Modulation of pyramidal cell output in the medial prefrontal cortex by mGluR5 interacting with CB1

Neuropharmacology

Volumn 66, Issue , 2013, Pages 170-178

  Kiritoshi, Takaki ^a   Sun, Hao ^a   Ren, Wenjie ^a   Stauffer, Shaun R ^b   Lindsley, Craig W ^b   Conn, P Jeffrey ^b   Neugebauer, Volker ^a  

^a University of Texas Medical Branch School of Medicine   (United States)

^b VANDERBILT UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

CB1; mGluR5; PAM; Positive allosteric modulator; Prefrontal cortex; Synaptic transmission

Indexed keywords

1 (2,4 DICHLOROPHENYL) 5 (4 IODOPHENYL) 4 METHYL N MORPHOLINO 1H PYRAZOLE 3 CARBOXAMIDE; 2 CHLORO 5 HYDROXYPHENYLGLYCINE; 3 [(2 METHYL 4 THIAZOLYL)ETHYNYL]PYRIDINE; CANNABINOID 1 RECEPTOR; METABOTROPIC RECEPTOR 5; N CYCLOBUTYL 6 [(3 FLUOROPHENYL)ETHYNYL]NICOTINAMIDE; NICOTINAMIDE; UNCLASSIFIED DRUG;

AMPLITUDE MODULATION; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BRAIN REGION; BRAIN SLICE; CONTROLLED STUDY; EVOKED RESPONSE; EXCITATORY POSTSYNAPTIC POTENTIAL; INHIBITORY POSTSYNAPTIC POTENTIAL; MALE; MOLECULAR DYNAMICS; NERVE CELL EXCITABILITY; NONHUMAN; PATCH CLAMP; PREFRONTAL CORTEX; PRIORITY JOURNAL; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; PYRAMIDAL NERVE CELL; RAT; SIGNAL TRANSDUCTION; SPIKE WAVE; SYNAPTIC TRANSMISSION; VOLTAGE CLAMP;

ANIMALS; ARACHIDONIC ACIDS; CANNABINOID RECEPTOR AGONISTS; CANNABINOID RECEPTOR ANTAGONISTS; EXCITATORY AMINO ACID AGONISTS; EXCITATORY AMINO ACID ANTAGONISTS; EXCITATORY POSTSYNAPTIC POTENTIALS; GLYCINE; INHIBITORY POSTSYNAPTIC POTENTIALS; MALE; MORPHOLINES; NEURAL INHIBITION; NIACINAMIDE; PHENYLACETATES; PREFRONTAL CORTEX; PYRAMIDAL CELLS; PYRAZOLES; PYRIDINES; RATS; RATS, SPRAGUE-DAWLEY; RECEPTOR, CANNABINOID, CB1; RECEPTORS, METABOTROPIC GLUTAMATE; SYNAPTIC TRANSMISSION; THIAZOLES;

EID: 84872153471     PISSN: 00283908     EISSN: 18737064     Source Type: Journal    
DOI: 10.1016/j.neuropharm.2012.03.024     Document Type: Article

References (95)

1. I. Akirav, and M. Maroun The role of the medial prefrontal cortex-Amygdala circuit in stress effects on the extinction of fear Neural Plast. 2007 2007 30873
2. S. Alagarsamy, M.J. Marino, S.T. Rouse, R.W. 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
3. A.V. Apkarian, M.N. Baliki, and P.Y. Geha Towards a theory of chronic pain Prog. Neurobiol. 87 2009 81 97
4. A.V. Apkarian, Y. Sosa, B.R. Krauss, P.S. Thomas, B.E. Fredrickson, R.E. Levy, R.N. Harden, and D.R. Chialvo Chronic pain patients are impaired on an emotional decision-making task Pain 108 2004 129 136
5. J.E. Ayala, Y. Chen, J.L. Banko, D.J. Sheffler, R. Williams, A.N. Telk, N.L. Watson, Z. Xiang, Y. Zhang, P.J. Jones, C.W. Lindsley, M.F. Olive, and P.J. Conn mGluR5 positive allosteric modulators facilitate both hippocampal LTP and LTD and enhance spatial learning Neuropsychopharmacology 34 2009 2057 2071
6. C.L. Baker, and J.J. McDougall The cannabinomimetic arachidonyl-2- chloroethylamide (ACEA) acts on capsaicin-sensitive TRPV1 receptors but not cannabinoid receptors in rat joints Br. J. Pharmacol. 142 2004 1361 1367
7. D.E. Berman, and Y. Dudai Memory extinction, learning anew, and learning the new: dissociations in the molecular machinery of learning in cortex Science 291 2001 2417 2419
8. C.R. Bowie, and P.D. Harvey Cognitive deficits and functional outcome in schizophrenia Neuropsychiatr. Dis. Treat. 2 2006 531 536
9. J.P. Burke, and J.J. Hablitz Presynaptic depression of synaptic transmission mediated by activation of metabotropic glutamate receptors in rat neocortex J. Neurosci. 14 1994 5120 5130
10. J.P. Burke, and J.J. Hablitz G-protein activation by metabotropic glutamate receptors reduces spike frequency adaptation in neocortical neurons Neuroscience 75 1996 123 131
11. P.C. Casarotto, A.L. Terzian, D.C. Aguiar, H. Zangrossi, F.S. Guimaraes, C.T. Wotjak, and F.A. Moreira Opposing roles for cannabinoid receptor type-1 (CB) and transient receptor potential vanilloid type-1 channel (TRPV1) on the modulation of panic-like responses in rats Neuropsychopharmacology 37 2012 478 486
12. B. Cauli, J.T. Porter, K. Tsuzuki, B. Lambolez, J. Rossier, B. Quenet, and E. Audinat Classification of fusiform neocortical interneurons based on unsupervised clustering Proc. Natl. Acad. Sci. Unit. Stat. Am. 97 2000 6144 6149
13. C.H. Chang, J.D. Berke, and S. Maren Single-unit activity in the medial prefrontal cortex during immediate and delayed extinction of fear in rats PLoS One 5 2010 e11971
14. C.H. Chang, and S. Maren Strain difference in the effect of infralimbic cortex lesions on fear extinction in rats Behav. Neurosci. 124 2010 391 397
15. Z. Chu, and J.J. Hablitz Activation of group I mGluRs increases spontaneous IPSC frequency in rat frontal cortex J. Neurophysiol. 80 1998 621 627
16. Y. Chudasama Animal models of prefrontal-executive function Behav. Neurosci. 125 2011 327 343
17. H.F. Clarke, J.W. Dalley, H.S. Crofts, T.W. Robbins, and A.C. Roberts Cognitive inflexibility after prefrontal serotonin depletion Science 304 2004 878 880
18. R.M. Cleva, and M.F. Olive Positive allosteric modulators of type 5 metabotropic glutamate receptors (mGluR5) and their therapeutic potential for the treatment of CNS disorders Molecules 16 2011 2097 2106
19. J.W. Dalley, B.J. Everitt, and T.W. Robbins Impulsivity, compulsivity, and top-down cognitive control Neuron 69 2011 680 694
20. V. Di Marzo Anandamide serves two masters in the brain Nat. Neurosci. 13 2010 1446 1448
21. V. Di Marzo Endocannabinoid signaling in the brain: biosynthetic mechanisms in the limelight Nat. Neurosci. 14 2011 9 15
22. A.J. Doherty, M.J. Palmer, J.M. Henley, G.L. Collingridge, and D.E. Jane (RS)-2-chloro-5-hydroxyphenylglycine (CHPG) activates mGlu5, but no mGlu1, receptors expressed in CHO cells and potentiates NMDA responses in the hippocampus Neuropharmacology 36 1997 265 267
23. D.E. Fontanez-Nuin, E. Santini, G.J. Quirk, and J.T. Porter Memory for fear extinction requires mGluR5-mediated activation of infralimbic neurons Cereb. Cortex 21 2011 727 735
24. V. Galhardo, and M. Pais-Vieira Decision-making cognitive deficits in a rat model of chronic pain Soc. Neurosci. Abstr 35 2005 Ref Type: Abstract: 50.3
25. R.W. Gereau, and S.F. Heinemann Role of protein kinase C phosphorylation in rapid desensitization of metabotropic glutamate receptor 5 Neuron 20 1998 143 151 Ref Type: Journal (Full)
26. C. Giordano, L. Cristino, L. Luongo, D. Siniscalco, S. Petrosino, F. Piscitelli, I. Marabese, L. Gatta, F. Rossi, R. Imperatore, E. Palazzo, N. de, V. de Novellis, V. Di Marzo, and S. Maione TRPV1-dependent and -independent alterations in the limbic cortex of neuropathic MICE: impact on glial caspases and pain perception Cereb. Cortex 2011
27. Y. Goto, C.R. Yang, and S. Otani Functional and dysfunctional synaptic plasticity in prefrontal cortex: roles in psychiatric disorders Biol. Psychiatry 67 2010 199 207
28. K.J. Gregory, E.N. Dong, J. Meiler, and P.J. Conn Allosteric modulation of metabotropic glutamate receptors: structural insights and therapeutic potential Neuropharmacology 60 2011 66 81
29. B.M. Gu, J.Y. Park, D.H. Kang, S.J. Lee, S.Y. Yoo, H.J. Jo, C.H. Choi, J.M. Lee, and J.S. Kwon Neural correlates of cognitive inflexibility during task-switching in obsessive-compulsive disorder Brain 131 2008 155 164
30. A.S. Hammond, A.L. Rodriguez, S.D. Townsend, C.M. Niswender, K.J. Gregory, C.W. Lindsley, and P.J. Conn Discovery of a novel chemical class of mGlu(5) allosteric ligands with distinct modes of pharmacology ACS Chem. Neurosci. 1 2010 702 716
31. C.A. Hartley, and E.A. Phelps Changing fear: the neurocircuitry of emotion regulation Neuropsychopharmacology 35 2010 136 146
32. K. Hefner, N. Whittle, J. Juhasz, M. Norcross, R.M. Karlsson, L.M. Saksida, T.J. Bussey, N. Singewald, and A. Holmes Impaired fear extinction learning and cortico-Amygdala circuit abnormalities in a common genetic mouse strain J. Neurosci. 28 2008 8074 8085
33. C. Herry, F. Ferraguti, N. Singewald, J.J. Letzkus, I. Ehrlich, and A. Luthi Neuronal circuits of fear extinction Eur. J. Neurosci. 31 2010 599 612
34. C.J. Hillard, S. Manna, M.J. Greenberg, R. DiCamelli, R.A. Ross, L.A. Stevenson, V. Murphy, R.G. Pertwee, and W.B. Campbell Synthesis and characterization of potent and selective agonists of the neuronal cannabinoid receptor (CB1) J. Pharmacol. Exp. Ther 289 1999 1427 1433
35. H. Homayoun, and B. Moghaddam Bursting of prefrontal cortex neurons in awake rats is regulated by metabotropic glutamate 5 (mGlu5) receptors: rate-dependent influence and interaction with NMDA receptors Cereb. Cortex 16 2006 93 105
36. H. Homayoun, and B. Moghaddam Group 5 metabotropic glutamate receptors: role in modulating cortical activity and relevance to cognition Eur. J. Pharmacol. 639 2010 33 39
37. Y. Izumi, and C.F. Zorumski NMDA receptors, mGluR5, and endocannabinoids are involved in a cascade leading to hippocampal long-term depression Neuropsychopharmacology 2011
38. G. Ji, and V. Neugebauer Pain-related deactivation of medial prefrontal cortical neurons involves mGluR1 and GABAA receptors J. Neurophysiol. 106 2011 2642 2652
39. G. Ji, H. Sun, Y. Fu, Z. Li, M. Pais-Vieira, V. Galhardo, and V. Neugebauer Cognitive impairment in pain through amygdala-driven prefrontal cortical deactivation J. Neurosci. 30 2010 5451 5464
40. M. Kano, T. Ohno-Shosaku, Y. Hashimotodani, M. Uchigashima, and M. Watanabe Endocannabinoid-mediated control of synaptic transmission Physiol. Rev. 89 2009 309 380
41. J.H. Kim, and R. Richardson New findings on extinction of conditioned fear early in development: theoretical and clinical implications Biol. Psychiatry 67 2010 297 303
42. S.C. Kim, Y.S. Jo, I.H. Kim, H. Kim, and J.S. Choi Lack of medial prefrontal cortex activation underlies the immediate extinction deficit J. Neurosci. 30 2010 832 837
43. E. Knapska, and S. Maren Reciprocal patterns of c-Fos expression in the medial prefrontal cortex and amygdala after extinction and renewal of conditioned fear Learn. Mem. 16 2009 486 493
44. M. Lafourcade, I. Elezgarai, S. Mato, Y. Bakiri, P. Grandes, and O.J. Manzoni Molecular components and functions of the endocannabinoid system in mouse prefrontal cortex PLoS One 2 2007 e709
45. R. Lan, J. Gatley, Q. Lu, P. Fan, S.R. Fernando, N.D. Volkow, R. Pertwee, and A. Makriyannis Design and synthesis of the CB1 selective cannabinoid antagonist AM281: a potential human SPECT ligand AAPS. PharmSci. 1 1999 1 7
46. P.M. Lea, and A.I. Faden Metabotropic glutamate receptor subtype 5 antagonists MPEP and MTEP CNS. Drug Rev. 12 2006 149 166
47. L. Lecourtier, H. Homayoun, G. Tamagnan, and B. Moghaddam Positive allosteric modulation of metabotropic glutamate 5 (mGlu5) receptors reverses N-methyl-d-Aspartate antagonist-induced alteration of neuronal firing in prefrontal cortex Biol. Psychiatry 62 2007 739 746
48. A. Lesage, and T. Steckler Metabotropic glutamate mGlu1 receptor stimulation and blockade: therapeutic opportunities in psychiatric illness Eur. J. Pharmacol. 639 2010 2 16
49. W. Li, and V. Neugebauer Differential roles of mGluR1 and mGluR5 in brief and prolonged nociceptive processing in central amygdala neurons J. Neurophysiol. 91 2004 13 24
50. Z. Li, G. Ji, and V. Neugebauer Mitochondrial reactive oxygen species are activated by mGluR5 through IP3 and activate ERK and PKA to increase excitability of amygdala neurons and pain behavior J. Neurosci. 31 2011 1114 1127
51. E. Likhtik, J.G. Pelletier, R. Paz, and D. Pare Prefrontal control of the amygdala J. Neurosci. 25 2005 7429 7437
52. H.C. Lin, S.C. Mao, C.L. Su, and P.W. Gean The role of prefrontal cortex CB1 receptors in the modulation of fear memory Cereb. Cortex 19 2009 165 175
53. D.M. Lovinger Presynaptic modulation by endocannabinoids Handbook Exp. Pharmacol. 2008 435 477
54. B. Lutz Endocannabinoid signals in the control of emotion Curr. Opin. Pharmacol. 9 2009 46 52
55. G.J. Marek, and C. Zhang Activation of metabotropic glutamate 5 (mGlu5) receptors induces spontaneous excitatory synaptic currents in layer V pyramidal cells of the rat prefrontal cortex Neurosci. Lett. 442 2008 239 243
56. S. Maren, and G.J. Quirk Neuronal signalling of fear memory Nat. Rev. Neurosci. 5 2004 844 852
57. G. Marsicano, and B. Lutz Expression of the cannabinoid receptor CB1 in distinct neuronal subpopulations in the adult mouse forebrain Eur. J. Neurosci. 11 1999 4213 4225
58. G. Marsicano, C.T. Wotjak, S.C. Azad, T. Bisogno, G. Rammes, M.G. Cascio, H. Hermann, J. Tang, C. Hofmann, W. Zieglgansberger, M. Di, V. Di Marzo, and B. Lutz The endogenous cannabinoid system controls extinction of aversive memories Nature 418 2002 530 534
59. E.A. Mayer, S. Berman, B. Suyenobu, J. Labus, M.A. Mandelkern, B.D. Naliboff, and L. Chang Differences in brain responses to visceral pain between patients with irritable bowel syndrome and ulcerative colitis Pain 115 2005 398 409
60. B.J. Melancon, C.R. Hopkins, M.R. Wood, K.A. Emmitte, C.M. Niswender, A. Christopoulos, P.J. Conn, and C.W. Lindsley Allosteric modulation of seven transmembrane spanning receptors: theory, practice, and opportunities for central nervous system drug discovery J. Med. Chem 2012
61. R.I. Melendez, J. Vuthiganon, and P.W. Kalivas Regulation of extracellular glutamate in the prefrontal cortex: focus on the cystine glutamate exchanger and group I metabotropic glutamate receptors J. Pharmacol. Exp. Ther. 314 2005 139 147
62. A.E. Metz, H.J. Yau, M.V. Centeno, A.V. Apkarian, and M. Martina Morphological and functional reorganization of rat medial prefrontal cortex in neuropathic pain Proc. Natl. Acad. Sci. Unit. Stat. Am. 2009
63. G.A. Mickley, Z. Hoxha, S. Bacik, C.L. Kenmuir, J.A. Wellman, J.M. Biada, and A. Disorbo Spontaneous recovery of a conditioned taste aversion differentially alters extinction-induced changes in c-Fos protein expression in rat amygdala and neocortex Brain Res. 1152 2007 139 157
64. G.A. Mickley, C.L. Kenmuir, A.M. Yocom, J.A. Wellman, and J.M. Biada A role for prefrontal cortex in the extinction of a conditioned taste aversion Brain Res. 1051 2005 176 182
65. R. Mueller, A.L. Rodriguez, E.S. Dawson, M. Butkiewicz, T.T. Nguyen, S. Oleszkiewicz, A. Bleckmann, C.D. Weaver, C.W. Lindsley, P.J. Conn, and J. Meiler Identification of metabotropic glutamate receptor subtype 5 potentiators using virtual high-throughput screening ACS Chem. Neurosci. 1 2010 288 305
66. E.C. Muly, M. Maddox, and Y. Smith Distribution of mGluR1alpha and mGluR5 immunolabeling in primate prefrontal cortex J. Comp. Neurol. 467 2003 521 535
67. K.M. Myers, and M. Davis Mechanisms of fear extinction Mol. Psychiatry 12 2007 120 150
68. V. Neugebauer, V. Galhardo, S. Maione, and S.C. Mackey Forebrain pain mechanisms Brain Res. Rev. 60 2009 226 242
69. V. Neugebauer, W. Li, G.C. Bird, G. Bhave, and R.W. Gereau Synaptic plasticity in the amygdala in a model of arthritic pain: differential roles of metabotropic glutamate receptors 1 and 5 J. Neurosci. 23 2003 52 63 Ref Type: Journal (Full)
70. F. Nicoletti, J. Bockaert, G.L. Collingridge, P.J. Conn, F. Ferraguti, D.D. Schoepp, J.T. Wroblewski, and J.P. Pin Metabotropic glutamate receptors: from the workbench to the bedside Neuropharmacology 60 2011 1017 1041
71. C.M. Niswender, and P.J. Conn Metabotropic glutamate receptors: physiology, pharmacology, and disease Annu. Rev. Pharmacol. Toxicol. 50 2010 295 322
72. M.J. Noetzel, J.M. Rook, P.N. Vinson, H. Cho, E. Days, Y. Zhou, A.L. Rodriguez, H. Lavreysen, S.R. Stauffer, C.M. Niswender, Z. Xiang, J.S. Daniels, C.K. Jones, C.W. Lindsley, C.D. Weaver, and P.J. Conn Functional impact of allosteric agonist activity of selective positive allosteric modulators of mGlu5 in regulating CNS function Mol. Pharmacol 2011
73. K.N. Ochsner, and J.J. Gross The cognitive control of emotion Trends Cogn. Sci. 9 2005 242 249
74. Z.Z. Pan, J.T. Williams, and P.B. Osborne Opioid actions on single nucleus raphe magnus neurons from rat and guinea-pig in vitro J. Physiol. 427 1990 519 532
75. H.C. Pape, and D. Pare Plastic synaptic networks of the amygdala for the acquisition, expression, and extinction of conditioned fear Physiol. Rev. 90 2010 419 463
76. R.G. Pertwee Receptors and channels targeted by synthetic cannabinoid receptor agonists and antagonists Curr. Med. Chem. 17 2010 1360 1381
77. G.J. Quirk, and J.S. Beer Prefrontal involvement in the regulation of emotion: convergence of rat and human studies Curr. Opin. Neurobiol. 16 2006 723 727
78. G.J. Quirk, D. Pare, R. Richardson, C. Herry, M.H. Monfils, D. Schiller, and A. Vicentic Erasing fear memories with extinction training J. Neurosci. 30 2010 14993 14997
79. W. Ren, and V. Neugebauer Pain-related increase of excitatory transmission and decrease of inhibitory transmission in the central nucleus of the amygdala are mediated by mGluR1 Mol. Pain 6 2010 93 107
80. A.L. Rodriguez, M.D. Grier, C.K. Jones, E.J. Herman, A.S. Kane, R.L. Smith, R. Williams, Y. Zhou, J.E. Marlo, E.L. Days, T.N. Blatt, S. Jadhav, U.N. Menon, P.N. Vinson, J.M. Rook, S.R. Stauffer, C.M. Niswender, C.W. Lindsley, C.D. Weaver, and P.J. Conn Discovery of novel allosteric modulators of metabotropic glutamate receptor subtype 5 reveals chemical and functional diversity and in vivo activity in rat behavioral models of anxiolytic and antipsychotic activity Mol. Pharmacol 2010
81. C. Romano, M.A. Sesma, C.T. McDonald, K. O'Malley, A.N. van den Pol, and J.W. Olney Distribution of metabotropic glutamate receptor mGluR5 immunoreactivity in rat brain J. Comp. Neurol 355 1995 455 469 Ref Type: Journal (Full)
82. T. Rubino, N. Realini, C. Castiglioni, C. Guidali, D. Vigano, E. Marras, S. Petrosino, G. Perletti, M. Maccarrone, V. Di Marzo, and D. Parolaro Role in anxiety behavior of the endocannabinoid system in the prefrontal cortex Cereb. Cortex 18 2008 1292 1301
83. N.B. Ruparel, A.M. Patwardhan, A.N. Akopian, and K.M. Hargreaves Desensitization of transient receptor potential ankyrin 1 (TRPA1) by the TRP vanilloid 1-selective cannabinoid arachidonoyl-2 chloroethanolamine Mol. Pharmacol. 80 2011 117 123
84. P. Sah, and R.F. Westbrook Behavioural neuroscience: the circuit of fear Nature 454 2008 589 590
85. D.D. Schoepp, D.E. Jane, and J.A. Monn Pharmacological agents acting at subtypes of metabotropic glutamate receptors Neuropharmacology 38 1999 1431 1476
86. G. Segovia, and F. Mora Effects of the metabotropic glutamate receptor agonist, ACPD, on the extracellular concentrations of GABA and acetylcholine in the prefrontal cortex of the rat during the normal process of aging Brain Res. Bull. 65 2005 11 16
87. A. Sheinin, G. Talani, M.I. Davis, and D.M. Lovinger Endocannabinoid- and mGluR5-dependent short-term synaptic depression in an isolated neuron/bouton preparation from the hippocampal CA1 region J. Neurophysiol. 100 2008 1041 1052
88. D. Sierra-Mercado, N. Padilla-Coreano, and G.J. Quirk Dissociable roles of prelimbic and infralimbic cortices, ventral hippocampus, and basolateral amygdala in the expression and extinction of conditioned fear Neuropsychopharmacology 36 2011 529 538
89. F. Sotres-Bayon, and G.J. Quirk Prefrontal control of fear: more than just extinction Curr. Opin. Neurobiol. 20 2010 231 235
90. T.A. Stalnaker, Y. Takahashi, M.R. Roesch, and G. Schoenbaum Neural substrates of cognitive inflexibility after chronic cocaine exposure Neuropharmacology 56 Suppl 1 2009 63 72
91. H. Sun, and V. Neugebauer mGluR1, but not mGluR5, activates feed-forward inhibition in the medial prefrontal cortex to impair decision making J. Neurophysiol. 106 2011 960 973
92. P.N. Vinson, and P.J. Conn Metabotropic glutamate receptors as therapeutic targets for schizophrenia Neuropharmacology 2011
93. K. Wedzony, and A. Chocyk Cannabinoid CB1 receptors in rat medial prefrontal cortex are colocalized with calbindin- but not parvalbumin- and calretinin-positive GABA-ergic neurons Pharmacol. Rep. 61 2009 1000 1007
94. J. Xu, Y. Zhu, A. Contractor, and S.F. Heinemann mGluR5 has a critical role in inhibitory learning J. Neurosci. 29 2009 3676 3684
95. F.M. Zhou, and J.J. Hablitz Metabotropic glutamate receptor enhancement of spontaneous IPSCs in neocortical interneurons J. Neurophysiol. 78 1997 2287 2295 Ref Type: Journal (Full)