000). Magnetite defines a vertebrate magnetoreceptor. Nature, 406, 299-302.
10. Fischer, Y., Gahwiler, B. H., & Thompson, S. M. (1999). Activation of intrinsic hippocampal theta oscillations by acetylcholine in rat septo-hippocampal cultures. Journal of Physiology, 519, 405-413.
11. Gould, J. L. (1978). Bees have magnetic remanance. Science, 201, 1026-1028.
12. Gould, J. L. (1980). The case for magnetic sensitivity in birds and bees (such as it is). American Scientist, 68, 256-267.
13. Gould, J. L. (1998). Sensory bases of navigation. Current Biology, 8, R731-738.
14. Hutcheon, B., & Yarom, Y. (2000). Resonance, oscillation and the intrinsic frequency preferences of neurons. Trends in Neuroscience, 23, 216-222.
15. Jenrow, K. A., Zhang, X., Renehan, W. E., & Liboff, A. R. (1998). Weak ELF magnetic field effects on hippocampal rhythmic slow activity. Experimental Neurology, 153, 328-334.
16. John, E. R. (1967). Mechanisms of memory. London: Academic Press.
17. Kavanau, J. L. (1996). Memory, sleep, and dynamic stabilization of neural circuitry: Evolutionary perspectives. Neuroscience and Biobehavioral Reviews, 20, 289-311.
18. Keeton, W. T., Larkin, T. S., & Windsor, D. M. (1974). Normal fluctuations in the earth's magnetic field influence pigeon orientation. Journal of Comparative Physiology [A], 95, 95-103.
19. Kimchi, T., & Terkel, J. (2001). Magnetic compass orientation in the blind mole rat Spalax ehrenbergi. Journal of Experimental Biology, 204, 751-758.
20. Kirschvink, J. L., & Gould, J. L. (1981). Biogenic magnetite as a basis for magnetic field detection in animals. Biosystems, 13, 181-201.
21. Kirschvink, J. L., Kobayashi-Kirschvink, A., Diaz-Ricci, J. C., & Kirschvink, S. J. (1992). Magnetite in human tissues: A mechanism for the biological effects of weak ELF magnetic fields. Bioelectromagnetics, 1, S101-S113
22. Kirschvink, J. L., Kobayashi-Kirschvink, A., & Woodford, B. J. (1992). Magnetite biomineralization in the human brain. Proceedings of the National Academy of Science USA, 89, 7683-7687.
23. Kolb, B., & Whishaw, I. Q. (1996). Fundamentals of human neuropsychology (4th ed). New York: W.H. Freeman & Company.
24. Lai, H. (1996). Spatial learning deficit in the rat after exposure to a 60 Hz magnetic field. Bioelectromagnetics, 17, 494-496.
25. Leask, M. J. M. (1977). A physicochemical mechanism for magnetic field detection by migratory birds and homing pigeons. Nature, 267, 144-145.
26. Lednev, V. V. (1991). Possible mechanism for the influence of weak magnetic fields on biological systems. Bioelectromagnetics, 12, 71-75.
27. Liboff, A. R. (1985). Cyclotron resonance in membrane transport. In A. Chiabrera, C. Nicolini, & H. P. Schwan (Eds.), Interactions between electromagnetic fields and cells (pp. 281-296). New York: Plenum Press.
28. Liboff, A. R., Smith, S. D., & McLeod, B. R. (1987). Experimental evidence for ion cyclotron resonance mediation of membrane transport. In M. Blank & E. Findl (Eds.), Mechanistic approaches to interactions of electric and electromagnetic fields with living systems (pp 109-132). London: Plenum Press.
29. Lohmann, K. J. (1993). Magnetic compass orientation. Nature, 362, 703.
30. Lohmann, K. J., & Lohmann, C. M. F. (1996). Detection of magnetic field intensity by sea turtles. Nature, 380, 59-61.
31. Louie, K., & Wilson, M. A. (2001). Temporally structured replay of awake hippocampal ensemble activity during rapid eye movement sleep. Neuron, 29, 145-156.
32. Mann, S., Sparks, N. H., Walker, M. M., & Kirschvink, J. L. (1988). Ultrastructure, morphology and organization of biogenic magnetite from sockeye salmon, Oncorhynchus nerka: Implications for magnetoreception. Journal of Experimental Biology, 40, 35-49.
33. Maren, S., De Oca, B., & Fanselow, M. S. (1994). Sex differences in hippocampal long-term potentiation (LTP) and Pavlovian fear conditioning in rats: Positive correlation between LTP and contextual learning. Brain Research, 661, 25-34.
34. Marhold, S., Wiltschko, W., & Burda, H. (1997). A magnetic polarity compass for direction finding in a subterranean mammal. Naturwissenschaften, 84, 421-423.
35. Martin, L. J., Koren, S. A., & Persinger, M. A. (2003). Thermal analgesic effects from weak, complex magnetic fields: critical parameters and pharmacological interactions. Pharmacology Biochemistry and Behavior, 78, 217-227.
36. Mather, J. G., & Baker, R. R. (1981). Magnetic sense of direction in woodmice for route-based navigation. Nature, 291, 152-155.
37. McKay, B. E., & Persinger, M. A. (1999). Geophysical variables and behavior: LXXXVII. Effects of synthetic and natural geomagnetic patterns on maze learning. Perceptual and Motor Skills, 89, 1023-1024.
38. McKay, B. E., & Persinger, M. A. (2000). Application timing of complex magnetic fields delineates windows of posttraining-pretesting vulnerability for spatial and motivational behaviors in rats. International Journal of Neuroscience, 103, 69-77.
39. McKay, B. E., Persinger, M. A., & Koren, S. A. (2000). Exposure to a theta-burst patterned magnetic field impairs memory acquisition and consolidation for contextual but not discrete conditioned fear in rats. Neuroscience Letters, 292, 99-102.
40. McKay, B. E., & Persinger, M. A. (2003). Combined effects of complex magnetic fields and agmatine for contextual fear learning deficits in rats. Life Sciences, 72, 2489-2498.
41. Moore, B. R. (1980). Is the homing pigeon's map geomagnetic? Nature, 285, 69-70.
42. Moser, M. B., Moser, E. I., Forrest, E., Andersen, P., & Morris, R. G. M. (1995). Spatial learning with a minislab in the dorsal hippocampus. Proceedings of the National Academy of Science, 92, 9697-9701.
43. O'Keefe, J., & Nadel, L. (1978). The hippocampus as cognitive map. Oxford: Clarendon Press.
44. O'Keefe, J., & Burgess, N. (1996). Geometric determinants of the place fields of hippocampal neurons. Nature, 381, 425-428.
45. Olton, D. S., & Samuelson, R. J. (1976). Remembrance of places passed: Spatial memory in rats. Journal of Experimental Psychology: Animal Behavior Processes, 2, 97-116.
46. Pardoe, H., & Dobson, J. (1999). Magnetic iron biomineralization in rat brains: Effects of iron loading. Biometals, 12, 77-82.
47. Parent, A. (1996). Carpenter's Human Neuroanatomy (9th ed). Baltimore: Williams and Wilkins.
48. Persinger, M. A., Richards, P. M., & Koren, S. A. (1997). Differential entrainment of electroencephalographic activity by weak complex electromagnetic fields. Perceptual and Motor Skills, 84, 527-536.
49. Persinger, M. A., St-Pierre, L. S., & Koren, S. A. (2001). Ambulatory behaviour in rats following prenatal exposures to complex magnetic fields designed to interact with genetic expression. Perceptual and Motor Skills, 89, 183-192.
50. Petersen, W. F. (1947). Man weather sun. Springfield, IL: Charles C Thomas.
51. Phillips, J. B., & Borland, S. C. (1992). Behavioral evidence for use of a light-dependent magnetoreception mechanism by a vertebrate. Nature, 359, 142-144.
52. Phillips, J. B., & Borland, S. C. (1994). Use of a specialized magnetoreception system for homing by the eastern red-spotted newt Notophthalmus viridescens. Journal of Experimental Biology, 188, 275-291.
53. Prato, F. S., Carson, J. J., Ossenkopp, K. P., & Kavaliers, M. (1995). Possible mechanisms by which extremely low frequency magnetic fields affect opioid function. FASEB Journal, 9, 807-814.
54. Prato, F. S., Kavaliers, M., Cullen, A. P., & Thomas, A. W. (1997). Light-dependent and independent behavioral effects of extremely low frequency magnetic fields in a land snail are consistent with a parametric resonance mechanism. Bioelectromagnetics, 18, 284-291.
55. Prato, F. S., Kavaliers, M., & Thomas, A. W. (2000). Extremely low frequency magnetic fields can either increase or decrease analgaesia in the land snail depending on field and light conditions. Bioelectromagnetics, 21, 287-301.
56. Presti, D., & Pettigrew, J. D. (1980). Ferromagnetic coupling to muscle receptors as a basis for geomagnetic sensitivity in animals. Nature, 285, 99-101.
57. Rawlins, J. N. P., & Deacon, R. M. J. (1993). Further developments of maze procedures. In A. Sahgal (Ed.), Behavioral neuroscience volume I-A practical approach (pp 95-106). Oxford: Oxford University Press.
58. Richards, P. M., Persinger, M. A., & Koren, S. A. (1996). Modification of semantic memory in normal subjects by application across the temporal lobes of a weak (1 microT) magnetic field structure that promotes long-term potentiation in hippocampal slices. Electro- and Magnetobiology, 15, 141-148.
59. Richmond, M. A., Yee, B. K., Pouzet, B., Veenman, L., Rawlins, J. N. P., Feldon, J., & Bannerman, D. M. (1999). Dissociating context and space within the hippocampus: Effects of complete, dorsal, and ventral excitotoxic hippocampal lesions on conditioned freezing and spatial learning. Behavioral Neuroscience, 113, 1189-1203.
60. Rocard, Y. (1964). Actions of a very weak magnetic gradient: The reflex of the dowser. In M. F. Barnothy (Ed.), Biological effects of magnetic fields (pp 279-286). New York: Plenum Press.
61. Rose, G. M., Diamond, D. M., Pang, K., & Dunwiddie, T. V. (1988). Primed burst potentiation: Lasting synaptic plasticity invoked by physiologically patterned stimulation. In H. L. Haas (Ed.), Synaptic plasticity in the hippocampus (pp. 96-98). Berlin: Springer-Verlag.
62. Semm, P., Nohr, D., Demaine, C., & Wiltschko, W. (1984). Neural basis of the magnetic compass: Interactions of visual, magnetic and vestibular inputs in the pigeon's brain. Journal of Comparative Physiology [A], 155, 283-288.
63. Semm, P., & Demaine, C. (1986). Neurophysiological properties of magnetic cells in the pigeon's visual system. Journal of Comparative Physiology [A], 159, 619-625.
64. Semm, P., & Beason, R. C. (1990). Responses to small magnetic variations by the trigeminal system of the bobolink. Brain Research Bulletin, 25, 735-740.
65. Southern, W. E. (1971). Gull orientation by magnetic cues: A hypothesis revisited. Annals of the New York Academy of Science, 188, 295-311.
66. Spain, J. W., & Newsom, G. C. (1991). Chronic opioids impair acquisition of both radial maze and Y-maze choice escape. Psychopharmacology (Berl), 105, 101-106.
67. Srinivasan, R., Russell, D. P., Edelman, G. M., & Tononi, G. (1999). Increased synchronization of neuromagnetic responses during conscious perception. Journal of Neuroscience, 19, 5435-5448.
68. Steriade, M., & Besehenes, M. (1984). The thalamus as a neuronal oscillator. Brain Research Reviews, 8, 1-63.
69. Thomas, A. W., & Persinger, M. A. (1997). Daily posttraining exposure to pulsed magnetic fields that evoke morphine-like analgesia affects consequent motivation but not proficiency in maze learning in rats. Electro- and Magnetobiology, 16, 33-41.
70. Thomas, A. W., Kavaliers, M., Prato, F. S., & Ossenkopp, K. P. (1997). Pulsed magnetic field induced "analgesia" in the land snail, Cepaea nemoralis, and the effects of mu, delta, and kappa opioid receptor agonists/antagonists. Peptides, 18, 703-709.
71. Thomas, A. W., Kavaliers, M., Prato, F. S., & Ossenkopp, K. P. (1998). Analgesic effects of a specific pulsed magnetic field in the land snail, Cepaea nemoralis: Consequences of repeated exposures, relations to tolerance and cross-tolerance with DPDPE. Peptides, 19, 333-342.
72. Walcott, C., & Green, R. P. (1974). Orientation of homing pigeons altered by a change in the direction of an applied magnetic field. Science, 184, 180-182.
73. Walcott, C., Gould, J. L., & Kirschvink, J. L. (1979). Pigeons have magnets. Science, 205, 1027-1029.
74. Walker, M. M., Quinn, T. P., Kirschvink, J. L., & Groot, C. (1988). Production of single-domain magnetite throughout life by sockeye salmon, Oncorhynchus nerka. Journal of Experimental Biology, 140, 51-63.
75. Walker, M. M., Diebel, C. E., Haugh, C. V., Pankhurst, P. M., Montgomery, J. C., & Green, C. R. (1997). Structure and function of the vertebrate magnetic sense. Nature, 390, 371-376.
76. Watts, J., Stevens, R., & Robinson, C. (1981). Effects of scopolamine on radial maze performance in rats. Physiology & Behavior, 26, 845-851.
77. Wiltschko, W., Munro, U., Ford, H., & Wiltschko, R. (1993). Red light disrupts magnetic orientation of migratory birds. Nature, 364, 525-527.
78. Wiltschko, W., Munro, U., Ford, H., & Wiltschko, R. (1998). Effect of a magnetic pulse on the orientation of silvereyes, zosterops I. lateralis, during spring migration. Journal of Experimental Biology, 201, 3257-3261.
79. Wiltschko, W., & Wiltschko, R. (1972). Magnetic compass of European robins. Science, 176, 62-64.
80. Von Krosigk, M., Bal, T., & McCormick, D. A. (1993). Cellular mechanisms of a synchronized oscillation in the thalamus. Science, 261, 361-364.
81. Vorobyov, V. V., Sosunov, E. A., Kukushkin, N. I., & Lednev, V. V. (1998). Weak combined magnetic field affects basic and morphine-induced rat's EEG. Brain Research, 781, 182-187.
82. Zoeger, J., Dunn, J. R., & Fuller, M. (1981). Magnetic material in the head of the common pacific dolphin. Science, 213, 892-894.