How different priming stimulations affect the corticospinal excitability induced by noninvasive brain stimulation techniques: a systematic review and meta-analysis

References

Abbot, L.F. and Nelson, S.B. (2000). Synaptic plasticity: taming the beast. Nat. Neurosci. 3, 1178–1183.10.1038/81453Suche in Google Scholar

Abraham, W.C. and Bear, M.F. (1996). Metaplasticity: the plasticity of synaptic plasticity. Trends Neurosci. 19, 126–130.10.1016/S0166-2236(96)80018-XSuche in Google Scholar

Bastani, A. and Jaberzadeh, S. (2014). Within-session repeated a-tDCS: the effects of repetition rate and inter-stimulus interval on corticospinal excitability and motor performance. Clin. Neurophysiol. 125, 1809–1818.10.1016/j.clinph.2014.01.010Suche in Google Scholar PubMed

Bienenstock, E.L., Cooper, L.N., and Munro, P.W. (1982). Theory for the development of neuron selectivity: orientation specificity and binocular interaction in visual cortex. J. Neurosci. 2, 32–48.10.1142/9789812795885_0006Suche in Google Scholar

Cooper, L.N. and Bear, M.F. (2012). The BCM theory of synapse modification at 30: interaction of theory with experiment. Nat. Rev. Neurosci. 13, 798–810.10.1038/nrn3353Suche in Google Scholar PubMed

Cosentino, G., Fierro, B., Paladino, P., Talamanca, S., Vigneri, S., Palermo, A., Giglia, G., and Brighina, F. (2012). Transcranial direct current stimulation preconditioning modulates the effect of high-frequency repetitive transcranial magnetic stimulation in the human motor cortex. Eur. J. Neurosci. 35, 119–124.10.1111/j.1460-9568.2011.07939.xSuche in Google Scholar PubMed

Delvendahl, I., Jung, N.H., Mainberger, F., Kuhnke, N.G., Cronjaeger, M., and Mall, V. (2010). Occlusion of bidirectional plasticity by preceding low-frequency stimulation in the human motor cortex. Clin. Neurophysiol. 121, 594–602.10.1016/j.clinph.2009.09.034Suche in Google Scholar PubMed

Doeltgen, S.H. and Ridding, M.C. (2011). Modulation of cortical motor networks following primed theta burst transcranial magnetic stimulation. Exp. Brain Res. 215, 199–206.10.1007/s00221-011-2886-6Suche in Google Scholar PubMed

Downs, S.H. and Black, N. (1998). The feasibility of creating a checklist for the assessment of the methodological quality both of randomised and non-randomised studies of health care interventions. J. Epidemiol. Community Health 52, 377–384.10.1136/jech.52.6.377Suche in Google Scholar PubMed PubMed Central

Fricke, K., Seeber, A.A., Thirugnanasambandam, N., Paulus, W., Nitsche, M.A., and Rothwell, J.C. (2010). Time course of the induction of homeostatic plasticity generated by repeated transcranial direct current stimulation of the human motor cortex. J. Neurophysiol. 105, 1141–1149.10.1152/jn.00608.2009Suche in Google Scholar PubMed

Gamboa, O.L., Antal, A., Moliadze, V., and Paulus, W. (2010). Simply longer is not better: reversal of theta burst after-effect with prolonged stimulation. Exp. Brain Res. 204, 181–187.10.1007/s00221-010-2293-4Suche in Google Scholar PubMed PubMed Central

Gamboa, O.L., Antal, A., Laczo, B., Moliadze, V., Nitsche, M.A., and Paulus, W. (2011). Impact of repetitive theta burst stimulation on motor cortex excitability. Brain Stimul. 4, 145–151.10.1016/j.brs.2010.09.008Suche in Google Scholar PubMed

Gentner, R., Wankerl, K., Reinsberger, C., Zeller, D., and Classen, J. (2008). Depression of human corticospinal excitability induced by magnetic theta-burst stimulation: evidence of rapid polarity-reversing metaplasticity. Cereb. Cortex 18, 2046–2053.10.1093/cercor/bhm239Suche in Google Scholar PubMed

Goldsworthy, M.R., Pitcher, J.B., and Ridding, M.C. (2012). The application of spaced theta burst protocols induces long-lasting neuroplastic changes in the human motor cortex. Eur. J. Neurosci. 35, 125–134.10.1111/j.1460-9568.2011.07924.xSuche in Google Scholar PubMed

Goldsworthy, M.R., Pitcher, J.B., and Ridding, M.C. (2013). Neuroplastic modulation of inhibitory motor cortical networks by spaced theta burst stimulation protocols. Brain Stimul. 6, 340–345.10.1016/j.brs.2012.06.005Suche in Google Scholar PubMed

Goldsworthy, M.R., Muller-Dahlhaus, F., Ridding, M.C., and Ziemann, U. (2014). Inter-subject variability of LTD-like plasticity in human motor cortex: a matter of preceding motor activation. Brain Stimul. 7, 864–870.10.1016/j.brs.2014.08.004Suche in Google Scholar PubMed

Goldsworthy, M.R., Pitcher, J.B., and Ridding, M.C. (2015). Spaced noninvasive brain stimulation: prospects for inducing long-lasting human cortical plasticity. Neurorehabil. Neural Repair 29, 714–721.10.1177/1545968314562649Suche in Google Scholar PubMed

Hamada, M., Terao, Y., Hanajima, R., Shirota, Y., Nakatani-Enomoto, S., Furubayashi, T., Matsumoto, H., and Ugawa, Y. (2008). Bidirectional long-term motor cortical plasticity and metaplasticity induced by quadripulse transcranial magnetic stimulation. J. Physiol. 586, 3927–3947.10.1113/jphysiol.2008.152793Suche in Google Scholar PubMed PubMed Central

Hordacre, B., Ridding, M.C., and Goldsworthy, M.R. (2015). Response variability to non-invasive brain stimulation protocols. Clin. Neurophysiol. 126, 2249–2250.10.1016/j.clinph.2015.04.052Suche in Google Scholar PubMed

Huang, Y.Z., Edwards, M.J., Rounis, E., Bhatia, K.P., and Rothwell, J.C. (2005). Theta burst stimulation of the human motor cortex. Neuron 45, 201–206.10.1016/j.neuron.2004.12.033Suche in Google Scholar PubMed

Huang, Y.Z., Rothwell, J.C., Lu, C.S., Chuang, W.L., Lin, W.Y., and Chen, R.S. (2010). Reversal of plasticity-like effects in the human motor cortex. J. Physiol. 588, 3683–3693.10.1113/jphysiol.2010.191361Suche in Google Scholar PubMed PubMed Central

Iezzi, E., Suppa, A., Conte, A., Li Voti, P., Bologna, M., and Berardelli, A. (2011). Short-term and long-term plasticity interaction in human primary motor cortex. Eur. J. Neurosci. 33, 1908–1915.10.1111/j.1460-9568.2011.07674.xSuche in Google Scholar PubMed

Iyer, M., Schepler, N., and Wassermann, E. M. (2003). Priming stimulation enhances the depressant effect of low-frequency repetitive transcranial magnetic stimulation. J. Neurosci. 23, 10867–10872.10.1523/JNEUROSCI.23-34-10867.2003Suche in Google Scholar

Jaberzadeh, S., Bastani, A., and Kidgell, D. (2013). Does the longer application of anodal-transcranial direct current stimulation increase corticomotor excitability further? a pilot study. Basic Clin. Neurosci. 3, 28–35.Suche in Google Scholar

Joseph, A. Plot Digitizer 2.5.1 2011. Available at: http://plotdigitizer.sourceforge.net/.Suche in Google Scholar

Karabanov, A., Ziemann, U., Hamada, M., George, M.S., Quartarone, A., Classen, J., Massimin, M., Rothwell, J., and Siebner, H.R. (2015). Consensus paper: probing homeostatic plasticity of human cortex with non-invasive transcranial brain stimulation. Brain Stimul. 8, 442–454.10.1016/j.brs.2015.01.404Suche in Google Scholar PubMed

Lang, N., Siebner, H.R., Ernst, D., Nitsche, M.A., Paulus, W., Lemon, R.N., and Rothwell, J.C. (2004). Preconditioning with transcranial direct current stimulation sensitizes the motor cortex to rapid-rate transcranial magnetic stimulation and controls the direction of after-effects. Biol. Psychiatry 56, 634–639.10.1016/j.biopsych.2004.07.017Suche in Google Scholar PubMed

Mastroeni, C., Bergmann, T.O., Rizzo, V., Ritter, C., Klein, C., Pohlmann, I., Brueggemann, N., Quartarone, A., and Siebner, H. R. (2013). Brain-derived neurotrophic factor – a major player in stimulation-induced homeostatic metaplasticity of human motor cortex? PLoS One 8, e57957.10.1371/journal.pone.0057957Suche in Google Scholar PubMed PubMed Central

Moloney, T.M. and Witney, A.G. (2014). Pressure pain thresholds increase after preconditioning 1 Hz repetitive transcranial magnetic stimulation with transcranial direct current stimulation. PLoS One 9, e92540.10.1371/journal.pone.0092540Suche in Google Scholar PubMed PubMed Central

Monte-Silva, K., Kuo, M.F., Liebetanz, D., Paulus, W., and Nitsche, M.A. (2010). Shaping the optimal repetition interval for cathodal transcranial direct current stimulation (tDCS). J. Neurophysiol. 103, 1735–1740.10.1152/jn.00924.2009Suche in Google Scholar PubMed

Monte-Silva, K., Kuo, M.F., Hessenthaler, S., Fresnoza, S., Liebetanz, D., Paulus, W., and Nitsche, M.A. (2013). Induction of late LTP-like plasticity in the human motor cortex by repeated non-invasive brain stimulation. Brain Stimul. 6, 424–432.10.1016/j.brs.2012.04.011Suche in Google Scholar PubMed

Muller, J.F., Orekhov, Y., Liu, Y., and Ziemann, U. (2007). Homeostatic plasticity in human motor cortex demonstrated by two consecutive sessions of paired associative stimulation. Eur. J. Neurosci. 25, 3461–3468.10.1111/j.1460-9568.2007.05603.xSuche in Google Scholar PubMed

Müller-Dahlhaus, F. and Ziemann, U. (2015). Metaplasticity in human cortex. Neuroscientist 21, 185–202.10.1177/1073858414526645Suche in Google Scholar PubMed

Muller-Dahlhaus, F., Lucke, C., Lu, M. K., Arai, N., Fuhl, A., Herrmann, E., and Ziemann, U. (2015). Augmenting LTP-like plasticity in human motor cortex by spaced paired associative stimulation. PLoS One 10, e0131020.10.1371/journal.pone.0131020Suche in Google Scholar PubMed PubMed Central

Murakami, T., Muller-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, 5765–5781.10.1113/jphysiol.2012.238519Suche in Google Scholar PubMed PubMed Central

Ni, Z., Gunraj, C., Kailey, P., Cash, R.F., and Chen, R. (2014). Heterosynaptic modulation of motor cortical plasticity in human. J. Neurosci. 34, 7314–7321.10.1523/JNEUROSCI.4714-13.2014Suche in Google Scholar PubMed PubMed Central

Nitsche, M.A., Roth, A., Kuo, M.F., Fischer, A.K., Liebetanz, D., Lang, N., Tergau, F., and Paulus, W. (2007). Timing-dependent modulation of associative plasticity by general network excitability in the human motor cortex. J. Neurosci. 27, 3807–3812.10.1523/JNEUROSCI.5348-06.2007Suche in Google Scholar PubMed PubMed Central

Opie, G.M., Post, A.K., Ridding, M.C., Ziemann, U., and Semmler, J.G. (2017a). Modulating motor cortical neuroplasticity with priming paired associative stimulation in young and old adults. Clin. Neurophysiol. 128, 763–769.10.1016/j.clinph.2017.02.011Suche in Google Scholar PubMed

Opie, G.M., Vosnakis, E., Ridding, M.C., Ziemann, U., and Semmler, J.G. (2017b). Priming theta burst stimulation enhances motor cortex plasticity in young but not old adults. Brain Stimul. 10, 298–304.10.1016/j.brs.2017.01.003Suche in Google Scholar PubMed

Player, M.J., Taylor, J.L., Alonzo, A., and Loo, C.K. (2012). Paired associative stimulation increases motor cortex excitability more effectively than theta-burst stimulation. Clin. Neurophysiol. 123, 2220–2226.10.1016/j.clinph.2012.03.081Suche in Google Scholar PubMed

Potter-Nerger, M., Fischer, S., Mastroeni, C., Groppa, S., Deuschl, G., Volkmann, J., Quartarone, A., Munchau, A., and Siebner, H.R. (2009). Inducing homeostatic-like plasticity in human motor cortex through converging corticocortical inputs. J. Neurophysiol. 102, 3180–3190.10.1152/jn.91046.2008Suche in Google Scholar PubMed

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, 2291–2304.10.1113/jphysiol.2010.190314Suche in Google Scholar PubMed PubMed Central

Siebner, H.R., Lang, N., Rizzo, V., Nitsche, M.A., Paulus, W., Lemon, R.N., and Rothwell, J.C. (2004). Preconditioning of low-frequency repetitive transcranial magnetic stimulation with transcranial direct current stimulation: evidence for homeostatic plasticity in the human motor cortex. J. Neurosci. 24, 3379–3385.10.1523/JNEUROSCI.5316-03.2004Suche in Google Scholar PubMed PubMed Central

Stefan, K., Kunesch, E., Chen, L.G., Benecke, R., and Classen, J. (2000). Induction of plasticity in the human motor cortex by paired associative stimulation. Brain 123, 572–584.10.1093/brain/123.3.572Suche in Google Scholar PubMed

Todd, G., Flavel, S.C., and Ridding, M.C. (2009). Priming theta-burst repetitive transcranial magnetic stimulation with low- and high-frequency stimulation. Exp. Brain Res. 195, 307–315.10.1007/s00221-009-1791-8Suche in Google Scholar PubMed

Ziemann, U. and Siebner, H.R. (2008). Modifying motor learning through gating and homeostatic metaplasticity. Brain Stimul. 1, 60–66.10.1016/j.brs.2007.08.003Suche in Google Scholar PubMed