Impact of Ketamine on Neuronal Network Dynamics: Translational Modeling of Schizophrenia-Relevant Deficits

CNS Neuroscience and Therapeutics

Volumn 19, Issue 6, 2013, Pages 437-447

  Kocsis, Bernat ^a   Brown, Ritchie E ^a   Mccarley, Robert W ^a   Hajos, Mihaly ^b  

^a HARVARD MEDICAL SCHOOL   (United States)

^b YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Gamma oscillation; Mismatch negativity; N methyl d aspartate receptors receptors; P300; Theta rhythm

Indexed keywords

2 AMINO 7 PHOSPHONOHEPTANOIC ACID; DIZOCILPINE; KETAMINE; N METHYL DEXTRO ASPARTIC ACID RECEPTOR;

AUDITORY CORTEX; BEHAVIOR; BRAIN ELECTROPHYSIOLOGY; BRAIN STEM; COGNITIVE DEFECT; DISEASE MODEL; ELECTROSTIMULATION; ENDOPHENOTYPE; EVOKED AUDITORY RESPONSE; EVOKED CORTICAL RESPONSE; FOREBRAIN; HIPPOCAMPUS; HUMAN; IN VITRO STUDY; INTERNEURON; LEARNING; MEMORY; MISMATCH NEGATIVITY; MOTOR ACTIVITY; NEOCORTEX; NERVE CELL NETWORK; NONHUMAN; OSCILLATION; PHARMACOLOGICAL BLOCKING; REM SLEEP; REVIEW; SCHIZOPHRENIA; SPECTROSCOPY; VISUAL CORTEX;

ANALGESICS; ANIMALS; BRAIN; DISEASE MODELS, ANIMAL; ELECTROENCEPHALOGRAPHY; EVOKED POTENTIALS; HUMANS; KETAMINE; MODELS, NEUROLOGICAL; SCHIZOPHRENIA; TRANSLATIONAL MEDICAL RESEARCH;

EID: 84878139017     PISSN: 17555930     EISSN: 17555949     Source Type: Journal    
DOI: 10.1111/cns.12081     Document Type: Review

References (209)

1. Krystal JH, Karper LP, Seibyl JP, et al. Subanesthetic effects of the noncompetitive NMDA antagonist, ketamine, in humans. Psychotomimetic, perceptual, cognitive, and neuroendocrine responses. Arch Gen Psychiatry 1994;51:199-214.
2. Lahti AC, Koffel B, LaPorte D, Tamminga CA. Subanesthetic doses of ketamine stimulate psychosis in schizophrenia. Neuropsychopharmacology 1995;13:9-19.
3. Gouzoulis-Mayfrank E, Heekeren K, Neukirch A, et al. Psychological effects of (S)-ketamine and N, N-dimethyltryptamine (DMT): a double-blind, cross-over study in healthy volunteers. Pharmacopsychiatry 2005;38:301-311.
4. Vollenweider FX, Geyer MA. A systems model of altered consciousness: integrating natural and drug-induced psychoses. Brain Res Bull 2001;56:495-507.
5. Javitt DC. Glutamate and schizophrenia: phencyclidine, N-methyl-d-aspartate receptors, and dopamine-glutamate interactions. Int Rev Neurobiol 2007;78:69-108.
6. Adell A, Jimenez-Sanchez L, Lopez-Gil X, Romon T. Is the acute NMDA receptor hypofunction a valid model of schizophrenia? Schizophr Bull 2012;38:9-14.
7. Domino EF, Luby ED. Phencyclidine/schizophrenia: one view toward the past, the other to the future. Schizophr Bull 2012;38:914-919.
8. Gandal MJ, Edgar JC, Klook K, Siegel SJ. Gamma synchrony: towards a translational biomarker for the treatment-resistant symptoms of schizophrenia. Neuropharmacology 2012;62:1504-1518.
9. Amann LC, Gandal MJ, Halene TB, et al. Mouse behavioral endophenotypes for schizophrenia. Brain Res Bull 2010;83:147-161.
10. Gilmour G, Dix S, Fellini L, et al. NMDA receptors, cognition and schizophrenia-testing the validity of the NMDA receptor hypofunction hypothesis. Neuropharmacology 2012;62:1401-1412.
11. Lisman JE, Coyle JT, Green RW, et al. Circuit-based framework for understanding neurotransmitter and risk gene interactions in schizophrenia. Trends Neurosci 2008;31:234-242.
12. Javitt DC, Spencer KM, Thaker GK, Winterer G, Hajos M. Neurophysiological biomarkers for drug development in schizophrenia. Nat Rev Drug Discov 2008;7:68-83.
13. Neill JC, Barnes S, Cook S, et al. Animal models of cognitive dysfunction and negative symptoms of schizophrenia: focus on NMDA receptor antagonism. Pharmacol Ther 2010;128:419-432.
14. Gunduz-Bruce H. The acute effects of NMDA antagonism: from the rodent to the human brain. Brain Res Rev 2009;60:279-286.
15. Bubenikova-Valesova V, Horacek J, Vrajova M, Hoschl C. Models of schizophrenia in humans and animals based on inhibition of NMDA receptors. Neurosci Biobehav Rev 2008;32:1014-1023.
16. Morgan CJ, Curran HV. Acute and chronic effects of ketamine upon human memory: a review. Psychopharmacology 2006;188:408-424.
17. Fletcher PC, Honey GD. Schizophrenia, ketamine and cannabis: evidence of overlapping memory deficits. Trends Cogn Sci 2006;10:167-174.
18. Lipska BK, Weinberger DR. To model a psychiatric disorder in animals: schizophrenia as a reality test. Neuropsychopharmacology 2000;23:223-239.
19. Uhlhaas PJ, Singer W. Neuronal dynamics and neuropsychiatric disorders: toward a translational paradigm for dysfunctional large-scale networks. Neuron 2012;75:963-980.
20. Mion G, Villevieille T. Ketamine Pharmacology: An Update (Pharmacodynamics and Molecular Aspects, Recent Findings). CNS Neurosci Ther 2013; 19:370-380.
21. Jentsch JD, Roth RH. The neuropsychopharmacology of phencyclidine: from NMDA receptor hypofunction to the dopamine hypothesis of schizophrenia. Neuropsychopharmacology 1999;20:201-225.
22. Taffe MA, Davis SA, Yuan J, et al. Cognitive performance of MDMA-treated rhesus monkeys: sensitivity to serotonergic challenge. Neuropsychopharmacology 2002;27:993-1005.
23. Buccafusco JJ, Terry AV Jr. A reversible model of the cognitive impairment associated with schizophrenia in monkeys: potential therapeutic effects of two nicotinic acetylcholine receptor agonists. Biochem Pharmacol 2009;78:852-862.
24. Roberts BM, Holden DE, Shaffer CL, et al. Prevention of ketamine-induced working memory impairments by AMPA potentiators in a nonhuman primate model of cognitive dysfunction. Behav Brain Res 2010;212:41-48.
25. Pinault D. N-methyl d-aspartate receptor antagonists ketamine and MK-801 induce wake-related aberrant gamma oscillations in the rat neocortex. Biol Psychiatry 2008;63:730-735.
26. Lazarewicz MT, Ehrlichman RS, Maxwell CR, Gandal MJ, Finkel LH, Siegel SJ. Ketamine modulates theta and gamma oscillations. J Cogn Neurosci 2010;22:1452-1464.
27. Kittelberger K, Hur EE, Sazegar S, Keshavan V, Kocsis B. Comparison of the effects of acute and chronic administration of ketamine on hippocampal oscillations: relevance for the NMDA receptor hypofunction model of schizophrenia. Brain Struct Funct 2012;217:395-409.
28. Hong LE, Summerfelt A, Buchanan RW, et al. Gamma and delta neural oscillations and association with clinical symptoms under subanesthetic ketamine. Neuropsychopharmacology 2010;35:632-640.
29. Berman RM, Cappiello A, Anand A, et al. Antidepressant effects of ketamine in depressed patients. Biol Psychiatry 2000;47:351-354.
30. Zarate CA Jr, Singh JB, Carlson PJ, et al. A randomized trial of an N-methyl-d-aspartate antagonist in treatment-resistant major depression. Arch Gen Psychiatry 2006;63:856-864.
31. Anand A, Charney DS, Oren DA, et al. Attenuation of the neuropsychiatric effects of ketamine with lamotrigine: support for hyperglutamatergic effects of N-methyl-d-aspartate receptor antagonists. Arch Gen Psychiatry 2000;57:270-276.
32. Mathews DC, Henter ID, Zarate CA. Targeting the glutamatergic system to treat major depressive disorder: rationale and progress to date. Drugs 2012;72:1313-1333.
33. Marland S, Ellerton J, Andolfatto G, et al. Ketamine: Use in Anesthesia. CNS Neurosci Ther 2013; 19:381-389.
34. Salvdore G, Singh JB. Ketamine as a Fast Acting Antidepressant: Current Knowledge and Open Questions. CNS Neurosci Ther 2013; 19:428-436.
35. Gould TD, Gottesman II. Psychiatric endophenotypes and the development of valid animal models. Genes Brain Behav 2006;5:113-119.
36. O'Tuathaigh CM, Harte M, O'Leary C, et al. Schizophrenia-related endophenotypes in heterozygous neuregulin-1 'knockout' mice. Eur J Neurosci 2010;31:349-358.
37. Gornick MC, Addington AM, Sporn A, et al. Dysbindin (DTNBP1, 6p22.3) is associated with childhood-onset psychosis and endophenotypes measured by the Premorbid Adjustment Scale (PAS). J Autism Dev Disord 2005;35:831-838.
38. Benes FM. Searching for unique endophenotypes for schizophrenia and bipolar disorder within neural circuits and their molecular regulatory mechanisms. Schizophr Bull 2007;33:932-936.
39. Gottesman II, Gould TD. The endophenotype concept in psychiatry: etymology and strategic intentions. Am J Psychiatry 2003;160:636-645.
40. Braff DL, Greenwood TA, Swerdlow NR, Light GA, Schork NJ. Advances in endophenotyping schizophrenia. World Psychiatry 2008;7:11-18.
41. Braff DL, Light GA. The use of neurophysiological endophenotypes to understand the genetic basis of schizophrenia. Dialogues Clin Neurosci 2005;7:125-135.
42. Hall MH, Taylor G, Salisbury DF, Levy DL. Sensory gating event-related potentials and oscillations in schizophrenia patients and their unaffected relatives. Schizophr Bull 2011;37:1187-1199.
43. Hall MH, Taylor G, Sham P, et al. The early auditory gamma-band response is heritable and a putative endophenotype of schizophrenia. Schizophr Bull 2011;37:778-787.
44. Swerdlow NR, Braff DL, Geyer MA. Cross-species studies of sensorimotor gating of the startle reflex. Ann N Y Acad Sci 1999;877:202-216.
45. Swerdlow NR, Braff DL, Taaid N, Geyer MA. Assessing the validity of an animal model of deficient sensorimotor gating in schizophrenic patients. Arch Gen Psychiatry 1994;51:139-154.
46. Swerdlow NR, Weber M, Qu Y, Light GA, Braff DL. Realistic expectations of prepulse inhibition in translational models for schizophrenia research. Psychopharmacology 2008;199:331-388.
47. Geyer MA, Krebs-Thomson K, Braff DL, Swerdlow NR. Pharmacological studies of prepulse inhibition models of sensorimotor gating deficits in schizophrenia: a decade in review. Psychopharmacology 2001;156:117-154.
48. Kocsis B. Differential role of NR2A and NR2B subunits in N-methyl-d-aspartate receptor antagonist-induced aberrant cortical gamma oscillations. Biol Psychiatry 2012;71:987-995.
49. Spooren W, Mombereau C, Maco M, et al. Pharmacological and genetic evidence indicates that combined inhibition of NR2A and NR2B subunit containing NMDA receptors is required to disrupt prepulse inhibition. Psychopharmacology 2004;175:99-105.
50. Manahan-Vaughan D, von Haebler D, Winter C, Juckel G, Heinemann U. A single application of MK801 causes symptoms of acute psychosis, deficits in spatial memory, and impairment of synaptic plasticity in rats. Hippocampus 2008;18:125-134.
51. Linn GS, O'Keeffe RT, Lifshitz K, Schroeder C, Javitt DC. Behavioral effects of orally administered glycine in socially housed monkeys chronically treated with phencyclidine. Psychopharmacology 2007;192:27-38.
52. Shiigi Y, Casey DE. Behavioral effects of ketamine, an NMDA glutamatergic antagonist, in non-human primates. Psychopharmacology 1999;146:67-72.
53. Abel KM, Allin MP, Hemsley DR, Geyer MA. Low dose ketamine increases prepulse inhibition in healthy men. Neuropharmacology 2003;44:729-737.
54. Duncan EJ, Madonick SH, Parwani A, et al. Clinical and sensorimotor gating effects of ketamine in normals. Neuropsychopharmacology 2001;25:72-83.
55. van Berckel BN, Oranje B, van Ree JM, Verbaten MN, Kahn RS. The effects of low dose ketamine on sensory gating, neuroendocrine secretion and behavior in healthy human subjects. Psychopharmacology 1998;137:271-281.
56. Hong LE, Summerfelt A, Mitchell BD, et al. Sensory gating endophenotype based on its neural oscillatory pattern and heritability estimate. Arch Gen Psychiatry 2008;65:1008-1016.
57. Luck SJ, Mathalon DH, O'Donnell BF, et al. A roadmap for the development and validation of event-related potential biomarkers in schizophrenia research. Biol Psychiatry 2011;70:28-34.
58. Turetsky BI, Greenwood TA, Olincy A, et al. Abnormal auditory N100 amplitude: a heritable endophenotype in first-degree relatives of schizophrenia probands. Biol Psychiatry 2008;64:1051-1059.
59. Turetsky BI, Calkins ME, Light GA, Olincy A, Radant AD, Swerdlow NR. Neurophysiological endophenotypes of schizophrenia: the viability of selected candidate measures. Schizophr Bull 2007;33:69-94.
60. Javitt DC, Schoepp D, Kalivas PW, et al. Translating glutamate: from pathophysiology to treatment. Sci Transl Med 2011;3:102mr2.
61. Hajos M. Targeting information-processing deficit in schizophrenia: a novel approach to psychotherapeutic drug discovery. Trends Pharmacol Sci 2006;27:391-398.
62. Cromwell HC, Mears RP, Wan L, Boutros NN. Sensory gating: a translational effort from basic to clinical science. Clin EEG Neurosci 2008;39:69-72.
63. Hanlon FM, Miller GA, Thoma RJ, et al. Distinct M50 and M100 auditory gating deficits in schizophrenia. Psychophysiology 2005;42:417-427.
64. Mathiak K, Ackermann H, Rapp A, et al. Neuromagnetic oscillations and hemodynamic correlates of P50 suppression in schizophrenia. Psychiatry Res 2011;194:95-104.
65. Boeijinga PH, Soufflet L, Santoro F, Luthringer R. Ketamine effects on CNS responses assessed with MEG/EEG in a passive auditory sensory-gating paradigm: an attempt for modelling some symptoms of psychosis in man. J Psychopharmacol 2007;21:321-337.
66. Cromwell HC, Klein A, Mears RP. Single unit and population responses during inhibitory gating of striatal activity in freely moving rats. Neuroscience 2007;146:69-85.
67. Ma J, Tai SK, Leung LS. Septohippocampal GABAergic neurons mediate the altered behaviors induced by N-methyl-d-aspartate receptor antagonists. Hippocampus 2012;22:2208-2218.
68. Garrido MI, Friston KJ, Kiebel SJ, Stephan KE, Baldeweg T, Kilner JM. The functional anatomy of the MMN: a DCM study of the roving paradigm. Neuroimage 2008;42:936-944.
69. Garrido MI, Kilner JM, Stephan KE, Friston KJ. The mismatch negativity: a review of underlying mechanisms. Clin Neurophysiol 2009;120:453-463.
70. Todd J, Myers R, Pirillo R, Drysdale K. Neuropsychological correlates of auditory perceptual inference: a mismatch negativity (MMN) study. Brain Res 2010;1310:113-123.
71. Doeller CF, Opitz B, Mecklinger A, Krick C, Reith W, Schroger E. Prefrontal cortex involvement in preattentive auditory deviance detection: neuroimaging and electrophysiological evidence. Neuroimage 2003;20:1270-1282.
72. Opitz B, Rinne T, Mecklinger A, von Cramon DY, Schroger E. Differential contribution of frontal and temporal cortices to auditory change detection: fMRI and ERP results. Neuroimage 2002;15:167-174.
73. Rinne T, Alho K, Ilmoniemi RJ, Virtanen J, Naatanen R. Separate time behaviors of the temporal and frontal mismatch negativity sources. Neuroimage 2000;12:14-19.
74. Javitt DC. Intracortical mechanisms of mismatch negativity dysfunction in schizophrenia. Audiol Neurootol 2000;5:207-215.
75. Heekeren K, Daumann J, Neukirch A, et al. Mismatch negativity generation in the human 5HT2A agonist and NMDA antagonist model of psychosis. Psychopharmacology 2008;199:77-88.
76. Kreitschmann-Andermahr I, Rosburg T, Demme U, Gaser E, Nowak H, Sauer H. Effect of ketamine on the neuromagnetic mismatch field in healthy humans. Brain Res Cogn Brain Res 2001;12:109-116.
77. Umbricht D, Schmid L, Koller R, Vollenweider FX, Hell D, Javitt DC. Ketamine-induced deficits in auditory and visual context-dependent processing in healthy volunteers: implications for models of cognitive deficits in schizophrenia. Arch Gen Psychiatry 2000;57:1139-1147.
78. Gunduz-Bruce H, Reinhart RM, Roach BJ, et al. Glutamatergic modulation of auditory information processing in the human brain. Biol Psychiatry 2012;71:969-977.
79. Schmidt A, Bachmann R, Kometer M, et al. Mismatch negativity encoding of prediction errors predicts S-ketamine-induced cognitive impairments. Neuropsychopharmacology 2012;37:865-875.
80. Baldeweg T, Klugman A, Gruzelier J, Hirsch SR. Mismatch negativity potentials and cognitive impairment in schizophrenia. Schizophr Res 2004;69:203-217.
81. Umbricht D, Krljes S. Mismatch negativity in schizophrenia: a meta-analysis. Schizophr Res 2005;76:1-23.
82. Schmidt A, Diaconescu AO, Kometer M, Friston KJ, Stephan KE, Vollenweider FX. Modeling ketamine effects on synaptic plasticity during the mismatch negativity. Cereb Cortex 2012; doi: 10.1093/cercor/bhs238.
83. Uhlhaas PJ, Singer W. Abnormal neural oscillations and synchrony in schizophrenia. Nat Rev Neurosci 2010;11:100-113.
84. Benes FM, Berretta S. GABAergic interneurons: implications for understanding schizophrenia and bipolar disorder. Neuropsychopharmacology 2001;25:1-27.
85. Benes FM, Lim B, Matzilevich D, Subburaju S, Walsh JP. Circuitry-based gene expression profiles in GABA cells of the trisynaptic pathway in schizophrenics versus bipolars. Proc Natl Acad Sci U S A 2008;105:20935-20940.
86. Lewis DA, Hashimoto T, Volk DW. Cortical inhibitory neurons and schizophrenia. Nat Rev Neurosci 2005;6:312-324.
87. Reynolds GP, Abdul-Monim Z, Neill JC, Zhang ZJ. Calcium binding protein markers of GABA deficits in schizophrenia-postmortem studies and animal models. Neurotox Res 2004;6:57-61.
88. Todtenkopf MS, Benes FM. Distribution of glutamate decarboxylase65 immunoreactive puncta on pyramidal and nonpyramidal neurons in hippocampus of schizophrenic brain. Synapse 1998;29:323-332.
89. Lodge DJ, Behrens MM, Grace AA. A loss of parvalbumin-containing interneurons is associated with diminished oscillatory activity in an animal model of schizophrenia. J Neurosci 2009;29:2344-2354.
90. Kaalund SS, Riise J, Broberg B, et al. Differential expression of parvalbumin interneurons in neonatal phencyclidine treated rats and socially isolated rats. J Neurochem 2012;124:548-557.
91. Turner CP, DeBenedetto D, Ware E, et al. Postnatal exposure to MK801 induces selective changes in GAD67 or parvalbumin. Exp Brain Res 2010;201:479-488.
92. Jenkins TA, Harte MK, Reynolds GP. Effect of subchronic phencyclidine administration on sucrose preference and hippocampal parvalbumin immunoreactivity in the rat. Neurosci Lett 2010;471:144-147.
93. Xi D, Zhang W, Wang HX, Stradtman GG, Gao WJ. Dizocilpine (MK-801) induces distinct changes of N-methyl-d-aspartic acid receptor subunits in parvalbumin-containing interneurons in young adult rat prefrontal cortex. Int J Neuropsychopharmacol 2009;12:1395-1408.
94. Francois J, Ferrandon A, Koning E, Angst MJ, Sandner G, Nehlig A. Selective reorganization of GABAergic transmission in neonatal ventral hippocampal-lesioned rats. Int J Neuropsychopharmacol 2009;12:1097-1110.
95. Abekawa T, Ito K, Nakagawa S, Koyama T. Prenatal exposure to an NMDA receptor antagonist, MK-801 reduces density of parvalbumin-immunoreactive GABAergic neurons in the medial prefrontal cortex and enhances phencyclidine-induced hyperlocomotion but not behavioral sensitization to methamphetamine in postpubertal rats. Psychopharmacology 2007;192:303-316.
96. Penschuck S, Flagstad P, Didriksen M, Leist M, Michael-Titus AT. Decrease in parvalbumin-expressing neurons in the hippocampus and increased phencyclidine-induced locomotor activity in the rat methylazoxymethanol (MAM) model of schizophrenia. Eur J Neurosci 2006;23:279-284.
97. Gizerian SS, Morrow AL, Lieberman JA, Grobin AC. Neonatal neurosteroid administration alters parvalbumin expression and neuron number in medial dorsal thalamus of adult rats. Brain Res 2004;1012:66-74.
98. Hajos M, Hoffmann WE, Kocsis B. Activation of cannabinoid-1 receptors disrupts sensory gating and neuronal oscillation: relevance to schizophrenia. Biol Psychiatry 2008;63:1075-1083.
99. Lanre-Amos T, Kocsis B. Hippocampal oscillations in the rodent model of schizophrenia induced by amygdala GABA receptor blockade. Front Psychiatry 2010;1:132.
100. Kocsis B. State-dependent increase of cortical gamma activity during REM sleep after selective blockade of NR2B subunit containing NMDA receptors. Sleep 2012;35:1011-1016.
101. Kocsis B, Dybvik M, Harper J, Ronnestad K. Changes in background and ketamine induced gamma oscillations in the MAM-model of schizophrenia. Biol Psychiatry 2012;71:39S.
102. Dzirasa K, Santos LM, Ribeiro S, et al. Persistent hyperdopaminergia decreases the peak frequency of hippocampal theta oscillations during quiet waking and REM sleep. PLoS ONE 2009;4:e5238.
103. Ehrlichman RS, Gandal MJ, Maxwell CR, et al. N-methyl-d-aspartic acid receptor antagonist-induced frequency oscillations in mice recreate pattern of electrophysiological deficits in schizophrenia. Neuroscience 2009;158:705-712.
104. Phillips KG, Cotel MC, McCarthy AP, et al. Differential effects of NMDA antagonists on high frequency and gamma EEG oscillations in a neurodevelopmental model of schizophrenia. Neuropharmacology 2012;62:1359-1370.
105. Vohs JL, Chambers RA, Krishnan GP, et al. Auditory sensory gating in the neonatal ventral hippocampal lesion model of schizophrenia. Neuropsychobiology 2009;60:12-22.
106. Vohs JL, Chambers RA, Krishnan GP, O'Donnell BF, Berg S, Morzorati SL. GABAergic modulation of the 40 Hz auditory steady-state response in a rat model of schizophrenia. Int J Neuropsychopharmacol 2010;13:487-497.
107. Carlson GC, Talbot K, Halene TB, et al. Dysbindin-1 mutant mice implicate reduced fast-phasic inhibition as a final common disease mechanism in schizophrenia. Proc Natl Acad Sci U S A 2011;108:E962-E970.
108. Lodge DJ, Grace AA. Gestational methylazoxymethanol acetate administration: a developmental disruption model of schizophrenia. Behav Brain Res 2009;204:306-312.
109. Hakami T, Jones NC, Tolmacheva EA, et al. NMDA receptor hypofunction leads to generalized and persistent aberrant gamma oscillations independent of hyperlocomotion and the state of consciousness. PLoS ONE 2009;4:e6755.
110. Kiss T, Hoffmann WE, Scott L, et al. Role of thalamic projection in NMDA receptor-induced disruption of cortical slow oscillation and short-term plasticity. Front Psychiatry 2011;2:14.
111. Kiss T, Hoffmann WE, Hajos M. Delta oscillation and short-term plasticity in the rat medial prefrontal cortex: modelling NMDA hypofunction of schizophrenia. Int J Neuropsychopharmacol 2011;14:29-42.
112. Spencer KM. Baseline gamma power during auditory steady-state stimulation in schizophrenia. Front Hum Neurosci 2011;5:190.
113. Basar E, Rosen B, Basar-Eroglu C, Greitschus F. The associations between 40 Hz-EEG and the middle latency response of the auditory evoked potential. Int J Neurosci 1987;33:103-117.
114. Brenner CA, Sporns O, Lysaker PH, O'Donnell BF. EEG synchronization to modulated auditory tones in schizophrenia, schizoaffective disorder, and schizotypal personality disorder. Am J Psychiatry 2003;160:2238-2240.
115. Spencer KM, Niznikiewicz MA, Shenton ME, McCarley RW. Sensory-evoked gamma oscillations in chronic schizophrenia. Biol Psychiatry 2008;63:744-747.
116. Brenner CA, Krishnan GP, Vohs JL, et al. Steady state responses: electrophysiological assessment of sensory function in schizophrenia. Schizophr Bull 2009;35:1065-1077.
117. Haenschel C, Linden D. Exploring intermediate phenotypes with EEG: working memory dysfunction in schizophrenia. Behav Brain Res 2011;216:481-495.
118. Barr MS, Farzan F, Tran LC, Chen R, Fitzgerald PB, Daskalakis ZJ. Evidence for excessive frontal evoked gamma oscillatory activity in schizophrenia during working memory. Schizophr Res 2010;121:146-152.
119. 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.
120. Minzenberg MJ, Firl AJ, Yoon JH, Gomes GC, Reinking C, Carter CS. Gamma oscillatory power is impaired during cognitive control independent of medication status in first-episode schizophrenia. Neuropsychopharmacology 2010;35:2590-2599.
121. Basar-Eroglu C, Brand A, Hildebrandt H, Karolina Kedzior K, Mathes B, Schmiedt C. Working memory related gamma oscillations in schizophrenia patients. Int J Psychophysiol 2007;64:39-45.
122. Baldeweg T, Spence S, Hirsch SR, Gruzelier J. Gamma-band electroencephalographic oscillations in a patient with somatic hallucinations. Lancet 1998;352:620-621.
123. Tan HY, Callicott JH, Weinberger DR. Intermediate phenotypes in schizophrenia genetics redux: is it a no brainer? Mol Psychiatry 2008;13:233-238.
124. Plourde G, Baribeau J, Bonhomme V. Ketamine increases the amplitude of the 40-Hz auditory steady-state response in humans. Br J Anaesth 1997;78:524-529.
125. Rivolta D, Sauer A, Heidegger T, et al. Effects of ketamine on gamma-band oscillations in MEG-data: a comparison with chronic schizophrenia. Soc Neurosci Abstr 2012;38:867.08.
126. Jones NC, Reddy M, Anderson P, Salzberg MR, O'Brien TJ, Pinault D. Acute administration of typical and atypical antipsychotics reduces EEG gamma power, but only the preclinical compound LY379268 reduces the ketamine-induced rise in gamma power. Int J Neuropsychopharmacol 2012;15:657-668.
127. Ma J, Leung LS. Relation between hippocampal gamma waves and behavioral disturbances induced by phencyclidine and methamphetamine. Behav Brain Res 2000;111:1-11.
128. Ma J, Leung LS. The supramammillo-septal-hippocampal pathway mediates sensorimotor gating impairment and hyperlocomotion induced by MK-801 and ketamine in rats. Psychopharmacology 2007;191:961-974.
129. Roopun AK, Cunningham MO, Racca C, Alter K, Traub RD, Whittington MA. Region-specific changes in gamma and beta2 rhythms in NMDA receptor dysfunction models of schizophrenia. Schizophr Bull 2008;34:962-973.
130. McNally JM, McCarley RW, McKenna JT, Yanagawa Y, Brown RE. Complex receptor mediation of acute ketamine application on in vitro gamma oscillations in mouse prefrontal cortex: modeling gamma band oscillation abnormalities in schizophrenia. Neuroscience 2011;199:51-63.
131. Anver H, Ward PD, Magony A, Vreugdenhil M. NMDA receptor hypofunction phase couples independent gamma-oscillations in the rat visual cortex. Neuropsychopharmacology 2011;36:519-528.
132. Spencer KM. Visual gamma oscillations in schizophrenia: implications for understanding neural circuitry abnormalities. Clin EEG Neurosci 2008;39:65-68.
133. Hamm JP, Gilmore CS, Clementz BA. Augmented gamma band auditory steady-state responses: support for NMDA hypofunction in schizophrenia. Schizophr Res 2012;138:1-7.
134. Spencer KM, Nestor PG, Perlmutter R, et al. Neural synchrony indexes disordered perception and cognition in schizophrenia. Proc Natl Acad Sci U S A 2004;101:17288-17293.
135. Lee KH, Williams LM, Haig A, Gordon E. "Gamma (40 Hz) phase synchronicity" and symptom dimensions in schizophrenia. Cogn Neuropsychiatry 2003;8:57-71.
136. Carlen 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.
137. Korotkova T, Fuchs EC, Ponomarenko A, von Engelhardt J, Monyer H. NMDA receptor ablation on parvalbumin-positive interneurons impairs hippocampal synchrony, spatial representations, and working memory. Neuron 2010;68:557-569.
138. Kikuchi M, Hashimoto T, Nagasawa T, et al. Frontal areas contribute to reduced global coordination of resting-state gamma activities in drug-naive patients with schizophrenia. Schizophr Res 2011;130:187-194.
139. Spencer FA, Iorio A, You J, et al. Uncertainties in baseline risk estimates and confidence in treatment effects. BMJ 2012;345:e7401.
140. Itil TM, Saletu B, Davis S. EEG findings in chronic schizophrenics based on digital computer period analysis and analog power spectra. Biol Psychiatry 1972;5:1-13.
141. Itil TM. Qualitative and quantitative EEG findings in schizophrenia. Schizophr Bull 1977;3:61-79.
142. Kulikova SP, Tolmacheva EA, Anderson P, et al. Opposite effects of ketamine and deep brain stimulation on rat thalamocortical information processing. Eur J Neurosci 2012;36:3407-3419.
143. Clementz BA, Wang J, Keil A. Normal electrocortical facilitation but abnormal target identification during visual sustained attention in schizophrenia. J Neurosci 2008;28:13411-13418.
144. Wang J, Brown R, Dobkins KR, McDowell JE, Clementz BA. Diminished parietal cortex activity associated with poor motion direction discrimination performance in schizophrenia. Cereb Cortex 2010;20:1749-1755.
145. Goutagny R, Manseau F, Jackson J, Danik M, Williams S. In vitro activation of the medial septum-diagonal band complex generates atropine-sensitive and atropine-resistant hippocampal theta rhythm: an investigation using a complete septohippocampal preparation. Hippocampus 2008;18:531-535.
146. Middleton S, Jalics J, Kispersky T, et al. NMDA receptor-dependent switching between different gamma rhythm-generating microcircuits in entorhinal cortex. Proc Natl Acad Sci U S A 2008;105:18572-18577.
147. Oke OO, Magony A, Anver H, et al. High-frequency gamma oscillations coexist with low-frequency gamma oscillations in the rat visual cortex in vitro. Eur J Neurosci 2010;31:1435-1445.
148. Breier A, Malhotra AK, Pinals DA, Weisenfeld NI, Pickar D. Association of ketamine-induced psychosis with focal activation of the prefrontal cortex in healthy volunteers. Am J Psychiatry 1997;154:805-811.
149. Whittington MA, Traub RD, Jefferys JG. Synchronized oscillations in interneuron networks driven by metabotropic glutamate receptor activation. Nature 1995;373:612-615.
150. Fisahn A, Contractor A, Traub RD, Buhl EH, Heinemann SF, McBain CJ. Distinct roles for the kainate receptor subunits GluR5 and GluR6 in kainate-induced hippocampal gamma oscillations. J Neurosci 2004;24:9658-9668.
151. Fisahn A, Pike FG, Buhl EH, Paulsen O. Cholinergic induction of network oscillations at 40 Hz in the hippocampus in vitro. Nature 1998;394:186-189.
152. Brown RE, Basheer R, McKenna JT, Strecker RE, McCarley RW. Control of sleep and wakefulness. Physiol Rev 2012;92:1087-1187.
153. Hajos N, Paulsen O. Network mechanisms of gamma oscillations in the CA3 region of the hippocampus. Neural Netw 2009;22:1113-1119.
154. Whittington MA, Cunningham MO, LeBeau FE, Racca C, Traub RD. Multiple origins of the cortical gamma rhythm. Dev Neurobiol 2011;71:92-106.
155. Hajos N, Ellender TJ, Zemankovics R, et al. Maintaining network activity in submerged hippocampal slices: importance of oxygen supply. Eur J Neurosci 2009;29:319-327.
156. Scheeringa R, Fries P, Petersson KM, et al. Neuronal dynamics underlying high- and low-frequency EEG oscillations contribute independently to the human BOLD signal. Neuron 2011;69:572-583.
157. Gloveli T, Dugladze T, Saha S, et al. Differential involvement of oriens/pyramidale interneurones in hippocampal network oscillations in vitro. J Physiol 2005;562:131-147.
158. Kwon JS, O'Donnell BF, Wallenstein GV, et al. Gamma frequency-range abnormalities to auditory stimulation in schizophrenia. Arch Gen Psychiatry 1999;56:1001-1005.
159. Vierling-Claassen D, Siekmeier P, Stufflebeam S, Kopell N. Modeling GABA alterations in schizophrenia: a link between impaired inhibition and altered gamma and beta range auditory entrainment. J Neurophysiol 2008;99:2656-2671.
160. Kopell N, Ermentrout GB, Whittington MA, Traub RD. Gamma rhythms and beta rhythms have different synchronization properties. Proc Natl Acad Sci U S A 2000;97:1867-1872.
161. Ford JM, Mathalon DH, Whitfield S, Faustman WO, Roth WT. Reduced communication between frontal and temporal lobes during talking in schizophrenia. Biol Psychiatry 2002;51:485-492.
162. Koenig T, Lehmann D, Saito N, Kuginuki T, Kinoshita T, Koukkou M. Decreased functional connectivity of EEG theta-frequency activity in first-episode, neuroleptic-naive patients with schizophrenia: preliminary results. Schizophr Res 2001;50:55-60.
163. Bates AT, Kiehl KA, Laurens KR, Liddle PF. Low-frequency EEG oscillations associated with information processing in schizophrenia. Schizophr Res 2009;115:222-230.
164. Basar-Eroglu C, Schmiedt-Fehr C, Marbach S, Brand A, Mathes B. Altered oscillatory alpha and theta networks in schizophrenia. Brain Res 2008;1235:143-152.
165. Schmiedt C, Brand A, Hildebrandt H, Basar-Eroglu C. Event-related theta oscillations during working memory tasks in patients with schizophrenia and healthy controls. Brain Res Cogn Brain Res 2005;25:936-947.
166. Klausberger T, Somogyi P. Neuronal diversity and temporal dynamics: the unity of hippocampal circuit operations. Science 2008;321:53-57.
167. Buzsaki G, Horvath Z, Urioste R, Hetke J, Wise K. High frequency network oscillation in the hippocampus. Science 1992;256:1025-1027.
168. Lisman J, Buzsaki G. A neural coding scheme formed by the combined function of gamma and theta oscillations. Schizophr Bull 2008;34:974-980.
169. Lakatos P, Karmos G, Mehta AD, Ulbert I, Schroeder CE. Entrainment of neuronal oscillations as a mechanism of attentional selection. Science 2008;320:110-113.
170. Bragin A, Jando G, Nadasdy Z, Hetke J, Wise K, Buzsaki G. Gamma (40-100 Hz) oscillation in the hippocampus of the behaving rat. J Neurosci 1995;15:47-60.
171. Lakatos P, Shah AS, Knuth KH, Ulbert I, Karmos G, Schroeder CE. An oscillatory hierarchy controlling neuronal excitability and stimulus processing in the auditory cortex. J Neurophysiol 2005;94:1904-1911.
172. Canolty RT, Edwards E, Dalal SS, et al. High gamma power is phase-locked to theta oscillations in human neocortex. Science 2006;313:1626-1628.
173. Dzirasa K, Ramsey AJ, Takahashi DY, et al. Hyperdopaminergia and NMDA receptor hypofunction disrupt neural phase signaling. J Neurosci 2009;29:8215-8224.
174. Galderisi S, Mucci A, Volpe U, Boutros N. Evidence-based medicine and electrophysiology in schizophrenia. Clin EEG Neurosci 2009;40:62-77.
175. Zhang Y, Llinas RR, Lisman JE. Inhibition of NMDARs in the nucleus reticularis of the thalamus produces delta frequency bursting. Front Neural Circuits 2009;3:20.
176. Feng J, Hoffmann WE, Kiss K, Hajos M. Effects of AMPA receptor positive allosteric modulator in pharmacological and genetic models of schizophrenia NMDA receptor hypofunction. Soc Neurosc Abstr 2011;37:163.22.
177. Gonzalez-Burgos G, Lewis DA. GABA neurons and the mechanisms of network oscillations: implications for understanding cortical dysfunction in schizophrenia. Schizophr Bull 2008;34:944-961.
178. Buzsaki G. Rhythms of the brain. Oxford: Oxford University Press, 2006.
179. Sohal VS, Zhang F, Yizhar O, Deisseroth K. Parvalbumin neurons and gamma rhythms enhance cortical circuit performance. Nature 2009;459:698-702.
180. Spencer KM, Niznikiewicz MA, Nestor PG, Shenton ME, McCarley RW. Left auditory cortex gamma synchronization and auditory hallucination symptoms in schizophrenia. BMC Neurosci 2009;10:85.
181. Sigurdsson T, Stark KL, Karayiorgou M, Gogos JA, Gordon JA. Impaired hippocampal-prefrontal synchrony in a genetic mouse model of schizophrenia. Nature 2010;464:763-767.
182. Kinney JW, Davis CN, Tabarean I, Conti B, Bartfai T, Behrens MM. A specific role for NR2A-containing NMDA receptors in the maintenance of parvalbumin and GAD67 immunoreactivity in cultured interneurons. J Neurosci 2006;26:1604-1615.
183. Anastasio NC, Johnson KM. Differential regulation of the NMDA receptor by acute and sub-chronic phencyclidine administration in the developing rat. J Neurochem 2008;104:1210-1218.
184. Anastasio NC, Xia Y, O'Connor ZR, Johnson KM. Differential role of N-methyl-d-aspartate receptor subunits 2A and 2B in mediating phencyclidine-induced perinatal neuronal apoptosis and behavioral deficits. Neuroscience 2009;163:1181-1191.
185. Hardingham GE, Bading H. Synaptic versus extrasynaptic NMDA receptor signalling: implications for neurodegenerative disorders. Nat Rev Neurosci 2010;11:682-696.
186. Becker A, Peters B, Schroeder H, Mann T, Huether G, Grecksch G. Ketamine-induced changes in rat behaviour: a possible animal model of schizophrenia. Prog Neuropsychopharmacol Biol Psychiatry 2003;27:687-700.
187. Belforte JE, Zsiros V, Sklar ER, et al. Postnatal NMDA receptor ablation in corticolimbic interneurons confers schizophrenia-like phenotypes. Nat Neurosci 2010;13:76-83.
188. Keilhoff G, Becker A, Grecksch G, Wolf G, Bernstein HG. Repeated application of ketamine to rats induces changes in the hippocampal expression of parvalbumin, neuronal nitric oxide synthase and cFOS similar to those found in human schizophrenia. Neuroscience 2004;126:591-598.
189. von Engelhardt J, Doganci B, Seeburg PH, Monyer H. Synaptic NR2A- but not NR2B-containing NMDA receptors increase with blockade of ionotropic glutamate receptors. Front Mol Neurosci 2009;2:19.
190. Wilson MA, Kinsman SL, Johnston MV. Expression of NMDA receptor subunit mRNA after MK-801 treatment in neonatal rats. Brain Res Dev Brain Res 1998;109:211-220.
191. Allen NC, Bagade S, McQueen MB, et al. Systematic meta-analyses and field synopsis of genetic association studies in schizophrenia: the SzGene database. Nat Genet 2008;40:827-834.
192. Homayoun H, Moghaddam B. NMDA receptor hypofunction produces opposite effects on prefrontal cortex interneurons and pyramidal neurons. J Neurosci 2007;27:11496-11500.
193. Grunze HC, Rainnie DG, Hasselmo ME, et al. NMDA-dependent modulation of CA1 local circuit inhibition. J Neurosci 1996;16:2034-2043.
194. Rotaru DC, Yoshino H, Lewis DA, Ermentrout GB, Gonzalez-Burgos G. Glutamate receptor subtypes mediating synaptic activation of prefrontal cortex neurons: relevance for schizophrenia. J Neurosci 2011;31:142-156.
195. Hajos N, Freund TF, Mody I. Comparison of single NMDA receptor channels recorded on hippocampal principal cells and oriens/alveus interneurons projecting to stratum lacunosum-moleculare (O-LM cells). Acta Biol Hung 2002;53:465-472.
196. Klausberger T, Magill PJ, Marton LF, et al. Brain-state- and cell-type-specific firing of hippocampal interneurons in vivo. Nature 2003;421:844-848.
197. Gillies MJ, Traub RD, LeBeau FE, et al. A model of atropine-resistant theta oscillations in rat hippocampal area CA1. J Physiol 2002;543:779-793.
198. Tort AB, Rotstein HG, Dugladze T, Gloveli T, Kopell NJ. On the formation of gamma-coherent cell assemblies by oriens lacunosum-moleculare interneurons in the hippocampus. Proc Natl Acad Sci U S A 2007;104:13490-13495.
199. Neymotin SA, Lazarewicz MT, Sherif M, Contreras D, Finkel LH, Lytton WW. Ketamine disrupts theta modulation of gamma in a computer model of hippocampus. J Neurosci 2011;31:11733-11743.
200. Moghaddam B, Adams B, Verma A, Daly D. Activation of glutamatergic neurotransmission by ketamine: a novel step in the pathway from NMDA receptor blockade to dopaminergic and cognitive disruptions associated with the prefrontal cortex. J Neurosci 1997;17:2921-2927.
201. Corlett PR, Frith CD, Fletcher PC. From drugs to deprivation: a Bayesian framework for understanding models of psychosis. Psychopharmacology 2009;206:515-530.
202. Vertes RP, Kocsis B. Brainstem-diencephalo-septohippocampal systems controlling the theta rhythm of the hippocampus. Neuroscience 1997;81:893-926.
203. Kocsis B, Li S. In vivo contribution of h-channels in the septal pacemaker to theta rhythm generation. Eur J Neurosci 2004;20:2149-2158.
204. Kinney GG, Kocsis B, Vertes RP. Injections of excitatory amino acid antagonists into the median raphe nucleus produce hippocampal theta rhythm in the urethane-anesthetized rat. Brain Res 1994;654:96-104.
205. Rujescu D, Bender A, Keck M, et al. A pharmacological model for psychosis based on N-methyl-d-aspartate receptor hypofunction: molecular, cellular, functional and behavioral abnormalities. Biol Psychiatry 2006;59:721-729.
206. Stefani MR, Moghaddam B. Transient N-methyl-d-aspartate receptor blockade in early development causes lasting cognitive deficits relevant to schizophrenia. Biol Psychiatry 2005;57:433-436.
207. Mansbach RS, Geyer MA. Effects of phencyclidine and phencyclidine biologs on sensorimotor gating in the rat. Neuropsychopharmacology 1989;2:299-308.
208. Vohs JL, Chambers RA, O'Donnell BF, Krishnan GP, Morzorati SL. Auditory steady state responses in a schizophrenia rat model probed by excitatory/inhibitory receptor manipulation. Int J Psychophysiol 2012;86:136-142.
209. McNally JM, Kim T, Yanagawa Y, McCarley RW, Brown RE. Acute and chronic effects of ketamine on gamma oscillations in mouse prefrontal cortex. Soc Neurosci Abstr 2011;37:661.07.