Transcranial Magnetic Stimulation in the Research of Cortical Inhibition in Depressive Disorder and Schizophrenia, the Effect of Antipsychotics
Authors:
L. Ustohal
Authors‘ workplace:
CEITEC – Středoevropský technologický institut, MU, Brno
; Psychiatrická klinika LF MU a FN Brno
Published in:
Cesk Slov Neurol N 2017; 80/113(2): 157-162
Category:
Review Article
doi:
https://doi.org/10.14735/amcsnn2017157
Tato práce byla finančně podpořena projektem (Ministerstva zdravotnictví) koncepčního rozvoje výzkumné organizace 65269705 (FN Brno).
Overview
Transcranial magnetic stimulation enables exploration of cortical inhibition in various neuropsychiatric disorders, including depressive disorder and schizophrenia. Cortical inhibition can be defined as a neurophysiological mechanism (not pathological) through which GABAergic interneurons influence the activity of other neurons. The most frequently studied cortical inhibition parameters include cortical silent period, short-interval cortical inhibition, long-interval cortical inhibition, amplitude of motor-evoked potential, resting motor threshold, and intracortical facilitation. Published cross-sectional studies suggest impairment of cortical inhibition in both above mentioned mental disorders. Some inconsistent results in these cross-sectional studies can be explained by their design and by heterogeneous samples of patients. It might be difficult to differentiate the effect of the disorder and the effect of the treatment. This problem can be resolved with recent prospective longitudinal studies aimed at the effect of selected antipsychotics on cortical inhibition in schizophrenia. They confirmed impairment of cortical inhibition and they identified the potential antipsychotics have to change this impairment. Some researchers believe that this potential is a newly discovered mechanism of action. Some researchers also suppose that the new data on pathophysiology and treatment of (not only) depressive disorder and schizophrenia discovered using the transcranial magnetic stimulation help (partially) to rebuild psychiatry on new grounds, sometimes called Circuit-based Psychiatry.
Key words:
cortical inhibition – transcranial magnetic stimulation – depressive disorder – schizophrenia – antipsychotics
The authors declare they have no potential conflicts of interest concerning drugs, products, or services used in the study.
The Editorial Board declares that the manuscript met the ICMJE “uniform requirements” for biomedical papers.
Sources
1. Camprodon JA, Pascual-Leone A. Multimodal applications of transcranial magnetic stimulation for circuit-based psychiatry. JAMA Psychiatry 2016;73(4):407– 8.
2. Lefaucheur J-P, André-Obadia N, Antal A, et al. Evidence-based guidelines on the therapeutic use of repetitive transcranial magnetic stimulation (rTMS). Clin Neurophysiol 2014;125(11):2150– 206.
3. Ustohal L, Přikrylová Kučerová H, Přikryl R, et al. Repetitivní transkraniální magnetická stimulace v léčbě depresivní poruchy – randomizovaná, jednoduše slepá, antidepresivy kontrolovaná studie. Cesk Slov Neurol N 2014;77/ 110(5):602– 7.
4. DeFelipe J, Conley M, Jones EG. Long-range focal collateralization of axons arising from corticocortical cells in monkey sensory-motor cortex. J Neurosci 1986;6(12):3749– 66.
5. Schieber MH, Hibbard LS. How somatotopic is the motor cortex hand area? Science 1993;261(5120):489– 92.
6. Radhu N, de Jesus DR, Ravindran LN, et al. A meta-analysis of cortical inhibition and excitability using transcranial magnetic stimulation in psychiatric disorders. Clin Neurophysiol 2013;124(7):1309– 20.
7. Daskalakis ZJ, Fitzgerald PB, Christensen BK. The role of cortical inhibition in the pathophysiology and treatment of schizophrenia. Brain Res Rev 2007;56(2):427– 42.
8. Liu SK, Fitzgerald PB, Daigle M, et al. The relationship between cortical inhibition, antipsychotic treatment, and the symptoms of schizophrenia. Biol Psychiatry 2009;65(6):503– 9.
9. Bunse T, Wobrock T, Strube W, et al. Motor cortex excitability assessed by transcranial magnetic stimulation in psychiatric disorders: a systematic review. Brain Stimul 2014;7(2):158– 69. doi: 10.1016/ j.brs.2013.08.009.
10. Daskalakis ZJ, Christensen BK, Fitzgerald PB, et al. Increased cortical inhibition in persons with schizophrenia treated with clozapine. J Psychopharmacol 2008;22(2):203– 9. doi: 10.1177/ 0269881107084002.
11. Fuhr P, Agostino R, Hallett M. Spinal motor neuron excitability during the silent period after cortical stimulation. Electroencephalograf Clin Neurophysiol 1991;81(4):257– 62.
12. Kaster TS, de Jesus D, Radhu N, et al. Clozapine potentiation of GABA mediated cortical inhibition in treatment resistant schizophrenia. Schizophr Res 2015;165(2– 3):157– 62. doi: 10.1016/ j.schres.2015.04.015.
13. Kujirai T, Caramia MD, Rothwell JC, et al. Corticocortical inhibition in human motor cortex. J Physiol 1993;471:501– 19.
14. Radhu N, Garcia Dominguez L, Farzan F, et al. Evidence for inhibitory deficits in the prefrontal cortex in schizophrenia. Brain 2015;138(2):483– 97. doi: 10.1093/ brain/ awu 360.
15. Rogasch NC, Daskalakis ZJ, Fitzgerald PB. Cortical inhibition, excitation, and connectivity in schizophrenia: a review of insights from transcranial magnetic stimulation. Schizophr Bull 2014;40(3):685– 96.
16. Ustohal L, Mayerova M, Hublova V, et al. Risperidone increases the cortical silent period in drug-naive patients with first-episode schizophrenia: a transcranial magnetic stimulation study. J Psychopharmacol 2016 Aug 15 pii: 0269881116662650. [Epub ahead of print].
17. Cantello R, Gianelli M, Civardi C, et al. Magnetic brain stimulation: the silent period after the motor evoked potential. Neurology 1992;42(10):1951– 9.
18. McCormick DA. GABA as an inhibitory neurotransmitter in human cerebral cortex. J Neurophysiol 1989;62(5):1018– 27.
19. Siebner HR, Dressnandt J, Auer C, et al. Continuous intrathecal baclofen infusions induced a marked increase of the transcranially evoked silent period in a patient with generalized dystonia. Muscle Nerve 1998;21(9):1209– 12.
20. Valls-Sole J, Pascual-Leone A, Wassermann EM, et al. Human motor evoked responses to paired transcranial magnetic stimuli. Electroencephalogr Clin Neurophysiol 1992;85(6):355– 64.
21. Werhahn KJ, Kunesch E, Noachtar S, et al. Differential effects on motorcortical inhibition induced by blockade of GABA uptake in humans. J Physiol 1999;517(2):591– 7.
22. Rothwell JC, Hallett M, Berardelli A, et al. Magnetic stimulation: motor evoked potentials. The International Federation of Clinical Neurophysiology. Electroencephalogr Clin Neurophysiol Suppl 1999;52:97– 103.
23. Rossini PM, Barker AT, Berardelli A, et al. Non-invasive electrical and magnetic stimulation of the brain, spinal cord and roots: basic principles and procedures for routine clinical application. Report of an IFCN committee. Electroencephalogr Clin Neurophysiol 1994;91(2):79– 92.
24. Ziemann U. TMS and drugs. Clin Neurophysiol 2004;115(8):1717– 29.
25. Nakamura H, Kitagawa H, Kawaguchi Y, et al. Intracortical facilitation and inhibition after transcranial magnetic stimulation in conscious humans. J Physiol 1997;498(3):817– 23.
26. Bajbouj M, Lisanby SH, Lang UE, et al. Evidence for impaired cortical inhibition in patients with unipolar major depression. Biol Psychiatry 2006;59(5):395– 400.
27. Lefaucheur JP, Lucas B, Andraud F, et al. Inter-hemispheric asymmetry of motor corticospinal excitability in major depression studied by transcranial magnetic stimulation. J Psychiatr Res 2008;42(5):389– 98.
28. Levinson AJ, Fitzgerald PB, Favalli G, et al. Evidence of cortical inhibitory deficits in major depressive disorder. Biol Psychiatry 2010;67(5):458– 64. doi: 10.1016/ j.biopsych.2009.09.025.
29. Steele JD, Glabus MF, Shajahan PM, et al. Increased cortical inhibition in depression: a prolonged silent period with transcranial magnetic stimulation (TMS). Psychol Med 2000;30(3):565– 70.
30. Chroni E, Lekka NP, Tsoussis I, et al. Effect of exercise on motor evoked potentials elicited by transcranial magnetic stimulation in psychiatric patients. J Clin Neurophysiol 2002;19(3):240– 4.
31. Reid PD, Daniels B, Rybak M, et al. Cortical excitability of psychiatric disorders: reduced post-exercise facilitation in depression compared to schizophrenia and controls. Aust N Z J Psychiatry 2002;36(5):669– 73.
32. Shajahan PM, Glabus MF, Gooding PA, et al. Reduced cortical excitability in depression. Impaired post-exercise motor facilitation with transcranial magnetic stimulation. Br J Psychiatry 1999;174:449– 54.
33. Abarbanel JM, Lemberg T, Yaroslavski U, et al. Electrophysiological response to transcranial magnetic stimulation in depression and schizophrenia. Biol Psychiatry 1996;40(2):148– 50.
34. Grunhaus L, Polak D, Amiaz R, et al. Motor-evoked potential amplitudes elicited by transcranial magnetic stimulation do not differentiate between patients and normal controls. Int J Neuropsychopharmacol 2003;6(4):371– 8.
35. Maeda F, Keenan JP, Pascual-Leone A. Interhemispheric asymmetry of motor cortical excitability in major depression as measured by transcranial magnetic stimulation. Br J Psychiatry 2000;177:169– 73.
36. Chistyakov AV, Kaplan B, Rubichek O, et al. Effect of electroconvulsive therapy on cortical excitability in patients with major depression: a transcranial magnetic stimulation study. Clin Neurophysiol 2005;116(2):386– 92.
37. Chistyakov AV, Kaplan B, Rubichek O, et al. Antidepressant effects of different schedules of repetitive transcranial magnetic stimulation vs. clomipramine in patients with major depression: a relationship to changes in cortical excitability. Int J Neuropsychopharmacol 2005;8(2):223– 33.
38. Bajbouj M, Gallinat J, Niehaus L, et al. Abnormalities of inhibitory neuronal mechanisms in the motor cortex of patients with schizophrenia. Pharmacopsychiatry 2004;37(2):74– 80.
39. Daskalakis ZJ, Christensen BK, Chen R, et al. Evidence for impaired cortical inhibition in schizophrenia using transcranial magnetic stimulation. Arch Gen Psychiatry 2002;59(4):347– 54.
40. Fitzgerald PB, Brown TL, Daskalakis ZJ, et al. A transcranial magnetic stimulation study of inhibitory deficits in the motor cortex in patients with schizophrenia. Psychiatry Res 2002;114(1):11– 22.
41. Fitzgerald PB, Brown TL, Daskalakis ZJ, et al. A transcranial magnetic stimulation study of the effects of olanzapine and risperidone on motor cortical excitability in patients with schizophrenia. Psychopharmacology (Berl) 2002;162(1):74– 81.
42. Fitzgerald PB, Brown TL, Marston NA, et al. Reduced plastic brain responses in schizophrenia: a transcranial magnetic stimulation study. Schizophr Res 2004;71(1):17– 26.
43. Hasan A, Wobrock T, Grefkes C, et al. 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 2012;72(9):744– 51. doi: 10.1016/ j.biopsych.2012.03.005.
44. Herbsman T, Forster L, Molnar C, et al. Motor threshold in transcranial magnetic stimulation: the impact of white matter fiber orientation and skull-to-cortex distance. Hum Brain Mapp 2009;30(7):2044– 55. doi: 10.1002/ hbm.20649.
45. Soubasi E, Chroni E, Gourzis P, et al. Cortical motor neurophysiology of patients with schizophrenia: a study using transcranial magnetic stimulation. Psychiatry Res 2010;176(2– 3):132– 6. doi: 10.1016/ j.psychres.2009.04.003.
46. Wobrock T, Schneider-Axmann T, Retz W, et al. Motor circuit abnormalities in first-episode schizophrenia assessed with transcranial magnetic stimulation. Pharmacopsychiatry 2009;42(5):194– 201. doi: 10.1055/ s-0029-1224137.
47. Eichhammer P, Wiegand R, Kharraz A, et al. Cortical excitability in neuroleptic-naive first-episode schizophrenic patients. Schizophr Res 2004;67(2– 3):253– 9.
48. Oxley T, Fitzgerald PB, Brown TL, et al. Repetitive transcranial magnetic stimulation reveals abnormal plastic response to premotor cortex stimulation in schizophrenia. Biol Psychiatry 2004;56(9):628– 33.
49. Wobrock T, Schneider M, Kadovic D, et al. Reduced cortical inhibition in first-episode schizophrenia. Schizophr Res 2008;105(1– 3):252– 61. doi: 10.1016/ j.schres.2008.06.001.
50. Pascual-Leone A, Manoach DS, Birnbaum R, et al. Motor cortical excitability in schizophrenia. Biol Psychiatry 2002;52(1):24– 31.
51. Enticott PG, Hoy KE, Herring SE, et al. Reduced motor facilitation during action observation in schizophrenia: a mirror neuron deficit? Schizophr Res 2008;102(1– 3):116– 21. doi: 10.1016/ j.schres.2008.04.001.
52. Boroojerdi B, Topper R, Foltys H, et al. Transcallosal inhibition and motor conduction studies in patients with schizophrenia using transcranial magnetic stimulation. Br J Psychiatry 1999;175:375– 9.
53. Fitzgerald PB, Brown TL, Daskalakis ZJ, et al. A study of transcallosal inhibition in schizophrenia using transcranial magnetic stimulation. Schizophr Res 2002;56(3):199– 209.
54. Fitzgerald PB, Brown TL, Marston NA, et al. A transcranial magnetic stimulation study of abnormal cortical inhibition in schizophrenia. Psychiatry Res 2003;118(3):197– 207.
55. Hoy KE, Georgiou-Karistianis N, Laycock R, et al. Using transcranial magnetic stimulation to investigate the cortical origins of motor overflow: a study in schizophrenia and healthy controls. Psychol Med 2007;37(4):583– 94.
56. Lewis DA, Hashimoto T, Volk DW. Cortical inhibitory neurons and schizophrenia. Nat Rev Neurosci 2005;6(4):312– 24.
57. Hashimoto T, Bazmi HH, Mirnics K, et al. Conserved regional patterns of GABA-related transcript expression in the neocortex of subjects with schizophrenia. Am J Psychiatry 2008;165(4):479– 89.
58. Benes FM, Lim B, Matzilevich D, et al. Regulation of the GABA cell phenotype in hippocampus of schizophrenics and bipolars. Proc Natl Acad Sci U S A 2007; 104(24):10164– 9.
59. Benes FM. Model generation and testing to probe neural circuitry in the cingulate cortex of postmortem schizophrenic brain. Schizophr Bull 1998;24(2):219– 30.
60. Benes FM. Regulation of cell cycle and DNA repair in post-mitotic GABA neurons in psychotic disorders. Neuropharmacology 2011;60(7– 8):1232– 42. doi: 10.1016/ j.neuropharm.2010.12.011.
61. Benes FM, McSparren J, Bird ED, et al. Deficits in small interneurons in prefrontal and cingulate cortices of schizophrenic and schizoaffective patients. Arch Gen Psychiatry 1991;48(11):996– 1001.
62. Cohen SM, Tsien RW, Goff DC, et al. The impact of NMDA receptor hypofunction on GABAergic neurons in the pathophysiology of schizophrenia. Schizophr Res 2015;167(1– 3):98– 107. doi: 10.1016/ j.schres.2014.12.026.
63. Taylor SF, Tso IF. GABA abnormalities in schizophrenia: a methodological review of in vivo studies. Schizophr Res 2015;167(1– 3):84– 90. doi: 10.1016/ j.schres.2014.10.011.
64. Strube W, Wobrock T, Bunse T, et al. Impairments in motor-cortical inhibitory network across recent-onset and chronic schizophrenia: a cross-sectional TMS study. Behav Brain Res 2014;264:17– 25. doi: 10.1016/ j.bbr.2014.01.041.
65. Přikryl R, Ustohal L, Kucerová HP, et al. Effect of electroconvulsive therapy on cortical excitability in a patient with long-term remission of schizophrenia: a transcranial magnetic stimulation study. J ECT 2011;27(1):e9– 11. doi: 10.1097/ YCT.0b013e3181dbf785.
66. Zohar J, Stahl S, Moller HJ, et al. A review of the current nomenclature for psychotropic agents and an introduction to the Neuroscience-based Nomenclature. Eur Neuropsychopharmacol 2015;25(12):2318– 25. doi: 10.1016/ j.euroneuro.2015.08.019.
67. Ustohal L. Nová nomenklatura psychofarmak. Psychiatr Praxi 2016;17(3):98– 102.
68. Prikryl R, Ustohal L, Kucerova HP, et al. Paliperidon mediated modification of cortical inhibition. Neuroendocrinol Lett 2009;30(3):396– 9.
69. Frank E, Landgrebe M, Poeppl TB, et al. Antipsychotic treatment with quetiapine increases the cortical silent period. Schizophr Res 2014;156(1):128– 32. doi: 10.1016/ j.schres.2014.03.028.
70. Cha DS, Kudlow PA, Baskaran A, et al. Implications of epigenetic modulation for novel treatment approaches in patients with schizophrenia. Neuropharmacology 2014;77:481– 6. doi: 10.1016/ j.neuropharm.2013.08.038.
71. Hasan A, Mitchell A, Schneider A, et al. Epigenetic dysregulation in schizophrenia: molecular and clinical aspects of histone deacetylase inhibitors. Eur Arch Psychiat Clin Neurosci 2013;263(4):273– 84. doi: 10.1007/ s00406-013-0395-2.
72. Ota VK, Noto C, Gadelha A, et al. Evaluation of neurotransmitter receptor gene expression identifies GABA receptor changes: a follow-up study in antipsychotic-naive patients with first-episode psychosis. J Psychiatr Res 2014;56:130– 6. doi: 10.1016/ j.jpsychires.2014.05.012.
73. Ota VK, Noto C, Gadelha A, et al. Changes in gene expression and methylation in the blood of patients with first-episode psychosis. Schizophr Res 2014;159(2– 3): 358– 64. doi: 10.1016/ j.schres.2014.09.008.
74. Hosák L, Kovařík A, Ustohal L, et al. Duševní poruchy – epigenetické mechanizmy jejich vzniku a farmakologické léčby. Psychiatr Praxi 2015;16(2):45– 8.
75. Concerto C, Lanza G, Cantone M, et al. Different patterns of cortical excitability in major depression and vascular depression: a transcranial magnetic stimulation study. BMC Psychiatry 2013;13:300. doi: 10.1186/ 1471-244X-13-300.
76. Manganotti P, Bortolomasi M, Zanette G, et al. Intravenous clomipramine decreases excitability of human cortex. A study with paired magnetic stimulation. J Neurol Sci 2001;184(1):27– 32.
77. Minelli A, Bortolomasi M, Scassellati C, et al. Effects of intravenous antidepressant drugs on the excitability of human motor cortex: a study with paired magnetic stimulation on depressed patients. Brain Stimul 2010;3(1):15– 21. doi: 10.1016/ j.brs.2009.04.003.
78. Sun Y, Farzan F, Mulsant BH, et al. Indicators for remission of suicidal ideation following magnetic seizure therapy in patients with treatment-resistant depression. JAMA Psychiatry 2016;73(4):337– 45. doi: 10.1001/ jamapsychiatry.2015.3097.
79. Veronezi BP, Moffa AH, Carvalho AF, et al. Evidence for increased motor cortical facilitation and decreased inhibition in atypical depression. Acta Psychiatr Scand 2016;134(2):172– 8. doi: 10.1111/ acps.12565.
80. Croarkin PE, Nakonezny PA, Husain MM, et al. Evidence for pretreatment LICI deficits among depressed children and adolescents with nonresponse to fluoxetine. Brain Stimul 2014;7(2):243– 51. doi: 10.1016/ j.brs.2013.11.006.
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