Advertisement

Neuropsychology Review

, Volume 26, Issue 3, pp 295–309 | Cite as

Does Therapeutic Repetitive Transcranial Magnetic Stimulation Cause Cognitive Enhancing Effects in Patients with Neuropsychiatric Conditions? A Systematic Review and Meta-Analysis of Randomised Controlled Trials

  • Donel M. Martin
  • Shawn M. McClintock
  • Jane Forster
  • Colleen K. Loo
Review

Abstract

Repetitive transcranial magnetic stimulation (rTMS) is increasingly used as a therapeutic intervention for neuropsychiatric illnesses and has demonstrated efficacy for treatment of major depression. However, an unresolved question is whether a course of rTMS treatment results in effects on cognitive functioning. In this systematic review and meta-analysis we aimed to quantitatively determine whether a course of rTMS has cognitive enhancing effects. We examined cognitive outcomes from randomised, sham-controlled studies conducted in patients with neuropsychiatric conditions where rTMS was administered to the dorsolateral prefrontal cortex (DLPFC) across repeated sessions, searched from PubMed/MEDLINE and other databases up until October 2015. Thirty studies met our inclusion criteria. Cognitive outcomes were pooled and examined across the following domains: Global cognitive function, executive function, attention, working memory, processing speed, visual memory, verbal memory and visuospatial ability. Active rTMS treatment was unassociated with generalised gains across the majority of domains of cognitive functioning examined. Secondary analyses revealed a moderate sized positive effect for improved working memory in a small number of studies in patients with schizophrenia (k = 3, g = 0.507, 95 % CI = [0.183–0.831], p < .01). Therapeutic rTMS when administered to the DLPFC in patients with neuropsychiatric conditions does not result in robust cognitive enhancing effects.

Keywords

Repetitive transcranial magnetic stimulation Cognition Neuropsychiatric Working memory Depression Schizophrenia 

Notes

Compliance with Ethical Standards

Conflict of Interest

Author Martin declares that he has no conflict of interest. Author McClintock has received research support from the NIH/NIMH (K23 MH087739) and has received honoraria for teaching from TMS Health Solutions. Author Forster declares that she has no conflict of interest. Author Loo has received equipment on loan from the Neuronetics company.

Ethical Approval

All procedures performed in studies involving human participants were in accordance with the ethical standards of the institutional and/or national research committee and with the 1964 Helsinki declaration and its later amendments or comparable ethical standards.

Informed Consent

Informed consent was obtained from all individual participants included in studies conducted by the authors.

References

  1. Avery, D. H., Claypoole, K., Robinson, L., Neumaier, J. F., Dunner, D. L., Scheele, L., et al. (1999). Repetitive transcranial magnetic stimulation in the treatment of medication-resistant depression: preliminary data. The Journal of Nervous and Mental Disease, 187(2), 114–117.PubMedCrossRefGoogle Scholar
  2. Barr, M. S., Farzan, F., Rusjan, P. M., Chen, R., Fitzgerald, P. B., & Daskalakis, Z. J. (2009). Potentiation of gamma oscillatory activity through repetitive transcranial magnetic stimulation of the dorsolateral prefrontal cortex. Neuropsychopharmacology, 34(11), 2359–2367.PubMedCrossRefGoogle Scholar
  3. Barr, M. S., Farzan, F., Rajji, T. K., Voineskos, A. N., Blumberger, D. M., Arenovich, T., et al. (2013). Can repetitive magnetic stimulation improve cognition in schizophrenia? Pilot data from a randomized controlled trial. Biological Psychiatry, 73(6), 510–517.PubMedCrossRefGoogle Scholar
  4. Berlim, M. T., Neufeld, N. H., & Van den Eynde, F. (2013a). Repetitive transcranial magnetic stimulation (rTMS) for obsessive-compulsive disorder (OCD): an exploratory meta-analysis of randomized and sham-controlled trials. Journal of Psychiatric Research, 47(8), 999–1006.PubMedCrossRefGoogle Scholar
  5. Berlim, M. T., Van den Eynde, F., & Jeff Daskalakis, Z. (2013b). Clinically meaningful efficacy and acceptability of low-frequency repetitive transcranial magnetic stimulation (rTMS) for treating primary major depression: a meta-analysis of randomized, double-blind and sham-controlled trials. Neuropsychopharmacology, 38(4), 543–551.PubMedCrossRefGoogle Scholar
  6. Berlim, M. T., van den Eynde, F., Tovar-Perdomo, S., & Daskalakis, Z. J. (2014). Response, remission and drop-out rates following high-frequency repetitive transcranial magnetic stimulation (rTMS) for treating major depression: a systematic review and meta-analysis of randomized, double-blind and sham-controlled trials. Psychological Medicine, 44(2), 225–239.PubMedCrossRefGoogle Scholar
  7. Blumberger, D. M., Mulsant, B. H., Fitzgerald, P. B., Rajji, T. K., Ravindran, A. V., Young, L. T., et al. (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(6), 423–435.PubMedCrossRefGoogle Scholar
  8. Boggio, P. S., Fregni, F., Bermpohl, F., Mansur, C. G., Rosa, M., Rumi, D. O., et al. (2005). Effect of repetitive TMS and fluoxetine on cognitive function in patients with Parkinson's disease and concurrent depression. Movement Disorders, 20(9), 1178–1184.PubMedCrossRefGoogle Scholar
  9. Boggio, P. S., Rocha, M., Oliveira, M. O., Fecteau, S., Cohen, R. B., Campanha, C., et al. (2010). Noninvasive brain stimulation with high-frequency and low-intensity repetitive transcranial magnetic stimulation treatment for posttraumatic stress disorder. The Journal of Clinical Psychiatry, 71(8), 992–999.PubMedCrossRefGoogle Scholar
  10. Brunoni, A. R., & Vanderhasselt, M. A. (2014). Working memory improvement with non-invasive brain stimulation of the dorsolateral prefrontal cortex: a systematic review and meta-analysis. Brain and Cognition, 86, 1–9.PubMedCrossRefGoogle Scholar
  11. Cabeza, R., & Nyberg, L. (2000). Imaging cognition II: An empirical review of 275 PET and fMRI studies. Journal of Cognitive Neuroscience, 12(1), 1–47.PubMedCrossRefGoogle Scholar
  12. Cappa, S. F., Sandrini, M., Rossini, P. M., Sosta, K., & Miniussi, C. (2002). The role of the left frontal lobe in action naming: rTMS evidence. Neurology, 59(5), 720–723.PubMedCrossRefGoogle Scholar
  13. Chen, C. M., Stanford, A. D., Mao, X., Abi-Dargham, A., Shungu, D. C., Lisanby, S. H., et al. (2014). GABA level, gamma oscillation, and working memory performance in schizophrenia. Neuroimage Clinic, 4, 531–539.CrossRefGoogle Scholar
  14. Coffman, B. A., Clark, V. P., & Parasuraman, R. (2014). Battery powered thought: enhancement of attention, learning, and memory in healthy adults using transcranial direct current stimulation. NeuroImage, 85(Pt 3), 895–908.PubMedCrossRefGoogle Scholar
  15. Deeks, J.J., & Higgins, J.P.T. 2010. Statistical algorithms in Review Manager 5. Retrieved from http://ims.cochrane.org/revman/documentation/Statistical-methods-in-RevMan-5.pdf
  16. Deppermann, S., Vennewald, N., Diemer, J., Sickinger, S., Haeussinger, F. B., Notzon, S., et al. (2014). Does rTMS alter neurocognitive functioning in patients with panic disorder/agoraphobia? An fNIRS-based investigation of prefrontal activation during a cognitive task and its modulation via sham-controlled rTMS. Biomed Research International, 2014, 542526.PubMedPubMedCentralCrossRefGoogle Scholar
  17. Dlabac-de Lange, J. J., Bais, L., van Es, F. D., Visser, B. G. J., Reinink, E., Bakker, B., et al. (2015a). Efficacy of bilateral repetitive transcranial magnetic stimulation for negative symptoms of schizophrenia: results of a multicenter double-blind randomized controlled trial. Psychological Medicine, 45(6), 1263–1275.PubMedCrossRefGoogle Scholar
  18. Dlabac-de Lange, J. J., Liemburg, E. J., Bais, L., Renken, R. J., Knegtering, H., & Aleman, A. (2015b). Effect of rTMS on brain activation in schizophrenia with negative symptoms: A proof-of-principle study. Schizophrenia Research, 168(1–2), 475–482.PubMedCrossRefGoogle Scholar
  19. Dougall, N., Maayan, N., Soares-Weiser, K., McDermott, L. M., & McIntosh, A. (2015). Transcranial magnetic stimulation (TMS) for schizophrenia. Cochrane Database of Systematic Reviews, 8, CD006081. doi: 10.1002/14651858.CD006081.pub2.PubMedGoogle Scholar
  20. Fitzgerald, P. B., Herring, S., Hoy, K., McQueen, S., Segrave, R., Kulkarni, J., et al. (2008). A study of the effectiveness of bilateral transcranial magnetic stimulation in the treatment of the negative symptoms of schizophrenia. Brain Stimulation, 1(1), 27–32.PubMedCrossRefGoogle Scholar
  21. Fitzgerald, P. B., Hoy, K., McQueen, S., Maller, J. J., Herring, S., Segrave, R., et al. (2009). A randomized trial of rTMS targeted with MRI based neuro-navigation in treatment-resistant depression. Neuropsychopharmacology, 34(5), 1255–1262.PubMedCrossRefGoogle Scholar
  22. Fox, M. D., Buckner, R. L., White, M. P., Greicius, M. D., & Pascual-Leone, A. (2012). Efficacy of transcranial magnetic stimulation targets for depression is related to intrinsic functional connectivity with the subgenual cingulate. Biological Psychiatry, 72(7), 595–603.PubMedPubMedCentralCrossRefGoogle Scholar
  23. Gaillard, W. D., Hertz-Pannier, L., Mott, S. H., Barnett, A. S., LeBihan, D., & Theodore, W. H. (2000). Functional anatomy of cognitive development: fMRI of verbal fluency in children and adults. Neurology, 54(1), 180–185.PubMedCrossRefGoogle Scholar
  24. George, M. S., Lisanby, S. H., Avery, D., McDonald, W. M., Durkalski, V., Pavlicova, M., et al. (2010). Daily left prefrontal transcranial magnetic stimulation therapy for major depressive disorder: a sham-controlled randomized trial. Archives of General Psychiatry, 67(5), 507–516.PubMedCrossRefGoogle Scholar
  25. Grimm, S., Beck, J., Schuepbach, D., Hell, D., Boesiger, P., Bermpohl, F., et al. (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(4), 369–376.PubMedCrossRefGoogle Scholar
  26. Guse, B., Falkai, P., Gruber, O., Whalley, H., Gibson, L., Hasan, A., et al. (2013). The effect of long-term high frequency repetitive transcranial magnetic stimulation on working memory in schizophrenia and healthy controls--a randomized placebo-controlled, double-blind fMRI study. Behavioural Brain Research, 237, 300–307.PubMedCrossRefGoogle Scholar
  27. Guse, B., Falkai, P., & Wobrock, T. (2010). Cognitive effects of high-frequency repetitive transcranial magnetic stimulation: a systematic review. Journal of Neural Transmission (Vienna), 117(1), 105–122.CrossRefGoogle Scholar
  28. Haatveit, B. C., Sundet, K., Hugdahl, K., Ueland, T., Melle, I., & Andreassen, O. A. (2010). The validity of d prime as a working memory index: Results from the “Bergen n-back task”. Journal of Clinical and Experimental Neuropsychology, 32(8), 871–880.PubMedCrossRefGoogle Scholar
  29. Harvey, P. O., Le Bastard, G., Pochon, J. B., Levy, R., Allilaire, J. F., Dubois, B., & Fossati, P. (2004). Executive functions and updating of the contents of working memory in unipolar depression. Journal of Psychiatric Research, 38(6), 567–576.PubMedCrossRefGoogle Scholar
  30. Hasan, A., Guse, B., Cordes, J., Wolwer, W., Winterer, G., Gaebel, et al. (2015). Cognitive Effects of High-Frequency rTMS in Schizophrenia Patients With Predominant Negative Symptoms: Results From a Multicenter Randomized Sham-Controlled Trial. Schizophr Bull. doi:  10.1093/schbul/sbv142
  31. Hausmann, A., Pascual-Leone, A., Kemmler, G., Rupp, C. I., Lechner-Schoner, T., Kramer-Reinstadler, K., et al. (2004). No deterioration of cognitive performance in an aggressive unilateral and bilateral antidepressant rTMS add-on trial. The Journal of Clinical Psychiatry, 65(6), 772–782.PubMedCrossRefGoogle Scholar
  32. Herbsman, T., Avery, D., Ramsey, D., Holtzheimer, P., Wadjik, C., Hardaway, F., et al. (2009). More lateral and anterior prefrontal coil location is associated with better repetitive transcranial magnetic stimulation antidepressant response. Biological Psychiatry, 66(5), 509–515.PubMedCrossRefGoogle Scholar
  33. Higgins, J. P., Altman, D. G., Gotzsche, P. C., Juni, P., Moher, D., Oxman, A. D., et al. (2011). The Cochrane Collaboration's tool for assessing risk of bias in randomised trials. BMJ, 343, d5928.PubMedPubMedCentralCrossRefGoogle Scholar
  34. Higgins, J. P. T., & Green, S. (2008). Assessing risk of bias in included studies. In J. P. T. Higgins & S. Green (Eds.), Cochrane Handbook for Systematic Reviews of Interventions (pp. 197–241). Chichester (UK): John Wiley & Sons.CrossRefGoogle Scholar
  35. Holtzheimer 3rd, P. E., Russo, J., Claypoole, K. H., Roy-Byrne, P., & Avery, D. H. (2004). Shorter duration of depressive episode may predict response to repetitive transcranial magnetic stimulation. Depression and Anxiety, 19(1), 24–30.PubMedCrossRefGoogle Scholar
  36. Hoy, K. E., Bailey, N., Michael, M., Fitzgibbon, B., Rogasch, N. C., Saeki, T., et al. (2015). Enhancement of Working Memory and Task-Related Oscillatory Activity Following Intermittent Theta Burst Stimulation in Healthy Controls. Cerebral Cortex. doi: 10.1093/cercor/bhv193.Google Scholar
  37. Hoy, K. E., Segrave, R. A., Daskalakis, Z. J., & Fitzgerald, P. B. (2012). Investigating the relationship between cognitive change and antidepressant response following rTMS: a large scale retrospective study. Brain Stimulation, 5(4), 539–546.PubMedCrossRefGoogle Scholar
  38. Huang, M. L., Luo, B. Y., Hu, J. B., Wang, S. S., Zhou, W. H., Wei, N., et al. (2012). Repetitive transcranial magnetic stimulation in combination with citalopram in young patients with first-episode major depressive disorder: a double-blind, randomized, sham-controlled trial. The Australian and New Zealand Journal of Psychiatry, 46(3), 257–264.PubMedCrossRefGoogle Scholar
  39. Johnson, K. A., Baig, M., Ramsey, D., Lisanby, S. H., Avery, D., McDonald, W. M., et al. (2013). Prefrontal rTMS for treating depression: location and intensity results from the OPT-TMS multi-site clinical trial. Brain Stimulation, 6(2), 108–117.PubMedCrossRefGoogle Scholar
  40. Jorge, R. E., Robinson, R. G., Tateno, A., Narushima, K., Acion, L., Moser, D., et al. (2004). Repetitive transcranial magnetic stimulation as treatment of poststroke depression: a preliminary study. Biological Psychiatry, 55(4), 398–405.PubMedCrossRefGoogle Scholar
  41. Khundakar, A., Morris, C., Oakley, A., McMeekin, W., & Thomas, A. J. (2009). Morphometric analysis of neuronal and glial cell pathology in the dorsolateral prefrontal cortex in late-life depression. The British Journal of Psychiatry, 195(2), 163–169.PubMedCrossRefGoogle Scholar
  42. Klimesch, W., Sauseng, P., & Gerloff, C. (2003). Enhancing cognitive performance with repetitive transcranial magnetic stimulation at human individual alpha frequency. The European Journal of Neuroscience, 17(5), 1129–1133.PubMedCrossRefGoogle Scholar
  43. Kolbinger, H., Koflich, G., Hufnagel, A., Moller, H., & Kasper, S. (1995). Transcranial magnetic stimulation (TMS) in treatment of major depression: A pilot study. Human Psychopharmacology, 10, 305–310.CrossRefGoogle Scholar
  44. Lan, M. J., Chhetry, B. T., Liston, C., Mann, J. J., & Dubin, M. (2016). Transcranial Magnetic Stimulation of Left Dorsolateral Prefrontal Cortex Induces Brain Morphological Changes in Regions Associated with a Treatment Resistant Major Depressive Episode: An Exploratory Analysis. Brain Stimul. doi: 10.1016/j.brs.2016.02.011
  45. Lefaucheur, J. P., Andre-Obadia, N., Antal, A., Ayache, S. S., Baeken, C., Benninger, D. H., et al. (2014). Evidence-based guidelines on the therapeutic use of repetitive transcranial magnetic stimulation (rTMS. Clinical Neurophysiology, 125(11), 2150–2206.PubMedCrossRefGoogle Scholar
  46. Liberati, A., Altman, D. G., Tetzlaff, J., Mulrow, C., Gotzsche, P. C., Ioannidis, J. P., et al. (2009). The PRISMA statement for reporting systematic reviews and meta-analyses of studies that evaluate healthcare interventions: explanation and elaboration. BMJ, 339, b2700.PubMedPubMedCentralCrossRefGoogle Scholar
  47. Loo, C., Sachdev, P., Elsayed, H., McDarmont, B., Mitchell, P., Wilkinson, M., et al. (2001). Effects of a 2- to 4-week course of repetitive transcranial magnetic stimulation (rTMS) on neuropsychologic functioning, electroencephalogram, and auditory threshold in depressed patients. Biological Psychiatry, 49(7), 615–623.PubMedCrossRefGoogle Scholar
  48. Loo, C. K., Mitchell, P. B., Croker, V. M., Malhi, G. S., Wen, W., Gandevia, S. C., et al. (2003a). Double-blind controlled investigation of bilateral prefrontal transcranial magnetic stimulation for the treatment of resistant major depression. Psychological Medicine, 33(1), 33–40.PubMedCrossRefGoogle Scholar
  49. Loo, C. K., Sachdev, P. S., Haindl, W., Wen, W., Mitchell, P. B., Croker, V. M., et al. (2003b). High (15 Hz) and low (1 Hz) frequency transcranial magnetic stimulation have different acute effects on regional cerebral blood flow in depressed patients. Psychological Medicine, 33(6), 997–1006.PubMedCrossRefGoogle Scholar
  50. Loo, C. K., Mitchell, P. B., McFarquhar, T. F., Malhi, G. S., & Sachdev, P. S. (2007). A sham-controlled trial of the efficacy and safety of twice-daily rTMS in major depression. Psychological Medicine, 37(3), 341–349.PubMedCrossRefGoogle Scholar
  51. Luber, B., & Lisanby, S. H. (2014). Enhancement of human cognitive performance using transcranial magnetic stimulation (TMS). NeuroImage, 85(Pt 3), 961–970.PubMedCrossRefGoogle Scholar
  52. Marquand, A. F., Mourao-Miranda, J., Brammer, M. J., Cleare, A. J., & Fu, C. H. (2008). Neuroanatomy of verbal working memory as a diagnostic biomarker for depression. Neuroreport, 19(15), 1507–1511.PubMedCrossRefGoogle Scholar
  53. McDonald, W. M., Easley, K., Byrd, E. H., Holtzheimer, P., Tuohy, S., Woodard, J. L., et al. (2006). Combination rapid transcranial magnetic stimulation in treatment refractory depression. Neuropsychiatric Disease and Treatment, 2(1), 85–94.PubMedPubMedCentralGoogle Scholar
  54. Mesholam-Gately, R. I., Giuliano, A. J., Goff, K. P., Faraone, S. V., & Seidman, L. J. (2009). Neurocognition in first-episode schizophrenia: a meta-analytic review. Neuropsychology, 23(3), 315–336.PubMedCrossRefGoogle Scholar
  55. Meyer-Lindenberg, A., Miletich, R. S., Kohn, P. D., Esposito, G., Carson, R. E., Quarantelli, M., et al. (2002). Reduced prefrontal activity predicts exaggerated striatal dopaminergic function in schizophrenia. Nature Neuroscience, 5(3), 267–271.PubMedCrossRefGoogle Scholar
  56. Mogg, A., Pluck, G., Eranti, S. V., Landau, S., Purvis, R., Brown, R. G., et al. (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(3), 323–333.PubMedCrossRefGoogle Scholar
  57. Mogg, A., Purvis, R., Eranti, S., Contell, F., Taylor, J. P., Nicholson, T., et al. (2007). Repetitive transcranial magnetic stimulation for negative symptoms of schizophrenia: a randomized controlled pilot study. Schizophrenia Research, 93(1–3), 221–228.PubMedCrossRefGoogle Scholar
  58. Moser, D. J., Jorge, R. E., Manes, F., Paradiso, S., Benjamin, M. L., & Robinson, R. G. (2002). Improved executive functioning following repetitive transcranial magnetic stimulation. Neurology, 58(8), 1288–1290.PubMedCrossRefGoogle Scholar
  59. Mosimann, U. P., Schmitt, W., Greenberg, B. D., Kosel, M., Muri, R. M., Berkhoff, M., et al. (2004). Repetitive transcranial magnetic stimulation: a putative add-on treatment for major depression in elderly patients. Psychiatry Research, 126(2), 123–133.PubMedCrossRefGoogle Scholar
  60. Moll, J., de Oliveira-Souza, R., Moll, F. T., Bramati, I. E., & Andreiuolo, P. A. (2002). The cerebral correlates of set-shifting: an fMRI study of the trail making test. Arquivos de Neuro-Psiquiatria, 60(4), 900–905.PubMedCrossRefGoogle Scholar
  61. Mull, B. R., & Seyal, M. (2001). Transcranial magnetic stimulation of left prefrontal cortex impairs working memory. Clinical Neurophysiology, 112(9), 1672–1675.PubMedCrossRefGoogle Scholar
  62. Myczkowski, M. L., Dias, A. M., Luvisotto, T., Arnaut, D., Bellini, B. B., Mansur, C. G., et al. (2012). Effects of repetitive transcranial magnetic stimulation on clinical, social, and cognitive performance in postpartum depression. Neuropsychiatric Disease and Treatment, 8, 491–500.PubMedPubMedCentralCrossRefGoogle Scholar
  63. Nadeau, S. E., Bowers, D., Jones, T. L., Wu, S. S., Triggs, W. J., & Heilman, K. M. (2014). Cognitive effects of treatment of depression with repetitive transcranial magnetic stimulation. Cognitive and Behavioral Neurology, 27(2), 77–87.PubMedCrossRefGoogle Scholar
  64. Nikolin, S., Loo, C. K., Bai, S., Dokos, S., & Martin, D. M. (2015). Focalised stimulation using high definition transcranial direct current stimulation (HD-tDCS) to investigate declarative verbal learning and memory functioning. NeuroImage, 117, 11–19.PubMedCrossRefGoogle Scholar
  65. Noda, Y., Silverstein, W. K., Barr, M. S., Vila-Rodriguez, F., Downar, J., Rajji, T., et al. (2015). Neurobiological mechanisms of repetitive transcranial magnetic stimulation of the dorsolateral prefrontal cortex in depression: a systematic review. Psychological Medicine, 45, 3411–3432.PubMedCrossRefGoogle Scholar
  66. Opitz, A., Fox, M. D., Craddock, R. C., Colcombe, S., & Milham, M. P. (2015). An integrated framework for targeting functional networks via transcranial magnetic stimulation. NeuroImage. doi: 10.1016/j.neuroimage.2015.11.040.Google Scholar
  67. O’Reardon, J. P., Solvason, H. B., Janicak, P. G., Sampson, S., Isenberg, K. E., Nahas, Z., et al. (2007). Efficacy and safety of transcranial magnetic stimulation in the acute treatment of major depression: a multisite randomized controlled trial. Biological Psychiatry, 62(11), 1208–1216.Google Scholar
  68. Pal, E., Nagy, F., Aschermann, Z., Balazs, E., & Kovacs, N. (2010). The impact of left prefrontal repetitive transcranial magnetic stimulation on depression in Parkinson's disease: a randomized, double-blind, placebo-controlled study. Movement Disorders, 25(14), 2311–2317.PubMedCrossRefGoogle Scholar
  69. Ragland, J. D., Laird, A. R., Ranganath, C., Blumenfeld, R. S., Gonzales, S. M., & Glahn, D. C. (2009). Prefrontal activation deficits during episodic memory in schizophrenia. The American Journal of Psychiatry, 166(8), 863–874.PubMedPubMedCentralCrossRefGoogle Scholar
  70. Ragland, J. D., Ranganath, C., Phillips, J., Boudewyn, M. A., Kring, A. M., Lesh, T. A., et al. (2015). Cognitive control of episodic memory in schizophrenia: differential role of dorsolateral and ventrolateral prefrontal cortex. Frontiers in Human Neuroscience, 9, 604.PubMedPubMedCentralCrossRefGoogle Scholar
  71. Rimol, L. M., Hartberg, C. B., Nesvag, R., Fennema-Notestine, C., Hagler, D. J., Jr., Pung, C. J., et al. (2010). Cortical thickness and subcortical volumes in schizophrenia and bipolar disorder. Biological Psychiatry, 68(1), 41–50.Google Scholar
  72. Rollnik, J. D., Huber, T. J., Mogk, H., Siggelkow, S., Kropp, S., Dengler, R., et al. (2000). High frequency repetitive transcranial magnetic stimulation (rTMS) of the dorsolateral prefrontal cortex in schizophrenic patients. Neuroreport, 11(18), 4013–4015.PubMedCrossRefGoogle Scholar
  73. Sachdev, P. S., Loo, C. K., Mitchell, P. B., McFarquhar, T. F., & Malhi, G. S. (2007). Repetitive transcranial magnetic stimulation for the treatment of obsessive compulsive disorder: a double-blind controlled investigation. Psychological Medicine, 37(11), 1645–1649.PubMedCrossRefGoogle Scholar
  74. Schaefer, J., Giangrande, E., Weinberger, D. R., & Dickinson, D. (2013). The global cognitive impairment in schizophrenia: consistent over decades and around the world. Schizophrenia Research, 150(1), 42–50.PubMedPubMedCentralCrossRefGoogle Scholar
  75. Serafini, G., Pompili, M., Belvederi Murri, M., Respino, M., Ghio, L., Girardi, P., et al. (2015). The effects of repetitive transcranial magnetic stimulation on cognitive performance in treatment-resistant depression. A systematic review. Neuropsychobiology, 71(3), 125–139.PubMedCrossRefGoogle Scholar
  76. Vanderhasselt, M. A., De Raedt, R., Baeken, C., Leyman, L., & D'Haenen, H. (2006). The influence of rTMS over the left dorsolateral prefrontal cortex on Stroop task performance. Experimental Brain Research, 169(2), 279–282.PubMedCrossRefGoogle Scholar
  77. Wajdik, C., Claypoole, K. H., Fawaz, W., Holtzheimer, P. E., 3rd, Neumaier, J., Dunner, D. L., et al. (2014). No change in neuropsychological functioning after receiving repetitive transcranial magnetic stimulation treatment for major depression. The Journal of ECT, 30(4), 320–324.Google Scholar
  78. Watts, B. V., Landon, B., Groft, A., & Young-Xu, Y. (2012). A sham controlled study of repetitive transcranial magnetic stimulation for posttraumatic stress disorder. Brain Stimulation, 5(1), 38–43.PubMedCrossRefGoogle Scholar
  79. Weickert, T. W., Goldberg, T. E., Callicott, J. H., Chen, Q., Apud, J. A., Das, S., et al. (2009). Neural correlates of probabilistic category learning in patients with schizophrenia. The Journal of Neuroscience, 29(4), 1244–1254.PubMedPubMedCentralCrossRefGoogle Scholar
  80. Wobrock, T., Guse, B., Cordes, J., Wolwer, W., Winterer, G., Gaebel, W., et al. (2015). Left prefrontal high-frequency repetitive transcranial magnetic stimulation for the treatment of schizophrenia with predominant negative symptoms: a sham-controlled, randomized multicenter trial. Biological Psychiatry, 77(11), 979–988.PubMedCrossRefGoogle Scholar
  81. Yeo, B. T., Krienen, F. M., Sepulcre, J., Sabuncu, M. R., Lashkari, D., Hollinshead, M., et al. (2011). The organization of the human cerebral cortex estimated by intrinsic functional connectivity. Journal of Neurophysiology, 106(3), 1125–1165.PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2016

Authors and Affiliations

  • Donel M. Martin
    • 1
    • 2
  • Shawn M. McClintock
    • 3
    • 4
  • Jane Forster
    • 1
  • Colleen K. Loo
    • 2
  1. 1.School of PsychiatryUniversity of New South WalesSydneyAustralia
  2. 2.Black Dog InstituteSydneyAustralia
  3. 3.Neurocognitive Research Laboratory, Department of PsychiatryUniversity of Texas Southwestern Medical CenterDallasUSA
  4. 4.Department of Psychiatry and Behavioral SciencesDuke University School of MedicineDurhamUSA

Personalised recommendations