Journal of the Neurological Sciences
Volume 211, Issue 1 , Pages 5-14 , 15 July 2003

Effects of repetitive transcranial magnetic stimulation on behavioral and neurochemical changes in rats during an elevated plus-maze test

  • Manabu Kanno

      Affiliations

    • Corresponding Author InformationCorresponding author. Tel.: +81-11-706-6066; fax: +81-11-706-6067.
    • Department of Rehabilitation Medicine, Hokkaido University Graduate School of Medicine, Nishi 7, Kita 15, Kita-ku, Sapporo 060-8638, Japan
  • ,
  • Machiko Matsumoto

      Affiliations

    • Department of Pharmacology, Hokkaido University Graduate School of Medicine, Nishi 7, Kita 15, Kita-ku, Sapporo 060-8638, Japan
  • ,
  • Hiroko Togashi

      Affiliations

    • Department of Pharmacology, Hokkaido University Graduate School of Medicine, Nishi 7, Kita 15, Kita-ku, Sapporo 060-8638, Japan
  • ,
  • Mitsuhiro Yoshioka

      Affiliations

    • Department of Pharmacology, Hokkaido University Graduate School of Medicine, Nishi 7, Kita 15, Kita-ku, Sapporo 060-8638, Japan
  • ,
  • Yukio Mano

      Affiliations

    • Department of Rehabilitation Medicine, Hokkaido University Graduate School of Medicine, Nishi 7, Kita 15, Kita-ku, Sapporo 060-8638, Japan

Received 16 September 2002 ,Revised 23 December 2002 ,Accepted 20 January 2003.

References 

  1. Barker AT. An introduction to the basic principles of magnetic stimulation. J. Clin. Physiol. 1991;8:26–37
  2. Hallet M, Cohen LG. Magnetism: a new method for stimulation of nerve and brain. JAMA. 1989;262:538–541
  3. Mano Y, Nakamuro T, Tamura R, Takayanagi T, Kawanishi K, Tamai S, et al.  Central motor reorganization after anastomosis of the musculocutaneous and intercostal nerves following cervical root avulsion. Ann. Neurol. 1995;38:15–20
  4. Jennum P, Friberg L, Fuglsang-Frederiksen A, Dam M. Speech localization using repetitive transcranial magnetic stimulation. Neurology. 1994;44:269–273
  5. Post A, Keck ME. Transcranial magnetic stimulation as a therapeutic tool in psychiatry: what we know about the neurobiological mechanisms?. J. Psychiatr. Res. 2001;35:193–215
  6. Wassermann EM, Lisanby SH. Therapeutic application of repetitive transcranial magnetic stimulation: a review. Clin. Neurophysiol. 2001;112:1367–1377
  7. Mally J, Stone TW. Improvement in Parkinsonian symptoms after repetitive transcranial magnetic stimulation. J. Neurol. Sci. 1999;162:179–184
  8. Siebner HR, Rossmeier C, Mentschel C, Peinemann A, Conrad B. Short-term motor improvement after sub-threshold 5-Hz repetitive transcranial magnetic stimulation of primary motor hand area in Parkinson's disease. J. Neurol. Sci. 2000;178:91–94
  9. Padberg F, Zwanzger P, Keck ME, Kathmann N, Mikhaiel P, Ella R, et al.  Repetitive transcranial magnetic stimulation (rTMS) in Major Depression: relation between efficacy and stimulation intensity. Neuropsychopharmacology. 2002;27:638–645
  10. George MS, Wassermann EM, Williams WA, Steppel J, Pascual-Leone A, Basser P, et al.  Changes in mood and hormone levels after rapid-rate transcranial magnetic stimulation (rTMS) of the prefrontal cortex. J. Neuropsychiatry Clin. Neurosci. 1996;8:172–180
  11. Pascual-Leone A, Catala MD, Pascual-Leone Pascual A. Lateralized effect of rapid-rate transcranial magnetic stimulation of the prefrontal cortex on mood. Neurology. 1996;46:499–502
  12. Schutter DJLD, van Hong J, d'Alfonso AAL, Postma A, de Haan EHF. Effects of slow rTMS at the right dorsolateral prefrontal cortex on EEG asymmetry and mood. NeuroReport. 2001;12:445–447
  13. Yoshioka M, Matsumoto M, Togashi H, Saito H. Effects of conditioned fear stress on 5-HT release in the rat prefrontal cortex. Pharmacol. Biochem. Behav. 1995;51:515–519
  14. Pellow S, Chopin P, File SE, Briley M. Validation of open: closed arm entries in an elevated plus-maze as a measure of anxiety in the rat. J. Neurosci. Methods. 1985;14:149–167
  15. Wall PM, Messier C. Methodological and conceptual issues in the use of the elevated plus-maze as a psychological measurement instrument of animal anxiety behavior. Neurosci. Biobehav. Rev. 1999;23:905–913
  16. Rex A, Marsden CA. Effect of diazepam on cortical 5-HT release and behaviour in the guinea-pig on exposure to the elevated plus-maze. Psychopharmacology. 1993;110:490–496
  17. Wright IK, Upton N, Marsden CA. Effect of established and putative anxiolytics on extracellular 5-HT and 5-HIAA in the ventral hippocampus of rats during behaviour on the elevated X-maze. Psychopharmacology. 1992;109:338–346
  18. Dunn RW, Corbett R, Fielding S. Effects of 5-HT1A receptor agonists and NMDA receptor antagonists in the social interaction test and elevated plus-maze. Eur. J. Pharmacol. 1989;169:1–10
  19. Sharp T, McQuade R, Bramwell S, Hjorth S. Effect of acute and repeated adminstration of 5-HT1A receptor agonists on 5-HT release in rat in vivo. Naunyn-Schmiedeberg's Arch. Pharmacol. 1993;348:339–346
  20. Keck ME, Engelmann M, Müller MB, Henniger MSH, Hermann B, Ruppercht R, et al.  Repetitive transcranial magnetic stimulation induces active coping strategies attenuates the neuroendcrine stress response in rats. J. Psychiatr. Res. 2000;34:265–276
  21. Keck ME, Welt T, Post A, Müller MB, Toschi N, Wigger A, et al.  Neuroendcrine and behavioral effects of repetitive transcranial magnetic stimulation in a psychopathological animal model are suggestive of antidepressant-like effects. Neuropsychopharmacology. 2001;24:337–349
  22. Ben-Shachar D, Belmaker RH, Grisau N, Klein E. Transcranial magnetic stimulation induces alterations in brain monoamines. J. Neural. Transm. 1997;104:191–197
  23. Ben-Shachar D, Gazawi H, Riboyad-Levin J, Klein E. Chronic repetitive transcranial magnetic stimulation alters β-adrenergic and 5-HT2 receptor characteristics in rat brain. Brain Res. 1999;816:78–83
  24. Kole HP, Fuchs E, Ziemann U, Paulus W, Ebert U. Changes in 5-HT1A and NMDA binding sites by a single rapid transcranial magnetic stimulation procedure in rats. Brain Res. 1999;826:309–312
  25. Gur E, Lerer B, Dremencov E, Newman ME. Chronic repetitive transcranial magnetic stimulation induces subsensitivity of presynaptic serotonergic autoreceptor activity in rat brain. NeuroReport. 2000;11:2925–2929
  26. Keck ME, Sillaber I, Ebner K, Welt T, Kaehler ST, Singewald N, et al.  Acute transcranial magnetic stimulation of frontal brain regions selectivity modulates the release of vasopressin, biogenic amines and amino acids in the rat brain. Eur. J. Neurosci. 2000;12:3713–3720
  27. Keck ME, Welt T, Müller MB, Erhardt A, Ohl F, Toschi N, et al.  Repetitive transcranial magnetic stimulation increases the release of dopamine in the mesolimbic and mesostriatal system. Neuropharmacology. 2002;43:101–109
  28. Belmaker RH, Grisaru N. Magnetic stimulation of the brain in animal depression models responsive to ECS. J. ECT. 1998;14:194–205
  29. Weissman JD, Epstein CM, Davey KR. Magnetic brain stimulation and brain size: relevance to animal studies. Electroencephalogr. Clin. Neurophysiol. 1992;85:215–219
  30. Fleischmann A, Prolov K, Abarbanel J, Belmaker RH. The effect of transcranial magnetic stimulation of rat brain on behavioral models of depression. Brain Res. 1995;699:130–132
  31. Maccabee PJ, Eberle L, Amassian VE, Cracco A, Rudell A, Jayachandra M. Spatial distribution of the electric field induced in volume by round and figure ‘8’ magnetic coil: relevance to activation of sensory nerve fibers. Electroencephalogr. Clin. Neurophysiol. 1990;76:131–141
  32. Abercrombee ED, Keefe KA, DiFrischia DS, Zigmond MJ. Differential effect of stress on in vivo dopamine release in striatum, nucleus accumbens, and medial frontal cortex. J. Neurochem. 1989;52:1655–1658
  33. Feenstra MGP, Botterblom MHA. Rapid sampling of extracellular dopamine in the rat prefrontal cortex during food consumption, handling exposure to novelty. Brain Res. 1996;742:17–24
  34. Sakai K, Ugawa Y, Terao Y, Hanajima R, Furubayashi T, Kanazawa I. Preferential activation of different I waves by transcranial magnetic stimulation with a figure-of-eight-shaped coil. Exp. Brain Res. 1997;113:24–32
  35. Paxinos G, Watson C. The rat brain in stereotaxic coodinates. Sydney: Academic Press; 1986;
  36. Luft AR, Kaelin-Lang A, Hauser T-K, Cohen LG, Thakor NV, Hanley DF. Transcranial magnetic stimulation in the rat. Exp. Brain Res. 2001;140:112–121
  37. Yoshioka M, Matsumoto M, Togashi H, Saito H. Effect of conditioned fear stress on dopamine release in the rat prefrontal cortex. Neurosci. Lett. 1996;209:203–210
  38. Matsumoto M, Yoshioka M, Togashi H, Mori K, Ueno K-I, Saito H. Effects of idazoxan on dopamine release in the prefrontal cortex of freely moving rats. Eur. J. Pharmacol. 1998;343:165–170
  39. Matsumoto M, Yoshioka M, Togashi H, Ikeda T, Saito H. Functional regulation by dopamine receptors of serotonin release from the rat hippocampus: in vivo microdialysis study. Naunyn-Schmiedeberg's Arch. Pharmacol. 1996;353:621–629
  40. Ueno K-I, Togashi H, Mori K, Matsumoto M, Ohashi S, Hoshino A, et al.  Behavioural and pharmacological relevance of stroke-prone spontaneously hypertensive rats as an animal model of a developmental disorder. Behav. Pharmacol. 2002;13:1–13
  41. Wassermann EM. Risk and safety of repetitive transcranial magnetic stimulation: report and suggested guidelines from the International Workshop on the Safety of Repetitive Transcranial Magnetic Stimulation, June 5–7, 1996. Electroencephalogr. Clin. Neurophysiol. 1998;108:1–16
  42. Mazzocchio R, Rothwell JC, Day BL, Thompson PD. Effect of tonic voluntary activity on excitability of human motor cortex. J. Physiol. (Lond.). 1994;474261–474267
  43. Massot O, Grimaldi B, Baily J-M, Kochanek M, Deschamps F, Lambrozo J, et al.  Magnetic field desensitizes 5-HT1B receptor in brain: pharmacological and functional sites. Brain Res. 2000;858:143–150
  44. George MS, Nahas Z, Molloy M, Speer AM, Oliver NC, Li XB, et al.  A controlled trial of daily left prefrontal cortex TMS for treating depression. Biol. Psychiatry. 2000;48:962–970
  45. Strafella AP, Paus T, Barrett J, Dagher A. Repetitive transcranial magnetic stimulation of the human prefrontal cortex induces dopamine release in the caudate nucleus. J. Neurosci. 2001;21: [RC157 (1–4)]
  46. Ji R-R, Sclaepfer TE, Aizenman CD, Epstein CM, Qiu D, Huang JC, et al.  Repetitive transcranial magnetic stimulation activates specific regions in rat brain. Proc. Natl. Acad. Sci. U. S. A. 1998;95:15635–15640

PII: S0022-510X(03)00030-3

doi: 10.1016/S0022-510X(03)00030-3

Journal of the Neurological Sciences
Volume 211, Issue 1 , Pages 5-14 , 15 July 2003