Reduction of excitatory postsynaptic responses by persistently active metabotropic glutamate receptors in the hippocampus

Journal of Neurophysiology

Volumn 89, Issue 4, 2003, Pages 1910-1919

  Losonczy, Attila ^a   Somogyi, Peter ^a,b   Nusser, Zoltan ^a,c  

^a INSTITUTE OF EXPERIMENTAL MEDICINE   (Hungary)

^b MEDICAL RESEARCH COUNCIL   (United Kingdom)

^c INSTITUTE OF EXPERIMENTAL MEDICINE   (Hungary)

Author keywords

[No Author keywords available]

Indexed keywords

2 AMINO 2 (2 CARBOXYCYCLOPROPYL) 3 (XANTHEN 9 YL)PROPIONIC ACID; 2 AMINO 4 PHOSPHONOBUTYRIC ACID; GLUTAMIC ACID; GLYCINE DERIVATIVE; METABOTROPIC RECEPTOR; METABOTROPIC RECEPTOR AGONIST; METABOTROPIC RECEPTOR ANTAGONIST;

ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DIFFUSION; EXCITATORY POSTSYNAPTIC POTENTIAL; GABAERGIC SYSTEM; HIPPOCAMPUS; INTERNEURON; MOUSE; NERVE CELL EXCITABILITY; NERVE CELL PLASTICITY; NERVE ENDING; NEUROTRANSMITTER RELEASE; NONHUMAN; PRIORITY JOURNAL; RECEPTOR UPREGULATION;

AMINO ACIDS; ANIMALS; ANTICONVULSANTS; CYCLOPROPANES; EXCITATORY AMINO ACID ANTAGONISTS; EXCITATORY POSTSYNAPTIC POTENTIALS; GLYCINE; HIPPOCAMPUS; INTERNEURONS; MEMBRANE POTENTIALS; MICE; MICE, INBRED C57BL; NEURONAL PLASTICITY; PRESYNAPTIC TERMINALS; PROPIONIC ACIDS; RECEPTORS, METABOTROPIC GLUTAMATE; XANTHENES;

EID: 0037387443     PISSN: 00223077     EISSN: None     Source Type: Journal    
DOI: 10.1152/jn.00842.2002     Document Type: Article

References (46)

1. Ali AB, Deuchars J, Pawelzik H, and Thomson AM. CA1 pyramidal to basket and bistratified cell EPSPs: dual intracellular recordings in rat hippocampal slices. J Physiol 507: 201-217, 1998.
2. Ali AB and Thomson AM. Facilitating pyramid to horizontal oriens-alveus interneuron inputs: dual intracellular recordings in slices of rat hippocampus. J Physiol 507: 185-199, 1998.
3. Blasco-Ibanez JM and Freund TF. Synaptic input of horizontal interneurons in stratum oriens of the hippocampal CA1 subfield: structural basis of feed-back activation. Eur J Neurosci 7: 2170-2180, 1995.
4. Conchilla AJ and Alford S. Metabotropic glutamate receptor-mediated control of neurotransmitter release. Neuron 20: 1007-1016, 1998.
5. Conn PJ and Pin JP. Pharmacology and functions of metabotropic glutamate receptors. Annu Rev Pharmacol Toxicol 37: 205-237, 1997.
6. Corti C, Aldegheri L, Somogyi P, and Ferraguti F. Distribution and synaptic localisation of the metabotropic glutamate receptor 4 (mGluR4) in the rodent central nervous system. Neuroscience 110: 403-420, 2002.
7. Dalezios Y, Lujan R, Shigemoto R, Roberts JDB, and Somogyi P. Group III metabotropic glutamate receptors (mGluRs) on GABAergic terminals of hippocampal and neocortical interneurons. Soc Neurosci Abstr 27: 259.5, 2001.
8. Dalezios Y, Lujan R, Shigemoto R, Roberts JDB, and Somogyi P. Enrichment of mGluR7a in the presynaptic acive zones of GABAergic and non-GABAergic terminals on interneurons in the rat somatosensory cortex. Cereb Cortex 12: 961-974, 2002.
9. Deller T, Adelmann G, Nitsch R, and Frotscher M. The alvear pathway of the rat hippocampus. Cell Tissue Res 286: 293-303, 1996.
10. Dobrunz LE and Stevens CF. Heterogeneity of release probability, facilitation, and depletion at central synapses. Neuron 18: 995-1008, 1997.
11. Dube RG and Marshall KC. Activity-dependent activation of presynaptic metabotropic glutamate receptors in Locus Coeruleus. J Neurophysiol 83: 1141-1149, 2000.
12. Frank K and Fourtes MGF. Presynaptic and postsynaptic inhibition of monosynaptic reflexes. Fed Proc 16: 39-40, 1957.
13. Jin X and Daw NW. The group III metabotropic glutamate receptor agonist, 1-AP4, reduces EPSPs in some layers of rat visual cortex. Brain Res 797: 218-224, 1998.
14. Kingston AE, Ornstein PL, Wright RA, Johnson BG, Mayne NG, Burnett JP, Belagaje R, Wu S, and Schoepp DD. LY341495 is a nanomolar potent and selective antagonist of group II metabotropic glutamate receptors. Neuropharmacology 37: 1-12, 1998.
15. Kinoshita A, Shigemoto R, Ohishi H, van der Putten H, and Mizuno N. Immunohistochemical localization of metabotropic glutamate receptors, mGluR7a and mGluR7b, in the central nervous system of the adult rat and mouse: a light and electron microscopic study. J Comp Neurol 393: 332-352, 1998.
16. Leazza F, Doherty JJ, and Dingledine R. Long-term depression in hippocampal interneurons: joint requirement for pre- and postsynaptic events. Science 285: 1411-1414, 1999.
17. Losonczy A, Zhang L, Shigemoto R, Nusser Z, and Somogyi P. Cell type dependence and variability in the short-term plasticity of EPSCs in identified mouse hippocampal interneurones. J Physiol 542: 193-210, 2002.
18. Lujan R, Roberts JDB, Shigemoto R, Ohishi H, and Somogyi P. Differential plasma membrane distribution of metabotropic glutamate receptors mGluR1a, mGluR2, and mGluR5, relative to neurotransmitter release sites. J Chem Neuroanat 13: 219-241, 1997.
19. Maccaferri G, Roberts JDB, Cottingham CA, and Somogyi P. Cell surface domain specific postsynaptic currents evoked by identified GABAergic neurones in rat hippocampus in vitro. J Physiol 524: 91-116, 2000.
20. Markram H, Wang Y, and Tsodyks M. Differential signaling via the same axon of neocortical pyramidal neurons. Proc Natl Acad Sci USA 95: 5323-5328, 1998.
21. McBain CJ, DiChiara TJ, and 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.
22. Mitchell SJ and Silver RA. Glutamate spillover suppresses inhibition by activating presynaptic mGluRs. Nature 404: 498-502, 2000.
23. Nomura A, Shigemoto R, Nakamura Y, Okamoto N, Mizuno N, and Nakanishi S. Developmentally regulated postsynaptic localization of a metabotropic glutamate receptor in rat rod bipolar cells. Cell 77: 361-369, 1994.
24. Nusser Z, Naylor D, and Mody I. Synapse-specific contribution of the variation of transmitter concentration to the decay of inhibitory postsynaptic currents. Biophys J 80: 1251-1261, 2001.
25. Okamoto N, Hori S, Akazawa C, Hayashi Y, Shigemoto R, Mizuno N, and Nakanishi S. Molecular characterization of a new metabotropic glutamate receptor mGluR7 coupled to inhibitopy cyclic AMP signal transduction. J Biol Chem 269: 1231-1236, 1994.
26. Oliet SHR, Piet R, and Poulain DA. Control of glutamate clearance and synaptic efficacy by glial coverage of neurons. Science 292: 923-926, 2001.
27. Ramon y Cajal S. Estructura del asta de ammon y fascia dentata. Anal Soc Espan Hist Natural 22: 53-114, 1893.
28. Reyes A, Lujan R, Rozov A, Burnashev N, Somogyi P, and Sakmann B. Target-cell-specific facilitation and depression in neocortical circuits. Nat Neurosci 1: 279-285, 1998.
29. 2+ buffers in facilitating and depressing nerve terminals of pyramidal cells in layer 2/3 of the rat neocortex indicates a target cell-specific difference in presynaptic calcium dynamics. J Physiol 531: 807-826, 2001.
30. Sansig G, Bushell TJ, Clarke VR, Rozov A, Burnashev N, Portet C, Gasparini F, Schmutz M, Klebs K, Shigemoto R, Flor PJ, Kuhn R, Knoepfel T, Schroeder M, Hampson DR, Collett VJ, Zhang C, Duvoisin RM, Collingridge GL, and van Der Putten H. Increased seizure susceptibility in mice lacking metabotropic glutamate receptor 7. J Neurosci 21: 8734-8745, 2001.
31. Scanziani M, Gahwiler BH, and Charpak S. Target cell-specific modulation of transmitter release at terminals from a single axon. Proc Natl Acad Sci USA 95: 12004-12009, 1998.
32. Scanziani M, Salin PA, Vogt KE, Malenka RC, and Nicoll RA. Use-dependent increases in glutamate concentration activate presynaptic metabotropic glutamate receptors. Nature 385: 630-634. 1997.
33. Schrader LA and Tasker JG. Presynaptic modulation of metabotropic glutamate receptors of excitatory and inhibitory synaptic inputs to hypothalamic magnocellular neurons. J Neurophysiol 77: 527-536, 1997.
34. Schulz HL, Stohr H, and Weber BHF. Characterization of three novel isoforms of the metabotrobic glutamate receptor 7 (GRM7). Neurosci Lett 326: 37-40, 2002.
35. Semyanov A and Kullmann DM. Modulation of GABAergic signaling among interneurons by metabotropic glutamate receptors. Neuron 25: 663-672, 2000.
36. Shigemoto R, Kinoshita A, Wada E, Nomura S, Ohishi H, Takada M, Flor PJ, Neki A, Abe T, Nakanishi S, and Mizuno N. Differential presynaptic localization of metabotropic glutamate receptor subtypes in the rat hippocampus. J Neurosci 17: 7503-7522, 1997.
37. Shigemoto R, Kulik A, Roberts JD, Ohishi H, Nusser Z, Kaneko T, and Somogyi P. Target-cell-specific concentration of a metabotropic glutamate receptor in the presynaptic active zone. Nature 381: 523-525, 1996.
38. Somogyi P, Ganter P, Kogo N, Maccaferri GM, Paspalas C, Paulsen O, Roberts JDB, Shigemoto R, and Szucs P. Compartmentalization and properties of synapses and receptors in a feedback circuit of the cerebral cortex. J Physiol 22S: 518P, 1999.
39. Stevens CF and Wesseling JF. Identification of a novel process limiting the rate of synaptic vesicle cycling at hippocampal synapses. Neuron 24: 1017-1028, 1999.
40. Takahashi T, Forsythe ID, Tsujimoto T, Barnes-Davies M, and Onodera K. Presynaptic calcium current modulation by a metabotropic glutamate receptor. Science 274: 594-597, 1996.
41. Thomson AM. Facilitation, augmentation and potentiation at central synapses. Trends Neurosci 23: 305-312, 2000.
42. Turner JP and Salt TE. Group III metabotropic glutamate receptors control corticothalamic synaptic transmission in the rat thalamus in vitro. J Physiol 519: 481-49, 1999.
43. Vizi ES and Kiss JP. Neurochemistry and pharmacology of the major hippocampal transmitter systems: synaptic and nonsynaptic interactions. Hippocampus 8: 566-607, 1998.
44. von Gersdorff H, Schneggenburger R, Weis S, and Neher E. Presynaptic depression at a calyx synapse: the small contribution of metabotropic glutamate receptors. J Neurosci 17: 8137-8146, 1997.
45. Wittmann M, Marino MJ, Bradley SR, and Conn PJ. Activation of group III mGluRs inhibits GABAergic and glutamatergic transmission in the substantia nigra pars reticulata. J Neurophysiol 85: 1960-1968, 2001.
46. Zucker RS. Short-term synaptic plasticity. Annu Rev Neurosci 12: 13-31, 1989.