Modulating neural plasticity with non-invasive brain stimulation in schizophrenia

European Archives of Psychiatry and Clinical Neuroscience

Volumn 263, Issue 8, 2013, Pages 621-631

  Hasan, Alkomiet ^a   Wobrock, Thomas ^b,c   Rajji, Tarek ^d   Malchow, Berend ^a   Daskalakis, Zafiris J ^d  

^a LUDWIG MAXIMILIANS UNIVERSITY   (Germany)

^b Darmstadt Dieburg Clinics   (Germany)

^c UNIVERSITY OF GÖTTINGEN   (Germany)

^d UNIVERSITY OF TORONTO   (Canada)

Author keywords

Plasticity; Schizophrenia; tDCS; TMS

Indexed keywords

4 AMINOBUTYRIC ACID RECEPTOR; ALCOHOL; CALBINDIN; CANNABIS; DEXTROMETHORPHAN; DOPAMINE 2 RECEPTOR; GLUTAMATE DECARBOXYLASE 67; LORAZEPAM; N METHYL DEXTRO ASPARTIC ACID; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; NICOTINE; PARVALBUMIN;

BRAIN DEPTH STIMULATION; CALCIUM HOMEOSTASIS; CEREBROVASCULAR ACCIDENT; COGNITION; COGNITIVE THERAPY; DEPRESSION; HUMAN; INTERMETHOD COMPARISON; KINESIOTHERAPY; MAGNETIC STIMULATION; MAINTENANCE THERAPY; MOTOR PERFORMANCE; NEGATIVE SYNDROME; NERVE CELL PLASTICITY; NERVE EXCITABILITY; NERVE STIMULATION; PAIRED ASSOCIATIVE STIMULATION; PARKINSON DISEASE; POSITIVE SYNDROME; PRIORITY JOURNAL; PSYCHOTHERAPY; REVIEW; SCHIZOPHRENIA; SUBSTANCE ABUSE; TRANSCRANIAL DIRECT CURRENT STIMULATION; TRANSCRANIAL MAGNETIC STIMULATION; TREATMENT DURATION; USE DEPENDENT PLASTICITY STIMULATION;

DEEP BRAIN STIMULATION; HUMANS; NEURONAL PLASTICITY; SCHIZOPHRENIA;

EID: 84889563380     PISSN: 09401334     EISSN: 14338491     Source Type: Journal    
DOI: 10.1007/s00406-013-0446-8     Document Type: Review

References (104)

1. Abraham WC (2008) Metaplasticity: tuning synapses and networks for plasticity. Nat Rev Neurosci 9:387
2. Andrade C (2013) Once- to Twice-Daily, 3-Year Domiciliary Maintenance Transcranial Direct Current Stimulation for Severe, Disabling. Clozapine-Refractory Continuous Auditory Hallucinations in Schizophrenia, J ECT
3. Andreasen NC, Nopoulos P, Magnotta V, Pierson R, Ziebell S, Ho BC (2011) Progressive brain change in schizophrenia: a prospective longitudinal study of first-episode schizophrenia. Biol Psychiatry 70:672-679
4. Antal A, Chaieb L, Moliadze V, Monte-Silva K, Poreisz C, Thirugnanasambandam N, Nitsche MA, Shoukier M, Ludwig H, Paulus W (2010) Brain-derived neurotrophic factor (BDNF) gene polymorphisms shape cortical plasticity in humans. Brain Stimul 3:230-237
5. Balu DT, Coyle JT (2011) Neuroplasticity signaling pathways linked to the pathophysiology of schizophrenia. Neurosci Biobehav Rev 35:848-870
6. Barr MS, Farzan F, Rajji TK, Voineskos AN, Blumberger DM, Arenovich T, Fitzgerald PB, Daskalakis ZJ (2012) Can repetitive magnetic stimulation improve cognition in schizophrenia? Pilot data from a randomized controlled trial. Biol Psychiatry
7. Batsikadze G, Paulus W, Kuo MF, Nitsche MA (2013) Effect of serotonin on paired associative stimulation-induced plasticity in the human motor cortex. Neuropsychopharmacology
8. Benes FM (1998) Model generation and testing to probe neural circuitry in the cingulate cortex of postmortem schizophrenic brain. Schizophr Bull 24:219-230
9. Benes FM (2011) Regulation of cell cycle and DNA repair in post-mitotic GABA neurons in psychotic disorders. Neuropharmacology 60:1232-1242
10. Benes FM, Lim B, Matzilevich D, Walsh JP, Subburaju S, Minns M (2007) Regulation of the GABA cell phenotype in hippocampus of schizophrenics and bipolars. Proc Natl Acad Sci USA 104:10164-10169
11. Benes FM, McSparren J, Bird ED, SanGiovanni JP, Vincent SL (1991) Deficits in small interneurons in prefrontal and cingulate cortices of schizophrenic and schizoaffective patients. Arch Gen Psychiatry 48:996-1001
12. Brunelin J, Mondino M, Gassab L, Haesebaert F, Gaha L, Suaud-Chagny MF, Saoud M, Mechri A, Poulet E (2012) Examining transcranial direct-current stimulation (tDCS) as a treatment for hallucinations in schizophrenia. Am J Psychiatry 169:719-724
13. Brunelin J, Mondino M, Haesebaert F, Saoud M, Suaud-Chagny MF, Poulet E (2012) Efficacy and safety of bifocal tDCS as an interventional treatment for refractory schizophrenia. Brain Stimul 5:431-432
14. Buchanan RW, Kreyenbuhl J, Kelly DL, Noel JM, Boggs DL, Fischer BA, Himelhoch S, Fang B, Peterson E, Aquino PR, Keller W (2010) The 2009 schizophrenia PORT psychopharmacological treatment recommendations and summary statements. Schizophr Bull 36:71-93
15. Buckley PF, Pillai A, Howell KR (2011) Brain-derived neurotrophic factor: findings in schizophrenia. Curr Opin Psychiatry 24:122-127
16. Butefisch CM, Davis BC, Wise SP, Sawaki L, Kopylev L, Classen J, Cohen LG (2000) Mechanisms of use-dependent plasticity in the human motor cortex. Proc Natl Acad Sci USA 97:3661-3665
17. Caroni P, Donato F, Muller D (2010) Structural plasticity upon learning: regulation and functions. Nat Rev Neurosci 13:478-490
18. Cheeran B, Talelli P, Mori F, Koch G, Suppa A, Edwards M, Houlden H, Bhatia K, Greenwood R, Rothwell JC (2008) A common polymorphism in the brain-derived neurotrophic factor gene (BDNF) modulates human cortical plasticity and the response to rTMS. J Physiol 586:5717-5725
19. Classen J, Liepert J, Wise SP, Hallett M, Cohen LG (1998) Rapid plasticity of human cortical movement representation induced by practice. J Neurophysiol 79:1117-1123
20. Corlett PR, Honey GD, Krystal JH, Fletcher PC (2011) Glutamatergic model psychoses: prediction error, learning, and inference. Neuropsychopharmacology 36:294-315
21. Coyle JT (2006) Glutamate and schizophrenia: beyond the dopamine hypothesis. Cell Mol Neurobiol 26:365-384
22. Creutzfeldt OD, Fromm GH, Kapp H (1962) Influence of transcortical d-c currents on cortical neuronal activity. Exp Neurol 5:436-452
23. Daskalakis ZJ, Christensen BK, Fitzgerald PB, Chen R (2008) Dysfunctional neural plasticity in patients with schizophrenia. Arch Gen Psychiatry 65:378-385
24. Daskalakis ZJ, Farzan F, Barr MS, Maller JJ, Chen R, Fitzgerald PB (2008) Long-interval cortical inhibition from the dorsolateral prefrontal cortex: a TMS-EEG study. Neuropsychopharmacology 33:2860-2869
25. Daskalakis ZJ, Moller B, Christensen BK, Fitzgerald PB, Gunraj C, Chen R (2006) The effects of repetitive transcranial magnetic stimulation on cortical inhibition in healthy human subjects. Exp Brain Res 174:403-412
26. Demirtas-Tatlidede A, Freitas C, Cromer JR, Safar L, Ongur D, Stone WS, Seidman LJ, Schmahmann JD, Pascual-Leone A (2010) Safety and proof of principle study of cerebellar vermal theta burst stimulation in refractory schizophrenia. Schizophr Res 124:91-100
27. Demirtas-Tatlidede A, Vahabzadeh-Hagh AM, Pascual-Leone A (2013) Can noninvasive brain stimulation enhance cognition in neuropsychiatric disorders? Neuropharmacology 64:566-578
28. Dlabac-de Lange JJ, Knegtering R, Aleman A (2010) Repetitive transcranial magnetic stimulation for negative symptoms of schizophrenia: review and meta-analysis. J Clin Psychiatry 71:411-418
29. Farzan F, Barr MS, Wong W, Chen R, Fitzgerald PB, Daskalakis ZJ (2009) Suppression of gamma-oscillations in the dorsolateral prefrontal cortex following long interval cortical inhibition: a TMS-EEG study. Neuropsychopharmacology 34:1543-1551
30. Ferrarelli F, Massimini M, Peterson MJ, Riedner BA, Lazar M, Murphy MJ, Huber R, Rosanova M, Alexander AL, Kalin N, Tononi G (2008) Reduced evoked gamma oscillations in the frontal cortex in schizophrenia patients: a TMS/EEG study. Am J Psychiatry 165:996-1005
31. Fitzgerald PB, Brown TL, Marston NA, Oxley T, De Castella A, Daskalakis ZJ, Kulkarni J (2004) Reduced plastic brain responses in schizophrenia: a transcranial magnetic stimulation study. Schizophr Res 71:17-26
32. Folsom TD, Hossein Fatemi S (2012) The involvement of Reelin in neurodevelopmental disorders. Neuropharmacology
33. Frantseva M, Cui J, Farzan F, Chinta LV, Perez Velazquez JL, Daskalakis ZJ (2012) Disrupted cortical conductivity in schizophrenia: TMS-EEG study. Cereb Cortex
34. Frantseva MV, Fitzgerald PB, Chen R, Moller B, Daigle M, Daskalakis ZJ (2008) Evidence for impaired long-term potentiation in schizophrenia and its relationship to motor skill learning. Cereb Cortex 18:990-996
35. Freitas C, Fregni F, Pascual-Leone A (2009) Meta-analysis of the effects of repetitive transcranial magnetic stimulation (rTMS) on negative and positive symptoms in schizophrenia. Schizophr Res 108:11-24
36. Fritsch B, Reis J, Martinowich K, Schambra HM, Ji Y, Cohen LG, Lu B (2010) Direct current stimulation promotes BDNF-dependent synaptic plasticity: potential implications for motor learning. Neuron 66:198-204
37. Funke K, Benali A (2011) Modulation of cortical inhibition by rTMS - findings obtained from animal models. J Physiol 589:4423-4435
38. Gamboa OL, Antal A, Laczo B, Moliadze V, Nitsche MA, Paulus W (2011) Impact of repetitive theta burst stimulation on motor cortex excitability. Brain Stimul 4:145-151
39. Gladding CM, Fitzjohn SM, Molnar E (2009) Metabotropic glutamate receptor-mediated long-term depression: molecular mechanisms. Pharmacol Rev 61:395-412
40. Green MJ, Matheson SL, Shepherd A, Weickert CS, Carr VJ (2011) Brain-derived neurotrophic factor levels in schizophrenia: a systematic review with meta-analysis. Mol Psychiatry 16:960-972
41. Grundey J, Thirugnanasambandam N, Kaminsky K, Drees A, Skwirba AC, Lang N, Paulus W, Nitsche MA (2012) Neuroplasticity in cigarette smokers is altered under withdrawal and partially restituted by nicotine exposition. J Neurosci 32:4156-4162
42. Hallett M (2007) Transcranial magnetic stimulation: a primer. Neuron 55:187-199
43. Hamada M, Murase N, Hasan A, Balaratnam M, Rothwell JC (2012) The role of interneuron networks in driving human motor cortical plasticity. Cereb Cortex 23(7):1593-1605
44. Hasan A, Aborowa R, Nitsche MA, Marshall L, Schmitt A, Gruber O, Falkai P, Wobrock T (2012) Abnormal bihemispheric responses in schizophrenia patients following cathodal transcranial direct stimulation. Eur Arch Psychiatry Clin Neurosci 262(5):415-423
45. Hasan A, Falkai P, Wobrock T, Lieberman J, Glenthoj B, Gattaz WF, Thibaut F, Moller HJ (2012) World federation of societies of biological psychiatry (WFSBP) guidelines for biological treatment of schizophrenia, part 1: update 2012 on the acute treatment of schizophrenia and the management of treatment resistance. World J Biol Psychiatry 13:318-378
46. Hasan A, Hamada M, Nitsche MA, Ruge D, Galea JM, Wobrock T, Rothwell JC (2011) Direct-current-dependent shift of theta-burst-induced plasticity in the human motor cortex. Exp Brain Res 217:15-23
47. Hasan A, Misewitsch K, Nitsche MA, Gruber O, Padberg F, Falkai P, Wobrock T (2013) Impaired motor cortex responses in non-psychotic first-degree relatives of schizophrenia patients: a cathodal tDCS pilot study. Brain Stimul
48. Hasan A, Nitsche MA, Herrmann M, Schneider-Axmann T, Marshall L, Gruber O, Falkai P, Wobrock T (2011) Impaired long-term depression in schizophrenia: a cathodal tDCS pilot study. Brain Stimul 5(4):475-483
49. Hasan A, Nitsche MA, Rein B, Schneider-Axmann T, Guse B, Gruber O, Falkai P, Wobrock T (2011) Dysfunctional long-term potentiation-like plasticity in schizophrenia revealed by transcranial direct current stimulation. Behav Brain Res 224:15-22
50. Hasan A, Wobrock T, Grefkes C, Labusga M, Levold K, Schneider-Axmann T, Falkai P, Muller H, Klosterkotter J, Bechdolf A (2012) Deficient inhibitory cortical networks in antipsychotic-naive subjects at risk of developing first-episode psychosis and first-episode schizophrenia patients: a cross-sectional study. Biol Psychiatry 72(9):744-751
51. Hashimoto T, Bazmi HH, Mirnics K, Wu Q, Sampson AR, Lewis DA (2008) Conserved regional patterns of GABA-related transcript expression in the neocortex of subjects with schizophrenia. Am J Psychiatry 165:479-489
52. Howes OD, Kapur S (2009) The dopamine hypothesis of schizophrenia: version III-the final common pathway. Schizophr Bull 35:549-562
53. Huang YZ, Edwards MJ, Rounis E, Bhatia KP, Rothwell JC (2005) Theta burst stimulation of the human motor cortex. Neuron 45:201-206
54. Huang YZ, Rothwell JC, Edwards MJ, Chen RS (2008) Effect of physiological activity on an NMDA-dependent form of cortical plasticity in human. Cereb Cortex 18:563-570
55. Kemp A, Manahan-Vaughan D (2007) Hippocampal long-term depression: master or minion in declarative memory processes? Trends Neurosci 30:111-118
56. Konradi C, Heckers S (2003) Molecular aspects of glutamate dysregulation: implications for schizophrenia and its treatment. Pharmacol Ther 97:153-179
57. Krystal JH, Tolin DF, Sanacora G, Castner SA, Williams GV, Aikins DE, Hoffman RE, D'Souza DC (2009) Neuroplasticity as a target for the pharmacotherapy of anxiety disorders, mood disorders, and schizophrenia. Drug Discov Today 14:690-697
58. Krystall JH, Moghaddam B (2011) Contributions of glutamate and GABA systems to the neurobiology and treatment of schizophrenia. In: Weinberger DR, Harrison PJ (eds) schizophrenia. Wiley-Blackwell, Chichester, pp 433-461
59. Kullmann DM, Lamsa KP (2011) LTP and LTD in cortical GABAergic interneurons: emerging rules and roles. Neuropharmacology 60:712-719
60. Kuo MF, Grosch J, Fregni F, Paulus W, Nitsche MA (2007) Focusing effect of acetylcholine on neuroplasticity in the human motor cortex. J Neurosci 27:14442-14447
61. Kuo MF, Paulus W, Nitsche MA (2013) Therapeutic effects of non-invasive brain stimulation with direct currents (tDCS) in neuropsychiatric diseases. Neuroimage
62. Lee KF, Soares C, Beique JC (2012) Examining form and function of dendritic spines. Neural Plast 2012:704103
63. Lewis DA (2009) Neuroplasticity of excitatory and inhibitory cortical circuits in schizophrenia. Dialogues Clin Neurosci 11:269-280
64. Lewis DA, Hashimoto T, Volk DW (2005) Cortical inhibitory neurons and schizophrenia. Nat Rev Neurosci 6:312-324
65. Liebetanz D, Nitsche MA, Tergau F, Paulus W (2002) Pharmacological approach to the mechanisms of transcranial DC-stimulation-induced after-effects of human motor cortex excitability. Brain 125:2238-2247
66. Luby ED, Cohen BD, Rosenbaum G, Gottlieb JS, Kelley R (1959) Study of a new schizophrenomimetic drug; sernyl. AMA Arch Neurol Psychiatry 81:363-369
67. Massey PV, Bashir ZI (2007) Long-term depression: multiple forms and implications for brain function. Trends Neurosci 30:176-184
68. Misonou H, Mohapatra DP, Park EW, Leung V, Zhen D, Misonou K, Anderson AE, Trimmer JS (2004) Regulation of ion channel localization and phosphorylation by neuronal activity. Nat Neurosci 7:711-718
69. Miyamoto E (2006) Molecular mechanism of neuronal plasticity: induction and maintenance of long-term potentiation in the hippocampus. J Pharmacol Sci 100:433-442
70. Monte-Silva K, Liebetanz D, Grundey J, Paulus W, Nitsche MA (2010) Dosage-dependent non-linear effect of L-dopa on human motor cortex plasticity. J Physiol 588:3415-3424
71. Nitsche MA, Cohen LG, Wassermann EM, Priori A, Lang N, Antal A, Paulus W, Hummel F, Boggio PS, Fregni F, Pascual-Leone A (2008) Transcranial direct current stimulation: state of the art 2008. Brain Stimul 1:206-223
72. Nitsche MA, Fricke K, Henschke U, Schlitterlau A, Liebetanz D, Lang N, Henning S, Tergau F, Paulus W (2003) Pharmacological modulation of cortical excitability shifts induced by transcranial direct current stimulation in humans. J Physiol 553:293-301
73. Nitsche MA, Grundey J, Liebetanz D, Lang N, Tergau F, Paulus W (2004) Catecholaminergic consolidation of motor cortical neuroplasticity in humans. Cereb Cortex 14:1240-1245
74. Nitsche MA, Jaussi W, Liebetanz D, Lang N, Tergau F, Paulus W (2004) Consolidation of human motor cortical neuroplasticity by D-cycloserine. Neuropsychopharmacology 29:1573-1578
75. Nitsche MA, Kuo MF, Karrasch R, Wachter B, Liebetanz D, Paulus W (2009) Serotonin affects transcranial direct current-induced neuroplasticity in humans. Biol Psychiatry 66:503-508
76. Nitsche MA, Lampe C, Antal A, Liebetanz D, Lang N, Tergau F, Paulus W (2006) Dopaminergic modulation of long-lasting direct current-induced cortical excitability changes in the human motor cortex. Eur J Neurosci 23:1651-1657
77. Nitsche MA, Monte-Silva K, Kuo MF, Paulus W (2010) Dopaminergic impact on cortical excitability in humans. Rev Neurosci 21:289-298
78. Nitsche MA, Nitsche MS, Klein CC, Tergau F, Rothwell JC, Paulus W (2003) Level of action of cathodal DC polarisation induced inhibition of the human motor cortex. Clin Neurophysiol 114:600-604
79. Nitsche MA, Paulus W (2000) Excitability changes induced in the human motor cortex by weak transcranial direct current stimulation. J Physiol 527(Pt 3):633-639
80. Oxley T, Fitzgerald PB, Brown TL, de Castella A, Daskalakis ZJ, Kulkarni J (2004) Repetitive transcranial magnetic stimulation reveals abnormal plastic response to premotor cortex stimulation in schizophrenia. Biol Psychiatry 56:628-633
81. Paz RD, Andreasen NC, Daoud SZ, Conley R, Roberts R, Bustillo J, Perrone-Bizzozero NI (2006) Increased expression of activity-dependent genes in cerebellar glutamatergic neurons of patients with schizophrenia. Am J Psychiatry 163:1829-1831
82. Paz RD, Tardito S, Atzori M, Tseng KY (2008) Glutamatergic dysfunction in schizophrenia: from basic neuroscience to clinical psychopharmacology. Eur Neuropsychopharmacol 18:773-786
83. Pilurzi G, Hasan A, Saifee TA, Tolu E, Rothwell JC, Deriu F (2013) Intracortical circuits, sensorimotor integration and plasticity in human motor cortical projections to muscles of the lower face. J Physiol
84. Purpura DP, McMurtry JG (1965) Intracellular activities and evoked potential changes during polarization of motor cortex. J Neurophysiol 28:166-185
85. Rajji TK, Sun Y, Zomorrodi-Moghaddam R, Farzan F, Blumenberger DM, Mulsant BH, Fitzgerald PB, Daskalakis ZJ (2013) PAS-induced potentiation of cortical evoked activity in the dorsolateral prefrontal cortex. Neuropsychopharmacology (in press)
86. Rapoport JL, Giedd JN, Gogtay N (2012) Neurodevelopmental model of schizophrenia: update 2012. Mol Psychiatry 17(12):1228-1238
87. Ridding MC, Ziemann U (2010) Determinants of the induction of cortical plasticity by non-invasive brain stimulation in healthy subjects. J Physiol 588:2291-2304
88. Schmidt A, Bachmann R, Kometer M, Csomor PA, Stephan KE, Seifritz E, Vollenweider FX (2012) Mismatch negativity encoding of prediction errors predicts S-ketamine-induced cognitive impairments. Neuropsychopharmacology 37:865-875
89. Schmitt A, Hasan A, Gruber O, Falkai P (2011) Schizophrenia as a disorder of disconnectivity. Eur Arch Psychiatry Clin Neurosci 261(2):150-154
90. Siebner HR, Dressnandt J, Auer C, Conrad B (1998) Continuous intrathecal baclofen infusions induced a marked increase of the transcranially evoked silent period in a patient with generalized dystonia. Muscle Nerve 21:1209-1212
91. Stefan K, Kunesch E, Benecke R, Cohen LG, Classen J (2002) Mechanisms of enhancement of human motor cortex excitability induced by interventional paired associative stimulation. J Physiol 543:699-708
92. Stefan K, Kunesch E, Cohen LG, Benecke R, Classen J (2000) Induction of plasticity in the human motor cortex by paired associative stimulation. Brain 123(Pt 3):572-584
93. Stephan KE, Friston KJ, Frith CD (2009) Dysconnection in schizophrenia: from abnormal synaptic plasticity to failures of self-monitoring. Schizophr Bull 35:509-527
94. Stern AJ, Savostyanova AA, Goldman A, Barnett AS, van der Veen JW, Callicott JH, Mattay VS, Weinberger DR, Marenco S (2008) Impact of the brain-derived neurotrophic factor Val66Met polymorphism on levels of hippocampal N-acetyl-aspartate assessed by magnetic resonance spectroscopic imaging at 3 Tesla. Biol Psychiatry 64:856-862
95. Thirugnanasambandam N, Grundey J, Paulus W, Nitsche MA (2011) Dose-dependent nonlinear effect of l-dopa on paired associative stimulation-induced neuroplasticity in humans. J Neurosci 31:5294-5299
96. Toro CT, Deakin JF (2007) Adult neurogenesis and schizophrenia: a window on abnormal early brain development? Schizophr Res 90:1-14
97. Voineskos AN, Farzan F, Barr MS, Lobaugh NJ, Mulsant BH, Chen R, Fitzgerald PB, Daskalakis ZJ (2010) The role of the corpus callosum in transcranial magnetic stimulation induced interhemispheric signal propagation. Biol Psychiatry 68:825-831
98. Weickert CS, Hyde TM, Lipska BK, Herman MM, Weinberger DR, Kleinman JE (2003) Reduced brain-derived neurotrophic factor in prefrontal cortex of patients with schizophrenia. Mol Psychiatry 8:592-610
99. Wobrock T, Hasan A, Falkai P (2012) Innovative treatment approaches in schizophrenia enhancing neuroplasticity: aerobic exercise, erythropoetin and repetitive transcranial magnetic stimulation. Curr Pharm Biotechnol 13:1595-1605
100. Wobrock T, Hasan A, Malchow B, Wolff-Menzler C, Guse B, Lang N, Schneider-Axmann T, Ecker UK, Falkai P (2010) Increased cortical inhibition deficits in first-episode schizophrenia with comorbid cannabis abuse. Psychopharmacology 208:353-363
101. Woo TU, Walsh JP, Benes FM (2004) Density of glutamic acid decarboxylase 67 messenger RNA-containing neurons that express the N-methyl-D-aspartate receptor subunit NR2A in the anterior cingulate cortex in schizophrenia and bipolar disorder. Arch Gen Psychiatry 61:649-657
102. Ziemann U (2004) TMS and drugs. Clin Neurophysiol 115:1717-1729
103. Ziemann U, Paulus W, Nitsche MA, Pascual-Leone A, Byblow WD, Berardelli A, Siebner HR, Classen J, Cohen LG, Rothwell JC (2008) Consensus: motor cortex plasticity protocols. Brain Stimul 1:164-182
104. Zorumski CF, Izumi Y (2012) NMDA receptors and metaplasticity: mechanisms and possible roles in neuropsychiatric disorders. Neurosci Biobehav Rev 36:989-1000