Differential metabotropic glutamate receptor expression and modulation in two neocortical inhibitory networks

Journal of Neurophysiology

Volumn 101, Issue 5, 2009, Pages 2679-2692

  Sun, Qian Quan ^a   Zhang, Zhi ^a   Jiao, Yuanyuan ^a   Zhang, Chunzhao ^a   Szabó, Gábor ^b   Erdelyi, Ferenc ^b  

^a UNIVERSITY OF WYOMING   (United States)

^b INSTITUTE OF EXPERIMENTAL MEDICINE   (Hungary)

Author keywords

[No Author keywords available]

Indexed keywords

METABOTROPIC RECEPTOR 1; METABOTROPIC RECEPTOR 2; METABOTROPIC RECEPTOR 3; METABOTROPIC RECEPTOR 5; METABOTROPIC RECEPTOR 8;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; ELECTROPHYSIOLOGY; EXCITATORY POSTSYNAPTIC POTENTIAL; IMMUNOREACTIVITY; INTERNEURON; MEMBRANE CONDUCTANCE; MODULATION; MOUSE; NEOCORTEX; NONHUMAN; POSTSYNAPTIC INHIBITION; PRIORITY JOURNAL; PROTEIN EXPRESSION; SOMATOSENSORY CORTEX; SPIKE WAVE; SYNAPTIC TRANSMISSION;

ACTION POTENTIALS; ANALYSIS OF VARIANCE; ANESTHETICS, LOCAL; ANIMALS; CELL COUNT; DRUG INTERACTIONS; EXCITATORY AMINO ACID AGONISTS; GAMMA-AMINOBUTYRIC ACID; GLUTAMATE DECARBOXYLASE; GLYCINE; GREEN FLUORESCENT PROTEINS; INTERNEURONS; MICE; MICE, TRANSGENIC; NEOCORTEX; NEURAL INHIBITION; NEURAL PATHWAYS; PARVALBUMINS; PHENYLACETATES; PROPIONIC ACIDS; RECEPTORS, METABOTROPIC GLUTAMATE; TETRODOTOXIN;

EID: 65649152992     PISSN: 00223077     EISSN: 15221598     Source Type: Journal    
DOI: 10.1152/jn.90566.2008     Document Type: Article

References (46)

1. 2+ signal transduction. J Biol Chem 267: 13361-13368, 1992.
2. Agmon A, Connors BW. Thalamocortical responses of mouse somatosensory (barrel) cortex in vitro. Neuroscience 41: 365-379, 1991.
3. Bacci A, Huguenard JR, Prince DA. Long-lasting self-inhibition of neocortical interneurons mediated by endocannabinoids. Nature 431: 312-316, 2004. (Pubitemid 39265666)
4. Bacci A, Rudolph U, Huguenard JR, Prince DA. Major differences in inhibitory synaptic transmission onto two neocortical interneuron subclasses. J Neurosci 23: 9664-9674, 2003. (Pubitemid 37352066)
5. Baskys A, Malenka RC. Agonists at metabotropic glutamate receptors presynaptically inhibit EPSCs in neonatal rat hippocampus. J Physiol 444: 687-701, 1991.
6. Baude A, Nusser Z, Roberts JD, Mulvihill E, McIlhinney RA, Somogyi P. The metabotropic glutamate receptor (mGluR1 alpha) is concentrated at perisynaptic membrane of neuronal subpopulations as detected by immunogold reaction. Neuron 11: 771-787, 1993. (Pubitemid 23321784)
7. Bear MF, Huber KM, Warren ST. The mGluR theory of fragile X mental retardation. Trends Neurosci 27: 370-377, 2004.
8. Beierlein M, Gibson JR, Connors BW. Two dynamically distinct inhibitory networks in layer 4 of the neocortex. J Neurophysiol 90: 2987-3000, 2003. (Pubitemid 37430000)
9. Brecht M, Sakmann B. Dynamic representation of whisker deflection by synaptic potentials in spiny stellate and pyramidal cells in the barrels and septa of layer 4 rat somatosensory cortex. J Physiol 543: 49-70, 2002.
10. Cai Z, Saugstad JA, Sorensen SD, Ciombor KJ, Zhang C, Schaffhauser H, Hubalek F, Pohl J, Duvoisin RM, Conn PJ. Cyclic AMP-dependent protein kinase phosphorylates group III metabotropic glutamate receptors and inhibits their function as presynaptic receptors. J Neurochem 78: 756-766, 2001. (Pubitemid 32777977)
11. Calabresi P, Pisani A, Mercuri NB, Bernardi G. Heterogeneity of metabotropic glutamate receptors in the striatum: electrophysiological evidence. Eur J Neurosci 5: 1370-1377, 1993. (Pubitemid 23300177)
12. Conn PJ, Pin JP. Pharmacology and functions of metabotropic glutamate receptors. Annu Rev Pharmacol Toxicol. 37: 205-237, 1997.
13. Dalezios Y, Lujan R, Shigemoto R, Roberts JD, Somogyi P. Enrichment of mGluR7a in the presynaptic active zones of GABAergic and non-GABAergic terminals on interneurons in the rat somatosensory cortex. Cereb Cortex 12: 961-974, 2002.
14. Desai MA, McBain CJ, Kauer JA, Conn PJ. Metabotropic glutamate receptor-induced disinhibition is mediated by reduced transmission at excitatory synapses onto interneurons and inhibitory synapses onto pyramidal cells. Neurosci Lett 181: 78-82, 1994. (Pubitemid 24343409)
15. Doherty AJ, Palmer MJ, Henley JM, Collingridge GL, Jane DE. (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: 265-267, 1997. (Pubitemid 27149516)
16. Fitzsimonds RM, Dichter MA. Heterologous modulation of inhibitory synaptic transmission by metabotropic glutamate receptors in cultured hippocampal neurons. J Neurophysiol 75: 885-893, 1996.
17. Gee CE, Lacaille JC. Group I metabotropic glutamate receptor actions in oriens/alveus interneurons of rat hippocampal CA1 region. Brain Res 1000: 92-101, 2004.
18. Gereau RW, Conn PJ. Multiple presynaptic metabotropic glutamate receptors modulate excitatory and inhibitory synaptic transmission in hippocampal area CA1. J Neurosci 15: 6879-6889, 1995.
19. Hubert GW, Paquet M, Smith Y. Differential subcellular localization of mGluR1a and mGluR5 in the rat and monkey substantia nigra. J Neurosci 21: 1838-1847, 2001. (Pubitemid 32221367)
20. Jiao YY, Zhang CZ, Yanagawa Y, Sun QQ. Major effects of sensory experiences on the neocortical inhibitory circuits. J Neurosci 26: 8691-8701, 2006. (Pubitemid 44319404)
21. Jin Y, Kim SJ, Kim J, Worley PF, Linden DJ. Long-term depression of mGluR1 signaling. Neuron 55: 277-287, 2007. (Pubitemid 47048914)
22. Kim SJ, Jin Y, Kim J, Shin JH, Worley PF, Linden DJ. Transient upregulation of postsynaptic IP3-gated Ca release underlies short-term potentiation of metabotropic glutamate receptor 1 signaling in cerebellar Purkinje cells. J Neurosci 28: 4350-4355, 1997.
23. Kumar SS, Huguenard JR. Properties of excitatory synaptic connections mediated by the corpus callosum in the developing rat neocortex. J Neurophysiol 86: 2973-2985, 2001. (Pubitemid 33139065)
24. Liu XB, Munoz A, Jones EG. Changes in subcellular localization of metabotropic glutamate receptor subtypes during postnatal development of mouse thalamus. J Comp Neurol 395: 450-465, 1998. (Pubitemid 28226091)
25. Lopez-Bendito G, Sturgess K, Erdelyi F, Szabo G, Molnar Z, Paulsen O. Preferential origin and layer destination of GAD65-GFP cortical interneurons. Cereb Cortex 14: 1122-1133, 2004. (Pubitemid 39258167)
26. Lujan R, Nusser Z, Roberts JD, Shigemoto R, Somogyi P. Perisynaptic location of metabotropic glutamate receptors mGluR1 and mGluR5 on dendrites and dendritic spines in the rat hippocampus. Eur J Neurosci 8: 1488-1500, 1996. (Pubitemid 126734660)
27. Mannaioni G, Attucci S, Missanelli A, Pellicciari R, Corradetti R, Moroni F. Biochemical and electrophysiological studies on (S)-(+)-2-(3′- carboxybicyclo[ 1.1.1]pentyl)-glycine (CBPG), a novel mGlu(5) receptor agonist endowed with mGlu(1) receptor antagonist activity. Neuropharmacology 38: 917-926, 1999. (Pubitemid 29240608)
28. Maccaferri G, Tóth K, McBain CJ. Target-specific expression of presynaptic mossy fiber plasticity. Science 279: 1368-1370, 1998. (Pubitemid 28119581)
29. McBain CJ, DiChiara TJ, Kauer JA. Activation of metabotropic glutamate receptors differentially affects two classes of hippocampal interneurons and potentiates excitatory synaptic transmission. J Neurosci 14: 4433-4445, 1994.
30. McBain CJ, Fisahn A. Interneurons unbound. Nat Rev Neurosci 2: 11-23, 2001. (Pubitemid 33673345)
31. Munoz A, Liu XB, Jones EG. Development of metabotropic glutamate receptors from trigeminal nuclei to barrel cortex in postnatal mouse. J Comp Neurol 409: 549-566, 1999. (Pubitemid 29258761)
32. Nakajima Y, Iwakabe H, Akazawa C, Nawa H, Shigemoto R, Mizuno N, Nakanishi S. Molecular characterization of a novel retinal metabotropic glutamate receptor mGluR6 with a high agonist selectivity for L-2-amino-4-phosphonobutyrate. J Biol Chem 268: 11868-11873, 1993. (Pubitemid 23168143)
33. Pelkey KA, Lavezzari G, Racca C, Roche KW, McBain CJ. mGluR7 is a metaplastic switch controlling bidirectional plasticity of feedforward inhibition. Neuron 46: 89-102, 2005. (Pubitemid 40488314)
34. Petralia RS, Wang YX, Singh S, Wu C, Shi L, Wei J, Wenthold RJ. A monoclonal antibody shows discrete cellular and subcellular localizations of mGluR1 alpha metabotropic glutamate receptors. J Chem Neuroanat 13: 77-93, 1997. (Pubitemid 27397129)
35. Pin JP, Waeber C, Prezeau L, Bockaert J, Heinemann SF. Alternative splicing generates metabotropic glutamate receptors inducing different patterns of calcium release in Xenopus oocytes. Proc Natl Acad Sci USA 89: 10331-10335, 1992.
36. Salt TE. Glutamate receptor functions in sensory relay in the thalamus. Philos Trans R Soc Lond B Biol Sci. 357: 1759-1766, 2002.
37. Sandstrom MI, Rebec GV. Extracellular ascorbate modulates glutamate dynamics: role of behavioral activation. BMC Neurosci 8: 32, 2007.
38. 2+ exchange current. J Neurophysiol 95: 882-892, 2006.
39. Schoepp DD, Jane DE, Monn JA. Pharmacological agents acting at subtypes of metabotropic glutamate receptors. Neuropharmacology 38: 1431-1476, 1999.
40. Sun QQ, Huguenard JR, Prince DA. Barrel cortex microcircuits: thalamocortical feedforward inhibition in spiny stellate cells is mediated by a small number of fast-spiking interneurons. J Neurosci 26: 1219-1230, 2006. (Pubitemid 43237055)
41. Tamamaki N, Yanagawa Y, Tomioka R, Miyazaki JI, Obata K, Kaneko T. Green fluorescent protein expression and colocalization with calretinin, parvalbumin, and somatostatin in the GAD67-GFP knock-in mouse. J Comp Neurol 467: 60-79, 2003. (Pubitemid 37339758)
42. Tóth K, McBain CJ. Target-specific expression of pre- and postsynaptic mechanisms. J Physiol 525: 41-51, 2000. (Pubitemid 30311932)
43. Wang Y, Gupta A, Toledo-Rodriguez M, Wu CZ, Markram H. Anatomical, physiological, molecular and circuit properties of nest basket cells in the developing somatosensory cortex. Cereb Cortex 12: 395-410, 2002. (Pubitemid 34226064)
44. Wong RK, Chuang SC, Bianchi R. Plasticity mechanisms underlying mGluR-induced epileptogenesis. Adv Exp Med Biol 548: 69-75, 2004. (Pubitemid 38979614)
45. Young A, Sun QQ. Long-term modifications in the strength of excitatory associative inputs in the piriform cortex. Chem Senses 32: 783-794, 2007. (Pubitemid 47578177)
46. Zhang C, Szabo G, Erdelyi F, Rose JD, Sun QQ. Novel interneuronal network in the mouse posterior piriform cortex. J Comp Neurol 499: 1000-1015, 2006.