Advanced search
Publication Cover
International Review of Psychiatry Volume 29, 2017 - Issue 2: Brain Stimulation
Submit an article Journal homepage
432
Views
8
CrossRef citations to date
0
Altmetric
Review Articles

Can neurophysiologic measures serve as biomarkers for the efficacy of repetitive transcranial magnetic stimulation treatment of major depressive disorder?

Brian KobayashiDavid Geffen School of Medicine, University of California Los Angeles, Los Angeles, CA, USA; ;Department of Psychiatry and Biobehavioral Sciences, David Geffen School of Medicine, University of California Los Angeles, Los Angeles, CA, USA; ;Neuromodulation Division, Semel Institute for Neuroscience and Human Behavior, University of California Los Angeles, Los Angeles, CA, USA;
,
Ian A. CookDavid Geffen School of Medicine, University of California Los Angeles, Los Angeles, CA, USA; ;Department of Psychiatry and Biobehavioral Sciences, David Geffen School of Medicine, University of California Los Angeles, Los Angeles, CA, USA; ;Neuromodulation Division, Semel Institute for Neuroscience and Human Behavior, University of California Los Angeles, Los Angeles, CA, USA; ;Department of Bioengineering, University of California Los Angeles, Los Angeles, CA, USA
,
Aimee M. HunterDavid Geffen School of Medicine, University of California Los Angeles, Los Angeles, CA, USA; ;Department of Psychiatry and Biobehavioral Sciences, David Geffen School of Medicine, University of California Los Angeles, Los Angeles, CA, USA; ;Neuromodulation Division, Semel Institute for Neuroscience and Human Behavior, University of California Los Angeles, Los Angeles, CA, USA;
,
Michael J. MinzenbergDavid Geffen School of Medicine, University of California Los Angeles, Los Angeles, CA, USA; ;Department of Psychiatry and Biobehavioral Sciences, David Geffen School of Medicine, University of California Los Angeles, Los Angeles, CA, USA; ;Neuromodulation Division, Semel Institute for Neuroscience and Human Behavior, University of California Los Angeles, Los Angeles, CA, USA;
,
David E. KrantzDavid Geffen School of Medicine, University of California Los Angeles, Los Angeles, CA, USA; ;Department of Psychiatry and Biobehavioral Sciences, David Geffen School of Medicine, University of California Los Angeles, Los Angeles, CA, USA; ;Neuromodulation Division, Semel Institute for Neuroscience and Human Behavior, University of California Los Angeles, Los Angeles, CA, USA;
&
Andrew F. LeuchterDavid Geffen School of Medicine, University of California Los Angeles, Los Angeles, CA, USA; ;Department of Psychiatry and Biobehavioral Sciences, David Geffen School of Medicine, University of California Los Angeles, Los Angeles, CA, USA; ;Neuromodulation Division, Semel Institute for Neuroscience and Human Behavior, University of California Los Angeles, Los Angeles, CA, USA; Correspondence[email protected]
Pages 98-114 | Received 11 Nov 2016, Accepted 16 Feb 2017, Published online: 31 Mar 2017

References

  • Albensi, B.C., Alasti, N., & Mueller, A.L. (2000). Long-term potentiation in the presence of NMDA receptor antagonist arylalkylamine spider toxins. Journal of Neuroscience Research, 62, 177–185. doi:10.1002/1097-4547(20001015)62:2 < 177::AID-JNR3 > 3.0.CO;2-D
  • Arai, N., Okabe, S., Furubayashi, T., Mochizuki, H., Iwata, N.K., Hanajima, R., … Ugawa, Y. (2007). Differences in after-effect between monophasic and biphasic high-frequency rTMS of the human motor cortex. Clinical Neurophysiology, 118, 2227–2233. doi:10.1016/j.clinph.2007.07.006
  • Arns, M., Cerquera, A., Gutiérrez, R.M., Hasselman, F., & Freund, J.A. (2014). Non-linear EEG analyses predict non-response to rTMS treatment in major depressive disorder. Clinical Neurophysiology, 125, 1392–1399. doi:10.1016/j.clinph.2013.11.022
  • Arns, M., Drinkenburg, W.H., Fitzgerald, P.B., & Kenemans, J.L. (2012). Neurophysiological predictors of non-response to rTMS in depression. Brain Stimulation, 5, 569–576. doi:10.1016/j.brs.2011.12.003
  • Aydin-Abidin, S., Moliadze, V., Eysel, U.T., & Funke, K. (2006). Effects of repetitive TMS on visually evoked potentials and EEG in the anaesthetized cat: Dependence on stimulus frequency and train duration. The Journal of Physiology, 574, 443–455. doi:10.1113/jphysiol.2006.108464
  • Bares, M., Brunovsky, M., Kopecek, M., Novak, T., Stopkova, P., Kozeny, J., & Höschl, C. (2008). Early reduction in prefrontal theta QEEG cordance value predicts response to venlafaxine treatment in patients with resistant depressive disorder. European Psychiatry, 23, 350–355. doi:10.1016/j.eurpsy.2008.03.001
  • Bares, M., Brunovsky, M., Kopecek, M., Stopkova, P., Novak, T., Kozeny, J., & Höschl, C. (2007). Changes in QEEG prefrontal cordance as a predictor of response to antidepressants in patients with treatment resistant depressive disorder: A pilot study. Journal of Psychiatric Research, 41, 319–325. doi:10.1016/j.jpsychires.2006.06.005
  • Bares, M., Brunovsky, M., Novak, T., Kopecek, M., Stopkova, P., Sos, P., & Höschl, C. (2015). QEEG theta cordance in the prediction of treatment outcome to prefrontal repetitive transcranial magnetic stimulation or venlafaxine ER in patients with major depressive disorder. Clinical EEG and Neuroscience, 46, 73–80. doi:10.1177/1550059413520442
  • Bares, M., Brunovsky, M., Novak, T., Kopecek, M., Stopkova, P., Sos, P., …Höschl, C. (2010). The change of prefrontal QEEG theta cordance as a predictor of response to bupropion treatment in patients who had failed to respond to previous antidepressant treatments. European Neuropsychopharmacology, 20, 459–466. doi:10.1016/j.euroneuro.2010.03.007
  • Bares, M., Novak, T., Kopecek, M., Brunovsky, M., Stopkova, P., & Höschl, C. (2015). The effectiveness of prefrontal theta cordance and early reduction of depressive symptoms in the prediction of antidepressant treatment outcome in patients with resistant depression: analysis of naturalistic data. European Archives of Psychiatry and Clinical Neuroscience, 265, 73–82. doi:10.1007/s00406-014-0506-8
  • Baskaran, A., Milev, R., & McIntyre, R.S. (2012). The neurobiology of the EEG biomarker as a predictor of treatment response in depression. Neuropharmacology, 63, 507–513. doi:10.1016/j.neuropharm.2012.04.021
  • Batsikadze, G., Paulus, W., Kuo, M., & Nitsche, M. (2013). Effect of serotonin on paired associative stimulation-induced plasticity in the human motor cortex. Neuropsychopharmacology, 38, 2260–2267. doi:10.1038/npp.2013.127
  • Berger, B., Minarik, T., Liuzzi, G., Hummel, F.C., & Sauseng, P. (2014). EEG oscillatory phase-dependent markers of corticospinal excitability in the resting brain. BioMed Research International, 2014, 936096. doi:10.1155/2014/936096
  • Bilek, E., Schäfer, A., Ochs, E., Esslinger, C., Zangl, M., Plichta, M.M., … Tost, H. (2013). Application of high-frequency repetitive transcranial magnetic stimulation to the DLPFC alters human prefrontal-hippocampal functional interaction. The Journal of Neuroscience: The Official Journal of the Society for Neuroscience, 33, 7050–7056. doi:10.1523/JNEUROSCI.3081-12.2013
  • Blumberger, D.M., Mulsant, B.H., Fitzgerald, P.B., Rajji, T.K., Ravindran, A.V., Young, L.T., …Daskalakis, Z.J. (2012). A randomized double-blind sham-controlled comparison of unilateral and bilateral repetitive transcranial magnetic stimulation for treatment-resistant major depression. The World Journal of Biological Psychiatry, 13, 423–435. doi:10.3109/15622975.2011.579163
  • Brunelin, J., Poulet, E., Boeuve, C., Zeroug-vial, H., d'Amato, T., & Saoud, M. (2007). Efficacy of repetitive transcranial magnetic stimulation (rTMS) in major depression: A review. Encephale, 33, 126–134. doi: ENC-4-2007-33-2-0013-7006-101019-200730012
  • Canali, P., Sferrazza Papa, G., Casali, A.G., Schiena, G., Fecchio, M., Pigorini, A., & Benedetti, F. (2014). Changes of cortical excitability as markers of antidepressant response in bipolar depression: Preliminary data obtained by combining transcranial magnetic stimulation (TMS) and electroencephalography (EEG). Bipolar Disorders, 16, 809–819. doi:10.1111/bdi.12249
  • Cárdenas-Morales, L., Nowak, D.A., Kammer, T., Wolf, R.C., & Schönfeldt-Lecuona, C. (2010). Mechanisms and applications of theta-burst rTMS on the human motor cortex. Brain Topography, 22, 294–306. doi:10.1007/s10548-009-0084-7
  • Carpenter, L.L., Janicak, P.G., Aaronson, S.T., Boyadjis, T., Brock, D.G., Cook, I.A., & Demitrack, M.A. (2012). Transcranial magnetic stimulation (TMS) for major depression: A multisite, naturalistic, observational study of acute treatment outcomes in clinical practice. Depression and Anxiety, 29, 587–596. doi:10.1002/da.21969
  • Casarotto, S., Romero Lauro, L.J., Bellina, V., Casali, A.G., Rosanova, M., Pigorini, A., & Massimini, M. (2010). EEG responses to TMS are sensitive to changes in the perturbation parameters and repeatable over time. PLoS One, 5, e10281. doi:10.1371/journal.pone.0010281
  • Casarotto, S., Canali, P., Rosanova, M., Pigorini, A., Fecchio, M., Mariotti, M., … Massimini, M. (2013). Assessing the effects of electroconvulsive therapy on cortical excitability by means of transcranial magnetic stimulation and electroencephalography. Brain Topography, 26, 326–337. doi:10.1007/s10548-012-0256-8
  • Casula, E.P., Tarantino, V., Basso, D., Arcara, G., Marino, G., Toffolo, G.M., … Bisiacchi, P.S. (2014). Low-frequency rTMS inhibitory effects in the primary motor cortex: Insights from TMS-evoked potentials. NeuroImage, 98, 225–232. doi:10.1016/j.neuroimage.2014.04.065
  • Chang, W.H., Kim, Y.H., Bang, O.Y., Kim, S.T., Park, Y.H., & Lee, P.K.W. (2010). Long-term effects of rTMS on motor recovery in patients after subacute stroke. Journal of Rehabilitation Medicine, 42, 758–764. doi:10.2340/16501977-0590
  • Chervyakov, A.V., Chernyavsky, A.Y., Sinitsyn, D.O., & Piradov, M.A. (2015). Possible mechanisms underlying the therapeutic effects of transcranial magnetic stimulation. Frontiers in Human Neuroscience, 9, 303. doi:10.3389/fnhum.2015.00303
  • Chung, S.W., Rogasch, N.C., Hoy, K.E., & Fitzgerald, P.B. (2015). Measuring brain stimulation induced changes in cortical properties using TMS-EEG. Brain Stimulation, 8, 1010–1020. doi:10.1016/j.brs.2015.07.029
  • Ciampi de Andrade, D., Mhalla, A., Adam, F., Texeira, M.J., & Bouhassira, D. (2014). Repetitive transcranial magnetic stimulation induced analgesia depends on N-methyl-D-aspartate glutamate receptors. Pain, 155, 598–605. doi:10.1016/j.pain.2013.12.022
  • Connolly, K.R., Helmer, A., Cristancho, M.A., Cristancho, P., & O'reardon, J.P. (2012). Effectiveness of transcranial magnetic stimulation in clinical practice post-FDA approval in the United States: Results observed with the first 100 consecutive cases of depression at an academic medical center. The Journal of Clinical Psychiatry, 73, e567–e573. doi:10.4088/JCP.11m07413
  • Cook, I.A., Hunter, A.M., Abrams, M., Siegman, B., & Leuchter, A.F. (2009). Midline and right frontal brain function as a physiologic biomarker of remission in major depression. Psychiatry Research, 174, 152–157. doi:10.1016/j.pscychresns.2009.04.011
  • Cook, I.A., Hunter, A.M., Korb, A.S., & Leuchter, A.F. (2014). Do prefrontal midline electrodes provide unique neurophysiologic information in Major Depressive Disorder? Journal of Psychiatric Research, 53, 69–75. doi:10.1016/j.jpsychires.2014.01.018
  • Cook, I.A., Leuchter, A.F., Morgan, M., Witte, E., Stubbeman, W.F., Abrams, M., & Uijtdehaage, S.H. (2002). Early changes in prefrontal activity characterize clinical responders to antidepressants. Neuropsychopharmacoly, 27, 120–131. doi:10.1016/S0893-133X(02)00294-4
  • Cosentino, G., Fierro, B., Vigneri, S., Talamanca, S., Paladino, P., Baschi, R., & Brighina, F. (2014). Cyclical changes of cortical excitability and metaplasticity in migraine: Evidence from a repetitive transcranial magnetic stimulation study. Pain, 155, 1070–1078. doi:10.1016/j.pain.2014.02.024
  • Daskalakis, Z.J., Farzan, F., Barr, M.S., Maller, J.J., Chen, R., & Fitzgerald, P.B. (2008). Long-interval cortical inhibition from the dorsolateral prefrontal cortex: A TMS-EEG study. Neuropsychopharmacology: Official Publication of the American College of Neuropsychopharmacology, 33, 2860–2869. doi:10.1038/npp.2008.22
  • de Geus, E.J. (2010). From genotype to EEG endophenotype: A route for postgenomic understanding of complex psychiatric disease? Genome Medicine, 2, 63. doi:10.1186/gm184 http://dx.doi.org/10.1186/gm184
  • Dell’Osso, B., Oldani, L., Camuri, G., Dobrea, C., Cremaschi, L., Benatti, B., & Altamura, A.C. (2015). Augmentative repetitive Transcranial Magnetic Stimulation (rTMS) in the acute treatment of poor responder depressed patients: A comparison study between high and low frequency stimulation. European Psychiatry: The Journal of the Association of European Psychiatrists, 30, 271–276. doi:10.1016/j.eurpsy.2014.12.001
  • Demitrack, M.A., & Thase, M.E. (2009). Clinical significance of transcranial magnetic stimulation (TMS) in the treatment of pharmacoresistant depression: Synthesis of recent data. Psychoparmacology Bulletin, 42, 5–38.
  • Di Lazzaro, V., Dileone, M., Pilato, F., Capone, F., Musumeci, G., Ranieri, F., … Profice, P. (2011). Modulation of motor cortex neuronal networks by rTMS: Comparison of local and remote effects of six different protocols of stimulation. Journal of Neurophysiology, 105, 2150–2156. doi:10.1152/jn.00781.2010
  • Di Lazzaro, V., Oliviero, A., Profice, P., Pennisi, M.A., Pilato, F., Zito, G., … Tonali, P.A. (2003). Ketamine increases human motor cortex excitability to transcranial magnetic stimulation. The Journal of Physiology, 547, 485–496. doi:10.1113/jphysiol.2002.030486
  • Di Lazzaro, V., Pilato, F., Dileone, M., Profice, P., Oliviero, A., Mazzone, P., & Rothwell, J.C. (2008). Low-frequency repetitive transcranial magnetic stimulation suppresses specific excitatory circuits in the human motor cortex. The Journal of Physiology, 586, 4481–4487. doi:10.1113/jphysiol.2008.159558
  • Downar, J., & Daskalakis, Z.J. (2013). New targets for rTMS in depression: A review of convergent evidence. Brain Stimulation, 6, 231–240. doi:10.1016/j.brs.2012.08.006
  • Du, X., Choa, F.S., Summerfelt, A., Rowland, L.M., Chiappelli, J., Kochunov, P., & Hong, L.E. (2016). N100 as a generic cortical electrophysiological marker based on decomposition of TMS-evoked potentials across five anatomic locations. Experimental Brain Research, 235, 69–81. doi:10.1007/s00221-016-4773-7
  • Dunner, D.L., Aaronson, S.T., Sackeim, H.A., Janicak, P.G., Carpenter, L.L., Boyadjis, T., …Demitrack, M.A. (2014). A multisite, naturalistic, observational study of transcranial magnetic stimulation for patients with pharmacoresistant major depressive disorder: Durability of benefit over a 1-year follow-up period. The Journal of Clinical Psychiatry, 75, 1394–1401. doi:10.4088/JCP.13m08977
  • Enomoto, H., Kadowaki, S., Abe, M., Nakamura, K., Kobayashi, S., Murakami, T., & Ugawa, Y. (2015). The inter-individual variability of quadripulse stimulation (QPS). Brain Stimulation, 8, 336–337. doi:10.1016/j.brs.2015.01.089
  • Esser, S.K., Huber, R., Massimini, M., Peterson, M.J., Ferrarelli, F., & Tononi, G. (2006). A direct demonstration of cortical LTP in humans: A combined TMS/EEG study. Brain Research Bulletin, 69, 86–94. doi:10.1016/j.brainresbull.2005.11.003
  • Fischer, M., & Orth, M. (2011). Short-latency sensory afferent inhibition: Conditioning stimulus intensity, recording site, and effects of 1 Hz repetitive TMS. Brain Stimulation, 4, 202–209. doi:10.1016/j.brs.2010.10.005
  • Fitzgerald, P.B., Daskalakis, Z.J., Hoy, K., Farzan, F., Upton, D.J., Cooper, N.R., & Maller, J.J. (2008). Cortical inhibition in motor and non-motor regions: A combined TMS-EEG study. Clinical EEG and Neuroscience, 39, 112–117. doi:10.1177/155005940803900304
  • Fitzgerald, P.B., Fountain, S., & Daskalakis, Z.J. (2006). A comprehensive review of the effects of rTMS on motor cortical excitability and inhibition. Clinical Neurophysiology: Official Journal of the International Federation of Clinical Neurophysiology, 117, 2584–2596. doi:10.1016/j.clinph.2006.06.712
  • Fond, G., Loundou, A., Rabu, C., Macgregor, A., Lançon, C., Brittner, M., … Boyer, L. (2014). Ketamine administration in depressive disorders: A systematic review and meta-analysis. Psychopharmacology, 231, 3663–3676. doi:10.1007/s00213-014-3664-5
  • Fröhlich, F. (2015). Experiments and models of cortical oscillations as a target for noninvasive brain stimulation. Progress in Brain Research, 222, 41–73. doi:10.1016/bs.pbr.2015.07.025
  • Fresnoza, S., Stiksrud, E., Klinker, F., Liebetanz, D., Paulus, W., Kuo, M.F., & Nitsche, M.A. (2014). Dosage-dependent effect of dopamine D2 receptor activation on motor cortex plasticity in humans. Journal of Neuroscience, 34, 10701–10709. doi:10.1523/JNEUROSCI.0832-14.2014
  • Gamboa, O.L., Antal, A., Moliadze, V., & Paulus, W. (2010). Simply longer is not better: Reversal of theta burst after-effect with prolonged stimulation. Experimental Brain Research, 204, 181–187. doi:10.1007/s00221-010-2293-4
  • Gao, F., Chu, H., Li, J., Yang, M., Du, L., Li, J., … Chan, C. (2016). Repetitive transcranial magnetic stimulation for pain after spinal cord injury: A systematic review and meta-analysis. Journal of Neurosurgical Sciences, Retrieved from http://www.ncbi.nlm.nih.gov/pubmed/27603408
  • Gilio, F., Conte, A., Vanacore, N., Frasca, V., Inghilleri, M., & Berardelli, A. (2007). Excitatory and inhibitory after-effects after repetitive magnetic transcranial stimulation (rTMS) in normal subjects. Experimental Brain Research, 176, 588–593. doi:10.1007/s00221-006-0638-9
  • Goldsworthy, M.R., Pitcher, J.B., & Ridding, M.C. (2012). A comparison of two different continuous theta burst stimulation paradigms applied to the human primary motor cortex. Clinical Neurophysiology: Official Journal of the International Federation of Clinical Neurophysiology, 123, 2256–2263. doi:10.1016/j.clinph.2012.05.001
  • Grimm, S., Beck, J., Schuepbach, D., Hell, D., Boesiger, P., Bermpohl, F., … Northoff, G. (2008). Imbalance between left and right dorsolateral prefrontal cortex in major depression is linked to negative emotional judgment: An fMRI study in severe major depressive disorder. Biological Psychiatry, 63, 369–376. doi:10.1016/j.biopsych.2007.05.033
  • Hamada, M., Hanajima, R., Terao, Y., Arai, N., Furubayashi, T., Inomata-Terada, S., & Ugawa, Y. (2007). Origin of facilitation in repetitive, 1.5ms interval, paired pulse transcranial magnetic stimulation (rPPS) of the human motor cortex. Clinical Neurophysiology: Official Journal of the International Federation of Clinical Neurophysiology, 118, 1596–1601. doi:10.1016/j.clinph.2007.03.009
  • Hamada, M., Terao, Y., Hanajima, R., Shirota, Y., Nakatani-Enomoto, S., Furubayashi, T., … Ugawa, Y. (2008). Bidirectional long-term motor cortical plasticity and metaplasticity induced by quadripulse transcranial magnetic stimulation. The Journal of Physiology, 586, 3927–3947. doi:10.1113/jphysiol.2008.152793
  • Henry, M.J., Herrmann, B., & Obleser, J. (2014). Entrained neural oscillations in multiple frequency bands comodulate behavior. Proceedings of the National Academy of Sciences of the United States of America, 111, 14935–14940. doi:10.1073/pnas.1408741111
  • Hill, A.T., Rogasch, N.C., Fitzgerald, P.B., & Hoy, K.E. (2016). TMS-EEG: A window into the neurophysiological effects of transcranial electrical stimulation in non-motor brain regions. Neuroscience & Biobehavioral Reviews, 64, 175–184.http://dx.doi.org/10.1016/j.neubiorev.2016.03.006
  • Höffken, O., Haussleiter, I.S., Westermann, A., Lötsch, J., Maier, C., Tegenthoff, M., & Schwenkreis, P. (2013). Influence of (S)-ketamine on human motor cortex excitability. Experimental Brain Research, 225, 47–53. doi:10.1007/s00221-012-3347-6
  • Horacek, J., Brunovsky, M., Novak, T., Tislerova, B., Palenicek, T., Bubenikova-Valesova, V., … Hoschl, C. (2010). Subanesthetic dose of ketamine decreases prefrontal theta cordance in healthy volunteers: Implications for antidepressant effect. Psychological Medicine, 40, 1443–1451. doi:10.1017/S0033291709991619
  • Hrabetova, S., & Sacktor, T.C. (1997). Long-term potentiation and long-term depression are induced through pharmacologically distinct NMDA receptors. Neuroscience Letters, 226, 107–110. doi:10.1016/S0304-3940(97)00252-8
  • Hsieh, T.H., Huang, Y.Z., Rotenberg, A., Pascual-Leone, A., Chiang, Y.H., Wang, J.Y., & Chen, J.J. (2015). Functional dopaminergic neurons in substantia nigra are required for transcranial magnetic stimulation-induced motor plasticity. Celebral Cortex, 25, 1806–1814. doi:10.1093/cercor/bht421
  • Huang, Y.Z., Chen, R.S., Rothwell, J.C., & Wen, H.Y. (2007). The after-effect of human theta burst stimulation is NMDA receptor dependent. Clinical Neurophysiology: Official Journal of the International Federation of Clinical Neurophysiology, 118, 1028–1032. doi:10.1016/j.clinph.2007.01.021
  • Huang, Y.Z., Edwards, M.J., Rounis, E., Bhatia, K.P., & Rothwell, J.C. (2005). Theta burst stimulation of the human motor cortex. Neuron, 45, 201–206. doi:10.1016/j.neuron.2004.12.033
  • Huang, Y.Z., Rothwell, J.C., Edwards, M.J., & Chen, R.S. (2008). Effect of physiological activity on an NMDA-dependent form of cortical plasticity in human. Cerebral Cortex, 18, 563–570. doi:10.1093/cercor/bhm087
  • Huber, R., Määttä, S., Esser, S.K., Sarasso, S., Ferrarelli, F., Watson, A., … Tononi, G. (2008). Measures of cortical plasticity after transcranial paired associative stimulation predict changes in electroencephalogram slow-wave activity during subsequent sleep. The Journal of Neuroscience, 28, 7911–7918. doi:10.1523/JNEUROSCI.1636-08.2008
  • Iezzi, E., Suppa, A., Conte, A., Li Voti, P., Bologna, M., & Berardelli, A. (2011). Short-term and long-term plasticity interaction in human primary motor cortex. European Journal of Neuroscience, 33, 1908–1915. doi:10.1111/j.1460-9568.2011.07674.x
  • Ilmoniemi, R.J., Virtanen, J., Ruohonen, J., Karhu, J., Aronen, H.J., Näätänen, R., & Katila, T. (1997). Neuronal responses to magnetic stimulation reveal cortical reactivity and connectivity. Neuroreport, 8, 3537–3540.
  • Janicak, P.G., & Dokucu, M.E. (2015). Transcranial magnetic stimulation for the treatment of major depression. Neuropsychiatric Disease and Treatment, 11, 1549–1560. doi:10.2147/NDT.S67477
  • Jung, S.H., Shin, J.E., Jeong, Y.S., & Shin, H.I. (2008). Changes in motor cortical excitability induced by high-frequency repetitive transcranial magnetic stimulation of different stimulation durations. Clinical Neurophysiology, 119, 71–79. doi:10.1016/j.clinph.2007.09.124
  • Kaelin-Lang, A., Luft, A.R., Sawaki, L., Burstein, A.H., Sohn, Y.H., & Cohen, L.G. (2002). Modulation of human corticomotor excitability by somatosensory input. The Journal of Physiology, 540, 623–633. doi:10.1113/jphysiol.2001.012801
  • Kähkönen, S., Komssi, S., Wilenius, J., & Ilmoniemi, R.J. (2005). Prefrontal TMS produces smaller EEG responses than motor-cortex TMS: implications for rTMS treatment in depression. Psychopharmacology, 181, 16–20. doi:10.1007/s00213-005-2197-3
  • Kähkönen, S., Wilenius, J., Komssi, S., & Ilmoniemi, R.J. (2004). Distinct differences in cortical reactivity of motor and prefrontal cortices to magnetic stimulation. Clinical Neurophysiology: Official Journal of the International Federation of Clinical Neurophysiology, 115, 583–588. doi:10.1016/j.clinph.2003.10.032
  • Khedr, E.M., Etraby, A.E., Hemeda, M., Nasef, A.M., & Razek, A.A.E. (2010). Long-term effect of repetitive transcranial magnetic stimulation on motor function recovery after acute ischemic stroke. Acta Neurologica Scandinavica, 121, 30–37. doi:10.1111/j.1600-0404.2009.01195.x
  • Khedr, E.M., Rothwell, J.C., Ahmed, M.A., Shawky, O.A., & Farouk, M. (2007). Modulation of motor cortical excitability following rapid-rate transcranial magnetic stimulation. Clinical Neurophysiology: Official Journal of the International Federation of Clinical Neurophysiology, 118, 140–145. doi:10.1016/j.clinph.2006.09.006
  • Khodayari-Rostamabad, A., Reilly, J.P., Hasey, G.M., deBruin, H., & MacCrimmon, D. (2011). Using pre-treatment electroencephalography data to predict response to transcranial magnetic stimulation therapy for major depression. IEEE Engineering in Medicine and Biology Society, 2011, 6418–6421. doi:10.1109/IEMBS.2011.6091584
  • Kim, M.S., Chang, W.H., Cho, J.W., Youn, J., Kim, Y.K., Kim, S.W., & Kim, Y.H. (2015). Efficacy of cumulative high-frequency rTMS on freezing of gait in Parkinson’s disease. Restorative Neurology and Neuroscience, 33, 521–530. doi:10.3233/RNN-140489
  • Korchounov, A., & Ziemann, U. (2011). Neuromodulatory neurotransmitters influence LTP-like plasticity in human cortex: A pharmaco-TMS study. Neuropsychopharmacology, 36, 1894–1902. doi:10.1038/npp.2011.75
  • Kozyrev, V., Eysel, U.T., & Jancke, D. (2014). Voltage-sensitive dye imaging of transcranial magnetic stimulation-induced intracortical dynamics. Proceedings of the National Academy of Sciences of the United States of America, 111, 13553–13558. doi:10.1073/pnas.1405508111
  • Kujirai, T., Sato, M., Rothwell, J.C., & Cohen, L.G. (1993). The effect of transcranial magnetic stimulation on median nerve somatosensory evoked potentials. Electroencephalography and Clinical Neurophysiology, 89, 227–234.http://dx.doi.org/10.1016/0168-5597(93)90100-4
  • Labedi, A., Benali, A., Mix, A., Neubacher, U., & Funke, K. (2014). Modulation of inhibitory activity markers by intermittent theta-burst stimulation in rat cortex is NMDA-receptor dependent. Brain Stimulation, 7, 394–400. doi:10.1016/j.brs.2014.02.010
  • Lehmann, D., & Skrandies, W. (1980). Reference-free identification of components of checkerboard-evoked multichannel potential fields. Electroencephalography and Clinical Neurophysiology, 48, 609–621.http://dx.doi.org/10.1016/0013-4694(80)90419-8
  • Leuchter, A.F., Cook, I.A., Gilmer, W.S., Marangell, L.B., Burgoyne, K.S., Howland, R.H., …Greenwald, S. (2009). Effectiveness of a quantitative electroencephalographic biomarker for predicting differential response or remission with escitalopram and bupropion in major depressive disorder. Psychiatry Research, 169, 132–138. doi:10.1016/j.psychres.2009.04.004
  • Leuchter, A.F., Cook, I.A., Marangell, L.B., Gilmer, W.S., Burgoyne, K.S., Howland, R.H., …Greenwald, S. (2009). Comparative effectiveness of biomarkers and clinical indicators for predicting outcomes of SSRI treatment in major depressive disorder: Results of the BRITE-MD study. Psychiatry Research, 169, 124–131. doi:10.1016/j.psychres.2009.06.004
  • Leuchter, A.F., Hunter, A.M., Krantz, D.E., & Cook, I.A. (2015). Rhythms and blues: Modulation of oscillatory synchrony and the mechanism of action of antidepressant treatments. Annals of the New York Academy of Sciences, 1344, 78–91. doi:10.1111/nyas.12742
  • Lioumis, P., Kicić, D., Savolainen, P., Mäkelä, J.P., & Kähkönen, S. (2009). Reproducibility of TMS-evoked EEG responses. Human Brain Mapping, 30, 1387–1396. doi:10.1002/hbm.20608
  • Lorenzano, C., Dinapoli, L., Gilio, F., Suppa, A., Bagnato, S., Currà, A., … Berardelli, A. (2006). Motor cortical excitability studied with repetitive transcranial magnetic stimulation in patients with Huntington’s disease. Clinical Neurophysiology: Official Journal of the International Federation of Clinical Neurophysiology, 117, 1677–1681. doi:10.1016/j.clinph.2006.04.012
  • Lüscher, C., & Malenka, R.C. (2012). NMDA receptor-dependent long-term potentiation and long-term depression (LTP/LTD). Cold Spring Harbor Perspectives in Biology, 4, a005710. doi:10.1101/cshperspect.a005710
  • Malcolm, M.P., & Paxton, R.J. (2015). High-frequency repetitive transcranial magnetic stimulation effects on motor intracortical neurophysiology: A Sham-controlled investigation. Journal of Clinical Neurophysiology: Official Publication of the American Electroencephalographic Society, 32, 428–433. doi:10.1097/WNP.0000000000000203
  • Malenka, R.C., & Bear, M.F. (2004). LTP and LTD: An embarrassment of riches. Neuron, 44, 5–21. doi:10.1016/j.neuron.2004.09.012
  • Matsunaga, K., Maruyama, A., Fujiwara, T., Nakanishi, R., Tsuji, S., & Rothwell, J.C. (2005). Increased corticospinal excitability after 5 Hz rTMS over the human supplementary motor area. The Journal of Physiology, 562, 295–306. doi:10.1113/jphysiol.2004.070755
  • Meintzschel, F., & Ziemann, U. (2006). Modification of practice-dependent plasticity in human motor cortex by neuromodulators. Celebral Cortex, 16, 1106–1115. doi:10.1093/cercor/bhj052
  • Monte-Silva, K., Kuo, M.F., Thirugnanasambandam, N., Liebetanz, D., Paulus, W., & Nitsche, M.A. (2009). Dose-dependent inverted U-shaped effect of dopamine (D2-like) receptor activation on focal and nonfocal plasticity in humans. Journal of Neuroscience, 29, 6124–6131. doi:10.1523/JNEUROSCI.0728-09.2009
  • Mueller, A.L., Albensi, B.C., Ganong, A.H., Reynolds, L.S., & Jackson, H. (1991). Arylamine spider toxins antagonize NMDA receptor-mediated synaptic transmission in rat hippocampal slices. Synapse, 9, 244–250. doi:10.1002/syn.890090403
  • Nakamura, K., Enomoto, H., Hanajima, R., Hamada, M., Shimizu, E., Kawamura, Y., & Ugawa, Y. (2011). Quadri-pulse stimulation (QPS) induced LTP/LTD was not affected by Val66Met polymorphism in the brain-derived neurotrophic factor (BDNF) gene. Neuroscience Letters, 487, 264–267. doi:10.1016/j.neulet.2010.10.034
  • Nakamura, H., Kitagawa, H., Kawaguchi, Y., & Tsuji, H. (1997). Intracortical facilitation and inhibition after transcranial magnetic stimulation in conscious humans. The Journal of Physiology, 498, 817–823.http://dx.doi.org/10.1113/jphysiol.1997.sp021905
  • Nakatani-Enomoto, S., Hanajima, R., Hamada, M., Terao, Y., Matsumoto, H., Shirota, Y., … Ugawa, Y. (2012). Bidirectional modulation of sensory cortical excitability by quadripulse transcranial magnetic stimulation (QPS) in humans. Clinical Neurophysiology, 123, 1415–1421. doi:10.1016/j.clinph.2011.11.037
  • Nettekoven, C., Volz, L.J., Kutscha, M., Pool, E.M., Rehme, A.K., Eickhoff, S.B., … Grefkes, C. (2014). Dose-dependent effects of theta burst rTMS on cortical excitability and resting-state connectivity of the human motor system. The Journal of Neuroscience: The Official Journal of the Society for Neuroscience, 34, 6849–6859. doi:10.1523/JNEUROSCI.4993-13.2014
  • Nitsche, M.A., Kuo, M.F., Grosch, J., Bergner, C., Monte-Silva, K., & Paulus, W. (2009). D1-receptor impact on neuroplasticity in humans. Journal of Neuroscience, 29, 2648–2653. doi:10.1523/JNEUROSCI.5366-08.2009
  • Noh, N.A. (2016). Exploring cortical plasticity and oscillatory brain dynamics via transcranial magnetic stimulation and resting-state electroencephalogram. The Malaysian Journal of Medical Sciences: MJMS, 23, 5–16. doi:10.21315/mjms2016.23.4.2
  • Nojima, K., Katayama, Y., Iramina, K. (2013). Predicting rTMS effect for deciding stimulation parameters. Conference Proceedings: Annual International Conference of the IEEE Engineering in Medicine and Biology Society. IEEE Engineering in Medicine and Biology Society. Annual Conference, 2013, 6369–6372. doi:10.1109/EMBC.2013.6611011
  • Nordmann, G., Azorina, V., Langguth, B., & Schecklmann, M. (2015). A systematic review of non-motor rTMS induced motor cortex plasticity. Frontiers in Human Neuroscience, 9, 416. doi:10.3389/fnhum.2015.00416
  • O'Reardon, J.P., Solvason, H.B., Janicak, P.G., Sampson, S., Isenberg, K.E., Nahas, Z., & Sackeim, H.A. (2007). Efficacy and safety of transcranial magnetic stimulation in the acute treatment of major depression: A multisite randomized controlled trial. Biological Psychiatry, 62, 1208–1216. doi:10.1016/j.biopsych.2007.01.018
  • Ogiue-Ikeda, M., Kawato, S., & Ueno, S. (2003). The effect of repetitive transcranial magnetic stimulation on long-term potentiation in rat hippocampus depends on stimulus intensity. Brain Research, 993, 222–226. doi:10.1016/j.brainres.2003.09.009
  • Padberg, F., Zwanzger, P., Thoma, H., Kathmann, N., Haag, C., D. Greenberg, B., & Möller, H.-J. (1999). Repetitive transcranial magnetic stimulation (rTMS) in pharmacotherapy-refractory major depression: Comparative study of fast, slow and sham rTMS. Psychiatry Research, 88, 163–171. doi:10.1016/S0165-1781(99)00092-X
  • Park, E., Kim, Y.H., Chang, W.H., Kwon, T.G., & Shin, Y.I. (2014). Interhemispheric modulation of dual-mode, noninvasive brain stimulation on motor function. Annals of Rehabilitation Medicine, 38, 297–303. doi:10.5535/arm.2014.38.3.297
  • Pathak, Y., Salami, O., Baillet, S., Li, Z., & Butson, C.R. (2016). Longitudinal changes in depressive circuitry in response to neuromodulation therapy. Frontiers in Neural Circuits, 10, 50. doi:10.3389/fncir.2016.00050
  • Pegado, F., Vankrunkelsven, H., Steyaert, J., Boets, B., & Op de Beeck, H. (2016). Exploring the use of sensorial LTP/LTD-like stimulation to modulate human performance for complex visual stimuli. PLoS One, 11, e0158312. doi:10.1371/journal.pone.0158312
  • Pellicciari, M.C., Brignani, D., & Miniussi, C. (2013). Excitability modulation of the motor system induced by transcranial direct current stimulation: A multimodal approach. NeuroImage, 83, 569–580. doi:10.1016/j.neuroimage.2013.06.076
  • Pellicciari, M.C., Cordone, S., Marzano, C., Bignotti, S., Gazzoli, A., Miniussi, C., & De Gennaro, L. (2013). Dorsolateral prefrontal transcranial magnetic stimulation in patients with major depression locally affects alpha power of REM sleep. Frontiers in Human Neuroscience, 7, 433. doi:10.3389/fnhum.2013.00433
  • Peng, Y., Zhao, J., Gu, Q.H., Chen, R.Q., Xu, Z., Yan, J.Z., & Lu, W. (2010). Distinct trafficking and expression mechanisms underlie LTP and LTD of NMDA receptor-mediated synaptic responses. Hippocampus, 20, 646–658. doi:10.1002/hipo.20654
  • Perera, T., George, M.S., Grammer, G., Janicak, P.G., Pascual-Leone, A.G., & Wirecki, T.S. (2016). The clinical TMS society consensus review and treatment recommendations for TMS therapy for major depressive disorder. Brain Stimulation, 9, 336–346. doi:10.1016/j.brs.2016.03.010
  • Philip, N.S., Ridout, S.J., Albright, S.E., Sanchez, G., & Carpenter, L.L. (2016). 5-Hz transcranial magnetic stimulation for comorbid posttraumatic stress disorder and major depression. Journal of Traumatic Stress, 29, 93–96. doi:10.1002/jts.22065
  • Reis, J., Tergau, F., Hamer, H.M., Müller, H.H., Knake, S., Fritsch, B., … Rosenow, F. (2002). Topiramate selectively decreases intracortical excitability in human motor cortex. Epilepsia, 43, 1149–1156. doi:10.1046/j.1528-1157.2002.09902.x
  • Reis, J., John, D., Heimeroth, A., Mueller, H.H., Oertel, W.H., Arndt, T., & Rosenow, F. (2006). Modulation of human motor cortex excitability by single doses of amantadine. Neuropsychopharmacology: Official Publication of the American College of Neuropsychopharmacology, 31, 2758–2766. doi:10.1038/sj.npp.1301122
  • Richieri, R., Boyer, L., Padovani, R., Adida, M., Colavolpe, C., Mundler, O., & Guedj, E. (2012). Equivalent brain SPECT perfusion changes underlying therapeutic efficiency in pharmacoresistant depression using either high-frequency left or low-frequency right prefrontal rTMS. Progress in Neuropsychopharmacology & Biological Psychiatry, 39, 364–370. doi:10.1016/j.pnpbp.2012.07.012
  • Rogasch, N.C., Daskalakis, Z.J., & Fitzgerald, P.B. (2015). Cortical inhibition of distinct mechanisms in the dorsolateral prefrontal cortex is related to working memory performance: a TMS-EEG study. Cortex: A Journal Devoted to the Study of the Nervous System and Behavior, 64, 68–77. doi:10.1016/j.cortex.2014.10.003
  • Rogasch, N.C., & Fitzgerald, P.B. (2013). Assessing cortical network properties using TMS-EEG. Human Brain Mapping, 34, 1652–1669.http://dx.doi.org/10.1002/hbm.22016
  • Romero Lauro, L.J., Rosanova, M., Mattavelli, G., Convento, S., Pisoni, A., Opitz, A., & Vallar, G. (2014). TDCS increases cortical excitability: Direct evidence from TMS-EEG. Cortex, 58, 99–111. doi:10.1016/j.cortex.2014.05.003
  • Rosanova, M., Casali, A., Bellina, V., Resta, F., Mariotti, M., & Massimini, M. (2009). Natural frequencies of human corticothalamic circuits. The Journal of Neuroscience, 29, 7679–7685. doi:10.1523/JNEUROSCI.0445-09.2009
  • Rossini, P.M., Barker, A.T., Berardelli, A., Caramia, M.D., Caruso, G., Cracco, R.Q., & Lücking, C.H. (1994). Non-invasive electrical and magnetic stimulation of the brain, spinal cord and roots: basic principles and procedures for routine clinical application. Report of an IFCN committee. Electroencephalography and Clinical Neurophysiology, 91, 79–92.
  • Sale, M.V., Rogasch, N.C., & Nordstrom, M.A. (2016). Different Stimulation Frequencies Alter Synchronous Fluctuations in Motor Evoked Potential Amplitude of Intrinsic Hand Muscles-a TMS Study. Frontiers in Human Neuroscience, 10, 100. doi:10.3389/fnhum.2016.00100
  • Samaha, J., Gosseries, O., & Postle, B.R. (2017). Distinct oscillatory frequencies underlie excitability of human occipital and parietal cortex. The Journal of Neuroscience, 8, 3413–3416. doi:10.1523/JNEUROSCI.3413-16.2017
  • Schalk, G. (2015). A general framework for dynamic cortical function: the function-through-biased-oscillations (FBO) hypothesis. Frontiers in Human Neuroscience, 9, 352. doi:10.3389/fnhum.2015.00352
  • Schwenkreis, P., Witscher, K., Janssen, F., Addo, A., Dertwinkel, R., Zenz, M., … Tegenthoff, M. (1999). Influence of the N-methyl-D-aspartate antagonist memantine on human motor cortex excitability. Neuroscience Letters, 270, 137–140. doi:10.1016/S0304-3940(99)00492-9
  • Sczesny-Kaiser, M., Tegenthoff, M., & Schwenkreis, P. (2009). Influence of 5 Hz repetitive transcranial magnetic stimulation on motor learning. Neuroscience Letters, 457, 71–74. doi:10.1016/j.neulet.2009.04.015
  • Simeoni, S., Hannah, R., Sato, D., Kawakami, M., Rothwell, J., Simeoni, S., … Kawakami, M. (2016). Effects of quadripulse stimulation on human motor cortex excitability: A replication study. Brain Stimulation, 9, 148–150. doi:10.1016/j.brs.2015.10.007
  • Simis, M., Adeyemo, B.O., Medeiros, L.F., Miraval, F., Gagliardi, R.J., & Fregni, F. (2013). Motor cortex-induced plasticity by noninvasive brain stimulation: A comparison between transcranial direct current stimulation and transcranial magnetic stimulation. Neuroreport, 24, 973–975. doi:10.1097/WNR.0000000000000021
  • Smit, D.J., Stam, C.J., Posthuma, D., Boomsma, D.I., & de Geus, E.J. (2008). Heritability of “small-world” networks in the brain: A graph theoretical analysis of resting-state EEG functional connectivity. Human Brain Mapping, 29, 1368–1378. doi:10.1002/hbm.20468
  • Sommer, M., Norden, C., Schmack, L., Rothkegel, H., Lang, N., & Paulus, W. (2013). Opposite optimal current flow directions for induction of neuroplasticity and excitation threshold in the human motor cortex. Brain Stimulation, 6, 363–370. doi:10.1016/j.brs.2012.07.003
  • Sommer, M., Rummel, M., Norden, C., Rothkegel, H., Lang, N., & Paulus, W. (2013). Mechanisms of human motor cortex facilitation induced by subthreshold 5-Hz repetitive transcranial magnetic stimulation. Journal of Neurophysiology, 109, 3060–3066. doi:10.1152/jn.01089.2012
  • Suppa, A., Li Voti, P., Rocchi, L., Papazachariadis, O., & Berardelli, A. (2015). Early visuomotor integration processes induce LTP/LTD-like plasticity in the human motor cortex. Celebral Cortex, 25, 703–712. doi:10.1093/cercor/bht264
  • Teo, J.T.H., Swayne, O.B., & Rothwell, J.C. (2007). Further evidence for NMDA-dependence of the after-effects of human theta burst stimulation. Clinical Neurophysiology: Official Journal of the International Federation of Clinical Neurophysiology, 118, 1649–1651. doi:10.1016/j.clinph.2007.04.010
  • Thirugnanasambandam, N., Grundey, J., Paulus, W., & Nitsche, M.A. (2011). Dose-dependent nonlinear effect of L-DOPA on paired associative stimulation-induced neuroplasticity in humans. Journal of Neuroscience, 31, 5294–5299. doi:10.1523/JNEUROSCI.6258-10.2011
  • Trebbastoni, A., Pichiorri, F., D’antonio, F., Campanelli, A., Onesti, E., Ceccanti, M., & Inghilleri, M. (2016). Altered cortical synaptic plasticity in response to 5-Hz repetitive transcranial magnetic stimulation as a new electrophysiological finding in amnestic mild cognitive impairment converting to Alzheimer’s disease: Results from a 4-year prospective cohorts. Frontiers in Aging Neuroscience, 7, 253. doi:10.3389/fnagi.2015.00253
  • Valls-Sole, J., Pascual-Leone, A., Wassermann, E.M., & Hallett, M. (1992). Human motor evoked responses to paired transcranial magnetic stimuli. Electroencephalography and Clinical Neurophysiology, 85, 355–364.http://dx.doi.org/10.1016/0168-5597(92)90048-G
  • Vasant, D.H., Michou, E., Mistry, S., Rothwell, J.C., & Hamdy, S. (2015). High-frequency focal repetitive cerebellar stimulation induces prolonged increases in human pharyngeal motor cortex excitability. The Journal of Physiology, 593, 4963–4977. doi:10.1113/JP270817
  • Veniero, D., Vossen, A., Gross, J., & Thut, G. (2015). Lasting EEG/MEG after effects of rhythmic transcranial brain stimulation: Level of control over oscillatory network activity. Frontiers of Cellular Neuroscience, 9, 477. doi:10.3389/fncel.2015.00477
  • Vernet, M., Bashir, S., Yoo, W.K., Oberman, L., Mizrahi, I., Ifert-Miller, F., & Pascual-Leone, A. (2014). Reproducibility of the effects of theta burst stimulation on motor cortical plasticity in healthy participants. Clinical Neurophysiology: Official Journal of the International Federation of Clinical Neurophysiology, 125, 320–326. doi:10.1016/j.clinph.2013.07.004
  • Walter, H., Wolf, R.C., Spitzer, M., & Vasic, N. (2007). Increased left prefrontal activation in patients with unipolar depression: An event-related, parametric, performance-controlled fMRI study. Journal of Affective Disorders, 101, 175–185. doi:10.1016/j.jad.2006.11.017
  • Watanabe, T., Hanajima, R., Shirota, Y., Ohminami, S., Tsutsumi, R., Terao, Y., & Ohtomo, K. (2014). Bidirectional effects on interhemispheric resting-state functional connectivity induced by excitatory and inhibitory repetitive transcranial magnetic stimulation. Human Brain Mapping, 35, 1896–1905. doi:10.1002/hbm.22300
  • Wischnewski, M., & Schutter, D.J. (2015). Efficacy and time course of theta burst stimulation in healthy humans. Brain Stimulation, 8, 685–692. doi:10.1016/j.brs.2015.03.004
  • Yin, Z., Shen, Y., Reinhardt, J.D., Chen, C.F., Jiang, X., Dai, W., & Shan, C. (2015). 5 Hz repetitive transcranial magnetic stimulation with maximum voluntary muscle contraction facilitates cerebral cortex excitability of normal subjects. CNS and Neurological Disorders Drug Targets, 14, 1298–1303. doi:10.2174/1871527315666151111124216
  • Ziemann, U., Paulus, W., Nitsche, M.A., Pascual-Leone, A., Byblow, W.D., Berardelli, A., & Rothwell, J.C. (2006). Consensus: Motor cortex plasticity protocols. Brain Stimulation, 1, 164–182. doi:10.1016/j.brs.2008.06.006

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Order Reprints Request Corporate Permissions

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

Request Academic Permissions

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.

Related research

People also read lists articles that other readers of this article have read.

Recommended articles lists articles that we recommend and is powered by our AI driven recommendation engine.

Cited by lists all citing articles based on Crossref citations.
Articles with the Crossref icon will open in a new tab.