Repetitive transcranial magnetic stimulation effectively facilitates spatial cognition and synaptic plasticity associated with increasing the levels of BDNF and synaptic proteins in Wistar rats

Neurobiology of Learning and Memory

Volumn 134, Issue , 2016, Pages 369-378

  Shang, Yingchun ^a   Wang, Xin ^b   Shang, Xueliang ^a   Zhang, Hui ^a   Liu, Zhipeng ^b   Yin, Tao ^b   Zhang, Tao ^a  

^a NANKAI UNIVERSITY   (China)

^b INSTITUTE OF BIOMEDICAL ENGINEERING   (China)

Author keywords

Brain derived neurotrophic factor (BDNF); Rats; Repetitive transcranial magnetic stimulation (rTMS); Spatial cognition; Synapse associated proteins; Synaptic plasticity

Indexed keywords

BRAIN DERIVED NEUROTROPHIC FACTOR; N METHYL DEXTRO ASPARTIC ACID RECEPTOR 2B; SYNAPTOPHYSIN; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; NR2B NMDA RECEPTOR; SYP PROTEIN, RAT;

ADULT; ANIMAL EXPERIMENT; ARTICLE; CONTROLLED STUDY; DEPOTENTIATION; EXECUTIVE FUNCTION; FACILITATION; HIPPOCAMPAL CA1 REGION; IN VIVO STUDY; LONG TERM POTENTIATION; MALE; MORRIS WATER MAZE TEST; NERVE CELL PLASTICITY; NEUROPHYSIOLOGY; NONHUMAN; PRESYNAPTIC POTENTIAL; PROTEIN DETERMINATION; PROTEIN EXPRESSION; RAT; REPETITIVE TRANSCRANIAL MAGNETIC STIMULATION; SPATIAL LEARNING; SPATIAL MEMORY; SYNAPTIC TRANSMISSION; TRANSCRANIAL MAGNETIC STIMULATION; UPREGULATION; WESTERN BLOTTING; ANIMAL; ANIMAL BEHAVIOR; HIPPOCAMPUS; METABOLISM; PHYSIOLOGY; PROCEDURES; WISTAR RAT;

ANIMALS; BEHAVIOR, ANIMAL; BRAIN-DERIVED NEUROTROPHIC FACTOR; HIPPOCAMPUS; MALE; NEURONAL PLASTICITY; RATS; RATS, WISTAR; RECEPTORS, N-METHYL-D-ASPARTATE; SPATIAL LEARNING; SPATIAL MEMORY; SYNAPTOPHYSIN; TRANSCRANIAL MAGNETIC STIMULATION;

EID: 84991244435     PISSN: 10747427     EISSN: 10959564     Source Type: Journal    
DOI: 10.1016/j.nlm.2016.08.016     Document Type: Article

References (75)

1. Ahmed, M.A., Darwish, E.S., Khedr, E.M., El Serogy, Y.M., Ali, A.M., Effects of low versus high frequencies of repetitive transcranial magnetic stimulation on cognitive function and cortical excitability in Alzheimer's dementia. Journal of Neurology 259 (2012), 83–92.
2. Ahmed, Z., Wieraszko, A., The mechanism of magnetic field-induced increase of excitability in hippocampal neurons. Brain Research 1221 (2008), 30–40.
3. An, L., Fu, J., Zhang, T., Reversible effects of vitamins C and E combination on cognitive deficits and oxidative stress in the hippocampus of melamine-exposed rats. Pharmacology, Biochemistry and Behavior 132 (2015), 152–159.
4. An, L., Yang, Z., Zhang, T., Imbalanced synaptic plasticity induced spatial cognition impairment in male offspring rats treated with chronic prenatal ethanol exposure. Alcoholism, Clinical and Experimental Research 37 (2013), 763–770.
5. Aydin-Abidin, S., Trippe, J., Funke, K., Eysel, U.T., Benali, A., High- and low-frequency repetitive transcranial magnetic stimulation differentially activates c-Fos and zif268 protein expression in the rat brain. Experimental Brain Research 188 (2008), 249–261.
6. Barker, A.T., Jalinous, R., Freeston, I.L., Non-invasive magnetic stimulation of human motor cortex. Lancet 1 (1985), 1106–1107.
7. Bliss, T.V., Collingridge, G.L., A synaptic model of memory: Long-term potentiation in the hippocampus. Nature 361 (1993), 31–39.
8. Castillo-Padilla, D.V., Funke, K., Effects of chronic iTBS-rTMS and enriched environment on visual cortex early critical period and visual pattern discrimination in dark-reared rats. Developmental Neurobiology 76 (2016), 19–33.
9. Cheeran, B., Talelli, P., Mori, F., Koch, G., Suppa, A., Edwards, M., Rothwell, J.C., A common polymorphism in the brain-derived neurotrophic factor gene (BDNF) modulates human cortical plasticity and the response to rTMS. Journal of Physiology 586 (2008), 5717–5725.
10. Erickson, M.A., Maramara, L.A., Lisman, J., A single brief burst induces GluR1-dependent associative short-term potentiation: A potential mechanism for short-term memory. Journal of Cognitive Neuroscience 22 (2010), 2530–2540.
11. Fu, J., Wang, H., Gao, J., Yu, M., Wang, R., Yang, Z., Zhang, T., Rapamycin effectively impedes melamine-induced impairments of cognition and synaptic plasticity in Wistar rats. Molecular Neurobiology, 2016, 10.1007/s12035-016-9687-7.
12. Gao, J., Zhang, X., Yu, M., Ren, G., Yang, Z., Cognitive deficits induced by multi-walled carbon nanotubes via the autophagic pathway. Toxicology 337 (2015), 21–29.
13. Garcia-Toro, M., Salva, J., Daumal, J., Andres, J., Romera, M., Lafau, O., Aguirre, I., High (20-Hz) and low (1-Hz) frequency transcranial magnetic stimulation as adjuvant treatment in medication-resistant depression. Psychiatry Research-Neuroimaging 146 (2006), 53–57.
14. Gersner, R., Kravetz, E., Feil, J., Pell, G., Zangen, A., Long-term effects of repetitive transcranial magnetic stimulation on markers for neuroplasticity: Differential outcomes in anesthetized and awake animals. Journal of Neuroscience 31 (2011), 7521–7526.
15. Gilio, F., Conte, A., Vanacore, N., Frasca, V., Inghilleri, M., Berardelli, A., Excitatory and inhibitory after-effects after repetitive magnetic transcranial stimulation (rTMS) in normal subjects. Experimental Brain Research 176 (2007), 588–593.
16. Hebb, D., The organization of behaviour. 1949, Wiley, New York.
17. Holscher, C., Synaptic plasticity and learning and memory: LTP and beyond. Journal of Neuroscience Research 58 (1999), 62–75.
18. Houdayer, E., Degardin, A., Cassim, F., Bocquillon, P., Derambure, P., Devanne, H., The effects of low- and high-frequency repetitive TMS on the input/output properties of the human corticospinal pathway. Experimental Brain Research 187 (2008), 207–217.
19. Huang, E.J., Reichardt, L.F., Neurotrophins: Roles in neuronal development and function. Annual Review of Neuroscience 24 (2001), 677–736.
20. Kemp, A., Manahan-Vaughan, D., Hippocampal long-term depression: Master or minion in declarative memory processes?. Trends in Neurosciences 30 (2007), 111–118.
21. Kulla, A., Reymann, K.G., Manahan-Vaughan, D., Time-dependent induction of depotentiation in the dentate gyrus of freely moving rats: Involvement of group 2 metabotropic glutamate receptors. European Journal of Neuroscience 11 (1999), 3864–3872.
22. Lauri, S.E., Palmer, M., Segerstrale, M., Vesikansa, A., Taira, T., Collingridge, G.L., Presynaptic mechanisms involved in the expression of STP and LTP at CA1 synapses in the hippocampus. Neuropharmacology 52 (2007), 1–11.
23. Li, W., Keifer, J., Rapid enrichment of presynaptic protein in boutons undergoing classical conditioning is mediated by brain-derived neurotrophic factor. Neuroscience 203 (2012), 50–58.
24. Li, W., Yang, Y., Ye, Q., Yang, B., Wang, Z., Effect of chronic and acute low-frequency repetitive transcranial magnetic stimulation on spatial memory in rats. Brain Research Bulletin 71 (2007), 493–500.
25. Li, Z.G., Hao, S., Yin, H.Q., Gao, J., Yang, Z., Autophagy ameliorates cognitive impairment through activation of PVT1 and apoptosis in diabetes mice. Behavioural Brain Research 305 (2016), 265–277.
26. Liu, L., Wong, T.P., Pozza, M.F., Lingenhoehl, K., Wang, Y., Sheng, M., Wang, Y.T., Role of NMDA receptor subtypes in governing the direction of hippocampal synaptic plasticity. Science 304 (2004), 1021–1024.
27. Loffler, S., Gasca, F., Richter, L., Leipscher, U., Trillenberg, P., Moser, A., The effect of repetitive transcranial magnetic stimulation on monoamine outflow in the nucleus accumbens shell in freely moving rats. Neuropharmacology 63 (2012), 898–904.
28. Lynch, M.A., Long-term potentiation and memory. Physiological Reviews 84 (2004), 87–136.
29. Ma, J., Zhang, Z.C., Kang, L., Geng, D.D., Wang, Y.Y., Wang, M.W., Cui, H.X., Repetitive transcranial magnetic stimulation (rTMS) influences spatial cognition and modulates hippocampal structural synaptic plasticity in aging mice. Experimental Gerontology 58 (2014), 256–268.
30. Ma, J., Zhang, Z.C., Su, Y.H., Kang, L., Geng, D.D., Wang, Y.Y., Cui, H.X., Magnetic stimulation modulates structural synaptic plasticity and regulates BDNF-TrkB signal pathway in cultured hippocampal neurons. Neurochemistry International 62 (2013), 84–91.
31. Makowiecki, K., Harvey, A.R., Sherrard, R.M., Rodger, J., Low-intensity repetitive transcranial magnetic stimulation improves abnormal visual cortical circuit topography and upregulates BDNF in mice. Journal of Neuroscience 34 (2014), 10780–10792.
32. Maruki, K., Izaki, Y., Nomura, M., Yamauchi, T., Differences in paired-pulse facilitation and long-term potentiation between dorsal and ventral CA1 regions in anesthetized rats. Hippocampus 11 (2001), 655–661.
33. Miranda, P.C., Hallett, M., Basser, P.J., The electric field induced in the brain by magnetic stimulation: A 3-D finite-element analysis of the effect of tissue heterogeneity and anisotropy. IEEE Transactions on Biomedical Engineering 50 (2003), 1074–1085.
34. Mix, A., Benali, A., Eysel, U.T., Funke, K., Continuous and intermittent transcranial magnetic theta burst stimulation modify tactile learning performance and cortical protein expression in the rat differently. European Journal of Neuroscience 32 (2010), 1575–1586.
35. Moser, M.B., Moser, E.I., Forrest, E., Andersen, P., Morris, R.G., Spatial learning with a minislab in the dorsal hippocampus. Proceedings of the National academy of Sciences of the United States of America 92 (1995), 9697–9701.
36. Mueller, M.B., Toschi, N., Kresse, A.E., Post, A., Keck, M.E., Long-term rTMS increases the expression of BDNF and CCK mRNA, but not NPY mRNA in specific areas of rat brain. Society for Neuroscience Abstracts, 26, 2000 Abstract No.-871.814.
37. Mulkey, R.M., Malenka, R.C., Mechanisms underlying induction of homosynaptic long-term depression in area CA1 of the hippocampus. Neuron 9 (1992), 967–975.
38. Muller, P.A., Dhamne, S.C., Vahabzadeh-Hagh, A.M., Pascual-Leone, A., Jensen, F.E., Rotenberg, A., Suppression of motor cortical excitability in anesthetized rats by low frequency repetitive transcranial magnetic stimulation. PLoS ONE, 9, 2014, e91065.
39. Neves, G., Cooke, S.F., Bliss, T.V., Synaptic plasticity, memory and the hippocampus: A neural network approach to causality. Nature Reviews Neuroscience 9 (2008), 65–75.
40. Ogiue-Ikeda, M., Kawato, S., Ueno, S., The effect of repetitive transcranial magnetic stimulation on long-term potentiation in rat hippocampus depends on stimulus intensity. Brain Research 993 (2003), 222–226.
41. Parthoens, J., Verhaeghe, J., Wyckhuys, T., Stroobants, S., Staelens, S., Small-animal repetitive transcranial magnetic stimulation combined with [F-18]-Fdg microPET to quantify the neuromodulation effect in the rat brain. Neuroscience 275 (2014), 436–443.
42. Paxinos, G., Watson, C., The rat brain in stereotaxic coordinates. 2005, Elsevier Academic Press, Burlington, MA.
43. Platz, T., Rothwell, J.C., Brain stimulation and brain repair – rTMS: From animal experiment to clinical trials – What do we know?. Restorative Neurology and Neuroscience 28 (2010), 387–398.
44. Podda, M.V., Cocco, S., Mastrodonato, A., Fusco, S., Leone, L., Barbati, S.A., Grassi, C., Anodal transcranial direct current stimulation boosts synaptic plasticity and memory in mice via epigenetic regulation of Bdnf expression. Scientific Reports, 6, 2016, 22180.
45. Pozzo-Miller, L.D., Gottschalk, W., Zhang, L., McDermott, K., Du, J., Gopalakrishnan, R., Lu, B., Impairments in high-frequency transmission, synaptic vesicle docking, and synaptic protein distribution in the hippocampus of BDNF knockout mice. Journal of Neuroscience 19 (1999), 4972–4983.
46. Qi, Y., Hu, N.W., Rowan, M.J., Switching off LTP: mGlu and NMDA receptor-dependent novelty exploration-induced depotentiation in the rat hippocampus. Cerebral Cortex 23 (2013), 932–939.
47. Ramat-Gun, The use of the morris water maze in the study of memory and learning. Journal of Neuroscience 48 (1989), 29–69.
48. Richter-Levin, G., Canevari, L., Bliss, T.V., Long-term potentiation and glutamate release in the dentate gyrus: Links to spatial learning. Behavioural Brain Research 66 (1995), 37–40.
49. Rossi, S., Hallett, M., Rossini, P.M., Pascual-Leone, A., Safety of, T. M. S. C. G. Safety, ethical considerations, and application guidelines for the use of transcranial magnetic stimulation in clinical practice and research. Clinical Neurophysiology 361 (2009), 31–39.
50. Schulz, P.E., Cook, E.P., Johnston, D., Using paired-pulse facilitation to probe the mechanisms for long-term potentiation (LTP). Journal of Physiology, Paris 89 (1995), 3–9.
51. Tan, T., Xie, J., Liu, T., Chen, X., Zheng, X., Tong, Z., Tian, X., Low-frequency (1 Hz) repetitive transcranial magnetic stimulation (rTMS) reverses Abeta(1–42)-mediated memory deficits in rats. Experimental Gerontology 48 (2013), 786–794.
52. Tang, A.D., Makowiecki, K., Bartlett, C., Rodger, J., Low intensity repetitive transcranial magnetic stimulation does not induce cell survival or regeneration in a mouse optic nerve crush model. PLoS ONE, 10, 2015, e0126949.
53. Tang, Y., Zucker, R.S., Mitochondrial involvement in post-tetanic potentiation of synaptic transmission. Neuron 18 (1997), 483–491.
54. Tokay, T., Holl, N., Kirschstein, T., Zschorlich, V., Kohling, R., High-frequency magnetic stimulation induces long-term potentiation in rat hippocampal slices. Neuroscience Letters 461 (2009), 150–154.
55. Trippe, J., Mix, A., Aydin-Abidin, S., Funke, K., Benali, A., Theta burst and conventional low-frequency rTMS differentially affect GABAergic neurotransmission in the rat cortex. Experimental Brain Research 199 (2009), 411–421.
56. Tsien, J.Z., Huerta, P.T., Tonegawa, S., The essential role of hippocampal CA1 NMDA receptor-dependent synaptic plasticity in spatial memory. Cell 87 (1996), 1327–1338.
57. Vaynman, S.S., Ying, Z., Yin, D., Gomez-Pinilla, F., Exercise differentially regulates synaptic proteins associated to the function of BDNF. Brain Research 1070 (2006), 124–130.
58. Vlachos, A., Muller-Dahlhaus, F., Rosskopp, J., Lenz, M., Ziemann, U., Deller, T., Repetitive magnetic stimulation induces functional and structural plasticity of excitatory postsynapses in mouse organotypic hippocampal slice cultures. Journal of Neuroscience 32 (2012), 17514–17523.
59. Vorhees, C.V., Williams, M.T., Morris water maze: Procedures for assessing spatial and related forms of learning and memory. Nature Protocols 1 (2006), 848–858.
60. Wang, F., Chang, G.M., Yu, Q., Geng, X., The neuroprotection of repetitive transcranial magnetic stimulation pre-treatment in vascular dementia rats. Journal of Molecular Neuroscience 56 (2015), 198–204.
61. Wang, F., Geng, X., Tao, H.Y., Cheng, Y., The restoration after repetitive transcranial magnetic stimulation treatment on cognitive ability of vascular dementia rats and its impacts on synaptic plasticity in hippocampal CA1 area. Journal of Molecular Neuroscience 41 (2010), 145–155.
62. Wang, H.-Y., Crupi, D., Liu, J., Stucky, A., Cruciata, G., Di Rocco, A., Ghilardi, M.F., Repetitive transcranial magnetic stimulation enhances BDNF-TrkB signaling in both brain and lymphocyte. Journal of Neuroscience 31 (2011), 11044–11054.
63. Wang, J.X., Rogers, L.M., Gross, E.Z., Ryals, A.J., Dokucu, M.E., Brandstatt, K.L., Voss, J.L., Targeted enhancement of cortical-hippocampal brain networks and associative memory. Science 345 (2014), 1054–1057.
64. Waterhouse, E.G., Xu, B.J., New insights into the role of brain-derived neurotrophic factor in synaptic plasticity. Molecular and Cellular Neuroscience 42 (2009), 81–89.
65. Wiedenmann, B., Franke, W.W., Identification and localization of synaptophysin, an integral membrane glycoprotein of Mr 38,000 characteristic of presynaptic vesicles. Cell 41 (1985), 1017–1028.
66. Wolwer, W., Lowe, A., Brinkmeyer, J., Streit, M., Habakuck, M., Agelink, M.W., Cordes, J., Repetitive transcranial magnetic stimulation (rTMS) improves facial affect recognition in schizophrenia. Brain Stimulation 7 (2014), 559–563.
67. Wong, T.P., Liu, L.D., Sheng, M., Wang, Y.T., Response to comment on “Role of NMDA receptor subtypes in governing the direction of hippocampal synaptic plasticity”. Science, 305, 2004 1912C-+.
68. Wu, L.G., Saggau, P., Presynaptic calcium is increased during normal synaptic transmission and paired-pulse facilitation, but not in long-term potentiation in area CA1 of hippocampus. Journal of Neuroscience 14 (1994), 645–654.
69. Xu, X., Li, Z., Yang, Z., Zhang, T., Decrease of synaptic plasticity associated with alteration of information flow in a rat model of vascular dementia. Neuroscience 206 (2012), 136–143.
70. Xu, X., Liu, C., Li, Z., Zhang, T., Effects of hydrogen sulfide on modulation of theta-gamma coupling in hippocampus in vascular dementia rats. Brain Topography 28 (2015), 879–894.
71. Yang, H.Y., Liu, Y., Xie, J.C., Liu, N.N., Tian, X., Effects of repetitive transcranial magnetic stimulation on synaptic plasticity and apoptosis in vascular dementia rats. Behavioural Brain Research 281 (2015), 149–155.
72. Yu, M., Zhang, Y., Chen, X.Y., Zhang, T., Antidepressant-like effects and possible mechanisms of amantadine on cognitive and synaptic deficits in a rat model of chronic stress. Stress – The International Journal on the Biology of Stress 19 (2016), 104–113.
73. Zhang, N., Xing, M., Wang, Y., Tao, H., Cheng, Y., Repetitive transcranial magnetic stimulation enhances spatial learning and synaptic plasticity via the VEGF and BDNF-NMDAR pathways in a rat model of vascular dementia. Neuroscience 311 (2015), 284–291.
74. Zheng, C., Zhang, T., Synaptic plasticity-related neural oscillations on hippocampus-prefrontal cortex pathway in depression. Neuroscience 292 (2015), 170–180.
75. Zucker, R.S., Regehr, W.G., Short-term synaptic plasticity. Annual Review of Physiology 64 (2002), 355–405.