Hostname: page-component-7b9c58cd5d-wdhn8 Total loading time: 0 Render date: 2025-03-15T10:00:10.447Z Has data issue: false hasContentIssue false
  • English
  • Français

Antidepressant efficacy of high-frequency transcranial magnetic stimulation over the left dorsolateral prefrontal cortex in double-blind sham-controlled designs: a meta-analysis

Published online by Cambridge University Press:  30 April 2008

D. J. L. G. Schutter
D. J. L. G. Schutter*
Affiliation:
Experimental Psychology, Utrecht University, Utrecht, The Netherlands
*
*Address for correspondence: D. J. L. G. Schutter, Ph.D., Experimental Psychology, Utrecht University, Heidelberglaan 2, 3584CS Utrecht, The Netherlands. (Email: d.schutter@uu.nl)
Get access Rights & Permissions [Opens in a new window]

Abstract

Background

For more than a decade high-frequency repetitive transcranial magnetic stimulation (rTMS) has been applied to the left dorsolateral prefrontal cortex (DLPFC) in search of an alternative treatment for depression. The aim of this study was to provide an update on its clinical efficacy by performing a meta-analysis involving double-blind sham-controlled studies.

Method

A literature search was conducted in the databases PubMed and Web of Science in the period between January 1980 and November 2007 with the search terms ‘depression’ and ‘transcranial magnetic stimulation’. Thirty double-blind sham-controlled parallel studies with 1164 patients comparing the percentage change in depression scores from baseline to endpoint of active versus sham treatment were included. A random effects meta-analysis was performed to investigate the clinical efficacy of fast-frequency rTMS over the left DLPFC in depression.

Results

The test for heterogeneity was not significant (QT=30.46, p=0.39). A significant overall weighted mean effect size, d=0.39 [95% confidence interval (CI) 0.25–0.54], for active treatment was observed (z=6.52, p<0.0001). Medication resistance and intensity of rTMS did not play a role in the effect size.

Conclusions

These findings show that high-frequency rTMS over the left DLPFC is superior to sham in the treatment of depression. The effect size is robust and comparable to at least a subset of commercially available antidepressant drug agents. Current limitations and future prospects are discussed.

Keywords

Depressiondorsolateral prefrontal cortexmeta-analysistranscranial magnetic stimulationtreatment
Type
Original Articles
Information
Psychological Medicine , Volume 39 , Issue 1 , January 2009 , pp. 65 - 75
Copyright
Copyright © 2008 Cambridge University Press

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Arana, AB, Borckardt, JJ, Ricci, R, Anderson, B, Li, X, Linder, KJ, Long, J, Sackeim, HA, George, MS (2008). Focal electrical stimulation as a sham control for repetitive transcranial magnetic stimulation: does it truly mimic the cutaneous sensation and pain of active prefrontal repetitive transcranial magnetic stimulation? Brain Stimulation 1, 44–51.CrossRefGoogle ScholarPubMed
Avery, DH, Claypoole, K, Robinson, L, Neumaier, JF, Dunner, DL, Scheele, L, Wilson, L, Roy-Byrne, P (1999). Repetitive transcranial magnetic stimulation in the treatment of medication-resistant depression: preliminary data. Journal of Nervous and Mental Disease 187, 114–117.CrossRefGoogle ScholarPubMed
Avery, DH, Holtzheimer, PE 3rd, Fawaz, W, Russo, J, Neumaier, J, Dunner, DL, Haynor, DR, Claypoole, KH, Wajdik, C, Roy-Byrne, P (2006). A controlled study of repetitive transcranial magnetic stimulation in medication-resistant major depression. Biological Psychiatry 59, 187–194.CrossRefGoogle ScholarPubMed
Baxter, LR Jr, Schwartz, JM, Phelps, ME, Mazziotta, JC, Guze, BH, Selin, CE (1989). Reduction of prefrontal cortex glucose metabolism common to three types of depression. Archives of General Psychiatry 46, 243–250.CrossRefGoogle ScholarPubMed
Berman, RM, Narasimhan, M, Sanacora, G, Miano, AP, Hoffman, RE, Hu, XS, Charney, DS, Boutros, NN (2000). A randomized clinical trial of repetitive transcranial magnetic stimulation in the treatment of major depression. Biological Psychiatry 47, 332–337.CrossRefGoogle ScholarPubMed
Bohning, DE (2000). Introduction and overview of TMS physics. In Transcranial Magnetic Stimulation in Neuropsychiatry (ed. George, M. S. and Belmaker, R. H.), pp. 3–44. American Psychiatric Press: Washington, DC.Google Scholar
Boutros, NN, Gueorguieva, R, Hoffman, RE, Oren, DA, Feingold, A, Berman, RM (2002). Lack of a therapeutic effect of a 2-week sub-threshold transcranial magnetic stimulation course for treatment-resistant depression. Psychiatry Research 113, 245–254.CrossRefGoogle ScholarPubMed
Burt, T, Lisanby, SH, Sackeim, HA (2002). Neuropsychiatric applications of transcranial magnetic stimulation: a meta-analysis. International Journal of Neuropsychopharmacology 5, 73–103.CrossRefGoogle ScholarPubMed
Chen, Y, Guo, JJ, Zhan, S, Patel, NC (2006). Treatment effects of antidepressants in patients with post-stroke depression: a meta-analysis. Annals of Pharmacotherapy 40, 2115–2122.CrossRefGoogle ScholarPubMed
Couturier, JL (2005). Efficacy of rapid-rate repetitive transcranial magnetic stimulation in the treatment of depression: a systematic review and meta-analysis. Journal of Psychiatry and Neuroscience 30, 83–90.Google ScholarPubMed
Dannon, PN, Dolberg, OT, Schreiber, S, Grunhaus, L (2002). Three- and six-month outcome following courses of either ECT or rTMS in a population of severely depressed individuals: preliminary report. Biological Psychiatry 51, 687–690.CrossRefGoogle ScholarPubMed
Davidson, RJ, Abercrombie, H, Nitschke, JB, Putnam, K (1999). Regional brain function, emotion and disorders of emotion. Current Opinion in Neurobiology 9, 228–234.CrossRefGoogle ScholarPubMed
Dunlop, BW, Nemeroff, CB (2007). The role of dopamine in the pathophysiology of depression. Archives of General Psychiatry 64, 327–337.CrossRefGoogle ScholarPubMed
Eschweiler, GW, Wegerer, C, Schlotter, W, Spandl, C, Stevens, A, Bartels, M, Buchkremer, G (2000). Left prefrontal activation predicts therapeutic effects of repetitive transcranial magnetic stimulation (rTMS) in major depression. Psychiatry Research 99, 161–172.CrossRefGoogle ScholarPubMed
Fitzgerald, PB, Benitez, J, de Castella, A, Daskalakis, ZJ, Brown, TL, Kulkarni, J (2006). A randomized, controlled trial of sequential bilateral repetitive transcranial magnetic stimulation for treatment-resistant depression. American Journal of Psychiatry 163, 88–94.CrossRefGoogle ScholarPubMed
Fitzgerald, PB, Brown, TL, Marston, NA, Daskalakis, ZJ, de Castella, A, Kulkarni, J (2003). Transcranial magnetic stimulation in the treatment of depression: a double-blind, placebo-controlled trial. Archives of General Psychiatry 60, 1002–1008.CrossRefGoogle ScholarPubMed
Garcia-Toro, M, Mayol, A, Arnillas, H, Capllonch, I, Ibarra, O, Crespi, M, Mico, J, Lafau, O, Lafuente, L (2001). Modest adjunctive benefit with transcranial magnetic stimulation in medication-resistant depression. Journal of Affective Disorders 64, 271–275.CrossRefGoogle ScholarPubMed
George, MS, Lisanby, SH, Sackeim, HA (1999). Transcranial magnetic stimulation: applications in neuropsychiatry. Archives of General Psychiatry 56, 300–311.CrossRefGoogle ScholarPubMed
George, MS, Nahas, Z, Lisanby, SH, Schlaepfer, T, Kozel, FA, Greenberg, BD (2003). Transcranial magnetic stimulation. Neurosurgery Clinics of North America 14, 283–301.CrossRefGoogle ScholarPubMed
George, MS, Nahas, Z, Molloy, M, Speer, AM, Oliver, NC, Li, XB, Arana, GW, Risch, SC, Ballenger, JC (2000). A controlled trial of daily left prefrontal cortex TMS for treating depression. Biological Psychiatry 48, 962–970.CrossRefGoogle ScholarPubMed
George, MS, Wassermann, EM, Kimbrell, TA, Little, JT, Williams, WE, Danielson, AL, Greenberg, BD, Hallett, M, Post, RM (1997). Mood improvement following daily left prefrontal repetitive transcranial magnetic stimulation in patients with depression: a placebo-controlled crossover trial. American Journal of Psychiatry 154, 1752–1756.CrossRefGoogle ScholarPubMed
Gershon, AA, Dannon, PN, Grunhaus, L (2003). Transcranial magnetic stimulation in the treatment of depression. American Journal of Psychiatry 160, 835–845.CrossRefGoogle ScholarPubMed
Grafman, J (2000). Conceptualizing functional neuroplasticity. Journal of Communication Disorders 33, 345–356.CrossRefGoogle ScholarPubMed
Gross, M, Nakamura, L, Pascual-Leone, A, Fregni, F (2007). Has repetitive transcranial magnetic stimulation (rTMS) treatment for depression improved? A systematic review and meta-analysis comparing the recent vs. the earlier rTMS studies. Acta Psychiatrica Scandinavica 116, 165–173.CrossRefGoogle ScholarPubMed
Haag, C, Padberg, F, Thoma, H, Zwanzger, P, Hampel, H, Moller, HJ (1997). Rapid transcranial magnetic stimulation (rTMS) in the treatment of major depression: a randomised placebo controlled study. Pharmacopsychiatry 30, 173.Google Scholar
Hedges, LV (1981). Distribution theory for Glass's estimator of effect size and related estimates. Journal of Educational Statistics 6, 107–128.CrossRefGoogle Scholar
Hedges, LV, Olkin, I (1985). Statistical Methods for Meta-Analysis. Academic Press: Orlando, FL.Google Scholar
Heo, W, Murphy, CF, Meyers, BS (2007). Relationship between the Hamilton Depression Rating Scale and the Montgomery–Åsberg Depression Rating Scale in depressed elderly: a meta-analysis. American Journal of Geriatric Psychiatry 15, 899–905.CrossRefGoogle ScholarPubMed
Herrmann, LL, Ebmeier, KP (2006). Factors modifying the efficacy of transcranial magnetic stimulation in the treatment of depression: a review. Journal of Clinical Psychiatry 67, 1870–1876.CrossRefGoogle ScholarPubMed
Herwig, U, Fallgatter, AJ, Höppner, J, Eschweiler, GW, Kron, M, Hajak, G, Padberg, F, Naderi-Heiden, A, Abler, B, Eichhammer, P, Grossheinrich, N, Hay, B, Kammer, T, Langguth, B, Laske, C, Plewnia, C, Richter, MM, Schulz, M, Unterecker, S, Zinke, A, Spitzer, M, Schönfeldt-Lecuona, C (2007). Antidepressant effects of augmentative transcranial magnetic stimulation: randomised multicentre trial. British Journal of Psychiatry 191, 441–448.CrossRefGoogle ScholarPubMed
Hoflich, G, Kaper, S, Hufnagel, A, Ruhrmann, S, Möller, HJ (1993). Application of transcranial magnetic stimulation in treatment of drug-resistant major depression: a report of two cases. Human Psychopharmacology 8, 361–365.CrossRefGoogle Scholar
Holtzheimer, PE, Russo, J, Avery, DH (2002). A meta-analysis of repetitive transcranial magnetic stimulation in the treatment of depression. Psychopharmacological Bulletin 35, 149–169.Google Scholar
Holtzheimer, PE, Russo, J, Claypoole, KH, Roy-Byrne, P, Avery, DH (2004). Shorter duration of depressive episode may predict response to repetitive transcranial magnetic stimulation. Depression and Anxiety 19, 24–30.CrossRefGoogle ScholarPubMed
Höppner, J, Schulz, M, Irmisch, G, Mau, R, Schlafke, D, Richter, J (2003). Antidepressant efficacy of two different rTMS procedures: high frequency over left versus low frequency over right prefrontal cortex compared with sham stimulation. European Archives of Psychiatry and Clinical Neuroscience 253, 103–109.CrossRefGoogle ScholarPubMed
Huang, YZ, Edwards, MJ, Rounis, E, Bhatia, KP, Rothwell, JC (2005). Theta burst stimulation of the human motor cortex. Neuron 45, 201–206.CrossRefGoogle ScholarPubMed
Joffe, R, Sokolov, S, Streiner, D (1996). Antidepressant treatment of depression: a meta- analysis. Canadian Journal of Psychiatry 41, 613–616.CrossRefGoogle Scholar
Joo, EY, Han, SJ, Chung, SH, Cho, JW, Seo, DW, Hong, SB (2007). Antiepileptic effects of low-frequency repetitive transcranial magnetic stimulation by different stimulation durations and locations. Clinical Neurophysiology 118, 702–708.CrossRefGoogle ScholarPubMed
Jorge, RE, Robinson, RG, Tateno, A, Narushima, K, Acion, L, Moser, D, Arndt, S, Chemerinski, E (2004). Repetitive transcranial magnetic stimulation as treatment of poststroke depression: a preliminary study. Biological Psychiatry 55, 398–405.CrossRefGoogle ScholarPubMed
Kauffmann, CD, Cheema, MA, Miller, BE (2004). Slow right prefrontal transcranial magnetic stimulation as a treatment for medication-resistant depression: a double-blind, placebo-controlled study. Depression and Anxiety 19, 59–62.CrossRefGoogle ScholarPubMed
Keller, J, Nitschke, JB, Bhargava, T, Deldin, PJ, Gergen, JA, Miller, GA, Heller, W (2000). Neuropsychological differentiation of depression and anxiety. Journal of Abnormal Psychology 109, 3–10.CrossRefGoogle ScholarPubMed
Kimbrell, TA, Little, JT, Dunn, RT, Frye, MA, Greenberg, BD, Wassermann, EM, Repella, JD, Danielson, AL, Willis, MW, Benson, BE, Speer, AM, Osuch, E, George, MS, Post, RM (1999). Frequency dependence of antidepressant response to left prefrontal repetitive transcranial magnetic stimulation (rTMS) as a function of baseline cerebral glucose metabolism. Biological Psychiatry 46, 1603–1613.CrossRefGoogle ScholarPubMed
Klein, E, Kreinin, I, Chistyakov, A, Koren, D, Mecz, L, Marmur, S, Ben-Shachar, D, Feinsod, M (1999). Therapeutic efficacy of right prefrontal slow repetitive transcranial magnetic stimulation in major depression: a double-blind controlled study. Archives of General Psychiatry 56, 315–320.CrossRefGoogle ScholarPubMed
Koerselman, F, Laman, DM, van Duijn, H, van Duijn, MA, Willems, MA (2004). A 3-month, follow-up, randomized, placebo-controlled study of repetitive transcranial magnetic stimulation in depression. Journal of Clinical Psychiatry 65, 1323–1328.CrossRefGoogle ScholarPubMed
Lisanby, SH, Gutman, D, Luber, B, Schroeder, C, Sackeim, HA (2001). Sham TMS: intracerebral measurement of the induced electrical field and the induction of motor-evoked potentials. Biological Psychiatry 49, 460–463.CrossRefGoogle ScholarPubMed
Loo, C, Mitchell, P, Sachdev, P, McDarmont, B, Parker, G, Gandevia, S (1999). Double-blind controlled investigation of transcranial magnetic stimulation for the treatment of resistant major depression. American Journal of Psychiatry 156, 946–948.CrossRefGoogle ScholarPubMed
Loo, CK, Mitchell, PB (2005). A review of the efficacy of transcranial magnetic stimulation (TMS) treatment for depression, and current and future strategies to optimize efficacy. Journal of Affective Disorders 88, 255–267.CrossRefGoogle ScholarPubMed
Loo, CK, Mitchell, PB, Croker, VM, Malhi, GS, Wen, W, Gandevia, SC, Sachdev, PS (2003). Double-blind controlled investigation of bilateral prefrontal transcranial magnetic stimulation for the treatment of resistant major depression. Psychological Medicine 33, 33–40.CrossRefGoogle ScholarPubMed
Loo, CK, Mitchell, PB, McFarquhar, TF, Malhi, GS, Sachdev, PR (2007). A sham-controlled trial of the efficacy and safety of twice-daily rTMS in major depression. Psychological Medicine 37, 341–349.CrossRefGoogle ScholarPubMed
Lyness, JM, Bruce, ML, Koenig, HG, Parmelee, PA, Schulz, R, Lawton, MP, Reynolds, C 3rd (1996). Depression and medical illness in late life: report of a symposium. Journal of the American Geriatrics Society 44, 198–203.CrossRefGoogle Scholar
Manes, F, Jorge, R, Morcuende, M, Yamada, T, Paradiso, S, Robinson, RG (2001). A controlled study of repetitive transcranial magnetic stimulation as a treatment of depression in the elderly. International Psychogeriatrics 13, 225–231.CrossRefGoogle ScholarPubMed
Martin, JL, Barbanoj, MJ, Schlaepfer, TE, Clos, S, Perez, V, Kulisevsky, J, Gironell, A (2002). Transcranial magnetic stimulation for treating depression. Cochrane Database of Systematic Reviews. Issue 2, Art. no.: CD003493.Google Scholar
Martin, JL, Barbanoj, MJ, Schlaepfer, TE, Thompson, E, Perez, V, Kulisevsky, J (2003). Repetitive transcranial magnetic stimulation for the treatment of depression. Systematic review and meta-analysis. British Journal of Psychiatry 182, 480–491.CrossRefGoogle ScholarPubMed
McNamara, B, Ray, JL, Arthurs, OJ, Boniface, S (2001). Transcranial magnetic stimulation for depression and other psychiatric disorders. Psychological Medicine 31, 1141–1146.CrossRefGoogle ScholarPubMed
Miniussi, C, Bonato, C, Bignotti, S, Gazzoli, A, Gennarelli, M, Pasqualetti, P, Tura, GB, Ventriglia, M, Rossini, PM (2005). Repetitive transcranial magnetic stimulation (rTMS) at high and low frequency: an efficacious therapy for major drug-resistant depression? Clinical Neurophysiology 116, 1062–1071.CrossRefGoogle ScholarPubMed
Mogg, A, Pluck, G, Eranti, SV, Landau, S, Purvis, R, Brown, RG, Curtis, V, Howard, R, Philpot, M, McLoughlin, DM (2008). A randomized controlled trial with 4-month follow-up of adjunctive repetitive transcranial magnetic stimulation of the left prefrontal cortex for depression. Psychological Medicine 38, 323–333.CrossRefGoogle ScholarPubMed
Moncrieff, J, Wessely, S, Hardy, R (1998). Meta-analysis of trials comparing antidepressants with active placebos. British Journal of Psychiatry 172, 227–231.CrossRefGoogle ScholarPubMed
Moncrieff, J, Wessely, S, Hardy, R (2004). Active placebos versus antidepressants for depression. Cochrane Database of Systematic Reviews. Issue 1, Art. no.: CD003012.Google Scholar
Mosimann, UP, Schmitt, W, Greenberg, BD, Kosel, M, Müri, RM, Berkhoff, M, Hess, CW, Fisch, HU, Schlaepfer, TE (2004). Repetitive transcranial magnetic stimulation: a putative add-on treatment for major depression in elderly patients. Psychiatry Research 126, 123–133.CrossRefGoogle ScholarPubMed
Nahas, Z, Kozel, FA, Li, X, Anderson, B, George, MS (2003). Left prefrontal transcranial magnetic stimulation (TMS) treatment of depression in bipolar affective disorder: a pilot study of acute safety and efficacy. Bipolar Disorders 5, 40–47.CrossRefGoogle ScholarPubMed
Nahas, Z, Li, X, Kozel, FA, Mirzki, D, Memon, M, Miller, K, Yamanaka, K, Anderson, B, Chae, JH, Bohning, DE, Mintzer, J, George, MS (2004). Safety and benefits of distance-adjusted prefrontal transcranial magnetic stimulation in depressed patients 55–75 years of age: a pilot study. Depression and Anxiety 19, 249–256.CrossRefGoogle ScholarPubMed
O'Reardon, JP, Solvason, HB, Janicak, PG, Sampson, S, Isenberg, KE, Nahas, Z, McDonald, WM, Avery, D, Fitzgerald, PB, Loo, C, Demitrack, MA, George, MS, Sackeim, HA (2007). Efficacy and safety of transcranial magnetic stimulation in the acute treatment of major depression: a multi-site randomized controlled trial. Biological Psychiatry 62, 1208–1216.CrossRefGoogle Scholar
Padberg, F, Moller, HJ (2003). Repetitive transcranial magnetic stimulation: does it have potential in the treatment of depression? CNS Drugs 17, 383–403.CrossRefGoogle ScholarPubMed
Padberg, F, Zwanzger, P, Keck, ME, Kathmann, N, Mikhaiel, P, Ella, R, Rupprecht, P, Thoma, H, Hampel, H, Toschi, N, Moller, HJ (2002). Repetitive transcranial magnetic stimulation (rTMS) in major depression: relation between efficacy and stimulation intensity. Neuropsychopharmacology 27, 638–645.CrossRefGoogle ScholarPubMed
Padberg, F, Zwanzger, P, Thoma, H, Kathmann, N, Haag, C, Greenberg, BD, Hampel, H, Moller, HJ (1999). Repetitive transcranial magnetic stimulation (rTMS) in pharmacotherapy-refractory major depression: comparative study of fast, slow and sham rTMS. Psychiatry Research 88, 163–171.CrossRefGoogle ScholarPubMed
Post, A, Muller, MB, Engelmann, M, Keck, ME (1999). Repetitive transcranial magnetic stimulation in rats: evidence for a neuroprotective effect in vitro and in vivo. European Journal of Neuroscience 11, 3247–3254.CrossRefGoogle ScholarPubMed
Poulet, E, Brunelin, J, Boeuve, C, Lerond, J, d'Amato, T, Dalery, J, Saoud, M (2004). Repetitive transcranial magnetic stimulation does not potentiate antidepressant treatment. European Psychiatry 19, 382–383.CrossRefGoogle Scholar
Prudic, J, Haskett, RF, Mulsant, B, Malone, KM, Pettinati, HM, Stephens, S, Greenberg, R, Rifas, SL, Sackeim, HA (1996). Resistance to antidepressant medications and short-term clinical response to ECT. American Journal of Psychiatry 153, 985–992.Google ScholarPubMed
Radziwon-Zaleska, M, Matsumoto, H, Skalski, M, Wilkowska, J, Januszko, P, Matoszko, D, Dziklinska, A, Gmaj, B, Szelenberger, W (2006). Therapeutic tricyclic antidepressant drug monitoring in younger and older depressive patients. Pharmacological Reports 58, 501–506.Google ScholarPubMed
Robinson, RG, Szetela, B (1981). Mood change following left hemispheric brain injury. Annals of Neurology 9, 447–453.CrossRefGoogle ScholarPubMed
Rosenberg, MS, Adams, DC, Gurevitch, J (2000). MetaWin. Statistical Software for Meta-Analysis. Version 2.0. Sinauer Associates: Sunderland, MA.Google Scholar
Rosenthal, R (1979). The ‘file drawer problem’ and tolerance for null effects. Psychological Bulletin 86, 638–641.CrossRefGoogle Scholar
Rosenthal, R, DiMatteo, MR (2001). Meta-analysis: recent developments in quantitative methods for literature reviews. Annual Review of Psychology 52, 59–82.CrossRefGoogle ScholarPubMed
Rossini, D, Lucca, A, Zanardi, R, Magri, L, Smeraldi, E (2005). Transcranial magnetic stimulation in treatment-resistant depressed patients: a double-blind, placebo-controlled trial. Psychiatry Research 137, 1–10.CrossRefGoogle ScholarPubMed
Roth, Y, Amir, A, Levkovitz, Y, Zangen, A (2007). Three-dimensional distribution of the electric field induced in the brain by transcranial magnetic stimulation using figure-8 and deep H-coils. Journal of Clinical Neurophysiology 24, 31–38.CrossRefGoogle ScholarPubMed
Rumi, DO, Gattaz, WF, Rigonatti, SP, Rosa, MA, Fregni, F, Rosa, MO, Mansur, C, Myczkowski, ML, Moreno, RA, Marcolin, MA (2005). Transcranial magnetic stimulation accelerates the antidepressant effect of amitriptyline in severe depression: a double-blind placebo-controlled study. Biological Psychiatry 57, 162–166.CrossRefGoogle ScholarPubMed
Sackeim, HA (1994). Continuation therapy following ECT: directions for future research. Psychopharmacological Bulletin 30, 501–521.Google ScholarPubMed
Schutter, DJLG, van Honk, J (2005 a). The cerebellum on the rise in human emotion. Cerebellum 4, 90–94.CrossRefGoogle ScholarPubMed
Schutter, DJLG, van Honk, J (2005 b). A framework for targeting alternative brain regions by repetitive transcranial magnetic stimulation (rTMS) in the treatment of depression. Journal of Psychiatry and Neuroscience 30, 91–97.Google ScholarPubMed
Schutter, DJLG, van Honk, J (2006). An electrophysiological link between the cerebellum, cognition and emotion: frontal theta EEG activity to single pulse cerebellar TMS. Neuroimage 33, 1227–1231.CrossRefGoogle ScholarPubMed
Schutter, DJLG, van Honk, J, d'Alfonso, AAL, Peper, JS, Panksepp, J (2003). High frequency rTMS over the medial cerebellum induces a shift in the prefrontal electroencephalography gamma spectrum: a pilot study in humans. Neuroscience Letters 336, 73–76.CrossRefGoogle ScholarPubMed
Szuba, MP, O'Reardon, JP, Rai, AS, Snyder-Kastenberg, J, Amsterdam, JD, Gettes, DR, Wassermann, E, Evans, DL (2001). Acute mood and thyroid stimulating hormone effects of transcranial magnetic stimulation in major depression. Biological Psychiatry 50, 22–27.CrossRefGoogle ScholarPubMed
Teneback, CC, Nahas, Z, Speer, AM, Molloy, M, Stallings, LE, Spicer, KM, Risch, SC, George, MS (1999). Changes in prefrontal cortex and paralimbic activity in depression following two weeks of daily left prefrontal TMS. Journal of Neuropsychiatry and Clinical Neuroscience 11, 426–435.Google ScholarPubMed
van Honk, J, Schutter, DJLG, Putman, P, de Haan, EHF, d'Alfonso, AAL (2003). Reductions in phenomenological, physiological and attentional indices of depressive mood after 2 Hz rTMS over the right parietal cortex in healthy human subjects. Psychiatry Research 120, 95–101.CrossRefGoogle ScholarPubMed
Wassermann, EM (1998). 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. Electroencephalography and Clinical Neurophysiology 108, 1–16.CrossRefGoogle ScholarPubMed