Investigations of motor-cortex cortical plasticity following facilitatory and inhibitory transcranial theta-burst stimulation in schizophrenia: A proof-of-concept study

Journal of Psychiatric Research

Volumn 61, Issue , 2015, Pages 196-204

  Hasan, Alkomiet ^a   Brinkmann, Caroline ^b   Strube, Wolfgang ^a   Palm, Ulrich ^a   Malchow, Berend ^a   Rothwell, John C ^c   Falkai, Peter ^a   Wobrock, Thomas ^b,d  

^a LUDWIG MAXIMILIANS UNIVERSITY   (Germany)

^b UNIVERSITY OF GÖTTINGEN   (Germany)

^c UNIVERSITY COLLEGE LONDON   (United Kingdom)

^d Darmstadt Dieburg Clinics   (Germany)

Author keywords

Calcium signaling; Cortical excitability; Neural plasticity; Schizophrenia; Theta burst stimulation

Indexed keywords

AGOMELATINE; ARIPIPRAZOLE; BIPERIDEN; CALCIUM ION; CITALOPRAM; FLUPENTIXOL; LAMOTRIGINE; OLANZAPINE; QUETIAPINE; RISPERIDONE; ZIPRASIDONE;

ADD ON THERAPY; ADULT; ARTICLE; CLINICAL ARTICLE; CLINICAL GLOBAL IMPRESSION SCALE; CONTROLLED STUDY; EVOKED MUSCLE RESPONSE; FEMALE; GLOBAL ASSESSMENT OF FUNCTIONING; HUMAN; LEFT HEMISPHERE; LONG TERM DEPRESSION; LONG TERM POTENTIATION; MALE; MOTOR CORTEX; NERVE CELL EXCITABILITY; NERVE CELL PLASTICITY; POSITIVE AND NEGATIVE SYNDROME SCALE; PRIMARY MOTOR CORTEX; PRIORITY JOURNAL; RIGHT HEMISPHERE; SCHIZOPHRENIA; THETA RHYTHM; TIME TO TREATMENT; TRANSCRANIAL MAGNETIC STIMULATION; TRANSCRANIAL MAGNETIC STIMULATION SYSTEM; TRANSCRANIAL THETA BURST STIMULATION; TREATMENT RESPONSE; ADOLESCENT; ANALYSIS OF VARIANCE; CASE CONTROL STUDY; PATHOPHYSIOLOGY; PROCEDURES; YOUNG ADULT;

ADOLESCENT; ADULT; ANALYSIS OF VARIANCE; CASE-CONTROL STUDIES; EVOKED POTENTIALS, MOTOR; FEMALE; HUMANS; LONG-TERM POTENTIATION; LONG-TERM SYNAPTIC DEPRESSION; MALE; MOTOR CORTEX; NEURONAL PLASTICITY; SCHIZOPHRENIA; TRANSCRANIAL MAGNETIC STIMULATION; YOUNG ADULT;

EID: 84921515446     PISSN: 00223956     EISSN: 18791379     Source Type: Journal    
DOI: 10.1016/j.jpsychires.2014.12.006     Document Type: Article

References (69)

1. Abraham W.C. Metaplasticity: tuning synapses and networks for plasticity. Nat Rev Neurosci 2008, 9:387.
2. Andreasen N.C., Liu D., Ziebell S., Vora A., Ho B.C. Relapse duration, treatment intensity, and brain tissue loss in schizophrenia: a prospective longitudinal MRI study. Am J Psychiatry 2013, 170:609-615.
3. Balu D.T., Coyle J.T. Neuroplasticity signaling pathways linked to the pathophysiology of schizophrenia. Neurosci Biobehav Rev 2011, 35:848-870.
4. Benali A., Trippe J., Weiler E., Mix A., Petrasch-Parwez E., Girzalsky W., et al. Theta-burst transcranial magnetic stimulation alters cortical inhibition. JNeurosci : official J Soc Neurosci 2011, 31:1193-1203.
5. Benes F.M. Regulation of cell cycle and DNA repair in post-mitotic GABA neurons in psychotic disorders. Neuropharmacology 2011, 60:1232-1242.
6. Benes F.M., Berretta S. GABAergic interneurons: implications for understanding schizophrenia and bipolar disorder. Neuropsychopharmacol: Off Publ Am Coll Neuropsychopharmacol 2001, 25:1-27.
7. Benes F.M., McSparren J., Bird E.D., SanGiovanni J.P., Vincent S.L. Deficits in small interneurons in prefrontal and cingulate cortices of schizophrenic and schizoaffective patients. Arch Gen Psychiatry 1991, 48:996-1001.
8. Berridge M.J. Calcium signalling and psychiatric disease: bipolar disorder and schizophrenia. Cell Tissue Res 2014, 357(2):477-492.
9. Brunelin J., Szekely D., Costes N., Mondino M., Bougerol T., Saoud M., et al. Theta burst stimulation in the negative symptoms of schizophrenia and striatal dopamine release. An iTBS-[11C]raclopride PET case study. Schizophrenia Res 2011, 131:264-265.
10. Bunse T., Wobrock T., Strube W., Padberg F., Palm U., Falkai P., et al. Motor cortical excitability assessed by transcranial magnetic stimulation in psychiatric disorders: a systematic review. Brain Stimul 2014, 7:158-169.
11. Chance S.A., Walker M., Crow T.J. Reduced density of calbindin-immunoreactive interneurons in the planum temporale in schizophrenia. Brain Res 2005, 1046:32-37.
12. Chiapponi C., Piras F., Fagioli S., Piras F., Caltagirone C., Spalletta G. Age-related brain trajectories in schizophrenia: a systematic review of structural MRI studies. Psychiatry Res 2013, 214:83-93.
13. Cotter D., Landau S., Beasley C., Stevenson R., Chana G., MacMillan L., et al. The density and spatial distribution of GABAergic neurons, labelled using calcium binding proteins, in the anterior cingulate cortex in major depressive disorder, bipolar disorder, and schizophrenia. Biol Psychiatry 2002, 51:377-386.
14. Cross-Disorder Group of the Psychiatric Genomics C, Genetic Risk Outcome of Psychosis C Identification of risk loci with shared effects on five major psychiatric disorders: a genome-wide analysis. Lancet 2013, 381:1371-1379.
15. Daskalakis Z.J., Christensen B.K., Fitzgerald P.B., Chen R. Dysfunctional neural plasticity in patients with schizophrenia. Arch Gen Psychiatry 2008, 65:378-385.
16. Day B.L., Dressler D., Maertens de Noordhout A., Marsden C.D., Nakashima K., Rothwell J.C., et al. Electric and magnetic stimulation of human motor cortex: surface EMG and single motor unit responses. JPhysiol 1989, 412:449-473.
17. Day B.L., Rothwell J.C., Thompson P.D., Dick J.P., Cowan J.M., Berardelli A., et al. Motor cortex stimulation in intact man. 2. Multiple descending volleys. Brain 1987, 110(Pt 5):1191-1209.
18. Demirtas-Tatlidede A., Freitas C., Cromer J.R., Safar L., Ongur D., Stone W.S., et al. Safety and proof of principle study of cerebellar vermal theta burst stimulation in refractory schizophrenia. Schizophrenia Res 2010, 124:91-100.
19. Eberle M.C., Wildgruber D., Wasserka B., Fallgatter A.J., Plewnia C. Relief from chronic intractable auditory hallucinations after long-term bilateral theta burst stimulation. Am J Psychiatry 2010, 167:1410.
20. Eggers C., Fink G.R., Nowak D.A. Theta burst stimulation over the primary motor cortex does not induce cortical plasticity in Parkinson's disease. JNeurology 2010, 257:1669-1674.
21. Endicott J., Spitzer R.L., Fleiss J.L., Cohen J. The global assessment scale. A procedure for measuring overall severity of psychiatric disturbance. Arch Gen Psychiatry 1976, 33:766-771.
22. Fitzgerald P.B., Brown T.L., Marston N.A., Oxley T., De Castella A., Daskalakis Z.J., et al. Reduced plastic brain responses in schizophrenia: a transcranial magnetic stimulation study. Schizophrenia Res 2004, 71:17-26.
23. Frantseva M.V., Fitzgerald P.B., Chen R., Moller B., Daigle M., Daskalakis Z.J. Evidence for impaired long-term potentiation in schizophrenia and its relationship to motor skill learning. Cereb Cortex 2008, 18:990-996.
24. Funke K., Benali A. Modulation of cortical inhibition by rTMS - findings obtained from animal models. JPhysiol 2011, 589:4423-4435.
25. Fusar-Poli P., Smieskova R., Kempton M.J., Ho B.C., Andreasen N.C., Borgwardt S. Progressive brain changes in schizophrenia related to antipsychotic treatment? A meta-analysis of longitudinal MRI studies. Neurosci Biobehav Rev 2013, 37(8):1680-1691.
26. Gentner R., Wankerl K., Reinsberger C., Zeller D., Classen J. Depression of human corticospinal excitability induced by magnetic theta-burst stimulation: evidence of rapid polarity-reversing metaplasticity. Cereb Cortex 2008, 18:2046-2053.
27. Goldsworthy M.R., Muller-Dahlhaus F., Ridding M.C., Ziemann U. Resistant against de-depression: LTD-like plasticity in the human motor cortex induced by spaced cTBS. Cereb cortex 2014.
28. Goldsworthy M.R., Pitcher J.B., Ridding M.C. The application of spaced theta burst protocols induces long-lasting neuroplastic changes in the human motor cortex. Eur J Neurosci 2012, 35:125-134.
29. Guy W.B.R. CGI: Clinical global impressions 1976, National Institute of Mental Health.
30. Hamada M., Murase N., Hasan A., Balaratnam M., Rothwell J.C. The role of interneuron networks in driving human motor cortical plasticity. Cereb Cortex 2013, 23:1593-1605.
31. Hasan A., Aborowa R., Nitsche M.A., Marshall L., Schmitt A., Gruber O., et al. Abnormal bihemispheric responses in schizophrenia patients following cathodal transcranial direct stimulation. Eur Arch Psychiatry Clin Neurosci 2012, 262(5):415-423.
32. Hasan A., Falkai P., Wobrock T., Lieberman J., Glenthoj B., Gattaz W.F., et al. World Federation of Societies of Biological Psychiatry (WFSBP) guidelines for biological treatment of schizophrenia, part 2: update 2012 on the long-term treatment of schizophrenia and management of antipsychotic-induced side effects. World J Biol Psychiatry 2013, 14:2-44.
33. Hasan A., Hamada M., Nitsche M.A., Ruge D., Galea J.M., Wobrock T., et al. Direct-current-dependent shift of theta-burst-induced plasticity in the human motor cortex. Exp Brain Res 2011, 217:15-23.
34. Hasan A., Misewitsch K., Nitsche M.A., Gruber O., Padberg F., Falkai P., et al. Impaired motor cortex responses in non-psychotic first-degree relatives of schizophrenia patients: a cathodal tDCS pilot study. Brain Stimul 2013, 6(5):821-829.
35. Hasan A., Nitsche M.A., Herrmann M., Schneider-Axmann T., Marshall L., Gruber O., et al. Impaired long-term depression in schizophrenia: a cathodal tDCS pilot study. Brain Stimul 2011, 5(4):475-483.
36. Hasan A., Nitsche M.A., Rein B., Schneider-Axmann T., Guse B., Gruber O., et al. Dysfunctional long-term potentiation-like plasticity in schizophrenia revealed by transcranial direct current stimulation. Behav Brain Res 2011, 224:15-22.
37. Hashimoto T., Bazmi H.H., Mirnics K., Wu Q., Sampson A.R., Lewis D.A. Conserved regional patterns of GABA-related transcript expression in the neocortex of subjects with schizophrenia. Am J Psychiatry 2008, 165:479-489.
38. Howes O.D., Kapur S. The dopamine hypothesis of schizophrenia: version III-the final common pathway. Schizophr Bull 2009, 35:549-562.
39. Hoy K.E., Arnold S.L., Emonson M.R., Daskalakis Z.J., Fitzgerald P.B. An investigation into the effects of tDCS dose on cognitive performance over time in patients with schizophrenia. Schizophr Res 2014, 155:96-100.
40. Huang Y.Z., Chen R.S., Rothwell J.C., Wen H.Y. The after-effect of human theta burst stimulation is NMDA receptor dependent. Clin Neurophysiol: Off J Int Fed Clin Neurophysiol 2007, 118:1028-1032.
41. Huang Y.Z., Edwards M.J., Rounis E., Bhatia K.P., Rothwell J.C. Theta burst stimulation of the human motor cortex. Neuron 2005, 45:201-206.
42. Huang Y.Z., Rothwell J.C., Chen R.S., Lu C.S., Chuang W.L. The theoretical model of theta burst form of repetitive transcranial magnetic stimulation. Clin Neurophysiol: Off J Int Fed Clin Neurophysiol 2011, 122:1011-1018.
43. Huang Y.Z., Rothwell J.C., Edwards M.J., Chen R.S. Effect of physiological activity on an NMDA-dependent form of cortical plasticity in human. Cereb Cortex 2008, 18:563-570.
44. Huang Y.Z., Rothwell J.C., Lu C.S., Chuang W.L., Chen R.S. Abnormal bidirectional plasticity-like effects in Parkinson's disease. Brain 2011, 134:2312-2320.
45. Huang Y.Z., Rothwell J.C., Lu C.S., Wang J., Chen R.S. Restoration of motor inhibition through an abnormal premotor-motor connection in dystonia. Mov Disord: Off J Mov Disord Soc 2010, 25:696-703.
46. Javitt D.C., Zukin S.R., Heresco-Levy U., Umbricht D. Has an angel shown the way? Etiological and therapeutic implications of the PCP/NMDA model of schizophrenia. Schizophr Bull 2012, 38:958-966.
47. Kay S.R., Fiszbein A., Opler L.A. The positive and negative syndrome scale (PANSS) for schizophrenia. Schizophr Bull 1987, 13:261-276.
48. Kindler J., Homan P., Flury R., Strik W., Dierks T., Hubl D. Theta burst transcranial magnetic stimulation for the treatment of auditory verbal hallucinations: results of a randomized controlled study. Psychiatry Res 2013, 209:114-117.
49. Koch G. Do studies on cortical plasticity provide a rationale for using non-invasive brain stimulation as a treatment for Parkinson's disease patients?. Front Neurology 2013, 4:180.
50. Kujirai T., Caramia M.D., Rothwell J.C., Day B.L., Thompson P.D., Ferbert A., et al. Corticocortical inhibition in human motor cortex. JPhysiol 1993, 471:501-519.
51. Lisman J.E. Three Ca2+ levels affect plasticity differently: the LTP zone, the LTD zone and no man's land. JPhysiol 2001, 532:285.
52. McAllister S.M., Rothwell J.C., Ridding M.C. Selective modulation of intracortical inhibition by low-intensity Theta Burst Stimulation. Clin Neurophysiol: Off J Int Fed Clin Neurophysiol 2009, 120:820-826.
53. McClintock S.M., Freitas C., Oberman L., Lisanby S.H., Pascual-Leone A. Transcranial magnetic stimulation: a neuroscientific probe of cortical function in schizophrenia. Biol Psychiatry 2011, 70:19-27.
54. Oldfield R.C. The assessment and analysis of handedness: the Edinburgh inventory. Neuropsychologia 1971, 9:97-113.
55. Oxley T., Fitzgerald P.B., Brown T.L., de Castella A., Daskalakis Z.J., Kulkarni J. Repetitive transcranial magnetic stimulation reveals abnormal plastic response to premotor cortex stimulation in schizophrenia. Biol Psychiatry 2004, 56:628-633.
56. Rachid F., Vianin P., Besse C. Safety and efficacy of continuous theta burst stimulation at 30 Hz in a patient with chronic auditory hallucinations: a case study in a private practice setting. Brain Stimul 2013, 6:707-708.
57. Radhu N., de Jesus D.R., Ravindran L.N., Zanjani A., Fitzgerald P.B., Daskalakis Z.J. Ameta-analysis of cortical inhibition and excitability using transcranial magnetic stimulation in psychiatric disorders. Clin Neurophysiol: Off J Int Fed Clin Neurophysiol 2013, 124:1309-1320.
58. Rapoport J.L., Giedd J.N., Gogtay N. Neurodevelopmental model of schizophrenia: update 2012. Mol Psychiatry 2012, 17(12):1228-1238.
59. Ribolsi M., Lisi G., Di Lorenzo G., Koch G., Oliveri M., Magni V., et al. Perceptual pseudoneglect in schizophrenia: candidate endophenotype and the role of the right parietal cortex. Schizophr Bull 2013, 39:601-607.
60. Rothwell J.C., Hallett M., Berardelli A., Eisen A., Rossini P., Paulus W. Magnetic stimulation: motor evoked potentials. The International Federation of clinical Neurophysiology. Electroencephalogr Clin Neurophysiol Suppl 1999, 52:97-103.
61. Sidhoumi D., Braha S., Bouaziz N., Brunelin J., Benadhira R., Januel D. 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: Off J Int Fed Clin Neurophysiol 2010, 121:802.
62. Stephan K.E., Friston K.J., Frith C.D. Dysconnection in schizophrenia: from abnormal synaptic plasticity to failures of self-monitoring. Schizophr Bull 2009, 35:509-527.
63. Strube W., Wobrock T., Bunse T., Palm U., Padberg F., Malchow B., et al. Impairments in motor-cortical inhibitory networks across recent-onset and chronic schizophrenia: a cross-sectional TMS Study. Behav Brain Res 2014, 264:17-25.
64. Todd G., Flavel S.C., Ridding M.C. Priming theta-burst repetitive transcranial magnetic stimulation with low- and high-frequency stimulation. Exp Brain Res 2009, 195:307-315.
65. Trippe J., Mix A., Aydin-Abidin S., Funke K., Benali A. theta burst and conventional low-frequency rTMS differentially affect GABAergic neurotransmission in the rat cortex. Exp Brain Res 2009, 199:411-421.
66. Vercammen A., Rushby J.A., Loo C., Short B., Weickert C.S., Weickert T.W. Transcranial direct current stimulation influences probabilistic association learning in schizophrenia. Schizophr Res 2011, 131:198-205.
67. Vita A., De Peri L., Deste G., Sacchetti E. Progressive loss of cortical gray matter in schizophrenia: a meta-analysis and meta-regression of longitudinal MRI studies. Transl Psychiatry 2012, 2:e190.
68. Wankerl K., Weise D., Gentner R., Rumpf J.J., Classen J. L-type voltage-gated Ca2+ channels: a single molecular switch for long-term potentiation/long-term depression-like plasticity and activity-dependent metaplasticity in humans. JNeurosci: Off J Soc Neurosci 2010, 30:6197-6204.
69. Ziemann U. TMS and drugs. Clin Neurophysiol 2004, 115:1717-1729.