Modeling "psychosis" in vitro by inducing disordered neuronal network activity in cortical brain slices

Psychopharmacology

Volumn 206, Issue 4, 2009, Pages 575-585

  Aghajanian, George K ^a  

^a Yale University School of Medicine   (United States)

Author keywords

Antipsychotic; Astrocyte; GABA; Glutamate; Hallucinogens; Network; Prefrontal cortex; Pyramidal cell; Schizophrenia; Serotonin

Indexed keywords

2,3,4,5 TETRAHYDRO 7,8 DIHYDROXY 1 PHENYL 1H 3 BENZAZEPINE; 4 [2 AMINO 4 (METHYLTHIO)BUTYRYLAMINO] 2 THIABICYCLO[3.1.0]HEXANE 4,6 DICARBOXYLIC ACID 2,2 DIOXIDE; 4 AMINO 2 THIABICYCLO[3.1.0]HEXANE 4,6 DICARBOXYLIC ACID 2,2 DIOXIDE; 4 AMINOBUTYRIC ACID A RECEPTOR BLOCKING AGENT; ATYPICAL ANTIPSYCHOTIC AGENT; DIHYDREXIDINE; DOPAMINE 1 RECEPTOR STIMULATING AGENT; DOPAMINE 5 RECEPTOR AGONIST; DOPAMINE RECEPTOR STIMULATING AGENT; EGLUMETAD; KETAMINE; LYSERGIDE; METABOTROPIC RECEPTOR 2 AGONIST; METABOTROPIC RECEPTOR 3 AGONIST; METABOTROPIC RECEPTOR AGONIST; MK 0777; N METHYL DEXTRO ASPARTIC ACID RECEPTOR BLOCKING AGENT; N,N DIMETHYLTRYPTAMINE; NEUROLEPTIC AGENT; OLANZAPINE; PHENCYCLIDINE; PSYCHEDELIC AGENT; RISPERIDONE; UNCLASSIFIED DRUG; VOLINANSERIN;

ASTROCYTE; BRAIN SLICE; CLINICAL TRIAL; DRUG EFFICACY; DRUG WITHDRAWAL; EXPERIMENTAL MODEL; EXTRAPYRAMIDAL SYMPTOM; HUMAN; IN VITRO STUDY; INTERNEURON; NERVE CELL NETWORK; NEUROPSYCHOLOGICAL TEST; NONHUMAN; PREFRONTAL CORTEX; PRIORITY JOURNAL; PROLACTIN BLOOD LEVEL; PSYCHOSIS; PYRAMIDAL NERVE CELL; REVIEW; SCHIZOPHRENIA; SIDE EFFECT; SINGLE DRUG DOSE; WEIGHT GAIN;

ANIMALS; ANTIPSYCHOTIC AGENTS; CLINICAL TRIALS, PHASE II AS TOPIC; DRUG DELIVERY SYSTEMS; HUMANS; MODELS, BIOLOGICAL; NERVE NET; PREFRONTAL CORTEX; PSYCHOTIC DISORDERS; SCHIZOPHRENIA;

EID: 70349652465     PISSN: 00333158     EISSN: 14322072     Source Type: Journal    
DOI: 10.1007/s00213-009-1484-9     Document Type: Review

References (67)

1. T Abekawa T Ohmori K Ito T Koyama 2000 D1 dopamine receptor activation reduces extracellular glutamate and GABA concentrations in the medial prefrontal cortex Brain Res 867 250 4 10837822 10.1016/S0006-8993(00)02298-8 1:CAS:528:DC%2BD3cXjs1Grurg%3D (Pubitemid 30317405)
2. A Abi-Dargham H Moore 2003 Prefrontal DA transmission at D1 receptors and the pathology of schizophrenia Neuroscientist 9 404 16 14580124 10.1177/1073858403252674 1:CAS:528:DC%2BD3sXoslajtr4%3D (Pubitemid 37204344)
3. GK Aghajanian GJ Marek 1997 Serotonin induces excitatory postsynaptic potentials in apical dendrites of neocortical pyramidal cells Neuropharmacology 36 589 599 9225284 10.1016/S0028-3908(97)00051-8 1:CAS:528:DyaK2sXktlSmsLo%3D (Pubitemid 27272104)
4. 2A receptors, increases EPSCs in layer V pyramidal cells of prefrontal cortex by an asynchronous mode of glutamate release Brain Res 825 161 171 10216183 10.1016/S0006-8993(99)01224-X 1:CAS:528:DyaK1MXisV2hu7c%3D (Pubitemid 29222872)
5. GK Aghajanian GJ Marek 2000 Serotonin model of schizophrenia: emerging role of glutamate mechanisms Brain Res Rev 31 302 312 10719157 10.1016/S0165-0173(99)00046-6 1:CAS:528:DC%2BD3cXhsleqtrs%3D (Pubitemid 30136185)
6. S Akbarian JJ Kim SG Potkin JO Hagman A Tafazzoli WE Bunney Jr EG Jones 1995 Gene expression for glutamic acid decarboxylase is reduced without loss of neurons in prefrontal cortex of schizophrenics Arch Gen Psychiatry 52 258 266 7702443 1:STN:280:DyaK2M3hslSiug%3D%3D
7. NC Andreasen DS O'Leary T Cizadlo S Arndt K Rezai LL Ponto GL Watkins RD Hichwa 1996 Schizophrenia and cognitive dysmetria: a positron-emission tomography study of dysfunctional prefrontal-thalamic-cerebellar circuitry Proc Natl Acad Sci U S A 93 9985 9990 8790444 10.1073/pnas.93.18.9985 1:CAS:528:DyaK28XlsFegsL4%3D (Pubitemid 26296722)
8. S Bandyopadhyay JJ Hablitz 2007 Dopaminergic modulation of local network activity in rat prefrontal cortex J Neurophysiol 97 4120 4128 17392423 10.1152/jn.00898.2006 1:CAS:528:DC%2BD2sXosF2hsbk%3D (Pubitemid 47080644)
9. M Beierlein CP Fall J Rinzel R Yuste 2002 Thalamocortical bursts trigger recurrent activity in neocortical networks: layer 4 as a frequency-dependent gate J Neurosci 22 9885 9894 12427845 1:CAS:528:DC%2BD38XovF2ksLg%3D
10. FM Benes S Berretta 2001 GABAergic interneurons: implications for understanding schizophrenia and bipolar disorder Neuropsychopharmacology 25 1 27 11377916 10.1016/S0893-133X(01)00225-1 1:CAS:528:DC%2BD3MXjslSlurg%3D (Pubitemid 32493819)
11. MA Benneyworth Z Xiang RL Smith EE Garcia PJ Conn E Sanders-Bush 2007 A selective positive allosteric modulator of metabotropic glutamate receptor subtype 2 blocks a hallucinogenic drug model of psychosis Mol Pharmacol 72 477 484 17526600 10.1124/mol.107.035170 1:CAS:528:DC%2BD2sXosVKrt7o%3D (Pubitemid 47124127)
12. JP Charton M Herkert CM Becker H Schroder 1999 Cellular and subcellular localization of the 2B-subunit of the NMDA receptor in the adult rat telencephalon Brain Res 816 609 617 9878886 10.1016/S0006-8993(98)01243-8 1:CAS:528:DyaK1MXhsVamsA%3D%3D (Pubitemid 29225411)
13. PJ Conn JP Pin 1997 Pharmacology and functions of metabotropic glutamate receptors Annu Rev Pharmacol Toxicol 37 205 237 9131252 10.1146/annurev. pharmtox.37.1.205 1:CAS:528:DyaK2sXisl2ktr0%3D
14. P Danos B Baumann HG Bernstein M Franz R Stauch G Northoff D Krell P Falkai B Bogerts 1998 Schizophrenia and anteroventral thalamic nucleus: selective decrease of parvalbumin-immunoreactive thalamocortical projection neurons Psychiatry Res 82 1 10 9645546 10.1016/S0925-4927(97)00071-1 1:STN:280:DyaK1czgslCmsQ%3D%3D (Pubitemid 28259574)
15. R de Beaurepaire A Labelle D Naber BD Jones TR Barnes 1995 An open trial of the D1 antagonist SCH 39166 in six cases of acute psychotic states Psychopharmacology (Berl) 121 323 327 10.1007/BF02246070
16. T de Paulis 2001 M-100907 (Aventis) Curr Opin Investig Drugs 2 123 32 11527004
17. MJ Fell KA Svensson BG Johnson DD Schoepp 2008 Evidence for the Role of metabotropic glutamate (mGlu) 2 not mGlu3 receptors in the preclinical antipsychotic pharmacology of the mGlu2/3 receptor agonist (-)-(1R, 4S, 5S, 6S)-4-amino-2-sulfonylbicyclo[3.1.0]hexane-4, 6-dicarboxylic acid (LY404039) J Pharmacol Ex Ther 326 209 217 10.1124/jpet.108.136861 1:CAS:528: DC%2BD1cXotlyltrw%3D (Pubitemid 351872145)
18. T Fellin O Pascual S Gobbo T Pozzan PG Haydon G Carmignoto 2004 Neuronal synchrony mediated by astrocytic glutamate through activation of extrasynaptic NMDA receptors Neuron 43 729 743 15339653 10.1016/j.neuron.2004.08.011 1:CAS:528:DC%2BD2cXns1yms7k%3D (Pubitemid 39179731)
19. JM Ford JH Krystal DH Mathalon 2007 Neural synchrony in schizophrenia: from networks to new treatments Schizophrenia Bulletin Schizophr Bull 33 848 852 10.1093/schbul/sbm062 (Pubitemid 47216662)
20. WJ Gao LS Krimer PS Goldman-Rakic 2001 Presynaptic regulation of recurrent excitation by D1 receptors in prefrontal circuits Proc Natl Acad Sci U S A 98 295 300 11134520 10.1073/pnas.011524298 1:CAS:528:DC%2BD3MXkslOhtw%3D%3D (Pubitemid 32095903)
21. MS George CE Molnar EL Grenesko B Anderson Q Mu K Johnson Z Nahas Z Knable P Fernandes J Juncos X Huang D Nichols RB Mailman 2007 A single 20 mg dose of dihydrexidine (DAR-0100), a full dopamine D1 agonist, is safe and tolerated in patients with schizophrenia Schizophrenia Research 93 42 50 17467956 10.1016/j.schres.2007.03.011 (Pubitemid 46817947)
22. J Gonzalez-Maeso RL Ang T Yuen P Chan NV Weisstaub JF Lopez-Gimenez M Zhou Y Okawa LF Callado G Milligan JA Gingrich M Filizola JJ Meana SC Sealfon 2008 Identification of a serotonin/glutamate receptor complex implicated in psychosis Nature 452 93 97 18297054 10.1038/nature06612 1:CAS:528: DC%2BD1cXivFynu7w%3D (Pubitemid 351355090)
23. N Gorelova JK Seamans CR Yang 2002 Mechanisms of dopamine activation of fast-spiking interneurons that exert inhibition in rat prefrontal cortex J Neurophysiol 88 3150 66 12466437 10.1152/jn.00335.2002 1:CAS:528: DC%2BD3sXjtV2lsQ%3D%3D
24. E Gouzoulis-Mayfrank K Heekeren A Neukirch M Stoll C Stock M Obradovic K-A Kovar 2005 Psychological effects of (S)-ketamine and N, N-dimethyltryptamine (DMT): a double-blind, cross-over study in healthy volunteers Pharmacopsychiatry 38 301 311 16342002 10.1055/s-2005-916185 1:CAS:528:DC%2BD28XktVagsA%3D%3D (Pubitemid 41815687)
25. HJ Groenewegen HB Uylings 2000 The prefrontal cortex and the integration of sensory, limbic and autonomic information Prog Brain Res 126 3 28 11105636 10.1016/S0079-6123(00)26003-2 1:STN:280:DC%2BD3M%2FosFWnsw%3D%3D (Pubitemid 35461278)
26. A Guidotti J Auta JM Davis E Dong DR Grayson M Veldic X Zhang E Costa 2005 GABAergic dysfunction in schizophrenia: new treatment strategies on the horizon Psychopharmacology (Berl) 180 191 205 10.1007/s00213-005-2212-8 1:CAS:528:DC%2BD2MXltVKnt7w%3D (Pubitemid 40909664)
27. B Haider A Duque AR Hasenstaub DA McCormick 2006 Neocortical network activity in vivo is generated through a dynamic balance of excitation and inhibition J Neurosci 26 4535 4545 16641233 10.1523/JNEUROSCI.5297-05.2006 1:CAS:528:DC%2BD28XksFWqtbo%3D (Pubitemid 44315353)
28. M Harte WT O'Connor 2004 Evidence for a differential medial prefrontal dopamine D1 and D2 receptor regulation of local and ventral tegmental glutamate and GABA release: a dual probe microdialysis study in the awake rat Brain Res 1017 120 129 15261107 10.1016/j.brainres.2004.05.027 1:CAS:528: DC%2BD2cXlsl2jur0%3D (Pubitemid 38917151)
29. GA Higgins TM Ballard M Enderlin M Haman JA Kemp 2005 Evidence for improved performance in cognitive tasks following selective NR2B NMDA receptor antagonist pre-treatment in the rat Psychopharmacology (Berl) 179 85 98 10.1007/s00213-005-2203-9 1:CAS:528:DC%2BD2MXjtV2iur8%3D (Pubitemid 40576695)
30. H Homayoun B Moghaddam 2007 NMDA receptor hypofunction produces opposite effects on prefrontal cortex interneurons and pyramidal neurons J Neurosci 27 11496 11500 17959792 10.1523/JNEUROSCI.2213-07.2007 1:CAS:528:DC%2BD2sXht1Kms7zK (Pubitemid 350006886)
31. PG Haydon G Carmignoto 2006 Astrocyte control of synaptic transmission and neurovascular coupling Physiol Rev 86 1009 1031 16816144 10.1152/physrev.00049.2005 1:CAS:528:DC%2BD28XnsFGgtbY%3D (Pubitemid 44033387)
32. 2 and D2 receptor occupancy of clozapine, risperidone, and olanzapine in schizophrenia Am J Psychiatry 156 286 293 9989565 1:STN:280:DyaK1M7kt1Kksw%3D%3D
33. JH Krystal LP Karper JP Seibyl, et al. 1994 Subanesthetic effects of the noncompetitive NMDA antagonist, ketamine, in humans. Psychotomimetic, perceptual, cognitive, and neuro-endocrine responses Arch Gen Psychiatry 51 199 214 8122957 1:CAS:528:DyaK2cXkslemtrY%3D
34. E Lambe G Aghajanian 2003 Hypocretin (orexin) induces calcium transients in single spines postsynaptic to identified thalamocortical boutons in prefrontal slice Neuron 40 139 150 14527439 10.1016/S0896-6273(03)00598-1 1:CAS:528:DC%2BD3sXnvVygtr8%3D (Pubitemid 37222469)
35. EK Lambe GK Aghajanian 2006 Hallucinogen-induced UP states in the brain slice of rat prefrontal cortex: role of glutamate spillover and NR2B-NMDA receptors Neuropsychopharmacology 31 1682 1689 16292328 10.1038/sj.npp.1300944 1:CAS:528:DC%2BD28XmvFCntb8%3D (Pubitemid 44106699)
36. EK Lambe GK Aghajanian 2007 Prefrontal cortical network activity: opposite effects of psychedelic hallucinogens and D1/D5 dopamine receptor activation Neuroscience 145 900 910 17293055 10.1016/j.neuroscience.2006.12.048 1:CAS:528:DC%2BD2sXjsVGmt7o%3D (Pubitemid 46441657)
37. EK Lambe P Olausson NK Horst JR Taylor GK Aghajanian 2005 Hypocretin and nicotine excite the same thalamocortical synapses in prefrontal cortex: correlation with improved attention in rat J Neurosci 25 5225 5229 15917462 10.1523/JNEUROSCI.0719-05.2005 1:CAS:528:DC%2BD2MXkslyqsLc%3D (Pubitemid 40726974)
38. DJ Lang B Khorram VM Goghari LC Kopala RA Vandorpe Q Rui GN Smith WG Honer 2006 Reduced anterior internal capsule and thalamic volumes in first-episode psychosis Schizophr Res 87 89 99 16793239 10.1016/j.schres.2006. 05.002 1:STN:280:DC%2BD28rnvFanuw%3D%3D (Pubitemid 44428117)
39. DA Lewis DA Cruz DS Melchitzky JN Pierri 2001 Lamina-specific deficits in parvalbumin-immunoreactive varicosities in the prefrontal cortex of subjects with schizophrenia: evidence for fewer projections from the thalamus Am J Psychiatry 158 1411 1422 11532725 10.1176/appi.ajp.158.9.1411 1:STN:280:DC%2BD3MvovFKrsA%3D%3D (Pubitemid 32847239)
40. DA Lewis T Hashimoto DW Volk 2005 Cortical inhibitory neurons and schizophrenia Nat Rev Neurosci 6 312 24 15803162 10.1038/nrn1648 1:CAS:528:DC%2BD2MXivVarsbc%3D (Pubitemid 40469985)
41. DA Lewis RY Cho CS Carter K Eklund S Forster MA Kelly D Montrose 2008 Subunit-selective modulation of GABA type A receptor neurotransmission and cognition in schizophrenia Am J Psychiatry 165 1585 1593 18923067 10.1176/appi.ajp.2008.08030395
42. HJ Luhmann DA Prince 1990 Transient expression of polysynaptic NMDA receptor-mediated activity during neocortical development Neurosci Lett 111 109 115 1970856 10.1016/0304-3940(90)90353-B 1:CAS:528:DyaK3cXhvFanurY%3D
43. 2 and D2/3 receptor blockade enhances cortical glutamatergic transmission and reverses cognitive impairment in the rat Int J Neuropsychopharmacol 8 315 327 15857571 10.1017/S1461145705005328 1:CAS:528:DC%2BD2MXlsFams70%3D (Pubitemid 41002487)
44. 2A and group II metabotropic glutamate receptors in prefrontal cortex J Pharmacol Exp Ther 292 76 8 10604933 1:CAS:528:DC%2BD3cXhslGntQ%3D%3D
45. DA McCormick 2005 Neuronal networks: flip-flops in the brain Curr Biol 15 R294 R296 15854894 10.1016/j.cub.2005.04.009 1:CAS:528:DC%2BD2MXjsFKiurg%3D (Pubitemid 40599916)
46. DA McCormick Y Shu A Hasenstaub M Sanchez-Vives M Badoual T Bal 2003 Persistent cortical activity: mechanisms of generation and effects on neuronal excitability Cereb Cortex 13 1219 31 14576213 10.1093/cercor/bhg104 (Pubitemid 37322998)
47. RE Merchant MR Bullock CA Carmack AK Shah KD Wilner G Ko, et al. 1999 A double-blind, placebo-controlled study of the safety, tolerability and pharmacokinetics of CP-101, 606 in patients with a mild or moderate traumatic brain injury Ann NY Acad Sci 890 42 50 10668412 10.1111/j.1749-6632.1999. tb07979.x 1:CAS:528:DC%2BD3cXnsVGjsg%3D%3D
48. B Moghaddam BW Adams 1998 Reversal of phencyclidine effects by a group II metabotropic glutamate receptor agonist in rats Science 281 1349 1352 9721099 10.1126/science.281.5381.1349 1:CAS:528:DyaK1cXlvVentrw%3D
49. B Moghaddam B Adams A Verma D Daly 1997 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 2921 2927 9092613 1:CAS:528:DyaK2sXisValurk%3D
50. JW Muschamp MJ Regina EM Hull JC Winter RA Rabin 2004 Lysergic acid diethylamide and [ ]-2, 5-dimethoxy-4-methylamphetamine increase extracellular glutamate in rat prefrontal cortex Brain Res 1023 134 140 15364028 10.1016/j.brainres.2004.07.044 1:CAS:528:DC%2BD2cXnsFSrtbs%3D (Pubitemid 39195343)
51. ST Patil L Zhang F Martenyi SL Lowe KA Jackson BV Andreev AS Avedisova LM Bardenstein IY Gurovich MA Morozova SN Mosolov NG Neznanov AM Reznik AB Smulevich VA Tochilov BG Johnson JA Monn DD Schoepp 2007 Activation of mGlu2/3 receptors as a new approach to treat schizophrenia: a andomized Phase 2 clinical trial Nat Med 13 1102 1107 17767166 10.1038/nm1632 1:CAS:528:DC%2BD2sXhtVSgtrvF (Pubitemid 47517511)
52. CC Petersen TT Hahn M Mehta A Grinvald B Sakmann 2003 Interaction of sensory responses with spontaneous depolarization in layer 2/3 barrel cortex Proc Natl Acad Sci U S A 100 13638 13643 14595013 10.1073/pnas.2235811100 1:CAS:528:DC%2BD3sXptFOitbw%3D (Pubitemid 37444792)
53. CM Portas JM Goldstein ME Shenton HH Hokama CG Wible I Fischer R Kikinis R Donnino FA Jolesz RW McCarley 1998 Volumetric evaluation of the thalamus in schizophrenic male patients using magnetic resonance imaging Biol Psychiatry 43 649 659 9582998 10.1016/S0006-3223(97)00339-9 1:STN:280:DyaK1c3ktlyiuw%3D%3D (Pubitemid 28222385)
54. G Rajkowska JJ Miguel-Hidalgo Z Makkos H Meltzer J Overholser C Stockmeier 2002 Layer-specific reductions in GFAP-reactive astroglia in the dorsolateral prefrontal cortex in schizophrenia Schizophr Res 57 127 138 12223243 10.1016/S0920-9964(02)00339-0 (Pubitemid 35240014)
55. P Rigas MA Castro-Alamancos 2007 Thalamocortical UP states: differential effects of intrinsic and extrinsic cortical inputs on persistent activity J Neurosci 27 4261 4272 17442810 10.1523/JNEUROSCI.0003-07.2007 1:CAS:528:DC%2BD2sXkvFCjsbs%3D (Pubitemid 46640713)
56. LM Rorick-Kehn BG Johnson KM Knitowski CR Salhoff JM Witkin KW Perry KI Griffey JP Tizzano JA Monn DL McKinzie DD Schoepp 2007 In vivo pharmacological characterization of the structurally novel, potent, selective mGlu2/3 receptor agonist LY404039 in animal models of psychiatric disorders Psychopharmacology (Berl) 193 121 136 10.1007/s00213-007-0758-3 1:CAS:528:DC%2BD2sXmtlGktr8%3D (Pubitemid 46906627)
57. A receptor subtype functions Curr Opin Pharmacol 6 18 23 16376150 10.1016/j.coph.2005.10.003 1:CAS:528:DC%2BD28XmsVyhsA%3D%3D (Pubitemid 43103815)
58. A Schotte PFM Janssen W Gommeren WHML Luyten P VanGompel AS Lesage K DeLoore JE Leysen 1996 Risperiidone compared with new and reference antipsychotic drugs: in vitro and in vivo receptor binding Psychopharmacology (Berl) 124 57 73 10.1007/BF02245606 1:CAS:528:DyaK28XjsFGktLk%3D (Pubitemid 26112775)
59. JL Scruggs D Schmidt AY Deutch 2003 The hallucinogen 1-[2, 5-dimethoxy-4-iodophenyl]-2-aminopropane (DOI) increases cortical extracellular glutamate levels in rats Neurosci Lett 346 137 140 12853103 10.1016/S0304- 3940(03)00547-0 1:CAS:528:DC%2BD3sXltF2gtLY%3D (Pubitemid 36829280)
60. JK Seamans D Durstewitz BR Christie CF Stevens TJ Sejnowski 2001 Dopamine D1/D5 receptor modulation of excitatory synaptic inputs to layer V prefrontal cortex neurons Proc Natl Acad Sci U S A 98 301 6 11134516 10.1073/pnas.011518798 1:CAS:528:DC%2BD3MXkslOhtQ%3D%3D (Pubitemid 32095904)
61. Y Shu A Hasenstaub DA McCormick 2003 Turning on and off recurrent balanced cortical activity Nature 423 288 93 12748642 10.1038/nature01616 1:CAS:528:DC%2BD3sXjs1ynuro%3D (Pubitemid 40852698)
62. AK Stark HB Uylings E Sanz-Arigita B Pakkenberg 2004 Glial cell loss in the anterior cingulate cortex, a subregion of the prefrontal cortex, in subjects with schizophrenia Am J Psychiatry 161 882 888 15121654 10.1176/appi.ajp.161.5. 882 (Pubitemid 38625342)
63. S Vijayraghavan M Wang SG Birnbaum CJ Bruce GV Williams AFT Arnsten 2007 Inverted-U dopamine D1 receptor actions on prefrontal neurons engaged in working memory Nat Neurosci 10 376 384 17277774 10.1038/nn1846 1:CAS:528: DC%2BD2sXitVGku74%3D (Pubitemid 46310465)
64. G Winterer DR Weinberger 2004 Genes, dopamine and cortical signal-to-noise ratio in schizophrenia Trends Neurosci 27 683 690 15474169 10.1016/j.tins.2004.08.002 1:CAS:528:DC%2BD2cXotlajsbo%3D (Pubitemid 39335839)
65. ML Woolley DJ Pemberton S Bate C Corti DNC Jones 2008 The mGlu2 but not the mGlu3 receptor mediates the actions of the mGluR2/3 agonist, LY379268, in mouse models predictive of antipsychotic activity Psychopharmacology (Berl) 196 431 440 10.1007/s00213-007-0974-x 1:CAS:528:DC%2BD1cXht1KnsLo%3D
66. A receptors in hippocampal neurons are high-affinity, low-conductance sensors for extracellular GABA Mol Pharmacol 63 2 8 12488530 10.1124/mol.63.1.2 1:CAS:528:DC%2BD3sXjsVGn (Pubitemid 36043802)
67. J Zahrt JR Taylor RG Mathew AF Arnsten 1997 Supranormal stimulation of D1 dopamine receptors in the rodent prefrontal cortex impairs spatial working memory performance J Neurosci 17 8528 35 9334425 1:CAS:528:DyaK2sXntVyju7s%3D