Differential effects of NMDA receptor antagonists at lower and higher doses on basal gamma band oscillation power in rat cortical electroencephalograms

Neuropharmacology

Volumn 85, Issue , 2014, Pages 384-396

  Hiyoshi, Tetsuaki ^a   Kambe, Daiji ^a   Karasawa, Jun Ichi ^a   Chaki, Shigeyuki ^a  

^a TAISHO PHARMACEUTICAL CO LTD   (Japan)

Author keywords

Delta band oscillation; Gamma band oscillation; High frequency oscillation; Hyperglutamatergic state; NMDA receptor antagonist; Schizophrenia

Indexed keywords

4 IODO 2,5 DIMETHOXYAMPHETAMINE; DIZOCILPINE; KETAMINE; MEMANTINE; METHAMPHETAMINE; N METHYL DEXTRO ASPARTIC ACID RECEPTOR BLOCKING AGENT; PHENCYCLIDINE; 4-IODO-2,5-DIMETHOXYPHENYLISOPROPYLAMINE; AMINO ACID RECEPTOR BLOCKING AGENT; AMPHETAMINE DERIVATIVE; DIZOCILPINE MALEATE; N METHYL DEXTRO ASPARTIC ACID RECEPTOR;

ANIMAL EXPERIMENT; ARTICLE; CONTROLLED STUDY; DELTA OSCILLATION; DRUG EFFECT; DRUG MEGADOSE; DRUG POTENCY; ELECTROENCEPHALOGRAM; GABAERGIC TRANSMISSION; GAMMA BAND OSCILLATION; HIGH FREQUENCY OSCILLATION; LOW DRUG DOSE; MALE; NEUROTRANSMISSION; NONHUMAN; PRIORITY JOURNAL; RAT; ANIMAL; ANTAGONISTS AND INHIBITORS; BRAIN; COMPARATIVE STUDY; DOSE RESPONSE; DRUG EFFECTS; ELECTRODE IMPLANT; ELECTROENCEPHALOGRAPHY; GAMMA RHYTHM; METABOLISM; PHYSIOLOGY; SPRAGUE DAWLEY RAT;

AMPHETAMINES; ANIMALS; BRAIN; DIZOCILPINE MALEATE; DOSE-RESPONSE RELATIONSHIP, DRUG; ELECTRODES, IMPLANTED; ELECTROENCEPHALOGRAPHY; EXCITATORY AMINO ACID ANTAGONISTS; GAMMA RHYTHM; KETAMINE; MALE; MEMANTINE; METHAMPHETAMINE; PHENCYCLIDINE; RATS, SPRAGUE-DAWLEY; RECEPTORS, N-METHYL-D-ASPARTATE;

EID: 84903277714     PISSN: 00283908     EISSN: 18737064     Source Type: Journal    
DOI: 10.1016/j.neuropharm.2014.05.037     Document Type: Article

References (72)

1. A. Adell, L. Jiménez-Sánchez, X. López-Gil, and T. Romón Is the acute NMDA receptor hypofunction a valid model of schizophrenia? Schizophr. Bull. 38 2012 9 14
2. T. Baldeweg, S. Spence, S.R. Hirsch, and J. Gruzelier Gamma-band electroencephalographic oscillations in a patient with somatic hallucinations Lancet 352 1998 620 621 (Pubitemid 28380147)
3. 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)
4. E. Başar, and B. Güntekin A review of brain oscillations in cognitive disorders and the role of neurotransmitters Brain Res. 1235 2008 172 193
5. A. Breier, A.K. Malhotra, D.A. Pinals, N.I. Weisenfeld, and D. Pickar Association of ketamine-induced psychosis with focal activation of the prefrontal cortex in healthy volunteers Am. J. Psychiatry 154 1997 805 811 (Pubitemid 27230103)
6. G. Buzsáki The thalamic clock: emergent network properties Neuroscience 41 1991 351 364
7. M. Carlén, K. Meletis, J.H. Siegle, J.A. Cardin, K. Futai, D. Vierling-Claassen, C. Rühlmann, S.R. Jones, K. Deisseroth, M. Sheng, C.I. Moore, and L.H. Tsai A critical role for NMDA receptors in parvalbumin interneurons for gamma rhythm induction and behavior Mol. Psychiatry 17 2012 537 548
8. J. Cartmell, J.A. Monn, and D.D. Schoepp The metabotropic glutamate 2/3 receptor agonists LY354740 and LY379268 selectively attenuate phencyclidine versus d-amphetamine motor behaviors in rats J. Pharmacol. Exp. Ther. 291 1999 161 170 (Pubitemid 29451586)
9. M.O. Cunningham, C.H. Davies, E.H. Buhl, N. Kopell, and M.A. Whittington Gamma oscillations induced by kainate receptor activation in the entorhinal cortex in vitro J. Neurosci. 23 2003 9761 9769 (Pubitemid 37371588)
10. J.F. Deakin, J. Lees, S. McKie, J.E. Hallak, S.R. Williams, and S.M. Dursun Glutamate and the neural basis of the subjective effects of ketamine: a pharmaco-magnetic resonance imaging study Arch. Gen. Psychiatry 65 2008 154 164 (Pubitemid 351214314)
11. S. Dedeurwaerdere, C. Wintmolders, R. Straetemans, D. Pemberton, and X. Langlois Memantine-induced brain activation as a model for the rapid screening of potential novel antipsychotic compounds: exemplified by activity of an mGlu2/3 receptor agonist Psychopharmacol. Berl. 214 2011 505 514
12. G.E. Duncan, S. Miyamoto, J.N. Leipzig, and J.A. Lieberman Comparison of brain metabolic activity patterns induced by ketamine, MK-801 and amphetamine in rats: support for NMDA receptor involvement in responses to subanesthetic dose of ketamine Brain Res. 843 1999 171 183 (Pubitemid 29488707)
13. P. Fries, D. Nikolić, and W. Singer The gamma cycle Trends Neurosci. 30 2007 309 316 (Pubitemid 46991120)
14. M.J. Gandal, J.C. Edgar, K. Klook, and S.J. Siegel Gamma synchrony: towards a translational biomarker for the treatment-resistant symptoms of schizophrenia Neuropharmacology 62 2012 1504 1518
15. W.B. Gentry, A.U. Ghafoor, W.D. Wessinger, E.M. Laurenzana, H.P. Hendrickson, and S.M. Owens (+)-Methamphetamine-induced spontaneous behavior in rats depends on route of (+)METH administration Pharmacol. Biochem. Behav. 79 2004 751 760 (Pubitemid 39600616)
16. J.C. Gewirtz, and G.J. Marek Behavioral evidence for interactions between a hallucinogenic drug and group II metabotropic glutamate receptors Neuropsychopharmacology 23 2000 569 576
17. G. Gonzalez-Burgos, T. Hashimoto, and D.A. Lewis Alterations of cortical GABA neurons and network oscillations in schizophrenia Curr. Psychiatry Rep. 12 2010 335 344
18. G. Gonzalez-Burgos, and D.A. Lewis NMDA receptor hypofunction, parvalbumin-positive neurons, and cortical gamma oscillations in schizophrenia Schizophr. Bull. 38 2012 950 957
19. H.C. Grunze, D.G. Rainnie, M.E. Hasselmo, E. Barkai, E.F. Hearn, R.W. McCarley, and R.W. Greene NMDA-dependent modulation of CA1 local circuit inhibition J. Neurosci. 16 1996 2034 2043 (Pubitemid 26144016)
20. T. Hakami, N.C. Jones, E.A. Tolmacheva, J. Gaudias, J. Chaumont, M. Salzberg, T.J. O'Brien, and D. Pinault NMDA receptor hypofunction leads to generalized and persistent aberrant gamma oscillations independent of hyperlocomotion and the state of consciousness PLoS One 4 2009 e6755
21. J.P. Hamm, C.S. Gilmore, and B.A. Clementz Augmented gamma band auditory steady-state responses: support for NMDA hypofunction in schizophrenia Schizophr. Res. 138 2012 1 7
22. M.B. Hesselink, A.G. De Boer, D.D. Breimer, and W. Danysz Dopamine release in the prefrontal cortex in response to memantine following sub-chronic NMDA receptor blockade with memantine: a microdialysis study in rats J. Neural. Transm. 106 1999 803 818 (Pubitemid 29516050)
23. 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)
24. L.E. Hong, A. Summerfelt, R.W. Buchanan, P. O'Donnell, G.K. Thaker, M.A. Weiler, and A.C. Lahti Gamma and delta neural oscillations and association with clinical symptoms under subanesthetic ketamine Neuropsychopharmacology 35 2010 632 640
25. M.J. Hunt, M. Falinska, and S. Kasicki Local injection of MK801 modifies oscillatory activity in the nucleus accumbens in awake rats J. Psychopharmacol. 24 2010 931 941
26. M.J. Hunt, B. Raynaud, and R. Garcia Ketamine dose-dependently induces high-frequency oscillations in the nucleus accumbens in freely moving rats Biol. Psychiatry 60 2006 1206 1214 (Pubitemid 44693529)
27. 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)
28. D.C. Javitt, and S.R. Zukin Recent advances in the phencyclidine model of schizophrenia Am. J. Psychiatry 148 1991 1301 1308
29. M. Kalinichev, M.J. Robbins, E.M. Hartfield, P.R. Maycox, S.H. Moore, K.M. Savage, N.E. Austin, and D.N. Jones Comparison between intraperitoneal and subcutaneous phencyclidine administration in Sprague-Dawley rats: a locomotor activity and gene induction study Prog. Neuropsychopharmacol. Biol. Psychiatry 32 2008 414 422 (Pubitemid 351178957)
30. E. Koros, H. Rosenbrock, G. Birk, C. Weiss, and F. Sams-Dodd The selective mGlu5 receptor antagonist MTEP, similar to NMDA receptor antagonists, induces social isolation in rats Neuropsychopharmacology 32 2007 562 576
31. J.H. Krystal, D.C. D'Souza, D. Mathalon, E. Perry, A. Belger, and R. Hoffman NMDA receptor antagonist effects, cortical glutamatergic function, and schizophrenia: toward a paradigm shift in medication development Psychopharmacol. Berl. 169 2003 215 233 (Pubitemid 37264943)
32. 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)
33. S.P. Kulikova, E.A. Tolmacheva, P. Anderson, J. Gaudias, B.E. Adams, T. Zheng, and D. Pinault Opposite effects of ketamine and deep brain stimulation on rat thalamocortical information processing Eur. J. Neurosci. 36 2012 3407 3419
34. A.C. Lahti, B. Koffel, D. LaPorte, and C.A. Tamminga Subanesthetic doses of ketamine stimulate psychosis in schizophrenia Neuropsychopharmacology 13 1995 9 19
35. J. Lisman Excitation, inhibition, local oscillations, or large-scale loops: what causes the symptoms of schizophrenia? Curr. Opin. Neurobiol. 22 2012 537 544
36. C.L. Littlewood, N. Jones, M.J. O'Neill, S.N. Mitchell, M. Tricklebank, and S.C. Williams Mapping the central effects of ketamine in the rat using pharmacological MRI Psychopharmacol. Berl. 186 2006 64 81 (Pubitemid 43668312)
37. X. López-Gil, Z. Babot, M. Amargós-Bosch, C. Suñol, F. Artigas, and A. Adell Clozapine and haloperidol differently suppress the MK-801-increased glutamatergic and serotonergic transmission in the medial prefrontal cortex of the rat Neuropsychopharmacology 32 2007 2087 2097 (Pubitemid 47417703)
38. E.O. Mann, C.A. Radcliffe, and O. Paulsen Hippocampal gamma-frequency oscillations: from interneurones to pyramidal cells, and back J. Physiol. 562 2005 55 63 (Pubitemid 40207784)
39. J.M. McNally, R.W. McCarley, and R.E. Brown Impaired GABAergic neurotransmission in schizophrenia underlies impairments in cortical gamma band oscillations Curr. Psychiatry Rep. 15 2013 346
40. J.M. McNally, R.W. McCarley, J.T. McKenna, Y. Yanagawa, and R.E. Brown Complex receptor mediation of acute ketamine application on in vitro gamma oscillations in mouse prefrontal cortex: modeling gamma band oscillation abnormalities in schizophrenia Neuroscience 199 2011 51 63
41. B. Moghaddam, B. Adams, A. Verma, and D. Daly 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. 17 1997 2921 2927 (Pubitemid 27155025)
42. B. Moghaddam, and B.W. Adams Reversal of phencyclidine effects by a group II metabotropic glutamate receptor agonist in rats Science 281 1998 1349 1352 (Pubitemid 28406826)
43. B. Moghaddam, and M.E. Jackson Glutamatergic animal models of schizophrenia Ann. N.Y. Acad. Sci. 1003 2003 131 137 (Pubitemid 38083051)
44. J.W. Newcomer, N.B. Farber, V. Jevtovic-Todorovic, G. Selke, A.K. Melson, T. Hershey, S. Craft, and J.W. Olney Ketamine-induced NMDA receptor hypofunction as a model of memory impairment and psychosis Neuropsychopharmacology 20 1999 106 118 (Pubitemid 29010370)
45. M.J. Nicolás, J. López-Azcárate, M. Valencia, M. Alegre, M. Pérez-Alcázar, J. Iriarte, and J. Artieda Ketamine-induced oscillations in the motor circuit of the rat basal ganglia PLoS One 6 2011 e21814
46. J.W. Olney, J.W. Newcomer, and N.B. Farber NMDA receptor hypofunction model of schizophrenia J. Psychiatr. Res. 33 1999 523 533
47. M. Olszewski, W. Dolowa, P. Matulewicz, S. Kasicki, and M.J. Hunt NMDA receptor antagonist-enhanced high frequency oscillations: are they generated broadly or regionally specific? Eur. Neuropsychopharmacol. 23 2013 1795 1805
48. T. Páleníček, M. Fujáková, M. Brunovský, M. Balíková, J. Horáček, I. Gorman, F. Tylš, B. Tišlerová, P. Soš, V. Bubeníková-Valešová, C. Höschl, and V. Krajča Electroencephalographic spectral and coherence analysis of ketamine in rats: correlation with behavioral effects and pharmacokinetics Neuropsychobiology 63 2011 202 218
49. C.G. Parsons, A. Stöffler, and W. Danysz Memantine: a NMDA receptor antagonist that improves memory by restoration of homeostasis in the glutamatergic system-too little activation is bad, too much is even worse Neuropharmacology 53 2007 699 723 (Pubitemid 47532143)
50. G. Paxinos, and C. Watson The Rat Brain in Stereotaxic Coordinates sixth ed. 2007 Elsevier
51. K.G. Phillips, M.C. Cotel, A.P. McCarthy, D.M. Edgar, M. Tricklebank, M.J. O'Neill, M.W. Jones, and K.A. Wafford Differential effects of NMDA antagonists on high frequency and gamma EEG oscillations in a neurodevelopmental model of schizophrenia Neuropharmacology 62 2012 1359 1370
52. 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)
53. N.V. Povysheva, and J.W. Johnson Tonic NMDA receptor-mediated current in prefrontal cortical pyramidal cells and fast-spiking interneurons J. Neurophysiol. 107 2012 2232 2243
54. D.C. Rotaru, H. Yoshino, D.A. Lewis, G.B. Ermentrout, and G. Gonzalez-Burgos Glutamate receptor subtypes mediating synaptic activation of prefrontal cortex neurons: relevance for schizophrenia J. Neurosci. 31 2011 142 156
55. L.M. Rowland, J.R. Bustillo, P.G. Mullins, R.E. Jung, R. Lenroot, E. Landgraf, R. Barrow, R. Yeo, J. Lauriello, and W.M. Brooks Effects of ketamine on anterior cingulate glutamate metabolism in healthy humans: a 4-T proton MRS study Am. J. Psychiatry 162 2005 394 396 (Pubitemid 40216226)
56. G. Sanacora, M.A. Smith, S. Pathak, H.L. Su, P.H. Boeijinga, D.J. McCarthy, and M.C. Quirk Lanicemine: a low-trapping NMDA channel blocker produces sustained antidepressant efficacy with minimal psychotomimetic adverse effects Mol. Psychiatry 2013 Oct. 15 10.1038/mp.2013.130 (Epub ahead of print)
57. F.R. Sharp, M. Tomitaka, M. Bernaudin, and S. Tomitaka Psychosis: pathological activation of limbic thalamocortical circuits by psychomimetics and schizophrenia? Trends Neurosci. 24 2001 330 334 (Pubitemid 32455433)
58. J.R. Shoblock, E.B. Sullivan, I.M. Maisonneuve, and S.D. Glick Neurochemical and behavioral differences between d-methamphetamine and d-amphetamine in rats Psychopharmacol. (Berl.) 165 2003 359 369 (Pubitemid 36223077)
59. K.M. Spencer, M.A. Niznikiewicz, P.G. Nestor, M.E. Shenton, and R.W. McCarley Left auditory cortex gamma synchronization and auditory hallucination symptoms in schizophrenia BMC Neurosci. 10 2009 85
60. M. Steriade Grouping of brain rhythms in corticothalamic systems Neuroscience 137 2006 1087 1106 (Pubitemid 43133136)
61. J.M. Stone, C. Dietrich, R. Edden, M.A. Mehta, S. De Simoni, L.J. Reed, J.H. Krystal, D. Nutt, and G.J. Barker Ketamine effects on brain GABA and glutamate levels with 1H-MRS: relationship to ketamine-induced psychopathology Mol. Psychiatry 17 2012 664 665
62. V. Suazo, Á. Díez, C. Martín, A. Ballesteros, P. Casado, M. Martín-Loeches, and V. Molina Elevated noise power in gamma band related to negative symptoms and memory deficit in schizophrenia Prog.Neuropsychopharmacol.Biol. Psychiatry 8 2012 270 275
63. 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)
64. R.D. Traub, J.G. Jefferys, and M.A. Whittington Simulation of gamma rhythms in networks of interneurons and pyramidal cells J. Comput. Neurosci. 4 1997 141 150 (Pubitemid 27196617)
65. P.J. Uhlhaas, and W. Singer Abnormal neural oscillations and synchrony in schizophrenia Nat. Rev. Neurosci. 11 2010 100 113
66. H.X. Wang, and W.J. Gao Development of calcium-permeable AMPA receptors and their correlation with NMDA receptors in fast-spiking interneurons of rat prefrontal cortex J. Physiol. 588 2010 2823 2838
67. N. Wegener, J. Nagel, R. Gross, C. Chambon, S. Greco, M. Pietraszek, A. Gravius, and W. Danysz Evaluation of brain pharmacokinetics of (+)MK-801 in relation to behaviour Neurosci. Lett. 503 2011 68 72
68. G. Winterer, R. Coppola, T.E. Goldberg, M.F. Egan, D.W. Jones, C.E. Sanchez, and D.R. Weinberger Prefrontal broadband noise, working memory, and genetic risk for schizophrenia Am. J. Psychiatry 161 2004 490 500 (Pubitemid 38326104)
69. T.U. Woo, K. Spencer, and R.W. McCarley Gamma oscillation deficits and the onset and early progression of schizophrenia Harv. Rev. Psychiatry 18 2010 173 189
70. P. Xia, H.S. Chen, D. Zhang, and S.A. Lipton Memantine preferentially blocks extrasynaptic over synaptic NMDA receptor currents in hippocampal autapses J. Neurosci. 30 2010 11246 11250
71. O. Yizhar, L.E. Fenno, M. Prigge, F. Schneider, T.J. Davidson, D.J. O'Shea, V.S. Sohal, I. Goshen, J. Finkelstein, J.T. Paz, K. Stehfest, R. Fudim, C. Ramakrishnan, J.R. Huguenard, P. Hegemann, and K. Deisseroth Neocortical excitation/inhibition balance in information processing and social dysfunction Nature 477 2011 171 178
72. Y. Zhang, R.R. Llinas, and J.E. Lisman Inhibition of NMDARs in the nucleus reticularis of the thalamus produces delta frequency bursting Front. Neural. Circuits 3 2009 20