Transcranial magnetic stimulation: A neuroscientific probe of cortical function in schizophrenia

Biological Psychiatry

Volumn 70, Issue 1, 2011, Pages 19-27

  McClintock, Shawn M ^a,b   Freitas, Catarina ^c   Oberman, Lindsay ^c   Lisanby, Sarah H ^d   Pascual Leone, Alvaro ^c,e,f  

^a UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

^b NEW YORK STATE PSYCHIATRIC INSTITUTE   (United States)

^c HARVARD MEDICAL SCHOOL   (United States)

^d DUKE UNIVERSITY MEDICAL CENTER   (United States)

^e University Institute affiliated with the Autonomous University of Barcelona   (Spain)

^f BETH ISRAEL DEACONESS MEDICAL CENTER   (United States)

Author keywords

Biological marker; Cognitive Neuroscience Treatment Research to Improve Cognition in Schizophrenia (CNTRICS); cortical function; schizophrenia; TMS; transcranial magnetic stimulation

Indexed keywords

BIOLOGICAL MARKER;

AGING; ARTICLE; BRAIN CORTEX; BRAIN DEPTH STIMULATION; BRAIN FUNCTION; ELECTROENCEPHALOGRAPHY; ELECTROPHYSIOLOGY; FUNCTIONAL MAGNETIC RESONANCE IMAGING; HUMAN; MAGNETOENCEPHALOGRAPHY; NEAR INFRARED SPECTROSCOPY; NERVE CELL DIFFERENTIATION; NERVE CELL PLASTICITY; NEUROIMAGING; NEUROPHYSIOLOGY; NUCLEAR MAGNETIC RESONANCE IMAGING; PAIRED ASSOCIATIVE STIMULATION; PRIORITY JOURNAL; SCHIZOPHRENIA; SINGLE PHOTON EMISSION COMPUTER TOMOGRAPHY; TRANSCRANIAL MAGNETIC STIMULATION;

EID: 79958857265     PISSN: 00063223     EISSN: 18732402     Source Type: Journal    
DOI: 10.1016/j.biopsych.2011.02.031     Document Type: Review

References (83)

1. S.H. Lisanby, B. Luber, T. Perera, and H.A. Sackeim Transcranial magnetic stimulation: Applications in basic neuroscience and neuropsychopharmacology Int J Neuropsychopharmacol 3 2000 259 273
2. A. Pascual-Leone Disrupting the brain to guide plasticity and improve behavior Prog Brain Res 157 2006 315 329
3. T. Wagner, A. Valero-Cabre, and A. Pascual-Leone Noninvasive human brain stimulation Annu Rev Biomed Eng 9 2007 527 565 (Pubitemid 350246667)
4. Carter CS, Barch DM, Bullmore E, the CNTRICS Executive Committee (in press): Cognitive Neuroscience Treatment Research to Improve Cognition (CNTRICS) II: Developing Imaging biomarkers to Enhance Treatment Development for Schizophrenia and Related Disorders. Biol Psychiatry.
5. C.S. Carter, D.M. Barch, R.W. Buchanan, E. Bullmore, J.H. Krystal, and J. Cohen Identifying cognitive mechanisms targeted for treatment development in schizophrenia: An overview of the first meeting of the Cognitive Neuroscience Treatment Research to Improve Cognition in Schizophrenia Initiative Biol Psychiatry 64 2008 4 10
6. C.S. Carter, and D.M. Barch Cognitive neuroscience-based approaches to measuring and improving treatment effects on cognition in schizophrenia: The CNTRICS initiative Schizophr Bull 33 2007 1131 1137 (Pubitemid 47347921)
7. R.E. Hoffman, N.N. Boutros, R.M. Berman, E. Roessler, A. Belger, and J.H. Krystal Transcranial magnetic stimulation of left temporoparietal cortex in three patients reporting hallucinated "voices" Biol Psychiatry 46 1999 130 132 (Pubitemid 29296826)
8. E. Cohen, M. Bernardo, J. Masana, F.J. Arrufat, V. Navarro, and S. Valls Repetitive transcranial magnetic stimulation in the treatment of chronic negative schizophrenia: A pilot study J Neurol Neurosurg, Psychiatry 67 1999 129 130 (Pubitemid 29278354)
9. A. Aleman, I.E. Sommer, and R.S. Kahn Efficacy of slow repetitive transcranial magnetic stimulation in the treatment of resistant auditory hallucinations in schizophrenia: A meta-analysis J Clin Psychiatry 68 2007 416 421 (Pubitemid 46506807)
10. C. Freitas, F. Fregni, and A. Pascual-Leone Meta-analysis of the effects of repetitive transcranial magnetic stimulation (rTMS) on negative and positive symptoms in schizophrenia Schizophr Res 108 2009 11 24
11. J.J. Dlabac-de Lange, R. Knegtering, and A. Aleman Repetitive transcranial magnetic stimulation for negative symptoms of schizophrenia: Review and meta-analysis J Clin Psychiatry 71 2010 411 418
12. A.D. Stanford, Z. Sharif, C. Corcoran, N. Urban, D. Malaspina, and S.H. Lisanby rTMS strategies for the study and treatment of schizophrenia: A review Int J Neuropsychopharmacol 11 2008 563 576 (Pubitemid 351744807)
13. F.A. Kozel, F. Tian, S. Dhamne, P.E. Croarkin, S.M. McClintock, and A. Elliott Using simultaneous repetitive Transcranial Magnetic Stimulation/ functional Near Infrared Spectroscopy (rTMS/fNIRS) to measure brain activation and connectivity Neuroimage 47 2009 1177 1184
14. S. Rossi, M. Hallett, P.M. Rossini, A. Pascual-Leone Safety of TMS Consensus Group Safety, ethical considerations, and application guidelines for the use of transcranial magnetic stimulation in clinical practice and research Clin Neurophysiol 120 2009 2008 2039
15. G. Thut, J.R. Ives, F. Kampmann, M.A. Pastor, and A. Pascual-Leone A new device and protocol for combining TMS and online recordings of EEG and evoked potentials J Neurosci Methods 141 2005 207 217 (Pubitemid 40126659)
16. J.R. Ives, A. Rotenberg, R. Poma, G. Thut, and A. Pascual-Leone Electroencephalographic recording during transcranial magnetic stimulation in humans and animals Clin Neurophysiol 117 2006 1870 1875 (Pubitemid 44094253)
17. G. Thut, and A. Pascual-Leone Integrating TMS with EEG: How and what for? Brain Topogr 22 2010 215 218
18. S. Komssi, S. Kahkonen, and R.J. Ilmoniemi The effect of stimulus intensity on brain responses evoked by transcranial magnetic stimulation Hum Brain Mapp 21 2004 154 164 (Pubitemid 38295899)
19. Z.J. Daskalakis, F. Farzan, M.S. Barr, J.J. Maller, R. Chen, and P.B. Fitzgerald Long-interval cortical inhibition from the dorsolateral prefrontal cortex: A TMS-EEG study Neuropsychopharmacology 33 2008 2860 2869
20. G. Thut, and A. Pascual-Leone A review of combined TMS-EEG studies to characterize lasting effects of repetitive TMS and assess their usefulness in cognitive and clinical neuroscience Brain Topogr 22 2010 219 232
21. E.A. Allen, B.N. Pasley, T. Duong, and R.D. Freeman Transcranial magnetic stimulation elicits coupled neural and hemodynamic consequences Science 317 2007 1918 1921 (Pubitemid 47509436)
22. M. Kobayashi, and A. Pascual-Leone Transcranial magnetic stimulation in neurology Lancet Neurol 2 2003 145 156 (Pubitemid 37443319)
23. P. Eichhammer, R. Wiegand, A. Kharraz, B. Langguth, H. Binder, and G. Hajak Cortical excitability in neuroleptic-naive first-episode schizophrenic patients Schizophr Res 67 2004 253 259 (Pubitemid 38251456)
24. N.J. Davey, B.K. Puri, H.S. Lewis, S.W. Lewis, and P.H. Ellaway Effects of antipsychotic medication on electromyographic responses to transcranial magnetic stimulation of the motor cortex in schizophrenia J Neurol Neurosurg, Psychiatry 63 1997 468 473 (Pubitemid 27423553)
25. U. Ziemann Pharmacology of TMS measures Z.U. Wassermann Em, V. Walsh, T. Paus, S. Lisanby, The Oxford Handbook of Transcranial Stimulation 2008 Oxford University Press New York 135 151
26. S.K. Liu, P.B. Fitzgerald, M. Daigle, R. Chen, and Z.J. Daskalakis The relationship between cortical inhibition, antipsychotic treatment, and the symptoms of schizophrenia Biol Psychiatry 65 2009 503 509
27. T. Wobrock, T. Schneider-Axmann, W. Retz, M. Rosler, D. Kadovic, and P. Falkai Motor circuit abnormalities in first-episode schizophrenia assessed with transcranial magnetic stimulation Pharmacopsychiatry 42 2009 194 201
28. P. Eichhammer, B. Langguth, M. Zowe, T. Kleinjung, P. Jacob, and P. Sand GABA-B-associated neuropsychiatric disorders Psychiatr Prax 31 suppl 1 2004 S44 S46
29. J. Classen, J. Liepert, S.P. Wise, M. Hallett, and L.G. Cohen Rapid plasticity of human cortical movement representation induced by practice J Neurophysiol 79 1998 1117 1123 (Pubitemid 28095925)
30. Z.J. Daskalakis, B.K. Christensen, P.B. Fitzgerald, and R. Chen Dysfunctional neural plasticity in patients with schizophrenia Arch Gen Psychiatry 65 2008 378 385 (Pubitemid 351519887)
31. A.N. Voineskos, F. Farzan, M.S. Barr, N.J. Lobaugh, B.H. Mulsant, and R. Chen The role of the corpus callosum in transcranial magnetic stimulation induced interhemispheric signal propagation Biol Psychiatry 68 2010 825 831
32. J. Driver, F. Blankenburg, S. Bestmann, and C.C. Ruff New approaches to the study of human brain networks underlying spatial attention and related processes Exp Brain Res 206 2010 153 162
33. F. Ferrarelli, M. Massimini, M.J. Peterson, B.A. Riedner, M. Lazar, and M.J. Murphy Reduced evoked gamma oscillations in the frontal cortex in schizophrenia patients: A TMS/EEG study Am J Psychiatry 165 2008 996 1005
34. D.C. Goff, and J.T. Coyle The emerging role of glutamate in the pathophysiology and treatment of schizophrenia Am J Psychiatry 158 2001 1367 1377 (Pubitemid 32847232)
35. T.U. Woo, K. Spencer, and R.W. McCarley Gamma oscillation deficits and the onset and early progression of schizophrenia Harv Rev Psychiatry 18 2010 173 189
36. D.A. Lewis, T. Hashimoto, and D.W. Volk Cortical inhibitory neurons and schizophrenia Nat Rev Neurosci 6 2005 312 324 (Pubitemid 40469985)
37. G. Gonzalez-Burgos, T. Hashimoto, and D.A. Lewis Alterations of cortical GABA neurons and network oscillations in schizophrenia Curr Psychiatry Rep 12 2010 335 344
38. P.J. Uhlhaas, and W. Singer Abnormal neural oscillations and synchrony in schizophrenia Nat Rev Neurosci 11 2010 100 113
39. H.R. Siebner, T.O. Bergmann, S. Bestmann, M. Massimini, H. Johansen-Berg, and H. Mochizuki Consensus paper: Combining transcranial stimulation with neuroimaging Brain Stimul 2 2009 58 80
40. C.C. Ruff, J. Driver, and S. Bestmann Combining TMS and fMRI: "virtual lesions" to functional-network accounts of cognition Cortex 45 2009 1043 1049
41. F. Ferreri, P. Pasqualetti, S. Maatta, D. Ponzo, F. Ferrarelli, and G. Tononi Human brain connectivity during single and paired pulse transcranial magnetic stimulation Neuroimage 54 2011 90 102
42. T. Kujirai, M.D. Caramia, J.C. Rothwell, B.L. Day, P.D. Thompson, and A. Ferbert Corticocortical inhibition in human motor cortex J Physiol 471 1993 501 519 (Pubitemid 23345592)
43. J. Valls-Sole, A. Pascual-Leone, E.M. Wassermann, and M. Hallett Human motor evoked responses to paired transcranial magnetic stimuli Electroencephalogr Clin Neurophysiol 85 1992 355 364 (Pubitemid 23011246)
44. U. Ziemann, R. Chen, L.G. Cohen, and M. Hallett Dextromethorphan decreases the excitability of the human motor cortex Neurology 51 1998 1320 1324 (Pubitemid 28520551)
45. C. Nauczyciel, P. Hellier, X. Morandi, S. Blestel, D. Drapier, and J.C. Ferre Assessment of standard coil positioning in transcranial magnetic stimulation in depression Psychiatry Res 186 2011 232 238
46. Z.J. Daskalakis, B.K. Christensen, R. Chen, P.B. Fitzgerald, R.B. Zipursky, and S. Kapur Evidence for impaired cortical inhibition in schizophrenia using transcranial magnetic stimulation Arch Gen Psychiatry 59 2002 347 354 (Pubitemid 34275253)
47. P.B. Fitzgerald, T.L. Brown, Z.J. Daskalakis, and J. Kulkarni A transcranial magnetic stimulation study of inhibitory deficits in the motor cortex in patients with schizophrenia Psychiatry Res 114 2002 11 22 (Pubitemid 34178343)
48. P.B. Fitzgerald, T.L. Brown, N.A. Marston, T.J. Oxley, A. de Castella, and Z.J. Daskalakis A transcranial magnetic stimulation study of abnormal cortical inhibition in schizophrenia Psychiatry Res 118 2003 197 207 (Pubitemid 36776648)
49. T. Wobrock, M. Schneider, D. Kadovic, T. Schneider-Axmann, U.K. Ecker, and W. Retz Reduced cortical inhibition in first-episode schizophrenia Schizophr Res 105 2008 252 261
50. Z.J. Daskalakis, B.K. Christensen, P.B. Fitzgerald, S.I. Fountain, and R. Chen Reduced cerebellar inhibition in schizophrenia: A preliminary study Am J Psychiatry 162 2005 1203 1205 (Pubitemid 40770706)
51. P.B. Fitzgerald, T.L. Brown, Z.J. Daskalakis, and J. Kulkarni A transcranial magnetic stimulation study of the effects of olanzapine and risperidone on motor cortical excitability in patients with schizophrenia Psychopharmacol Berl 162 2002 74 81 (Pubitemid 34639560)
52. Z.J. Daskalakis, B.K. Christensen, R. Chen, P.B. Fitzgerald, R.B. Zipursky, and S. Kapur Effect of antipsychotics on cortical inhibition using transcranial magnetic stimulation Psychopharmacol Berl 170 2003 255 262 (Pubitemid 37491604)
53. G. Koch, M. Ribolsi, F. Mori, L. Sacchetti, C. Codeca, and I.A. Rubino Connectivity between posterior parietal cortex and ipsilateral motor cortex is altered in schizophrenia Biol Psychiatry 64 2008 815 819
54. K.E. Hoy, N. Georgiou-Karistianis, R. Laycock, and P.B. Fitzgerald A transcranial magnetic stimulation study of transcallosal inhibition and facilitation in schizophrenia J Clin Neurosci 15 2008 863 867
55. M.C. Saka, E.C. Atbasoglu, H.D. Ozguven, H.O. Sener, and E. Ozay Cortical inhibition in first-degree relatives of schizophrenic patients assessed with transcranial magnetic stimulation Int J Neuropsychopharmacol 8 2005 595 599 (Pubitemid 41400890)
56. P.B. Fitzgerald, T.L. Brown, Z.J. Daskalakis, A. deCastella, and J. Kulkarni A study of transcallosal inhibition in schizophrenia using transcranial magnetic stimulation Schizophr Res 56 2002 199 209 (Pubitemid 34628811)
57. F. Farzan, M.S. Barr, A.J. Levinson, R. Chen, W. Wong, and P.B. Fitzgerald Evidence for gamma inhibition deficits in the dorsolateral prefrontal cortex of patients with schizophrenia Brain 133 2010 1505 1514
58. K. Stefan, E. Kunesch, L.G. Cohen, R. Benecke, and J. Classen Induction of plasticity in the human motor cortex by paired associative stimulation Brain 123 2000 572 584 (Pubitemid 30099541)
59. A. Wolters, F. Sandbrink, A. Schlottmann, E. Kunesch, K. Stefan, and L.G. Cohen A temporally asymmetric Hebbian rule governing plasticity in the human motor cortex J Neurophysiol 89 2003 2339 2345 (Pubitemid 36570197)
60. M.V. Frantseva, P.B. Fitzgerald, R. Chen, B. Moller, M. Daigle, and Z.J. Daskalakis Evidence for impaired long-term potentiation in schizophrenia and its relationship to motor skill learning Cereb Cortex 18 2008 990 996
61. R. Chen, and K. Udupa Measurement and modulation of plasticity of the motor system in humans using transcranial magnetic stimulation Mot Control 13 2009 442 453
62. P.B. Fitzgerald, T.L. Brown, N.A. Marston, T. Oxley, A. De Castella, and Z.J. Daskalakis Reduced plastic brain responses in schizophrenia: A transcranial magnetic stimulation study Schizophr Res 71 2004 17 26 (Pubitemid 39209471)
63. M.S. Barr, F. Farzan, P.M. Rusjan, R. Chen, P.B. Fitzgerald, and Z.J. Daskalakis Potentiation of gamma oscillatory activity through repetitive transcranial magnetic stimulation of the dorsolateral prefrontal cortex Neuropsychopharmacology 34 2009 2359 2367
64. D.A. Cohen, C. Freitas, J.M. Tormos, L. Oberman, M. Eldaief, and A. Pascual-Leone Enhancing plasticity through repeated rTMS sessions: The benefits of a night of sleep Clin Neurophysiol 121 2010 2159 2164
65. C. Plewnia, A.J. Rilk, S.R. Soekadar, C. Arfeller, H.S. Huber, and P. Sauseng Enhancement of long-range EEG coherence by synchronous bifocal transcranial magnetic stimulation Eur J Neurosci 27 2008 1577 1583 (Pubitemid 351406280)
66. M. Mittrach, J. Thunker, G. Winterer, M.W. Agelink, G. Regenbrecht, and M. Arends The tolerability of rTMS treatment in schizophrenia with respect to cognitive function Pharmacopsychiatry 43 2010 110 117
67. U. Ziemann, W. Paulus, M.A. Nitsche, A. Pascual-Leone, W.D. Byblow, and A. Berardelli Consensus: Motor cortex plasticity protocols Brain Stimul 1 2008 164 182
68. Y.Z. Huang, M.J. Edwards, E. Rounis, K.P. Bhatia, and J.C. Rothwell Theta burst stimulation of the human motor cortex Neuron 45 2005 201 206 (Pubitemid 40128115)
69. L. Cardenas-Morales, D.A. Nowak, T. Kammer, R.C. Wolf, and C. Schonfeldt-Lecuona Mechanisms and applications of theta-burst rTMS on the human motor cortex Brain Topogr 22 2010 294 306
70. Y.Z. Huang, R.S. Chen, J.C. Rothwell, and H.Y. Wen The after-effect of human theta burst stimulation is NMDA receptor dependent Clin Neurophysiol 118 2007 1028 1032 (Pubitemid 46518301)
71. C.J. Stagg, M. Wylezinska, P.M. Matthews, H. Johansen-Berg, P. Jezzard, and J.C. Rothwell Neurochemical effects of theta burst stimulation as assessed by magnetic resonance spectroscopy J Neurophysiol 101 2009 2872 2877
72. A. Demirtas-Tatlidede, C. Freitas, J.R. Cromer, L. Safar, D. Ongur, and W.S. Stone Safety and proof of principle study of cerebellar vermal theta burst stimulation in refractory schizophrenia Schizophr Res 124 2010 91 100
73. E. Poulet, J. Brunelin, W. Ben Makhlouf, T. D'Amato, and M. Saoud A case report of cTBS for the treatment of auditory hallucinations in a patient with schizophrenia Brain Stimul 2 2009 118 119
74. D. Sidhoumi, S. Braha, N. Bouaziz, J. Brunelin, R. Benadhira, and D. Januel Evaluation of the therapeutic effect of theta burst stimulation on drug-resistant auditory hallucinations in a schizophrenic patient and its impact on cognitive function and neuronal excitability: A case study Clin Neurophysiol 121 2010 802
75. M.C. Eberle, D. Wildgruber, B. Wasserka, A.J. Fallgatter, and C. Plewnia Relief from chronic intractable auditory hallucinations after long-term bilateral theta burst stimulation Am J Psychiatry 167 2010 1410
76. A. Benali, J. Trippe, E. Weiler, A. Mix, E. Petrasch-Parwez, and W. Girzalsky Theta-burst transcranial magnetic stimulation alters cortical inhibition J Neurosci 31 2011 1193 1203
77. J. Trippe, A. Mix, S. Aydin-Abidin, K. Funke, and A. Benali Theta burst and conventional low-frequency rTMS differentially affect GABAergic neurotransmission in the rat cortex Experiment Brain Res 2009 [published online ahead of print Aug 22]
78. R.I. Mesholam-Gately, A.J. Giuliano, K.P. Goff, S.V. Faraone, and L.J. Seidman Neurocognition in first-episode schizophrenia: A meta-analytic review Neuropsychology 23 2009 315 336
79. K.A. Woodberry, A.J. Giuliano, and L.J. Seidman Premorbid IQ in schizophrenia: A meta-analytic review Am J Psychiatry 165 2008 579 587 (Pubitemid 351705334)
80. P.S. Goldman-Rakic The physiological approach: Functional architecture of working memory and disordered cognition in schizophrenia Biol Psychiatry 46 1999 650 661 (Pubitemid 29401861)
81. A. Aleman, R. Hijman, E.H. de Haan, and R.S. Kahn Memory impairment in schizophrenia: A meta-analysis Am J Psychiatry 156 1999 1358 1366 (Pubitemid 29416531)
82. M.M. Sitskoorn, A. Aleman, S.J. Ebisch, M.C. Appels, and R.S. Kahn Cognitive deficits in relatives of patients with schizophrenia: A meta-analysis Schizophr Res 71 2004 285 295 (Pubitemid 39330506)
83. D.L. Braff, T.A. Greenwood, N.R. Swerdlow, G.A. Light, and N.J. Schork Advances in endophenotyping schizophrenia World Psychiatry 7 2008 11 18 (Pubitemid 351338180)