Gamma oscillations in schizophrenia: Mechanisms and clinical significance

Brain Research

Volumn 1413, Issue , 2011, Pages 98-114

  Sun, Yinming ^a   Farzan, Faranak ^a   Barr, Mera S ^a   Kirihara, Kenji ^b   Fitzgerald, Paul B ^c   Light, Gregory A ^b   Daskalakis, Zafiris J ^a  

^a UNIVERSITY OF TORONTO   (Canada)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c Australia   (Australia)

Author keywords

Electroencephalography; Endophenotype; GABAergic interneuron; Gamma oscillation; Schizophrenia

Indexed keywords

4 AMINOBUTYRIC ACID A RECEPTOR; 4 AMINOBUTYRIC ACID B RECEPTOR; GLUTAMATE RECEPTOR; N METHYL DEXTRO ASPARTIC ACID RECEPTOR;

AUDITORY STIMULATION; COGNITION; ELECTROENCEPHALOGRAPHY; ENDOPHENOTYPE; EVENT RELATED POTENTIAL; GABAERGIC TRANSMISSION; GAMMA OSCILLATION; HUMAN; NEUROBIOLOGY; OSCILLATION; PREFRONTAL CORTEX; PRIORITY JOURNAL; REVIEW; SCHIZOPHRENIA; SENSORY GATING; STEADY STATE;

ANIMALS; BRAIN WAVES; ELECTROCARDIOGRAPHY; ENDOPHENOTYPES; HUMANS; SCHIZOPHRENIA;

EID: 80052491314     PISSN: 00068993     EISSN: 18726240     Source Type: Journal    
DOI: 10.1016/j.brainres.2011.06.065     Document Type: Review

References (154)

1. A. Abi-Dargham, O. Mawlawi, I. Lombardo, R. Gil, D. Martinez, Y. Huang, D.R. Hwang, J. Keilp, L. Kochan, R. Van Heertum, J.M. Gorman, and M. Laruelle Prefrontal dopamine D1 receptors and working memory in schizophrenia J. Neurosci. 22 2002 3708 3719 (Pubitemid 37465776)
2. L.E. Adler, E. Pachtman, R.D. Franks, M. Pecevich, M.C. Waldo, and R. Freedman Neurophysiological evidence for a defect in neuronal mechanisms involved in sensory gating in schizophrenia Biol. Psychiatry 17 1982 639 654 (Pubitemid 12090209)
3. E.D. Adrian The impulses produced by sensory nerve endings: Part I J. Physiol. 61 1926 49 72
4. S. Akbarian, J.J. Kim, S.G. Potkin, J.O. Hagman, A. Tafazzoli, W.E. Bunney Jr.; and E.G. Jones Gene expression for glutamic acid decarboxylase is reduced without loss of neurons in prefrontal cortex of schizophrenics Arch. Gen. Psychiatry 52 1995 258 266
5. S. Alagarsamy, M.J. Marino, S.T. Rouse, R.W.t. Gereau, S.F. Heinemann, and P.J. Conn Activation of NMDA receptors reverses desensitization of mGluR5 in native and recombinant systems Nat. Neurosci. 2 1999 234 240 (Pubitemid 30491293)
6. V.L. Arvanov, and R.Y. Wang NMDA-induced response in pyramidal neurons of the rat medial prefrontal cortex slices consists of NMDA and non-NMDA components Brain Res. 768 1997 361 364 (Pubitemid 27433515)
7. N. Axmacher, M.M. Henseler, O. Jensen, I. Weinreich, C.E. Elger, and J. Fell Cross-frequency coupling supports multi-item working memory in the human hippocampus Proc. Natl. Acad. Sci. U.S.A. 107 2010 3228 3233
8. A. Baddeley Working memory Science 255 1992 556 559
9. A.T. Barker An introduction to the basic principles of magnetic nerve stimulation J. Clin. Neurophysiol. 8 1991 26 37
10. 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
11. M.S. Barr, F. Farzan, L.C. Tran, R. Chen, P.B. Fitzgerald, and Z.J. Daskalakis Evidence for excessive frontal evoked gamma oscillatory activity in schizophrenia during working memory Schizophr. Res. 121 2010 146 152
12. M.S. Barr, F. Farzan, T. Arenovich, R. Chen, P.B. Fitzgerald, and Z.J. Daskalakis The Effect of Repetitive Transcranial Magnetic Stimulation on Gamma Oscillatory Activity in Schizophrenia PLoS One 6 7 2011 e22627
13. M. Bartos, I. Vida, M. Frotscher, A. Meyer, H. Monyer, J.R. Geiger, and P. Jonas Fast synaptic inhibition promotes synchronized gamma oscillations in hippocampal interneuron networks Proc. Natl. Acad. Sci. U.S.A. 99 2002 13222 13227
14. M. Bartos, I. Vida, and P. Jonas Synaptic mechanisms of synchronized gamma oscillations in inhibitory interneuron networks Nat. Rev. Neurosci. 8 2007 45 56 (Pubitemid 46011998)
15. C. Basar-Eroglu, A. Brand, H. Hildebrandt, K. Karolina Kedzior, B. Mathes, and C. Schmiedt Working memory related gamma oscillations in schizophrenia patients Int. J. Psychophysiol. 64 2007 39 45 (Pubitemid 46483768)
16. A. Benali, J. Trippe, E. Weiler, A. Mix, E. Petrasch-Parwez, W. Girzalsky, U.T. Eysel, R. Erdmann, and K. Funke Theta-burst transcranial magnetic stimulation alters cortical inhibition J. Neurosci. 31 2011 1193 1203
17. F.M. Benes, and S. Berretta GABAergic interneurons: implications for understanding schizophrenia and bipolar disorder Neuropsychopharmacology 25 2001 1 27 (Pubitemid 32493819)
18. M.V. Bennett, and R.S. Zukin Electrical coupling and neuronal synchronization in the Mammalian brain Neuron 41 2004 495 511 (Pubitemid 38253063)
19. W. Bialek, F. Rieke, R.R. de Ruyter van Steveninck, and D. Warland Reading a neural code Science 252 1991 1854 1857 (Pubitemid 21917111)
20. N.N. Boutros, C. Arfken, S. Galderisi, J. Warrick, G. Pratt, and W. Iacono The status of spectral EEG abnormality as a diagnostic test for schizophrenia Schizophr. Res. 99 2008 225 237
21. C.A. Brenner, O. Sporns, P.H. Lysaker, and B.F. O'Donnell EEG synchronization to modulated auditory tones in schizophrenia, schizoaffective disorder, and schizotypal personality disorder Am. J. Psychiatry 160 2003 2238 2240 (Pubitemid 39619622)
22. J.T. Brown, C.H. Davies, and A.D. Randall Synaptic activation of GABA(B) receptors regulates neuronal network activity and entrainment Eur. J. Neurosci. 25 2007 2982 2990 (Pubitemid 46888799)
23. P. Brown, A. Oliviero, P. Mazzone, A. Insola, P. Tonali, and V. Di Lazzaro Dopamine dependency of oscillations between subthalamic nucleus and pallidum in Parkinson's disease J. Neurosci. 21 2001 1033 1038 (Pubitemid 32163143)
24. G. Buzsáki Rhythms of the Brain, Vol 2006 Oxford University Press
25. R.T. Canolty, E. Edwards, S.S. Dalal, M. Soltani, S.S. Nagarajan, H.E. Kirsch, M.S. Berger, N.M. Barbaro, and R.T. Knight High gamma power is phase-locked to theta oscillations in human neocortex Science 313 2006 1626 1628 (Pubitemid 44414034)
26. L. Chen, M. Muhlhauser, and C.R. Yang Glycine tranporter-1 blockade potentiates NMDA-mediated responses in rat prefrontal cortical neurons in vitro and in vivo J. Neurophysiol. 89 2003 691 703 (Pubitemid 36206118)
27. R.Y. Cho, R.O. Konecky, and C.S. Carter Impairments in frontal cortical gamma synchrony and cognitive control in schizophrenia Proc. Natl. Acad. Sci. U.S.A. 103 2006 19878 19883 (Pubitemid 46037524)
28. B.A. Clementz, L.D. Blumenfeld, and S. Cobb The gamma band response may account for poor P50 suppression in schizophrenia Neuroreport 8 1997 3889 3893 (Pubitemid 28027204)
29. B.A. Clementz, and L.D. Blumenfeld Multichannel electroencephalographic assessment of auditory evoked response suppression in schizophrenia Exp. Brain Res. 139 2001 377 390 (Pubitemid 32703944)
30. S.M. Cochran, M. Kennedy, C.E. McKerchar, L.J. Steward, J.A. Pratt, and B.J. Morris Induction of metabolic hypofunction and neurochemical deficits after chronic intermittent exposure to phencyclidine: differential modulation by antipsychotic drugs Neuropsychopharmacology 28 2003 265 275
31. F. Conde, J.S. Lund, D.M. Jacobowitz, K.G. Baimbridge, and D.A. Lewis Local circuit neurons immunoreactive for calretinin, calbindin D-28 k or parvalbumin in monkey prefrontal cortex: distribution and morphology J. Comp. Neurol. 341 1994 95 116 (Pubitemid 24054631)
32. I. Creese, D.R. Burt, and S.H. Snyder Dopamine receptor binding predicts clinical and pharmacological potencies of antischizophrenic drugs Science 192 1976 481 483
33. M.O. Cunningham, M.A. Whittington, A. Bibbig, A. Roopun, F.E. LeBeau, A. Vogt, H. Monyer, E.H. Buhl, and R.D. Traub A role for fast rhythmic bursting neurons in cortical gamma oscillations in vitro Proc. Natl. Acad. Sci. U.S.A. 101 2004 7152 7157 (Pubitemid 38596458)
34. M.O. Cunningham, J. Hunt, S. Middleton, F.E. LeBeau, M.J. Gillies, C.H. Davies, P.R. Maycox, M.A. Whittington, and C. Racca Region-specific reduction in entorhinal gamma oscillations and parvalbumin-immunoreactive neurons in animal models of psychiatric illness J. Neurosci. 26 2006 2767 2776 (Pubitemid 43357860)
35. 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)
36. Z.J. Daskalakis, B. Moller, B.K. Christensen, P.B. Fitzgerald, C. Gunraj, and R. Chen The effects of repetitive transcranial magnetic stimulation on cortical inhibition in healthy human subjects Exp. Brain Res. 174 2006 403 412 (Pubitemid 44451034)
37. Z.J. Daskalakis, P.B. Fitzgerald, and B.K. Christensen The role of cortical inhibition in the pathophysiology and treatment of schizophrenia Brain Res. Rev. 56 2007 427 442 (Pubitemid 350176600)
38. 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
39. K.L. Davis, R.S. Kahn, G. Ko, and M. Davidson Dopamine in schizophrenia: a review and reconceptualization Am. J. Psychiatry 148 1991 1474 1486
40. T. Demiralp, Z. Bayraktaroglu, D. Lenz, S. Junge, N.A. Busch, B. Maess, M. Ergen, and C.S. Herrmann Gamma amplitudes are coupled to theta phase in human EEG during visual perception Int. J. Psychophysiol. 64 2007 24 30 (Pubitemid 46483766)
41. S.K. Esser, S.L. Hill, and G. Tononi Modeling the effects of transcranial magnetic stimulation on cortical circuits J. Neurophysiol. 94 2005 622 639 (Pubitemid 40923274)
42. F. Farzan, M.S. Barr, W. Wong, R. Chen, P.B. Fitzgerald, and Z.J. Daskalakis Suppression of gamma-oscillations in the dorsolateral prefrontal cortex following long interval cortical inhibition: a TMS-EEG study Neuropsychopharmacology 34 2009 1543 1551
43. F. Farzan, M.S. Barr, A.J. Levinson, R. Chen, W. Wong, P.B. Fitzgerald, and Z.J. Daskalakis Reliability of long-interval cortical inhibition in healthy human subjects: a TMS-EEG study J. Neurophysiol. 104 2010 1339 1346
44. F. Farzan, M.S. Barr, A.J. Levinson, R. Chen, W. Wong, P.B. Fitzgerald, and Z.J. Daskalakis Evidence for gamma inhibition deficits in the dorsolateral prefrontal cortex of patients with schizophrenia Brain 133 2010 1505 1514
45. H.J. Faulkner, R.D. Traub, and M.A. Whittington Anaesthetic/amnesic agents disrupt beta frequency oscillations associated with potentiation of excitatory synaptic potentials in the rat hippocampal slice Br. J. Pharmacol. 128 1999 1813 1825 (Pubitemid 30011896)
46. A. Fisahn, F.G. Pike, E.H. Buhl, and O. Paulsen Cholinergic induction of network oscillations at 40 Hz in the hippocampus in vitro Nature 394 1998 186 189 (Pubitemid 28325972)
47. J.M. Ford, B.J. Roach, W.O. Faustman, and D.H. Mathalon Out-of-synch and out-of-sorts: dysfunction of motor-sensory communication in schizophrenia Biol. Psychiatry 63 2008 736 743 (Pubitemid 351400763)
48. R. Freedman, L.E. Adler, M. Myles-Worsley, H.T. Nagamoto, C. Miller, M. Kisley, K. McRae, E. Cawthra, and M. Waldo Inhibitory gating of an evoked response to repeated auditory stimuli in schizophrenic and normal subjects. Human recordings, computer simulation, and an animal model Arch. Gen. Psychiatry 53 1996 1114 1121 (Pubitemid 26422063)
49. I. Frund, J. Schadow, N.A. Busch, U. Korner, and C.S. Herrmann Evoked gamma oscillations in human scalp EEG are test-retest reliable Clin. Neurophysiol. 118 2007 221 227 (Pubitemid 44960932)
50. R. Galambos, S. Makeig, and P.J. Talmachoff A 40-Hz auditory potential recorded from the human scalp Proc. Natl. Acad. Sci. U.S.A. 78 1981 2643 2647 (Pubitemid 11067263)
51. M. Galarreta, and S. Hestrin A network of fast-spiking cells in the neocortex connected by electrical synapses Nature 402 1999 72 75
52. J. Gallinat, G. Winterer, C.S. Herrmann, and D. Senkowski Reduced oscillatory gamma-band responses in unmedicated schizophrenic patients indicate impaired frontal network processing Clin. Neurophysiol. 115 2004 1863 1874 (Pubitemid 38952954)
53. J.M. Gold Cognitive deficits as treatment targets in schizophrenia Schizophr. Res. 72 2004 21 28 (Pubitemid 39452902)
54. I.I. Gottesman, and T.D. Gould The endophenotype concept in psychiatry: etymology and strategic intentions Am. J. Psychiatry 160 2003 636 645 (Pubitemid 41079594)
55. C.M. Gray, and D.A. McCormick Chattering cells: superficial pyramidal neurons contributing to the generation of synchronous oscillations in the visual cortex Science 274 1996 109 113 (Pubitemid 26332736)
56. M.F. Green What are the functional consequences of neurocognitive deficits in schizophrenia? Am. J. Psychiatry 153 1996 321 330 (Pubitemid 26074706)
57. J. Griffith, L.D. Hoffer, L.E. Adler, G.O. Zerbe, and R. Freedman Effects of sound intensity on a midlatency evoked response to repeated auditory stimuli in schizophrenic and normal subjects Psychophysiology 32 1995 460 466
58. D. Grozeva, G. Kirov, D. Ivanov, I.R. Jones, L. Jones, E.K. Green, D.M. St Clair, A.H. Young, N. Ferrier, A.E. Farmer, P. McGuffin, P.A. Holmans, M.J. Owen, M.C. O'Donovan, and N. Craddock Rare copy number variants: a point of rarity in genetic risk for bipolar disorder and schizophrenia Arch. Gen. Psychiatry 67 2010 318 327
59. R. Guevara, J.L. Velazquez, V. Nenadovic, R. Wennberg, G. Senjanovic, and L.G. Dominguez Phase synchronization measurements using electroencephalographic recordings: what can we really say about neuronal synchrony? Neuroinformatics 3 2005 301 314
60. C. Haenschel, R.A. Bittner, J. Waltz, F. Haertling, M. Wibral, W. Singer, D.E. Linden, and E. Rodriguez Cortical oscillatory activity is critical for working memory as revealed by deficits in early-onset schizophrenia J. Neurosci. 29 2009 9481 9489
61. M.H. Hall, G. Taylor, P. Sham, K. Schulze, F. Rijsdijk, M. Picchioni, T. Toulopoulou, U. Ettinger, E. Bramon, R.M. Murray, and D.F. Salisbury The early auditory gamma-band response is heritable and a putative endophenotype of schizophrenia Schizophr. Bull. 37 2011 778 787
62. R. Hanajima, and Y. Ugawa Impaired motor cortex inhibition in patients with ALS: evidence from paired transcranial magnetic stimulation Neurology 51 1998 1771 1772 (Pubitemid 28565282)
63. T. Hashimoto, D.W. Volk, S.M. Eggan, K. Mirnics, J.N. Pierri, Z. Sun, A.R. Sampson, and D.A. Lewis Gene expression deficits in a subclass of GABA neurons in the prefrontal cortex of subjects with schizophrenia J. Neurosci. 23 2003 6315 6326 (Pubitemid 36875633)
64. T. Hashimoto, S.E. Bergen, Q.L. Nguyen, B. Xu, L.M. Monteggia, J.N. Pierri, Z. Sun, A.R. Sampson, and D.A. Lewis Relationship of brain-derived neurotrophic factor and its receptor TrkB to altered inhibitory prefrontal circuitry in schizophrenia J. Neurosci. 25 2005 372 383 (Pubitemid 40105607)
65. H. Homayoun, and B. Moghaddam NMDA receptor hypofunction produces opposite effects on prefrontal cortex interneurons and pyramidal neurons J. Neurosci. 27 2007 11496 11500 (Pubitemid 350006886)
66. L.E. Hong, A. Summerfelt, R. McMahon, H. Adami, G. Francis, A. Elliott, R.W. Buchanan, and G.K. Thaker Evoked gamma band synchronization and the liability for schizophrenia Schizophr. Res. 70 2004 293 302 (Pubitemid 39141107)
67. D.H. Hubel, and T.N. Wiesel Receptive fields of single neurones in the cat's striate cortex J. Physiol. 148 1959 574 591
68. M.E. Jackson, H. Homayoun, and B. Moghaddam NMDA receptor hypofunction produces concomitant firing rate potentiation and burst activity reduction in the prefrontal cortex Proc. Natl. Acad. Sci. U.S.A. 101 2004 8467 8472 (Pubitemid 38736598)
69. O. Jensen, and C.D. Tesche Frontal theta activity in humans increases with memory load in a working memory task Eur. J. Neurosci. 15 2002 1395 1399 (Pubitemid 35478001)
70. J.K. Johannesen, P.D. Kieffaber, B.F. O'Donnell, A. Shekhar, J.D. Evans, and W.P. Hetrick Contributions of subtype and spectral frequency analyses to the study of P50 ERP amplitude and suppression in schizophrenia Schizophr. Res. 78 2005 269 284 (Pubitemid 41254029)
71. E.G. Jones, and A. Peters Cerebral cortex, Vol. 1984 Plenum Press New York
72. E.G. Jones The thalamic matrix and thalamocortical synchrony Trends Neurosci. 24 2001 595 601 (Pubitemid 32913390)
73. S. Karakas, and E. Basar Early gamma response is sensory in origin: a conclusion based on cross-comparison of results from multiple experimental paradigms Int. J. Psychophysiol. 31 1998 13 31 (Pubitemid 29045659)
74. Y. Kawaguchi Physiological subgroups of nonpyramidal cells with specific morphological characteristics in layer II/III of rat frontal cortex J. Neurosci. 15 1995 2638 2655
75. Y. Kawaguchi, and Y. Kubota GABAergic cell subtypes and their synaptic connections in rat frontal cortex Cereb. Cortex 7 1997 476 486 (Pubitemid 27353633)
76. J. Kissler, M.M. Muller, T. Fehr, B. Rockstroh, and T. Elbert MEG gamma band activity in schizophrenia patients and healthy subjects in a mental arithmetic task and at rest Clin. Neurophysiol. 111 2000 2079 2087
77. W. Klimesch EEG alpha and theta oscillations reflect cognitive and memory performance: a review and analysis Brain Res. Brain Res. Rev. 29 1999 169 195 (Pubitemid 29191338)
78. C. Konradi, and S. Heckers Molecular aspects of glutamate dysregulation: implications for schizophrenia and its treatment Pharmacol. Ther. 97 2003 153 179 (Pubitemid 36138820)
79. N. Kopell, and B. Ermentrout Chemical and electrical synapses perform complementary roles in the synchronization of interneuronal networks Proc. Natl. Acad. Sci. U.S.A. 101 2004 15482 15487 (Pubitemid 39441567)
80. J.H. Krystal, L.P. Karper, J.P. Seibyl, G.K. Freeman, R. Delaney, J.D. Bremner, G.R. Heninger, M.B. Bowers Jr.; and D.S. Charney Subanesthetic effects of the noncompetitive NMDA antagonist, ketamine, in humans. Psychotomimetic, perceptual, cognitive, and neuroendocrine responses Arch. Gen. Psychiatry 51 1994 199 214 (Pubitemid 24081509)
81. J.S. Kwon, B.F. O'Donnell, G.V. Wallenstein, R.W. Greene, Y. Hirayasu, P.G. Nestor, M.E. Hasselmo, G.F. Potts, M.E. Shenton, and R.W. McCarley Gamma frequency-range abnormalities to auditory stimulation in schizophrenia Arch. Gen. Psychiatry 56 1999 1001 1005 (Pubitemid 29526383)
82. A.C. Lahti, B. Koffel, D. LaPorte, and C.A. Tamminga Subanesthetic doses of ketamine stimulate psychosis in schizophrenia Neuropsychopharmacology 13 1995 9 19
83. K.H. Lee, L.M. Williams, A. Haig, and E. Gordon "Gamma (40 Hz) phase synchronicity" and symptom dimensions in schizophrenia Cogn. Neuropsychiatry 8 2003 57 71 (Pubitemid 36168373)
84. L.S. Leung, and B. Shen GABAB receptor blockade enhances theta and gamma rhythms in the hippocampus of behaving rats Hippocampus 17 2007 281 291 (Pubitemid 46649580)
85. D.A. Lewis, T. Hashimoto, and D.W. Volk Cortical inhibitory neurons and schizophrenia Nat. Rev. Neurosci. 6 2005 312 324 (Pubitemid 40469985)
86. D.A. Lewis, and B. Moghaddam Cognitive dysfunction in schizophrenia: convergence of gamma-aminobutyric acid and glutamate alterations Arch. Neurol. 63 2006 1372 1376 (Pubitemid 44547546)
87. J.A. Lieberman, J.M. Kane, and J. Alvir Provocative tests with psychostimulant drugs in schizophrenia Psychopharmacology (Berl). 91 1987 415 433 (Pubitemid 17038204)
88. G.A. Light, J.L. Hsu, M.H. Hsieh, K. Meyer-Gomes, J. Sprock, N.R. Swerdlow, and D.L. Braff Gamma band oscillations reveal neural network cortical coherence dysfunction in schizophrenia patients Biol. Psychiatry 60 2006 1231 1240 (Pubitemid 44693537)
89. D.E. Linden, R.A. Bittner, L. Muckli, J.A. Waltz, N. Kriegeskorte, R. Goebel, W. Singer, and M.H. Munk Cortical capacity constraints for visual working memory: dissociation of fMRI load effects in a fronto-parietal network Neuroimage 20 2003 1518 1530 (Pubitemid 37468260)
90. R. Llinas, U. Ribary, D. Contreras, and C. Pedroarena The neuronal basis for consciousness Philos. Trans. R. Soc. Lond. B Biol. Sci. 353 1998 1841 1849 (Pubitemid 28537291)
91. R.R. Llinas, A.A. Grace, and Y. Yarom In vitro neurons in mammalian cortical layer 4 exhibit intrinsic oscillatory activity in the 10- to 50-Hz frequency range Proc. Natl. Acad. Sci. U.S.A. 88 1991 897 901 (Pubitemid 21916131)
92. R.R. Llinas, and D. Pare Of dreaming and wakefulness Neuroscience 44 1991 521 535
93. W.W. Lytton, and T.J. Sejnowski Simulations of cortical pyramidal neurons synchronized by inhibitory interneurons J. Neurophysiol. 66 1991 1059 1079
94. D.A. McCormick GABA as an inhibitory neurotransmitter in human cerebral cortex J. Neurophysiol. 62 1989 1018 1027 (Pubitemid 19278424)
95. E.K. Miller, and J.D. Cohen An integrative theory of prefrontal cortex function Annu. Rev. Neurosci. 24 2001 167 202 (Pubitemid 32695227)
96. B.A. Morrow, J.D. Elsworth, and R.H. Roth Repeated phencyclidine in monkeys results in loss of parvalbumin-containing axo-axonic projections in the prefrontal cortex Psychopharmacology (Berl). 192 2007 283 290 (Pubitemid 46669209)
97. L. Mrzljak, C. Bergson, M. Pappy, R. Huff, R. Levenson, and P.S. Goldman-Rakic Localization of dopamine D4 receptors in GABAergic neurons of the primate brain Nature 381 1996 245 248 (Pubitemid 26148034)
98. S.D. Muthukumaraswamy, K.D. Singh, J.B. Swettenham, and D.K. Jones Visual gamma oscillations and evoked responses: variability, repeatability and structural MRI correlates Neuroimage 49 2010 3349 3357
99. P.L. Nunez, and R. Srinivasan Electric fields of the Brain: the Neurophysics of EEG, Vol. 2006 Oxford University Press New York
100. J.W. Olney, and N.B. Farber Glutamate receptor dysfunction and schizophrenia Arch. Gen. Psychiatry 52 1995 998 1007
101. M.J. Owen, M.C. O'Donovan, and I.I. Gottesman Schizophrenia P. McGuffin, M.J. Owen, I.I. Gottesman, Psychiatric Genetics and Genomics 2002 Oxford University Press Oxford 247 266 Vol.
102. C. Pantev, S. Makeig, M. Hoke, R. Galambos, S. Hampson, and C. Gallen Human auditory evoked gamma-band magnetic fields Proc. Natl. Acad. Sci. U.S.A. 88 1991 8996 9000 (Pubitemid 21915555)
103. M. Penttonen, and G. Buzsaki Natural logarithmic relationship between brain oscillators Thalamus & Related Systems. 2003 145 152 (Pubitemid 36378143)
104. D. Pinault N-methyl d-aspartate receptor antagonists ketamine and MK-801 induce wake-related aberrant gamma oscillations in the rat neocortex Biol. Psychiatry 63 2008 730 735 (Pubitemid 351400766)
105. G. Plourde, J. Baribeau, and V. Bonhomme Ketamine increases the amplitude of the 40-Hz auditory steady-state response in humans Br. J. Anaesth. 78 1997 524 529 (Pubitemid 27226364)
106. N.V. Povysheva, G. Gonzalez-Burgos, A.V. Zaitsev, S. Kroner, G. Barrionuevo, D.A. Lewis, and L.S. Krimer Properties of excitatory synaptic responses in fast-spiking interneurons and pyramidal cells from monkey and rat prefrontal cortex Cereb. Cortex 16 2006 541 552
107. B.J. Roach, and D.H. Mathalon Event-related EEG time-frequency analysis: an overview of measures and an analysis of early gamma band phase locking in schizophrenia Schizophr. Bull. 34 2008 907 926
108. E. Rodriguez, N. George, J.P. Lachaux, J. Martinerie, B. Renault, and F.J. Varela Perception's shadow: long-distance synchronization of human brain activity Nature 397 1999 430 433
109. H. Roick, H.J. von Giesen, and R. Benecke On the origin of the postexcitatory inhibition seen after transcranial magnetic brain stimulation in awake human subjects Exp. Brain Res. 94 1993 489 498 (Pubitemid 23218106)
110. C.A. Ross, R.L. Margolis, S.A. Reading, M. Pletnikov, and J.T. Coyle Neurobiology of schizophrenia Neuron 52 2006 139 153 (Pubitemid 44466356)
111. L. Rutter, F.W. Carver, T. Holroyd, S.R. Nadar, J. Mitchell-Francis, J. Apud, D.R. Weinberger, and R. Coppola Magnetoencephalographic gamma power reduction in patients with schizophrenia during resting condition Hum. Brain Mapp. 30 2009 3254 3264
112. T.D. Sanger, R.R. Garg, and R. Chen Interactions between two different inhibitory systems in the human motor cortex J. Physiol. 530 2001 307 317 (Pubitemid 32998879)
113. P. Seeman, T. Lee, M. Chau-Wong, and K. Wong Antipsychotic drug doses and neuroleptic/dopamine receptors Nature 261 1976 717 719
114. T.J. Sejnowski Statistical constraints on synaptic plasticity J. Theor. Biol. 69 1977 385 389
115. L.D. Selemon, and P.S. Goldman-Rakic The reduced neuropil hypothesis: a circuit based model of schizophrenia Biol. Psychiatry 45 1999 17 25 (Pubitemid 29049200)
116. H.R. Siebner, N. Lang, V. Rizzo, M.A. Nitsche, W. Paulus, R.N. Lemon, and J.C. Rothwell Preconditioning of low-frequency repetitive transcranial magnetic stimulation with transcranial direct current stimulation: evidence for homeostatic plasticity in the human motor cortex J. Neurosci. 24 2004 3379 3385 (Pubitemid 38451903)
117. W. Singer Development and plasticity of cortical processing architectures Science 270 1995 758 764
118. W. Singer Neuronal synchrony: a versatile code for the definition of relations? Neuron 24 49-65 1999 111 125
119. A. Sirota, S. Montgomery, S. Fujisawa, Y. Isomura, M. Zugaro, and G. Buzsaki Entrainment of neocortical neurons and gamma oscillations by the hippocampal theta rhythm Neuron 60 2008 683 697
120. V.S. Sohal, F. Zhang, O. Yizhar, and K. Deisseroth Parvalbumin neurons and gamma rhythms enhance cortical circuit performance Nature 459 2009 698 702
121. P. Somogyi A specific 'axo-axonal' interneuron in the visual cortex of the rat Brain Res. 136 1977 345 350 (Pubitemid 8205709)
122. P. Somogyi, and T. Klausberger Defined types of cortical interneurone structure space and spike timing in the hippocampus J. Physiol. 562 2005 9 26 (Pubitemid 40207780)
123. K.M. Spencer, P.G. Nestor, M.A. Niznikiewicz, D.F. Salisbury, M.E. Shenton, and R.W. McCarley Abnormal neural synchrony in schizophrenia J. Neurosci. 23 2003 7407 7411 (Pubitemid 36999532)
124. K.M. Spencer, P.G. Nestor, R. Perlmutter, M.A. Niznikiewicz, M.C. Klump, M. Frumin, M.E. Shenton, and R.W. McCarley Neural synchrony indexes disordered perception and cognition in schizophrenia Proc. Natl. Acad. Sci. U.S.A. 101 2004 17288 17293 (Pubitemid 39627812)
125. K.M. Spencer, M.A. Niznikiewicz, M.E. Shenton, and R.W. McCarley Sensory-evoked gamma oscillations in chronic schizophrenia Biol. Psychiatry 63 2008 744 747
126. K.M. Spencer The functional consequences of cortical circuit abnormalities on gamma oscillations in schizophrenia: insights from computational modeling Front Hum Neurosci. 3 2009 33
127. M. Steriade, R. Curro Dossi, and D. Contreras Electrophysiological properties of intralaminar thalamocortical cells discharging rhythmic (approximately 40 HZ) spike-bursts at approximately 1000 HZ during waking and rapid eye movement sleep Neuroscience 56 1993 1 9 (Pubitemid 23261798)
128. M. Steriade Synchronized activities of coupled oscillators in the cerebral cortex and thalamus at different levels of vigilance Cereb. Cortex 7 1997 583 604
129. M. Steriade, I. Timofeev, N. Durmuller, and F. Grenier Dynamic properties of corticothalamic neurons and local cortical interneurons generating fast rhythmic (30-40 Hz) spike bursts J. Neurophysiol. 79 1998 483 490 (Pubitemid 28133840)
130. Y. Suzuki, E. Jodo, S. Takeuchi, S. Niwa, and Y. Kayama Acute administration of phencyclidine induces tonic activation of medial prefrontal cortex neurons in freely moving rats Neuroscience 114 2002 769 779 (Pubitemid 35247662)
131. C. Tallon-Baudry, and O. Bertrand Oscillatory gamma activity in humans and its role in object representation Trends Cogn. Sci. 3 1999 151 162 (Pubitemid 29155465)
132. G. Tamas, E.H. Buhl, A. Lorincz, and P. Somogyi Proximally targeted GABAergic synapses and gap junctions synchronize cortical interneurons Nat. Neurosci. 3 2000 366 371 (Pubitemid 30185487)
133. R.D. Traub, M.A. Whittington, S.B. Colling, G. Buzsaki, and J.G. Jefferys Analysis of gamma rhythms in the rat hippocampus in vitro and in vivo J. Physiol. 493 Pt 2 1996 471 484 (Pubitemid 26187506)
134. R.D. Traub, M.A. Whittington, I.M. Stanford, and J.G. Jefferys A mechanism for generation of long-range synchronous fast oscillations in the cortex Nature 383 1996 621 624
135. R.D. Traub, A. Bibbig, A. Fisahn, F.E. LeBeau, M.A. Whittington, and E.H. Buhl A model of gamma-frequency network oscillations induced in the rat CA3 region by carbachol in vitro Eur. J. Neurosci. 12 2000 4093 4106
136. R.D. Traub, N. Kopell, A. Bibbig, E.H. Buhl, F.E. LeBeau, and M.A. Whittington Gap junctions between interneuron dendrites can enhance synchrony of gamma oscillations in distributed networks J. Neurosci. 21 2001 9478 9486 (Pubitemid 33096892)
137. P.J. Uhlhaas, and W. Singer Neural synchrony in brain disorders: relevance for cognitive dysfunctions and pathophysiology Neuron 52 2006 155 168 (Pubitemid 44466360)
138. P.J. Uhlhaas, C. Haenschel, D. Nikolic, and W. Singer The role of oscillations and synchrony in cortical networks and their putative relevance for the pathophysiology of schizophrenia Schizophr. Bull. 34 2008 927 943
139. P.J. Uhlhaas, G. Pipa, B. Lima, L. Melloni, S. Neuenschwander, D. Nikolic, and W. Singer Neural synchrony in cortical networks: history, concept and current status Front Integr Neurosci. 3 2009 17
140. N.C. Venables, E.M. Bernat, and S.R. Sponheim Genetic and disorder-specific aspects of resting state EEG abnormalities in schizophrenia Schizophr. Bull. 35 2009 826 839
141. D. Volk, M. Austin, J. Pierri, A. Sampson, and D. Lewis GABA transporter-1 mRNA in the prefrontal cortex in schizophrenia: decreased expression in a subset of neurons Am. J. Psychiatry 158 2001 256 265 (Pubitemid 32116522)
142. D.W. Volk, M.C. Austin, J.N. Pierri, A.R. Sampson, and D.A. Lewis Decreased glutamic acid decarboxylase67 messenger RNA expression in a subset of prefrontal cortical gamma-aminobutyric acid neurons in subjects with schizophrenia Arch. Gen. Psychiatry 57 2000 237 245 (Pubitemid 30140433)
143. M. Waldo, M. Myles-Worsley, A. Madison, W. Byerley, and R. Freedman Sensory gating deficits in parents of schizophrenics Am. J. Med. Genet. 60 1995 506 511 (Pubitemid 26002117)
144. X.J. Wang, and G. Buzsaki Gamma oscillation by synaptic inhibition in a hippocampal interneuronal network model J. Neurosci. 16 1996 6402 6413 (Pubitemid 26337364)
145. C.S. Weickert, T.M. Hyde, B.K. Lipska, M.M. Herman, D.R. Weinberger, and J.E. Kleinman Reduced brain-derived neurotrophic factor in prefrontal cortex of patients with schizophrenia Mol. Psychiatry 8 2003 592 610 (Pubitemid 36898018)
146. C.S. Weickert, D.L. Ligons, T. Romanczyk, G. Ungaro, T.M. Hyde, M.M. Herman, D.R. Weinberger, and J.E. Kleinman Reductions in neurotrophin receptor mRNAs in the prefrontal cortex of patients with schizophrenia Mol. Psychiatry 10 2005 637 650 (Pubitemid 40961734)
147. M.A. Whittington, R.D. Traub, and J.G. Jefferys Synchronized oscillations in interneuron networks driven by metabotropic glutamate receptor activation Nature 373 1995 612 615
148. M.A. Whittington, I.M. Stanford, S.B. Colling, J.G. Jefferys, and R.D. Traub Spatiotemporal patterns of gamma frequency oscillations tetanically induced in the rat hippocampal slice J. Physiol. 502 Pt 3 1997 591 607 (Pubitemid 27365824)
149. M.A. Whittington, R.D. Traub, H.J. Faulkner, J.G. Jefferys, and K. Chettiar Morphine disrupts long-range synchrony of gamma oscillations in hippocampal slices Proc. Natl. Acad. Sci. U.S.A. 95 1998 5807 5811 (Pubitemid 28224178)
150. M.A. Whittington, R.D. Traub, N. Kopell, B. Ermentrout, and E.H. Buhl Inhibition-based rhythms: experimental and mathematical observations on network dynamics Int. J. Psychophysiol. 38 2000 315 336
151. G.V. Williams, and P.S. Goldman-Rakic Modulation of memory fields by dopamine D1 receptors in prefrontal cortex Nature 376 1995 572 575
152. T.U. Woo, A.M. Kim, and E. Viscidi Disease-specific alterations in glutamatergic neurotransmission on inhibitory interneurons in the prefrontal cortex in schizophrenia Brain Res. 1218 2008 267 277
153. M.K. Yamada, K. Nakanishi, S. Ohba, T. Nakamura, Y. Ikegaya, N. Nishiyama, and N. Matsuki Brain-derived neurotrophic factor promotes the maturation of GABAergic mechanisms in cultured hippocampal neurons J. Neurosci. 22 2002 7580 7585 (Pubitemid 35386359)
154. S. Yuval-Greenberg, O. Tomer, A.S. Keren, I. Nelken, and L.Y. Deouell Transient induced gamma-band response in EEG as a manifestation of miniature saccades Neuron 58 2008 429 441 (Pubitemid 351615190)