Unraveling the cellular and molecular mechanisms of repetitive magnetic stimulation

Frontiers in Molecular Neuroscience

Volumn 6, Issue DEC, 2013, Pages

  Müller Dahlhaus, Florian ^a   Vlachos, Andreas ^b  

^a UNIVERSITY OF TÜBINGEN   (Germany)

^b GOETHE UNIVERSITY   (Germany)

Author keywords

Hebbian plasticity; Metaplasticity; Neurological diseases; Neuropsychiatric disorders; Non invasive brain stimulation; Structural plasticity

Indexed keywords

ARTICLE; BRAIN ELECTROPHYSIOLOGY; CLINICAL PRACTICE; COGNITION; DEPOLARIZATION; ELECTROMAGNETIC FIELD; ELECTROPORATION; ELECTROSTIMULATION; HIPPOCAMPUS; HUMAN; LONG TERM DEPRESSION; NERVE CELL NETWORK; NERVE CELL PLASTICITY; NERVE EXCITABILITY; NONHUMAN; SYNAPSE; TRANSCRANIAL MAGNETIC STIMULATION;

EID: 84890808400     PISSN: 16625099     EISSN: None     Source Type: Journal    
DOI: 10.3389/fnmol.2013.00050     Document Type: Article

References (73)

1. Akerboom, J., Carreras Calderón, N., Tian, L., Wabnig, S., Prigge, M., Tolö, J., et al. (2013). Genetically encoded calcium indicators for multi-color neural activity imaging and combination with optogenetics. Front. Mol. Neurosci. 6:2. doi: 10.3389/fnmol.2013.00002
2. Barker, A. T., Jalinous, R., and Freeston, I. L. (1985). Non-invasive magnetic stimulation of human motor cortex. Lancet 1, 1106-1107. doi: 10.1016/S01406736(85)92413-4
3. Basser, P. J. (1994). Focal magnetic stimulation of an axon. IEEE Trans. Biomed. Eng. 41, 601-606. doi: 10.1109/10.293248
4. Basser, P. J., and Roth, B. J. (1991). Stimulation of a myelinated nerve axon by electromagnetic induction. Med. Biol. Eng. Comput. 29, 261-268. doi: 10.1007/BF02446708
5. Benali, A., Trippe, J., Weiler, E., Mix, A., Petrasch-Parwez, E., Girzalsky, W., et al. (2011). Theta-burst transcranial magnetic stimulation alters cortical inhibition. J. Neurosci. 31, 1193-1203. doi: 10.1523/JNEUROSCI.1379-10.2011
6. Berglund, K., Kuner, T., Feng, G., and Augustine, G. J. (2011). Imaging synaptic inhibition with the genetically encoded chloride indicator Clomeleon. Cold Spring Harb. Protoc. 2011, 1492-1497. doi: 10.1101/pdb.prot066985
7. Bhargava, Y., Hampden-Smith, K., Chachlaki, K., Wood, K. C., Vernon, J., Allerston, C. K., et al. (2013). Improved genetically-encoded, FlincG-type fluorescent biosensors for neural cGMP imaging. Front. Mol. Neurosci. 6:26. doi: 10.3389/fnmol.2013.00026
8. Bliss, T. V., and Lomo, T. (1973). Long-lasting potentiation of synaptic transmission in the dentate area of the anaesthetized rabbit following stimulation of the perforant path. J. Physiol. 232, 331-356.
9. Bosch, M., and Hayashi, Y. (2012). Structural plasticity of dendritic spines. Curr. Opin. Neurobiol. 22, 383-388. doi: 10.1016/j.conb.2011.09.002
10. Bregestovski, P., Waseem, T., and Mukhtarov, M. (2009). Genetically encoded optical sensors for monitoring of intracellular chloride and chloride-selective channel activity. Front. Mol. Neurosci. 2:15. doi: 10.3389/neuro.02.015.2009
11. Chen, T. W., Wardill, T. J., Sun, Y., Pulver, S. R., Renninger, S. L., Baohan, A., et al. (2013). Ultrasensitive fluorescent proteins for imaging neuronal activity. Nature 499, 295-300. doi: 10.1038/nature12354
12. Choquet, D., and Triller, A. (2013). The dynamic synapse. Neuron 80, 691-703. doi: 10.1016/j.neuron.2013.10.013
13. Chipchase, L., Schabrun, S., Cohen, L., Hodges, P., Ridding, M., Rothwell, J., et al. (2012). A checklist for assessing the methodological quality of studies using transcranial magnetic stimulation to study the motor system: an international consensus study. Clin. Neurophysiol. 123, 1698-1704. doi: 10.1016/j.clinph.2012.05.003
14. Colgan, L. A., and Yasuda, R. (2013). Plasticity of dendritic spines: subcompartmentalization of signaling. Annu. Rev. Physiol. 76, 16.2-16.21. doi: 10.1146/annurev-physiol-021113-170400
15. Davis, G. W. (2013). Homeostatic signaling and the stabilization of neural function. Neuron 80, 718-728. doi: 10.1016/j.neuron.2013.09.044
16. de Andrade, D. C., Mhalla, A., Adam, F., Texeira, M. J., and Bouhassira, D. (2011). Neuropharmacological basis of rTMS-induced analgesia: the role of endogenous opioids. Pain 152, 320-326. doi: 10.1016/j.pain.2010.10.032
17. Deisseroth, K., and Schnitzer, M. J. (2013). Engineering approaches to illuminating brain structure and dynamics. Neuron 80, 568-577. doi: 10.1016/j.neuron.2013.10.032
18. Edgley, S. A., Eyre, J. A., Lemon, R. N., and Miller, S. (1997). Comparison of activation of corticospinal neurons and spinal motor neurons by magnetic and electrical transcranial stimulation in the lumbosacral cord of the anaesthetized monkey. Brain 120, 839-853. doi: 10.1093/brain/120.5.839
19. Edwards, M. J., Talelli, P., and Rothwell, J. C. (2008). Clinical applications of transcranial magnetic stimulation in patients with movement disorders. Lancet Neurol. 7, 827-840. doi: 10.1016/S1474-4422(08)70190-X
20. Feldman, D. E. (2012). The spike-timing dependence of plasticity. Neuron 75, 556-571. doi: 10.1016/j.neuron.2012.08.001
21. Fifková, E., and Anderson, C. L. (1981). Stimulation-induced changes in dimensions of stalks of dendritic spines in the dentate molecular layer. Exp. Neurol. 74, 621-627. doi: 10.1016/0014-4886(81)90197-7
22. Fifková, E., and Van Harreveld, A. (1977). Long-lasting morphological changes in dendritic spines of dentate granular cells following stimulation of the entorhinal area. J. Neurocytol. 6, 211-230. doi: 10.1007/BF01261506
23. Fonoff, E. T., Dale, C. S., Pagano, R. L., Paccola, C. C., Ballester, G., Teixeira, M. J., et al. (2009). Antinociception induced by epidural motor cortex stimulation in naive conscious rats is mediated by the opioid system. Behav. Brain Res. 196, 63-70. doi: 10.1016/j.bbr.2008.07.027
24. Funke, K., and Benali, A. (2011). Modulation of cortical inhibition by rTMS-findings obtained from animal models. J. Physiol. 589, 4423-4434. doi: 10.1113/jphysiol.2011.206573
25. Galvani, A. (1791). De viribus electricitatis in motu musculari commentaris. Bononien Sci. Art Instit. Acad. Comm. 7, 363-418.
26. George, M. S., Taylor, J. J., and Short, E. B. (2013). The expanding evidence base for rTMS treatment of depression. Curr. Opin. Psychiatry 26, 13-18. doi: 10.1097/YCO.0b013e32835ab46d
27. Gersner, R., Kravetz, E., Feil, J., Pell, G., and Zangen, A. (2011). Long-term effects of repetitive transcranial magnetic stimulation on markers for neuroplasticity: differential outcomes in anesthetized and awake animals. J. Neurosci. 31, 7521-7526. doi: 10.1523/JNEUROSCI.6751-10.2011
28. Gray, E. G. (1959). Axo-somatic and axo-dendritic synapses of the cerebral cortex: an electron microscope study. J. Anat. 93, 420-433.
29. Grewe, B. F., Langer, D., Kasper, H., Kampa, B. M., and Helmchen, F. (2010). High-speed in vivo calcium imaging reveals neuronal network activity with nearmillisecond precision. Nat. Methods 7, 399-405. doi: 10.1038/nmeth.1453
30. Grienberger, C., and Konnerth, A. (2012). Imaging calcium in neurons. Neuron 73, 862-885. doi: 10.1016/j.neuron.2012.02.011
31. Grinvald, A., and Hildesheim, R. (2004). VSDI: a new era in functional imaging of cortical dynamics. Nat. Rev. Neurosci. 5, 874-885. doi: 10.1038/nrn1536
32. Hallett, M. (2007). Transcranial magnetic stimulation: a primer. Neuron 55, 187-199. doi: 10.1016/j.neuron.2007.06.026
33. Hamada, M., Murase, N., Hasan, A., Balaratnam, M., and Rothwell, J. C. (2013). The role of interneuron networks in driving human motor cortical plasticity. Cereb. Cortex 23, 1593-1605. doi: 10.1093/cercor/bhs147
34. Hamada, M., Terao, Y., Hanajima, R., Shirota, Y., Nakatani-Enomoto, S., Furubayashi, T., et al. (2008). Bidirectional long-term motor cortical plasticity and metaplasticity induced by quadripulse transcranial magnetic stimulation. J. Physiol. 586, 3927-3947. doi: 10.1113/jphysiol.2008.152793
35. Hebb, D. O. (1949). The Organization of Behavior: a Neuropsychological Theory. New York: Wiley.
36. Hoogendam, J. M., Ramakers, G. M., and Di Lazzarro, V. (2010). Physiology of repetitive transcranial magnetic stimulation of the human brain. Brain Stimul. 3, 95-118. doi: 10.1016/j.brs.2009.10.005
37. Holtmaat, A., Bonhoeffer, T., Chow, D. K., Chuckowree, J., De Paola, V., Hofer, S. B., et al. (2009). Long-term, high-resolution imaging in the mouse neocortex through a chronic cranial window. Nat. Protoc. 4, 1128-1144. doi: 10.1038/nprot.2009.89
38. Hulme, S. R., Jones, O. D., and Abraham, W. C. (2013). Emerging roles of metaplasticity in behaviour and disease. Trends Neurosci. 36, 353-362. doi: 10.1016/j.tins.2013.03.007
39. Levkovitz, Y., Marx, J., Grisaru, N., and Segal, M. (1999). Long-term effects of transcranial magnetic stimulation on hippocampal reactivity to afferent stimulation. J. Neurosci. 19, 3198-3203.
40. Maarrawi, J., Peyron, R., Mertens, P., Costes, N., Magnin, M., Sindou, M., et al. (2007). Motor cortex stimulation for pain control induces changes in the endogenous opioid system. Neurology 69, 827-834. doi: 10.1212/01.wnl.0000269783.86997.37
41. Malenka, R. C., and Bear, M. F. (2004). LTP and LTD: an embarrassment of riches. Neuron 44, 5-21. doi: 10.1016/j.neuron.2004.09.012
42. Marshel, J. H., and Deisseroth, K. (2013). Genetically encoded voltage sensor goes live. Nat. Biotechnol. 31, 994-995. doi: 10.1038/nbt.2738
43. Meyer, J. F., Wolf, B., and Gross, G. W. (2009). Magnetic stimulation and depression of mammalian networks in primary neuronal cell cultures. IEEE Trans. Biomed. Eng. 56, 1512-1523. doi: 10.1109/TBME.2009.2013961
44. Mix, A., Benali, A., and Funke, K. (2013). Strain differences in the effect of rTMS on cortical expression of calcium-binding proteins in rats. Exp. Brain Res. doi: 10.1007/s00221-013-3751-3756 [Epub ahead of print].
45. Müller-Dahlhaus, J. F., Orekhov, Y., Liu, Y., and Ziemann, U. (2008). Interindividual variability and age-dependency of motor cortical plasticity induced by paired associative stimulation. Exp. Brain Res. 187, 467-475. doi: 10.1007/s00221-008-1319-7
46. Murakami, T., Müller-Dahlhaus, F., Lu, M. K., and Ziemann, U. (2012). Homeostatic metaplasticity of corticospinal excitatory and intracortical inhibitory neural circuits in human motor cortex. J. Physiol. 590, 5765-5781. doi: 10.1113/jphysiol.2012.238519
47. Nitsche, M. A., Müller-Dahlhaus, F., Paulus, W., and Ziemann, U. (2012). The pharmacology of neuroplasticity induced by non-invasive brain stimulation: building models for the clinical use of CNS active drugs. J. Physiol. 590, 4641-4662. doi: 10.1113/jphysiol.2012.232975
48. Opitz, A., Windhoff, M., Heidemann, R. M., Turner, R., and Thielscher, A. (2011). How the brain tissue shapes the electric field induced by transcranial magnetic stimulation. Neuroimage 58, 849-859. doi: 10.1016/j.neuroimage.2011.06.069
49. Packer, A. M., Roska, B., and Hausser, M. (2013). Targeting neurons and photons for optogenetics. Nat. Neurosci. 16, 805-815. doi: 10.1038/nn.3427
50. Perron, A., Mutoh, H., Akemann, W., Gautam, S. G., Dimitrov, D., Iwamoto, Y., et al. (2009). Second and third generation voltage-sensitive fluorescent proteins for monitoring membrane potential. Front. Mol. Neurosci. 2:5. doi: 10.3389/neuro.02.005.2009
51. Raimondo, J. V., Irkle, A., Wefelmeyer, W., Newey, S. E., and Akerman, C. J. (2012). Genetically encoded proton sensors reveal activity-dependent pH changes in neurons. Front. Mol. Neurosci. 5:68. doi: 10.3389/fnmol.2012.00068
52. Redondo, R. L., and Morris, R. G. (2011). Making memories last: the synaptic tagging and capture hypothesis. Nat. Rev. Neurosci. 12, 17-30. doi: 10.1038/nrn2963
53. Ridding, M. C., and Ziemann, U. (2010). Determinants of the induction of cortical plasticity by non-invasive brain stimulation in healthy subjects. J. Physiol. 588, 2291-2304. doi: 10.1113/jphysiol.2010.190314
54. Rotem, A., and Moses, E. (2008). Magnetic stimulation of one-dimensional neuronal cultures. Biophys. J. 94, 5065-5078. doi: 10.1529/biophysj.107.125708
55. Scanziani, M., and Hausser, M. (2009). Electrophysiology in the age of light. Nature 461, 930-939. doi: 10.1038/nature08540
56. Smedemark-Margulies, N., and Trapani, J. G. (2013). Tools, methods, and applications for optophysiology in neuroscience. Front. Mol. Neurosci. 6:18. doi: 10.3389/fnmol.2013.00018
57. Spacek, J. (1985). Three-dimensional analysis of dendritic spines. II. Spine apparatus and other cytoplasmic components. Anat. Embryol. (Berl.) 171, 235-243. doi: 10.1007/BF00341418
58. Stuart, G. J., and Sakmann, B. (1994). Active propagation of somatic action potentials into neocortical pyramidal cell dendrites. Nature 367, 69-72. doi: 10.1038/367069a0
59. Tecchio, F., Zappasodi, F., Pasqualetti, P., De Gennaro, L., Pellicciari, M. C., Ercolani, M., et al. (2008). Age dependence of primary motor cortex plasticity induced by paired associative stimulation. Clin. Neurophysiol. 119, 675-682. doi: 10.1016/j.clinph.2007.10.023
60. Tokay, T., Holl, N., Kirschstein, T., Zschorlich, V., and Kohling, R. (2009). High-frequency magnetic stimulation induces long-term potentiation in rat hippocampal slices. Neurosci. Lett. 461, 150-154. doi: 10.1016/j.neulet.2009.06.032
61. Tonnesen, J., and Nagerl, U. V. (2013). Superresolution imaging for neuroscience. Exp. Neurol. 242, 33-40. doi: 10.1016/j.expneurol.2012.10.004
62. Turrigiano, G. (2012). Homeostatic synaptic plasticity: local and global mechanisms for stabilizing neuronal function. Cold Spring Harb. Perspect. Biol. 4, a005736. doi: 10.1101/cshperspect.a005736
63. Tye, K. M., and Deisseroth, K. (2012). Optogenetic investigation of neural circuits underlying brain disease in animal models. Nat. Rev. Neurosci. 13, 251-266. doi: 10.1038/nrn3171
64. Van Harreveld, A., and Fifková, E. (1975). Swelling of dendritic spines in the fascia dentata after stimulation of the perforant fibers as a mechanism of posttetanic potentiation. Exp. Neurol. 49, 736-749. doi: 10.1016/0014-4886(75) 90055-2
65. Vitureira, N., Letellier, M., and Goda, Y. (2012). Homeostatic synaptic plasticity: from single synapses to neural circuits. Curr. Opin. Neurobiol. 22, 516-521. doi: 10.1016/j.conb.2011.09.006
66. Vlachos, A., Maller-Dahlhaus, F., Rosskopp, J., Lenz, M., Ziemann, U., and Deller, T. (2012). Repetitive magnetic stimulation induces functional and structural plasticity of excitatory postsynapses in mouse organotypic hippocampal slice cultures. J. Neurosci. 32, 17514-17523. doi: 10.1523/JNEUROSCI.040912.2012
67. Vlachos, A., Helias, M., Becker, D., Diesmann, M., and Deller, T. (2013). NMDAreceptor inhibition increases spine stability of denervated mouse dentate granule cells and accelerates spine density recovery following entorhinal denervation in vitro. Neurobiol. Dis. 59, 267-276. doi: 10.1016/j.nbd.2013.07.018
68. Wang, H. Y., Crupi, D., Liu, J., Stucky, A., Cruciata, G., Di Rocco, A., et al. (2011). Repetitive transcranial magnetic stimulation enhances BDNF-TrkB signaling in both brain and lymphocyte. J. Neurosci. 31, 11044-11054. doi: 10.1523/JNEUROSCI.2125-11.2011
69. Wankerl, K., Weise, D., Gentner, R., Rumpf, J. J., and Classen, J. (2010). L-type voltage-gated Ca2+ channels: a single molecular switch for long-term potentiation/long-term depression-like plasticity and activity-dependent metaplasticity in humans. J. Neurosci. 30, 6197-6204. doi: 10.1523/JNEUROSCI.4673-09.2010
70. Ziemann, U. (2005). Improving disability in stroke with RTMS. Lancet Neurol. 4, 454-455. doi: 10.1016/S1474-4422(05)70126-5
71. Ziemann, U. (2011). Transcranial magnetic stimulation at the interface with other techniques: a powerful tool for studying the human cortex. Neuroscientist 17, 368-381. doi: 10.1177/1073858410390225
72. Ziemann, U., Paulus, W., Nitsche, M. A., Pascual-Leone, A., Byblow, W. D., Berardelli, A., et al. (2008). Consensus: motor cortex plasticity protocols. Brain Stimul. 1, 164-182. doi: 10.1016/j.brs.2008.06.006
73. Ziemann, U., and Siebner, H. R. (2008). Modifying motor learning through gating and homeostatic metaplasticity. Brain Stimul. 1, 60-66. doi: 10.1016/j.brs.2007.08.003