Positive allosteric modulation reveals a specific role for mGlu2 receptors in sensory processing in the thalamus

Journal of Physiology

Volumn 590, Issue 4, 2012, Pages 937-951

  Copeland, C S ^a   Neale, S A ^a   Salt, T E ^a  

^a UNIVERSITY COLLEGE LONDON   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

EGLUMETAD; LY 487379; METABOTROPIC RECEPTOR 2; METABOTROPIC RECEPTOR 3; METABOTROPIC RECEPTOR AGONIST; UNCLASSIFIED DRUG;

ALLOSTERISM; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DISEASE CONTROL; EVOKED CORTICAL RESPONSE; EVOKED SOMATOSENSORY RESPONSE; GABAERGIC TRANSMISSION; IN VIVO STUDY; MALE; NEUROMODULATION; NEUROTRANSMISSION; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; RAT; RECEPTOR BLOCKING; SENSORIMOTOR FUNCTION; SENSORY NERVE; SENSORY STIMULATION; SIGNAL TRANSDUCTION; SYNAPTIC POTENTIAL; THALAMUS; THALAMUS RETICULAR NUCLEUS; THALAMUS VENTRAL NUCLEUS;

ANIMALS; BICYCLO COMPOUNDS; EXCITATORY AMINO ACID AGONISTS; MALE; PHYSICAL STIMULATION; PYRIDINES; RATS; RATS, WISTAR; RECEPTORS, METABOTROPIC GLUTAMATE; SENSATION; SENSORY RECEPTOR CELLS; SULFONAMIDES; THALAMUS; VIBRISSAE;

EID: 84856876311     PISSN: 00223751     EISSN: 14697793     Source Type: Journal    
DOI: 10.1113/jphysiol.2011.218065     Document Type: Article

References (75)

1. Alexander GM & Godwin DW (2005). Presynaptic inhibition of corticothalamic feedback by metabotropic glutamate receptors. J Neurophysiol 94, 163-175.
2. Alexander GM & Godwin DW (2006). Unique presynaptic and postsynaptic roles of Group II metabotropic glutamate receptors in the modulation of thalamic network activity. Neuroscience 141, 501-513.
3. Arnth-Jensen N, Jabaudon D & Scanziani M (2002). Cooperation between independent hippocampal synapses is controlled by glutamate uptake. Nat Neurosci 5, 325-331.
4. Baker DA, Madayag A, Kristiansen LV, Meador-Woodruff JH, Haroutunian V & Raju I (2008). Contribution of cystine-glutamate antiporters to the psychotomimetic effects of phencyclidine. Neuropsychopharmacology 33, 1760-1772.
5. Barbaresi P, Spreafico R, Frassoni C & Rustioni A (1986). GABAergic neurons are present in the dorsal column nuclei but not in the ventroposterior complex of rats. Brain Res 382, 305-326.
6. Binns KE, Turner JP & Salt TE (2003). Kainate receptor (GluR5)-mediated disinhibition of responses in rat ventrobasal thalamus allows a novel sensory processing mechanism. J Physiol 551, 525-537.
7. Brecht M & Sakmann B (2002). Whisker maps of neuronal subclasses of the rat ventral posterior medial thalamus, identified by whole-cell voltage recording and morphological reconstruction. J Physiol 538, 495-515.
8. Chen CY & Bonham AC (2005). Glutamate suppresses GABA release via presynaptic metabotropic glutamate receptors at baroreceptor neurones in rats. J Physiol 562, 535-551.
9. Christopoulos A (2002). Allosteric binding sites on cell-surface receptors: novel targets for drug discovery. Nat Rev Drug Discov 1, 198-210.
10. Cirone J, Pothecary CA, Turner JP & Salt TE (2002). Group I metabotropic glutamate receptors (mGluRs) modulate visual responses in the superficial superior colliculus of the rat. J Physiol 541, 895-903.
11. Conn PJ & Pin JP (1997). Pharmacology and functions of metabotropic glutamate receptors. Annu Rev Pharmacol Toxicol 37, 205-237.
12. Crabtree JW (1999). Intrathalamic sensory connections mediated by the thalamic reticular nucleus. Cell Mol Life Sci 56, 683-700.
13. Crick F (1984). Function of the thalamic reticular complex: the searchlight hypothesis. Proc Natl Acad Sci U S A 81, 4586-4590.
14. Diamond ME, Armstrong-James M, Budway MJ & Ebner FF (1992). Somatic sensory responses in the rostral sector of the posterior group (POm) and in the ventral posterior medial nucleus (VPM) of the rat thalamus: dependence on the barrel field cortex. J Comp Neurol 319, 66-84.
15. Drummond GB (2009). Reporting ethical matters in The Journal of Physiology: standards and advice. J Physiol 587, 713-719.
16. Ehlert FJ (1986). 'Inverse agonists', cooperativity and drug action at benzodiazepine receptors. Trends Pharmacol Sci 7, 28-32.
17. Fitzsimonds RM & Dichter MA (1996). Heterologous modulation of inhibitory synaptic transmission by metabotropic glutamate receptors in cultured hippocampal neurons. J Neurophysiol 75, 885-893.
18. Flor PJ, Battaglia G, Nicoletti F, Gasparini F & Bruno V (2002). Neuroprotective activity of metabotropic glutamate receptor ligands. Adv Exp Med Biol 513, 197-223.
19. Galici R, Echemendia NG, Rodriguez AL & Conn PJ (2005). A selective allosteric potentiator of metabotropic glutamate (mGlu) 2 receptors has effects similar to an orthosteric mGlu2/3 receptor agonist in mouse models predictive of antipsychotic activity. J Pharmacol Exp Ther 315, 1181-1187.
20. Harich S, Gross G & Bespalov A (2007). Stimulation of the metabotropic glutamate 2/3 receptor attenuates social novelty discrimination deficits induced by neonatal phencyclidine treatment. Psychopharmacology (Berl) 192, 511-519.
21. Harris RM (1986). Morphology of physiologically identified thalamocortical relay neurons in the rat ventrobasal thalamus. J Comp Neurol 251, 491-505.
22. Harris RM & Hendrickson AE (1987). Local circuit neurons in the rat ventrobasal thalamus - a GABA immunocytochemical study. Neuroscience 21, 229-236.
23. Hartings JA & Simons DJ (2000). Inhibition suppresses transmission of tonic vibrissa-evoked activity in the rat ventrobasal thalamus. J Neurosci 20, RC100.
24. Hermes ML & Renaud LP (2010). Post- and presynaptic group II metabotropic glutamate receptors reduce neuronal excitability in rat midline paraventricular thalamic nucleus. J Pharmacol Exp Ther 336, 840-849.
25. Ito M (1988). Response properties and topography of vibrissa-sensitive VPM neurons in the rat. J Neurophysiol 60, 1181-1197.
26. Javitt DC (2009). Sensory processing in schizophrenia: neither simple nor intact. Schizophr Bull 35, 1059-1064.
27. Johnson MP, Baez M, Jagdmann GE Jr, Britton TC, Large TH, Callagaro DO, Tizzano JP, Monn JA & Schoepp DD (2003). Discovery of allosteric potentiators for the metabotropic glutamate 2 receptor: synthesis and subtype selectivity of N-(4-(2-methoxyphenoxy)phenyl)-N-(2, 2, 2- trifluoroethylsulfonyl)pyrid-3-ylmethylamine. J Med Chem 46, 3189-3192.
28. Jones EG (1985). The Thalamus. Raven, New York
29. Kingston AE, Ornstein PL, Wright RA, Johnson BG, Mayne NG, Burnett JP, Belagaje R, Wu S & Schoepp DD (1998). LY341495 is a nanomolar potent and selective antagonist of group II metabotropic glutamate receptors. Neuropharmacology 37, 1-12.
30. Lavallee P & Deschenes M (2004). Dendroarchitecture and lateral inhibition in thalamic barreloids. J Neurosci 24, 6098-6105.
31. B receptor antagonists on responses of VPM neurons. J Neurophysiol 71, 1716-1726.
32. Linden AM, Bergeron M & Schoepp DD (2005). Comparison of c-Fos induction in the brain by the mGlu2/3 receptor antagonist LY341495 and agonist LY354740: evidence for widespread endogenous tone at brain mGlu2/3 receptors in vivo. Neuropharmacology 49(Suppl 1), 120-134.
33. Liu XB, Munoz A & Jones EG (1998). Changes in subcellular localization of metabotropic glutamate receptor subtypes during postnatal development of mouse thalamus. J Comp Neurol 395, 450-465.
34. Mineff E & Valtschanoff J (1999). Metabotropic glutamate receptors 2 and 3 expressed by astrocytes in rat ventrobasal thalamus. Neurosci Lett 270, 95-98.
35. Mitchell SJ & Silver RA (2000). Glutamate spillover suppresses inhibition by activating presynaptic mGluRs. Nature 404, 498-502.
36. Moldrich RX, Chapman AG, De Sarro G & Meldrum BS (2003). Glutamate metabotropic receptors as targets for drug therapy in epilepsy. Eur J Pharmacol 476, 3-16.
37. Moran MM, Melendez R, Baker D, Kalivas PW & Seamans JK (2003). Cystine/glutamate antiporter regulation of vesicular glutamate release. Ann N Y Acad Sci 1003, 445-447.
38. Nakanishi S (1992). Molecular diversity of glutamate receptors and implications for brain function. Science 258, 597-603.
39. Neale SA & Salt TE (2006). Modulation of GABAergic inhibition in the rat superior colliculus by a presynaptic group II metabotropic glutamate receptor. J Physiol 577, 659-669.
40. Nicolelis MA & Chapin JK (1994). Spatiotemporal structure of somatosensory responses of many-neuron ensembles in the rat ventral posterior medial nucleus of the thalamus. J Neurosci 14, 3511-3532.
41. Nikiforuk A, Popik P, Drescher KU, van Gaalen MM, Relo AL, Mezler M, Marek G, Schoemaker H, Gross G & Bespalov A (2010). Effects of a positive allosteric modulator of mGlu2 receptors LY487379 on cognitive flexibility and impulsive-like responding in rats. J Pharmacol Exp Ther 335, 665-673.
42. Niswender CM & Conn PJ (2010). Metabotropic glutamate receptors: physiology, pharmacology, and disease. Annu Rev Pharmacol Toxicol 50, 295-322.
43. Nordquist RE, Steckler T, Wettstein JG, Mackie C & Spooren W (2008). Metabotropic glutamate receptor modulation, translational methods, and biomarkers: relationships with anxiety. Psychopharmacology (Berl) 199, 389-402.
44. Ohara PT & Havton LA (1994). Preserved features of thalamocortical projection neuron dendritic architecture in the somatosensory thalamus of the rat, cat and macaque. Brain Res 648, 259-264.
45. Ohara PT & Lieberman AR (1993). Some aspects of the synaptic circuitry underlying inhibition in the ventrobasal thalamus. J Neurocytol 22, 815-825.
46. Ohishi H, Ogawa-Meguro R, Shigemoto R, Kaneko T, Nakanishi S & Mizuno N (1994). Immunohistochemical localization of metabotropic glutamate receptors, mGluR2 and mGluR3, in rat cerebellar cortex. Neuron 13, 55-66.
47. Paxinos G & Watson C (1998). The Rat Brain in Stereotaxic Co-ordinates. Academic Press, San Diego, CA
48. Peschanski M, Lee CL & Ralston HJ 3rd (1984). The structural organization of the ventrobasal complex of the rat as revealed by the analysis of physiologically characterized neurons injected intracellularly with horseradish peroxidase. Brain Res 297, 63-74.
49. Piet R, Bonhomme R, Theodosis DT, Poulain DA & Oliet SH (2003). Modulation of GABAergic transmission by endogenous glutamate in the rat supraoptic nucleus. Eur J Neurosci 17, 1777-1785.
50. Piet R, Vargova L, Sykova E, Poulain DA & Oliet SH (2004). Physiological contribution of the astrocytic environment of neurons to intersynaptic crosstalk. Proc Natl Acad Sci U S A 101, 2151-2155.
51. Pinault D (2004). The thalamic reticular nucleus: structure, function and concept. Brain Res Brain Res Rev 46, 1-31.
52. Pinault D (2011). Dysfunctional thalamus-related networks in schizophrenia. Schizophr Bull 37, 238-243.
53. Pinault D & Deschenes M (1998). Anatomical evidence for a mechanism of lateral inhibition in the rat thalamus. Eur J Neurosci 10, 3462-3469.
54. Poisik O, Raju DV, Verreault M, Rodriguez A, Abeniyi OA, Conn PJ & Smith Y (2005). Metabotropic glutamate receptor 2 modulates excitatory synaptic transmission in the rat globus pallidus. Neuropharmacology 49(Suppl 1), 57-69.
55. Ralston HHI (1983). The synaptic organization of the ventrobasal thalamus in the rat, cat and monkey. In: Macchi G, Rustioni A, Spreafico R (eds) Somatosensory Integration in the Thalamus. Elsevier Science, Amsterdam, 241-250.
56. Salt TE (1986). Mediation of thalamic sensory input by both NMDA receptors and non-NMDA receptors. Nature 322, 263-265.
57. Salt TE (1987). Excitatory amino acid receptors and synaptic transmission in the rat ventrobasal thalamus. J Physiol 391, 499-510.
58. Salt TE (1989). Gamma-aminobutyric acid and afferent inhibition in the cat and rat ventrobasal thalamus. Neuroscience 28, 17-26.
59. Salt TE & Eaton SA (1989). Function of non-NMDA receptors and NMDA receptors in synaptic responses to natural somatosensory stimulation in the ventrobasal thalamus. Exp Brain Res 77, 646-652.
60. Salt TE & Eaton SA (1995a). Distinct presynaptic metabotropic receptors for L-AP4 and CCG1 on GABAergic terminals: pharmacological evidence using novel alpha-methyl derivative mGluR antagonists, MAP4 and MCCG, in the rat thalamus in vivo. Neuroscience 65, 5-13.
61. Salt TE & Eaton SA (1995b). Modulation of sensory neurone excitatory and inhibitory responses in the ventrobasal thalamus by activation of metabotropic excitatory amino acid receptors. Neuropharmacology 34, 1043-1051.
62. Salt TE & Eaton SA (1996). Functions of ionotropic and metabotropic glutamate receptors in sensory transmission in the mammalian thalamus. Prog Neurobiol 48, 55-72.
63. Salt TE, Eaton SA & Turner JP (1996). Characterization of the metabotropic glutamate receptors (mGluRs) which modulate GABA-mediated inhibition in the ventrobasal thalamus. Neurochem Int 29, 317-322.
64. Salt TE & Turner JP (1998). Modulation of sensory inhibition in the ventrobasal thalamus via activation of group II metabotropic glutamate receptors by 2R, 4R-aminopyrrolidine-2, 4-dicarboxylate. Exp Brain Res 121, 181-185.
65. Schaffhauser H, Rowe BA, Morales S, Chavez-Noriega LE, Yin R, Jachec C, Rao SP, Bain G, Pinkerton AB, Vernier JM, Bristow LJ, Varney MA & Daggett LP (2003). Pharmacological characterization and identification of amino acids involved in the positive modulation of metabotropic glutamate receptor subtype 2. Mol Pharmacol 64, 798-810.
66. Schoepp DD, Jane DE & Monn JA (1999). Pharmacological agents acting at subtypes of metabotropic glutamate receptors. Neuropharmacology 38, 1431-1476.
67. Schoepp DD, Wright RA, Levine LR, Gaydos B & Potter WZ (2003). LY354740, an mGlu2/3 receptor agonist as a novel approach to treat anxiety/stress. Stress 6, 189-197.
68. Semyanov A & Kullmann DM (2000). Modulation of GABAergic signaling among interneurons by metabotropic glutamate receptors. Neuron 25, 663-672.
69. Shosaku A, Kayama Y, Sumitomo I, Sugitani M & Iwama K (1989). Analysis of recurrent inhibitory circuit in rat thalamus: neurophysiology of the thalamic reticular nucleus. Prog Neurobiol 32, 77-102.
70. Tamaru Y, Nomura S, Mizuno N & Shigemoto R (2001). Distribution of metabotropic glutamate receptor mGluR3 in the mouse CNS: differential location relative to pre- and postsynaptic sites. Neuroscience 106, 481-503.
71. Turner JP & Salt TE (2000). Synaptic activation of the group I metabotropic glutamate receptor mGlu1 on the thalamocortical neurons of the rat dorsal lateral geniculate nucleus in vitro. Neuroscience 100, 493-505.
72. Turner JP & Salt TE (2003). Group II and III metabotropic glutamate receptors and the control of the nucleus reticularis thalami input to rat thalamocortical neurones in vitro. Neuroscience 122, 459-469.
73. Vogt KE & Nicoll RA (1999). Glutamate and γ-aminobutyric acid mediate a heterosynaptic depression at mossy fiber synapses in the hippocampus. Proc Natl Acad Sci U S A 96, 1118-1122.
74. Wada E, Shigemoto R, Kinoshita A, Ohishi H & Mizuno N (1998). Metabotropic glutamate receptor subtypes in axon terminals of projection fibers from the main and accessory olfactory bulbs: a light and electron microscopic immunohistochemical study in the rat. J Comp Neurol 393, 493-504.
75. Xi ZX, Baker DA, Shen H, Carson DS & Kalivas PW (2002). Group II metabotropic glutamate receptors modulate extracellular glutamate in the nucleus accumbens. J Pharmacol Exp Ther 300, 162-171.