Cortical inhibition, excitation, and connectivity in schizophrenia: A review of insights from transcranial magnetic stimulation

Schizophrenia Bulletin

Volumn 40, Issue 3, 2014, Pages 685-696

  Rogasch, Nigel C ^a   Daskalakis, Zafiris J ^b   Fitzgerald, Paul B ^a  

^a Monash Alfred Psychiatry Research Centre Central Clinical School Alfred and Monash University ^*  (Australia)

^b UNIVERSITY OF TORONTO   (Canada)

Author keywords

connectivity; cortical inhibition; GABA; NMDA

Indexed keywords

4 AMINOBUTYRIC ACID A RECEPTOR; 4 AMINOBUTYRIC ACID B RECEPTOR;

ARTICLE; CELL POPULATION; CONNECTOME; ELECTROENCEPHALOGRAPHY; HUMAN; NERVE CELL INHIBITION; NERVE CELL STIMULATION; NONHUMAN; PRIORITY JOURNAL; SCHIZOPHRENIA; TRANSCRANIAL MAGNETIC STIMULATION; BRAIN CORTEX; NERVE TRACT; PATHOPHYSIOLOGY; PHYSIOLOGY;

CEREBRAL CORTEX; ELECTROENCEPHALOGRAPHY; HUMANS; NEURAL INHIBITION; NEURAL PATHWAYS; SCHIZOPHRENIA; TRANSCRANIAL MAGNETIC STIMULATION;

EID: 84898946128     PISSN: 05867614     EISSN: 17451701     Source Type: Journal    
DOI: 10.1093/schbul/sbt078     Document Type: Article

References (113)

1. Saha S, Chant D, Welham J, McGrath J. A systematic review of the prevalence of schizophrenia. PLoS Med. 2005;2:e141.
2. van Os J, Kapur S. Schizophrenia. Lancet. 2009;374:635-645.
3. Gold JM. Cognitive deficits as treatment targets in schizophrenia. Schizophr Res. 2004;72:21-28.
4. Lisman J. Excitation, inhibition, local oscillations, or largescale loops: What causes the symptoms of schizophrenia? Curr Opin Neurobiol. 2012;22:537-544.
5. Stephan KE, Friston KJ, Frith CD. Dysconnection in schizophrenia: From abnormal synaptic plasticity to failures of selfmonitoring. Schizophr Bull. 2009;35:509-527.
6. Lewis DA, Hashimoto T, Volk DW. Cortical inhibitory neurons and schizophrenia. Nat Rev Neurosci. 2005;6:312-324.
7. Coyle JT. Glutamate and schizophrenia: Beyond the dopamine hypothesis. Cell Mol Neurobiol. 2006;26:365-384.
8. Hallett M. Transcranial magnetic stimulation: A primer. Neuron. 2007;55:187-199.
9. Reis J, Swayne OB, Vandermeeren Y, et al. Contribution of transcranial magnetic stimulation to the understanding of cortical mechanisms involved in motor control. J Physiol. 2008;586:325-351.
10. Rogasch NC, Fitzgerald PB. Assessing cortical network properties using TMS-EEG [published online ahead of print February 29, 2012]. Hum Brain Mapp. doi: 10.1002/ hbm.22016.
11. Siebner HR, Bergmann TO, Bestmann S, et al. Consensus paper: Combining transcranial stimulation with neuroimaging. Brain Stimul. 2009;2:58-80.
12. Akbarian S, Kim JJ, Potkin SG, et al. Gene expression for glutamic acid decarboxylase is reduced without loss of neurons in prefrontal cortex of schizophrenics. Arch Gen Psychiatry. 1995;52:258-266.
13. Hashimoto T, Volk DW, Eggan SM, et al. Gene expression deficits in a subclass of GABA neurons in the prefrontal cortex of subjects with schizophrenia. J Neurosci. 2003;23:6315-6326.
14. Beneyto M, Meador-Woodruff JH. Lamina-specific abnormalities of NMDA receptor-Associated postsynaptic protein transcripts in the prefrontal cortex in schizophrenia and bipolar disorder. Neuropsychopharmacology. 2008;33:2175-2186.
15. Akbarian S, Sucher NJ, Bradley D, et al. Selective alterations in gene expression for NMDA receptor subunits in prefrontal cortex of schizophrenics. J Neurosci. 1996;16:19-30.
16. Bitanihirwe BK, Lim MP, Kelley JF, Kaneko T, Woo TU. Glutamatergic deficits and parvalbumin-containing inhibitory neurons in the prefrontal cortex in schizophrenia. BMC Psychiatry. 2009;9:71.
17. Glantz LA, Lewis DA. Decreased dendritic spine density on prefrontal cortical pyramidal neurons in schizophrenia. Arch Gen Psychiatry. 2000;57:65-73.
18. Hashimoto T, Bazmi HH, Mirnics K, Wu Q, Sampson AR, Lewis DA. Conserved regional patterns of GABA-related transcript expression in the neocortex of subjects with schizophrenia. Am J Psychiatry. 2008;165:479-489.
19. Kujirai T, Caramia MD, Rothwell JC, et al. Corticocortical inhibition in human motor cortex. J Physiol. 1993;471: 501-519.
20. McCormick DA. GABA as an inhibitory neurotransmitter in human cerebral cortex. J Neurophysiol. 1989;62:1018-1027.
21. Di Lazzaro V, Oliviero A, Meglio M, et al. Direct demonstration of the effect of lorazepam on the excitability of the human motor cortex. Clin Neurophysiol. 2000;111:794-799.
22. Ziemann U, Lönnecker S, Steinhoff BJ, Paulus W. The effect of lorazepam on the motor cortical excitability in man. Exp Brain Res. 1996;109:127-135.
23. 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;72:744-751.
24. Wobrock T, Schneider M, Kadovic D, et al. Reduced cortical inhibition in first-episode schizophrenia. Schizophr Res. 2008;105:252-261.
25. Wobrock T, Schneider-Axmann T, Retz W, et al. Motor circuit abnormalities in first-episode schizophrenia assessed with transcranial magnetic stimulation. Pharmacopsychiatry. 2009;42:194-201.
26. Wobrock T, Hasan A, Malchow B, et al. Increased cortical inhibition deficits in first-episode schizophrenia with comorbid cannabis abuse. Psychopharmacology (Berl). 2010;208:353-363.
27. Hasan A, Nitsche MA, Rein B, et al. Dysfunctional longterm potentiation-like plasticity in schizophrenia revealed by transcranial direct current stimulation. Behav Brain Res. 2011;224:15-22.
28. Fitzgerald PB, Brown TL, Daskalakis ZJ, Kulkarni J. A transcranial magnetic stimulation study of inhibitory deficits in the motor cortex in patients with schizophrenia. Psychiatry Res. 2002;114:11-22.
29. Daskalakis ZJ, Christensen BK, Chen R, Fitzgerald PB, Zipursky RB, Kapur S. Evidence for impaired cortical inhibition in schizophrenia using transcranial magnetic stimulation. Arch Gen Psychiatry. 2002;59:347-354.
30. Pascual-Leone A, Manoach DS, Birnbaum R, Goff DC. Motor cortical excitability in schizophrenia. Biol Psychiatry. 2002;52:24-31.
31. Fitzgerald PB, Brown TL, Marston NA, et al. Reduced plastic brain responses in schizophrenia: A transcranial magnetic stimulation study. Schizophr Res. 2004;71:17-26.
32. Oxley T, Fitzgerald PB, Brown TL, de Castella A, Daskalakis ZJ, Kulkarni J. Repetitive transcranial magnetic stimulation reveals abnormal plastic response to premotor cortex stimulation in schizophrenia. Biol Psychiatry. 2004;56:628-633.
33. Eichhammer P, Wiegand R, Kharraz A, Langguth B, Binder H, Hajak G. Cortical excitability in neuroleptic-naive first-episode schizophrenic patients. Schizophr Res. 2004;67:253-259.
34. Daskalakis ZJ, Christensen BK, Fitzgerald PB, Moller B, Fountain SI, Chen R. Increased cortical inhibition in persons with schizophrenia treated with clozapine. J Psychopharmacol. 2008;22:203-209.
35. Liu SK, Fitzgerald PB, Daigle M, Chen R, Daskalakis ZJ. The relationship between cortical inhibition, antipsychotic treatment, and the symptoms of schizophrenia. Biol Psychiatry. 2009;65:503-509.
36. Hasan A, Nitsche MA, Herrmann M, et al. Impaired longterm depression in schizophrenia: A cathodal tDCS pilot study. Brain Stimul. 2012;5:475-483.
37. Fitzgerald PB, Brown TL, Daskalakis ZJ, Kulkarni J. A transcranial magnetic stimulation study of the effects of olanzapine and risperidone on motor cortical excitability in patients with schizophrenia. Psychopharmacology (Berl). 2002;162:74-81.
38. Valls-Solé J, Pascual-Leone A, Wassermann EM, Hallett M. Human motor evoked responses to paired transcranial magnetic stimuli. Electroencephalogr Clin Neurophysiol. 1992;85:355-364.
39. Fuhr P, Agostino R, Hallett M. Spinal motor neuron excitability during the silent period after cortical stimulation. Electroencephalogr Clin Neurophysiol. 1991;81:257-262.
40. Deisz RA. GABA(B) receptor-mediated effects in human and rat neocortical neurones in vitro. Neuropharmacology. 1999;38:1755-1766.
41. Farzan F, Barr MS, Levinson AJ, et al. Reliability of longinterval cortical inhibition in healthy human subjects: A TMS-EEG study. J Neurophysiol. 2010;104:1339-1346.
42. Sanger TD, Garg RR, Chen R. Interactions between two different inhibitory systems in the human motor cortex. J Physiol. 2001;530:307-317.
43. Fitzgerald PB, Brown TL, Marston NA, et al. A transcranial magnetic stimulation study of abnormal cortical inhibition in schizophrenia. Psychiatry Res. 2003;118:197-207.
44. Fitzgerald PB, Brown TL, Daskalakis ZJ, deCastella A, Kulkarni J. A study of transcallosal inhibition in schizophrenia using transcranial magnetic stimulation. Schizophr Res. 2002;56:199-209.
45. Bajbouj M, Gallinat J, Niehaus L, Lang UE, Roricht S, Meyer BU. Abnormalities of inhibitory neuronal mechanisms in the motor cortex of patients with schizophrenia. Pharmacopsychiatry. 2004;37:74-80.
46. Soubasi E, Chroni E, Gourzis P, Zisis A, Beratis S, Papathanasopoulos P. Cortical motor neurophysiology of patients with schizophrenia: A study using transcranial magnetic stimulation. Psychiatry Res. 2010;176:132-136.
47. Puri BK, Davey NJ, Ellaway PH, Lewis SW. An investigation of motor function in schizophrenia using transcranial magnetic stimulation of the motor cortex. Br J Psychiatry. 1996;169:690-695.
48. Davey NJ, Puri BK, Lewis HS, Lewis SW, Ellaway PH. Effects of antipsychotic medication on electromyographic responses to transcranial magnetic stimulation of the motor cortex in schizophrenia. J Neurol Neurosurg Psychiatry. 1997;63:468-473.
49. Frantseva MV, Fitzgerald PB, Chen R, Möller B, Daigle M, Daskalakis ZJ. Evidence for impaired long-Term potentiation in schizophrenia and its relationship to motor skill learning. Cereb Cortex. 2008;18:990-996.
50. Hasan A, Aborowa R, Nitsche MA, et al. Abnormal bihemispheric responses in schizophrenia patients following cathodal transcranial direct stimulation. Eur Arch Psychiatry Clin Neurosci. 2012;262:415-423.
51. Saka MC, Atbasoglu EC, Ozgüven HD, Sener HO, Ozay E. Cortical inhibition in first-degree relatives of schizophrenic patients assessed with transcranial magnetic stimulation. Int J Neuropsychopharmacol. 2005;8:595-599.
52. Wu Y, Blichowski M, Daskalakis ZJ, et al. Evidence that clozapine directly interacts on the GABAB receptor. Neuroreport. 2011;22:637-641.
53. Gandal MJ, Sisti J, Klook K, et al. GABAB-mediated rescue of altered excitatory-inhibitory balance, gamma synchrony and behavioral deficits following constitutive NMDARhypofunction. Transl Psychiatry. 2012;2:e142.
54. Ziemann U, Tergau F, Wassermann EM, Wischer S, Hildebrandt J, Paulus W. Demonstration of facilitatory I wave interaction in the human motor cortex by paired transcranial magnetic stimulation. J Physiol. 1998;511:181-190.
55. Ziemann U, Chen R, Cohen LG, Hallett M. Dextromethorphan decreases the excitability of the human motor cortex. Neurology. 1998;51:1320-1324.
56. Schwenkreis P, Witscher K, Janssen F, et al. Influence of the N-methyl-D-Aspartate antagonist memantine on human motor cortex excitability. Neurosci Lett. 1999;270:137-140.
57. Mori F, Ribolsi M, Kusayanagi H, et al. Genetic variants of the NMDA receptor influence cortical excitability and plasticity in humans. J Neurophysiol. 2011;106:1637-1643.
58. Di Lazzaro V, Oliviero A, Profice P, et al. Ketamine increases human motor cortex excitability to transcranial magnetic stimulation. J Physiol. 2003;547:485-496.
59. Ziemann U, Tergau F, Wischer S, Hildebrandt J, Paulus W. Pharmacological control of facilitatory I-wave interaction in the human motor cortex. A paired transcranial magnetic stimulation study. Electroencephalogr Clin Neurophysiol. 1998;109:321-330.
60. Bullmore E, Sporns O. Complex brain networks: Graph theoretical analysis of structural and functional systems. Nat Rev Neurosci. 2009;10:186-198.
61. Fries P. A mechanism for cognitive dynamics: Neuronal communication through neuronal coherence. Trends Cogn Sci. 2005;9:474-480.
62. Friston KJ, Frith CD. Schizophrenia: A disconnection syndromé Clin Neurosci. 1995;3:89-97.
63. Fornito A, Zalesky A, Pantelis C, Bullmore ET. Schizophrenia, neuroimaging and connectomics. Neuroimage. 2012; 62:2296-2314.
64. Ellison-Wright I, Bullmore E. Meta-Analysis of diffusion tensor imaging studies in schizophrenia. Schizophr Res. 2009;108:3-10.
65. Uhlhaas PJ. Dysconnectivity, large-scale networks and neuronal dynamics in schizophrenia. Curr Opin Neurobiol. 2013;23:283-290.
66. Ferbert A, Priori A, Rothwell JC, Day BL, Colebatch JG, Marsden CD. Interhemispheric inhibition of the human motor cortex. J Physiol. 1992;453:525-546.
67. Daskalakis ZJ, Christensen BK, Fitzgerald PB, Roshan L, Chen R. The mechanisms of interhemispheric inhibition in the human motor cortex. J Physiol. 2002;543:317-326.
68. Boroojerdi B, Diefenbach K, Ferbert A. Transcallosal inhibition in cortical and subcortical cerebral vascular lesions. J Neurol Sci. 1996;144:160-170.
69. Hoy KE, Georgiou-Karistianis N, Laycock R, Fitzgerald PB. A transcranial magnetic stimulation study of transcallosal inhibition and facilitation in schizophrenia. J Clin Neurosci. 2008;15:863-867.
70. Boroojerdi B, Töpper R, Foltys H, Meincke U. Transcallosal inhibition and motor conduction studies in patients with schizophrenia using transcranial magnetic stimulation. Br J Psychiatry. 1999;175:375-379.
71. Höppner J, Kunesch E, Grossmann A, et al. Dysfunction of transcallosally mediated motor inhibition and callosal morphology in patients with schizophrenia. Acta Psychiatr Scand. 2001;104:227-235.
72. Lee H, Gunraj C, Chen R. The effects of inhibitory and facilitatory intracortical circuits on interhemispheric inhibition in the human motor cortex. J Physiol. 2007;580:1021-1032.
73. Hoy KE, Georgiou-Karistianis N, Farrow M, Fitzgerald PB. Neurological soft signs in schizophrenia: Investigating motor overflow. World J Biol Psychiatry. 2009;10:763-771.
74. Hoy KE, Georgiou-Karistianis N, Laycock R, Fitzgerald PB. Using transcranial magnetic stimulation to investigate the cortical origins of motor overflow: A study in schizophrenia and healthy controls. Psychol Med. 2007;37:583-594.
75. Stagg CJ, Nitsche MA. Physiological basis of transcranial direct current stimulation. Neuroscientist. 2011;17:37-53.
76. Mochizuki H, Huang YZ, Rothwell JC. Interhemispheric interaction between human dorsal premotor and contralateral primary motor cortex. J Physiol. 2004;561:331-338.
77. Bäumer T, Bock F, Koch G, et al. Magnetic stimulation of human premotor or motor cortex produces interhemispheric facilitation through distinct pathways. J Physiol. 2006;572:857-868.
78. Fadiga L, Fogassi L, Pavesi G, Rizzolatti G. Motor facilitation during action observation: A magnetic stimulation study. J Neurophysiol. 1995;73:2608-2611.
79. Maeda F, Kleiner-Fisman G, Pascual-Leone A. Motor facilitation while observing hand actions: Specificity of the effect and role of observer's orientation. J Neurophysiol. 2002;87:1329-1335.
80. Cattaneo L, Rizzolatti G. The mirror neuron system. Arch Neurol. 2009;66:557-560.
81. Gerschlager W, Siebner HR, Rothwell JC. Decreased corticospinal excitability after subthreshold 1 Hz rTMS over lateral premotor cortex. Neurology. 2001;57:449-455.
82. Ribolsi M, Mori F, Magni V, et al. Impaired inter-hemispheric facilitatory connectivity in schizophrenia. Clin Neurophysiol. 2011;122:512-517.
83. Enticott PG, Hoy KE, Herring SE, Johnston PJ, Daskalakis ZJ, Fitzgerald PB. Reduced motor facilitation during action observation in schizophrenia: A mirror neuron deficit? Schizophr Res. 2008;102:116-121.
84. Koch G, Fernandez Del Olmo M, Cheeran B, et al. Focal stimulation of the posterior parietal cortex increases the excitability of the ipsilateral motor cortex. J Neurosci. 2007;27:6815-6822.
85. Koch G, Ribolsi M, Mori F, et al. Connectivity between posterior parietal cortex and ipsilateral motor cortex is altered in schizophrenia. Biol Psychiatry. 2008;64:815-819.
86. Guller Y, Ferrarelli F, Shackman AJ, et al. Probing thalamic integrity in schizophrenia using concurrent transcranial magnetic stimulation and functional magnetic resonance imaging. Arch Gen Psychiatry. 2012;69:662-671.
87. Ugawa Y, Uesaka Y, Terao Y, Hanajima R, Kanazawa I. Magnetic stimulation over the cerebellum in humans. Ann Neurol. 1995;37:703-713.
88. Daskalakis ZJ, Paradiso GO, Christensen BK, Fitzgerald PB, Gunraj C, Chen R. Exploring the connectivity between the cerebellum and motor cortex in humans. J Physiol. 2004;557:689-700.
89. Daskalakis ZJ, Christensen BK, Fitzgerald PB, Fountain SI, Chen R. Reduced cerebellar inhibition in schizophrenia: A preliminary study. Am J Psychiatry. 2005;162:1203-1205.
90. Yizhar O, Fenno LE, Prigge M, et al. Neocortical excitation/ inhibition balance in information processing and social dysfunction. Nature. 2011;477:171-178.
91. Sohal VS, Zhang F, Yizhar O, Deisseroth K. Parvalbumin neurons and gamma rhythms enhance cortical circuit performance. Nature. 2009;459:698-702.
92. Cardin JA, Carlén M, Meletis K, et al. Driving fast-spiking cells induces gamma rhythm and controls sensory responses. Nature. 2009;459:663-667.
93. Carlén M, Meletis K, Siegle JH, et al. A critical role for NMDA receptors in parvalbumin interneurons for gamma rhythm induction and behavior. Mol Psychiatry. 2012;17:537-548.
94. Sun Y, Farzan F, Barr MS, et al. ? oscillations in schizophrenia: Mechanisms and clinical significance. Brain Res. 2011;1413:98-114.
95. Uhlhaas PJ, Singer W. Abnormal neural oscillations and synchrony in schizophrenia. Nat Rev Neurosci. 2010;11:100-113.
96. Ilmoniemi RJ, Virtanen J, Ruohonen J, et al. Neuronal responses to magnetic stimulation reveal cortical reactivity and connectivity. Neuroreport. 1997;8:3537-3540.
97. McClintock SM, Freitas C, Oberman L, Lisanby SH, Pascual-Leone A. Transcranial magnetic stimulation: A neuroscientific probe of cortical function in schizophrenia. Biol Psychiatry. 2011;70:19-27.
98. Massimini M, Ferrarelli F, Huber R, Esser SK, Singh H, Tononi G. Breakdown of cortical effective connectivity during sleep. Science. 2005;309:2228-2232.
99. Litvak V, Komssi S, Scherg M, et al. Artifact correction and source analysis of early electroencephalographic responses evoked by transcranial magnetic stimulation over primary motor cortex. Neuroimage. 2007;37:56-70.
100. Rosanova M, Casali A, Bellina V, Resta F, Mariotti M, Massimini M. Natural frequencies of human corticothalamic circuits. J Neurosci. 2009;29:7679-7685.
101. Levit-Binnun N, Litvak V, Pratt H, Moses E, Zaroor M, Peled A. Differences in TMS-evoked responses between schizophrenia patients and healthy controls can be observed without a dedicated EEG system. Clin Neurophysiol. 2010;121:332-339.
102. Ferrarelli F, Sarasso S, Guller Y, et al. Reduced natural oscillatory frequency of frontal thalamocortical circuits in schizophrenia. Arch Gen Psychiatry. 2012;69:766-774.
103. Frantseva M, Cui J, Farzan F, et al. Disrupted cortical conductivity in schizophrenia: TMS-EEG study [published online ahead of print October 05, 2012]. Cereb Cortex. doi: 10.1093/cercor/bhs304.
104. Ferrarelli F, Massimini M, Peterson MJ, et al. Reduced evoked gamma oscillations in the frontal cortex in schizophrenia patients: A TMS/EEG study. Am J Psychiatry. 2008;165:996-1005.
105. Kohl MM, Paulsen O. The roles of GABAB receptors in cortical network activity. Adv Pharmacol. 2010;58:205-229.
106. Daskalakis ZJ, Farzan F, Barr MS, Maller JJ, Chen R, Fitzgerald PB. Long-interval cortical inhibition from the dorsolateral prefrontal cortex: A TMS-EEG study. Neuropsychopharmacology. 2008;33:2860-2869.
107. Rogasch NC, Daskalakis ZJ, Fitzgerald PB. Mechanisms underlying long-interval cortical inhibition in the human motor cortex: A TMS-EEG study. J Neurophysiol. 2013;109:89-98.
108. Fitzgerald PB, Maller JJ, Hoy K, Farzan F, Daskalakis ZJ. GABA and cortical inhibition in motor and non-motor regions using combined TMS-EEG: A time analysis. Clin Neurophysiol. 2009;120:1706-1710.
109. Fitzgerald PB, Daskalakis ZJ, Hoy K, et al. Cortical inhibition in motor and non-motor regions: A combined TMSEEG study. Clin EEG Neurosci. 2008;39:112-117.
110. Farzan F, Barr MS, Wong W, Chen R, Fitzgerald PB, Daskalakis ZJ. Suppression of gamma-oscillations in the dorsolateral prefrontal cortex following long interval cortical inhibition: A TMS-EEG study. Neuropsychopharmacology. 2009;34:1543-1551.
111. Farzan F, Barr MS, Levinson AJ, et al. Evidence for gamma inhibition deficits in the dorsolateral prefrontal cortex of patients with schizophrenia. Brain. 2010;133:1505-1514.
112. Daskalakis ZJ, Farzan F, Barr MS, et al. Evaluating the relationship between long interval cortical inhibition, working memory and gamma band activity in the dorsolateral prefrontal cortex. Clin EEG Neurosci. 2008;39:150-155.
113. Voineskos AN, Farzan F, Barr MS, et al. The role of the corpus callosum in transcranial magnetic stimulation induced interhemispheric signal propagation. Biol Psychiatry. 2010; 68:825-831.