Skip to main content
PMC home page
Proceedings of the Royal Society B: Biological Sciences logoLink to Proceedings of the Royal Society B: Biological Sciences
. 2002 Jan 22;269(1487):193–201. doi: 10.1098/rspb.2001.1866

Shielding, but not zeroing of the ambient magnetic field reduces stress-induced analgesia in mice.

E Choleris 1, C Del Seppia 1, A W Thomas 1, P Luschi 1, G Ghione 1, G R Moran 1, F S Prato 1
PMCID: PMC1690875  PMID: 11798436

Abstract

Magnetic field exposure was consistently found to affect pain inhibition (i.e. analgesia). Recently, we showed that an extreme reduction of the ambient magnetic and electric environment, by mu-metal shielding, also affected stress-induced analgesia (SIA) in C57 mice. Using CD1 mice, we report here the same findings from replication studies performed independently in Pisa, Italy and London, ON, Canada. Also, neither selective vector nulling of the static component of the ambient magnetic field with Helmholtz coils, nor copper shielding of only the ambient electric field, affected SIA in mice. We further show that a pre-stress exposure to the mu-metal box is necessary for the anti-analgesic effects to occur. The differential effects of the two near-zero magnetic conditions may depend on the elimination (obtained only by mu-metal shielding) of the extremely weak time-varying component of the magnetic environment. This would provide the first direct and repeatable evidence for a behavioural and physiological effect of very weak time-varying magnetic fields, suggesting the existence of a very sensitive magnetic discrimination in the endogenous mechanisms that underlie SIA. This has important implications for other reported effects of exposures to very weak magnetic fields and for the theoretical work that considers the mechanisms underlying the biological detection of weak magnetic fields.

Full Text

The Full Text of this article is available as a PDF (138.8 KB).

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Adair R. K. A physical analysis of the ion parametric resonance model. Bioelectromagnetics. 1998;19(3):181–191. [PubMed] [Google Scholar]
  2. Adair R. K. Constraints of thermal noise on the effects of weak 60-Hz magnetic fields acting on biological magnetite. Proc Natl Acad Sci U S A. 1994 Apr 12;91(8):2925–2929. doi: 10.1073/pnas.91.8.2925. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Akil H., Watson S. J., Young E., Lewis M. E., Khachaturian H., Walker J. M. Endogenous opioids: biology and function. Annu Rev Neurosci. 1984;7:223–255. doi: 10.1146/annurev.ne.07.030184.001255. [DOI] [PubMed] [Google Scholar]
  4. Asashima M., Shimada K., Pfeiffer C. J. Magnetic shielding induces early developmental abnormalities in the newt, Cynops pyrrhogaster. Bioelectromagnetics. 1991;12(4):215–224. doi: 10.1002/bem.2250120403. [DOI] [PubMed] [Google Scholar]
  5. Betancur C., Dell'Omo G., Alleva E. Magnetic field effects on stress-induced analgesia in mice: modulation by light. Neurosci Lett. 1994 Dec 5;182(2):147–150. doi: 10.1016/0304-3940(94)90784-6. [DOI] [PubMed] [Google Scholar]
  6. Bliss V. L., Heppner F. H. Circadian activity rhythm influenced by near zero magnetic field. Nature. 1976 Jun 3;261(5559):411–412. doi: 10.1038/261411a0. [DOI] [PubMed] [Google Scholar]
  7. Bookman M. A. Sensitivity of the homing pigeon to an earth-strength magnetic field. Nature. 1977 May 26;267(5609):340–342. doi: 10.1038/267340a0. [DOI] [PubMed] [Google Scholar]
  8. Brocklehurst B., McLauchlan K. A. Free radical mechanism for the effects of environmental electromagnetic fields on biological systems. Int J Radiat Biol. 1996 Jan;69(1):3–24. doi: 10.1080/095530096146147. [DOI] [PubMed] [Google Scholar]
  9. Burch J. L. The fury of space storms. Sci Am. 2001 Apr;284(4):86–94. doi: 10.1038/scientificamerican0401-86. [DOI] [PubMed] [Google Scholar]
  10. Dawson B. V., Robertson I. G., Wilson W. R., Zwi L. J., Boys J. T., Green A. W. Evaluation of potential health effects of 10 kHz magnetic fields: a rodent reproductive study. Bioelectromagnetics. 1998;19(3):162–171. doi: 10.1002/(sici)1521-186x(1998)19:3<162::aid-bem4>3.0.co;2-#. [DOI] [PubMed] [Google Scholar]
  11. Del Seppia C., Ghione S., Luschi P., Papi F. Exposure to oscillating magnetic fields influences sensitivity to electrical stimuli. I. Experiments on pigeons. Bioelectromagnetics. 1995;16(5):290–294. doi: 10.1002/bem.2250160504. [DOI] [PubMed] [Google Scholar]
  12. Del Seppia C., Luschi P., Ghione S., Crosio E., Choleris E., Papi F. Exposure to a hypogeomagnetic field or to oscillating magnetic fields similarly reduce stress-induced analgesia in C57 male mice. Life Sci. 2000 Feb 25;66(14):1299–1306. doi: 10.1016/s0024-3205(00)00437-9. [DOI] [PubMed] [Google Scholar]
  13. Giraud A. L., Chéry-Croze S., Fischer G., Fischer C., Vighetto A., Grégoire M. C., Lavenne F., Collet L. A selective imaging of tinnitus. Neuroreport. 1999 Jan 18;10(1):1–5. doi: 10.1097/00001756-199901180-00001. [DOI] [PubMed] [Google Scholar]
  14. Kavaliers M., Choleris E., Prato F. S., Ossenkopp K. 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. Brain Res. 1998 Oct 26;809(1):50–57. doi: 10.1016/s0006-8993(98)00844-0. [DOI] [PubMed] [Google Scholar]
  15. Kavaliers M., Ossenkopp K. P. Calcium channel involvement in magnetic field inhibition of morphine-induced analgesia. Naunyn Schmiedebergs Arch Pharmacol. 1987 Sep;336(3):308–315. doi: 10.1007/BF00172683. [DOI] [PubMed] [Google Scholar]
  16. Kavaliers M., Ossenkopp K. P. Day-night rhythms of opioid and non-opioid stress-induced analgesia: differential inhibitory effects of exposure to magnetic fields. Pain. 1988 Feb;32(2):223–229. doi: 10.1016/0304-3959(88)90071-1. [DOI] [PubMed] [Google Scholar]
  17. Kavaliers M., Ossenkopp K. P., Hirst M. Magnetic fields abolish the enhanced nocturnal analgesic response to morphine in mice. Physiol Behav. 1984 Feb;32(2):261–264. doi: 10.1016/0031-9384(84)90139-2. [DOI] [PubMed] [Google Scholar]
  18. Kavaliers M., Ossenkopp K. P., Lipa S. M. Day-night rhythms in the inhibitory effects of 60 Hz magnetic fields on opiate-mediated 'analgesic' behaviors of the land snail, Cepaea nemoralis. Brain Res. 1990 May 28;517(1-2):276–282. doi: 10.1016/0006-8993(90)91038-i. [DOI] [PubMed] [Google Scholar]
  19. Kavaliers M., Ossenkopp K. P. Magnetic fields inhibit opioid-mediated 'analgesic' behaviours of the terrestrial snail, Cepaea nemoralis. J Comp Physiol A. 1988 Mar;162(4):551–558. doi: 10.1007/BF00612520. [DOI] [PubMed] [Google Scholar]
  20. Kavaliers M., Ossenkopp K. P. Stress-induced opioid analgesia and activity in mice: inhibitory influences of exposure to magnetic fields. Psychopharmacology (Berl) 1986;89(4):440–443. doi: 10.1007/BF02412118. [DOI] [PubMed] [Google Scholar]
  21. Kopanev V. I., Efimenko G. D., Shakula A. V. Biological effect of a hypogeomagnetic environment on an organism. Biol Bull Acad Sci USSR. 1979 May-Jun;6(3):289–298. [PubMed] [Google Scholar]
  22. Lednev V. V. Bioéffekty slabykh kombinirovannykh, postoiannykh i peremennykh magnitnykh polei. Biofizika. 1996 Jan-Feb;41(1):224–232. [PubMed] [Google Scholar]
  23. Lednev V. V. Possible mechanism for the influence of weak magnetic fields on biological systems. Bioelectromagnetics. 1991;12(2):71–75. doi: 10.1002/bem.2250120202. [DOI] [PubMed] [Google Scholar]
  24. Lohmann K. J., Johnsen S. The neurobiology of magnetoreception in vertebrate animals. Trends Neurosci. 2000 Apr;23(4):153–159. doi: 10.1016/s0166-2236(99)01542-8. [DOI] [PubMed] [Google Scholar]
  25. Miro L., Deltour G., Pfister A., Kaiser R., Grandpierre R. Action biologique des ambiances hypomagnétiques. Presse Therm Clim. 1970;107(1):32–34. [PubMed] [Google Scholar]
  26. Mogil J. S., Wilson S. G., Bon K., Lee S. E., Chung K., Raber P., Pieper J. O., Hain H. S., Belknap J. K., Hubert L. Heritability of nociception I: responses of 11 inbred mouse strains on 12 measures of nociception. Pain. 1999 Mar;80(1-2):67–82. doi: 10.1016/s0304-3959(98)00197-3. [DOI] [PubMed] [Google Scholar]
  27. Mogil J. S., Wilson S. G., Bon K., Lee S. E., Chung K., Raber P., Pieper J. O., Hain H. S., Belknap J. K., Hubert L. Heritability of nociception II. 'Types' of nociception revealed by genetic correlation analysis. Pain. 1999 Mar;80(1-2):83–93. doi: 10.1016/s0304-3959(98)00196-1. [DOI] [PubMed] [Google Scholar]
  28. Mouritsen H. Redstarts, Phoenicurus phoenicurus, can orient in a true-zero magnetic field. Anim Behav. 1998 May;55(5):1311–1324. doi: 10.1006/anbe.1997.0696. [DOI] [PubMed] [Google Scholar]
  29. Olcese J., Reuss S., Semm P. Geomagnetic field detection in rodents. Life Sci. 1988;42(6):605–613. doi: 10.1016/0024-3205(88)90451-1. [DOI] [PubMed] [Google Scholar]
  30. Ossenkopp K. P., Kavaliers M., Hirst M. Reduced nocturnal morphine analgesia in mice following a geomagnetic disturbance. Neurosci Lett. 1983 Oct 10;40(3):321–325. doi: 10.1016/0304-3940(83)90059-9. [DOI] [PubMed] [Google Scholar]
  31. Ossenkopp K. P., Kavaliers M. Morphine-induced analgesia and exposure to low-intensity 60-Hz magnetic fields: inhibition of nocturnal analgesia in mice is a function of magnetic field intensity. Brain Res. 1987 Aug 25;418(2):356–360. doi: 10.1016/0006-8993(87)90103-x. [DOI] [PubMed] [Google Scholar]
  32. Ossenkopp K. P., Kavaliers M., Prato F. S., Teskey G. C., Sestini E., Hirst M. Exposure to nuclear magnetic resonance imaging procedure attenuates morphine-induced analgesia in mice. Life Sci. 1985 Oct 21;37(16):1507–1514. doi: 10.1016/0024-3205(85)90182-1. [DOI] [PubMed] [Google Scholar]
  33. Papi F., Ghione S., Rosa C., Del Seppia C., Luschi P. Exposure to oscillating magnetic fields influences sensitivity to electrical stimuli. II. Experiments on humans. Bioelectromagnetics. 1995;16(5):295–300. doi: 10.1002/bem.2250160505. [DOI] [PubMed] [Google Scholar]
  34. Polk C. Effects of extremely-low-frequency magnetic fields on biological magnetite. Bioelectromagnetics. 1994;15(3):261–270. doi: 10.1002/bem.2250150308. [DOI] [PubMed] [Google Scholar]
  35. Prato F. S., Carson J. J., Ossenkopp K. P., Kavaliers M. Possible mechanisms by which extremely low frequency magnetic fields affect opioid function. FASEB J. 1995 Jun;9(9):807–814. doi: 10.1096/fasebj.9.9.7601344. [DOI] [PubMed] [Google Scholar]
  36. Prato F. S., Kavaliers M., Carson J. J. Behavioural evidence that magnetic field effects in the land snail, Cepaea nemoralis, might not depend on magnetite or induced electric currents. Bioelectromagnetics. 1996;17(2):123–130. doi: 10.1002/(SICI)1521-186X(1996)17:2<123::AID-BEM6>3.0.CO;2-5. [DOI] [PubMed] [Google Scholar]
  37. Prato F. S., Kavaliers M., Thomas A. W. Extremely low frequency magnetic fields can either increase or decrease analgaesia in the land snail depending on field and light conditions. Bioelectromagnetics. 2000 May;21(4):287–301. doi: 10.1002/(sici)1521-186x(200005)21:4<287::aid-bem5>3.0.co;2-n. [DOI] [PubMed] [Google Scholar]
  38. Sartucci F., Bonfiglio L., Del Seppia C., Luschi P., Ghione S., Murri L., Papi F. Changes in pain perception and pain-related somatosensory evoked potentials in humans produced by exposure to oscillating magnetic fields. Brain Res. 1997 Sep 26;769(2):362–366. doi: 10.1016/s0006-8993(97)00755-5. [DOI] [PubMed] [Google Scholar]
  39. Thomas A. W., Drost D. J., Prato F. S. Magnetic field exposure and behavioral monitoring system. Bioelectromagnetics. 2001 Sep;22(6):401–407. doi: 10.1002/bem.67. [DOI] [PubMed] [Google Scholar]
  40. Thomas A. W., Kavaliers M., Prato F. S., Ossenkopp K. P. 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. 1998;19(2):333–342. doi: 10.1016/s0196-9781(97)00380-x. [DOI] [PubMed] [Google Scholar]
  41. Thomas A. W., Kavaliers M., Prato F. S., Ossenkopp K. P. Antinociceptive effects of a pulsed magnetic field in the land snail, Cepaea nemoralis. Neurosci Lett. 1997 Jan 31;222(2):107–110. doi: 10.1016/s0304-3940(97)13359-6. [DOI] [PubMed] [Google Scholar]
  42. Thomas A. W., Kavaliers M., Prato F. S., Ossenkopp K. P. Pulsed magnetic field induced "analgesia" in the land snail, Cepaea nemoralis, and the effects of mu, delta, and kappa opioid receptor agonists/antagonists. Peptides. 1997;18(5):703–709. doi: 10.1016/s0196-9781(97)00004-1. [DOI] [PubMed] [Google Scholar]
  43. Tipping D. R., Chapman K. E., Birley A. J., Anderson M. Observations on the effects of low frequency electromagnetic fields on cellular transcription in Drosophila larvae reared in field-free conditions. Bioelectromagnetics. 1999;20(2):129–131. [PubMed] [Google Scholar]
  44. Vorobyov V. V., Sosunov E. A., Kukushkin N. I., Lednev V. V. Weak combined magnetic field affects basic and morphine-induced rat's EEG. Brain Res. 1998 Jan 19;781(1-2):182–187. doi: 10.1016/s0006-8993(97)01228-6. [DOI] [PubMed] [Google Scholar]
  45. Weaver J. C., Astumian R. D. The response of living cells to very weak electric fields: the thermal noise limit. Science. 1990 Jan 26;247(4941):459–462. doi: 10.1126/science.2300806. [DOI] [PubMed] [Google Scholar]
  46. Weiss J., Herrick R. C., Taber K. H., Contant C., Plishker G. A. Bio-effects of high magnetic fields: a study using a simple animal model. Magn Reson Imaging. 1992;10(4):689–694. doi: 10.1016/0730-725x(92)90021-q. [DOI] [PubMed] [Google Scholar]

Articles from Proceedings of the Royal Society B: Biological Sciences are provided here courtesy of The Royal Society

RESOURCES