Synapse-specific mGluR1-dependent long-term potentiation in interneurones regulates mouse hippocampal inhibition

Journal of Physiology

Volumn 555, Issue 1, 2004, Pages 125-135

  Lapointe, Valérie ^a   Morin, France ^a   Ratté, Stéphanie ^a   Croce, Ariane ^a   Conquet, François ^b   Lacaille, Jean Claude ^a  

^a UNIVERSITÉ DE MONTRÉAL   (Canada)

^b GlaxoSmithKline   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

CALCIUM ION; METABOTROPIC RECEPTOR 1;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BRAIN SLICE; CELL SYNCHRONIZATION; CONSTANTS AND COEFFICIENTS; CONTROLLED STUDY; CORRELATION ANALYSIS; EXCITATORY POSTSYNAPTIC POTENTIAL; FACILITATION; HIPPOCAMPUS; HIPPOCAMPUS THETA RHYTHM; INTERNEURON; KNOCKOUT MOUSE; LONG TERM POTENTIATION; MOUSE; NERVE CELL EXCITABILITY; NERVE CELL MEMBRANE STEADY POTENTIAL; NERVE CELL PLASTICITY; NEUROMODULATION; NONHUMAN; PRESYNAPTIC POTENTIAL; PRIORITY JOURNAL; PYRAMIDAL NERVE CELL; REGULATORY MECHANISM; SYNAPTIC INHIBITION; ALVEUS; HIPPOCAMPAL CA1 REGION; HIPPOCAMPAL SLICE; NERVE CELL STIMULATION; PRESYNAPTIC NERVE; STRATUM ORIENS; THETA RHYTHM;

ANIMALS; EGTAZIC ACID; HIPPOCAMPUS; INTERNEURONS; LONG-TERM POTENTIATION; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; NEURAL INHIBITION; RECEPTORS, METABOTROPIC GLUTAMATE; SYNAPSES;

EID: 1542269781     PISSN: 00223751     EISSN: None     Source Type: Journal    
DOI: 10.1113/jphysiol.2003.053603     Document Type: Article

References (41)

1. Ali AB & Thomson AM (1998). Facilitating pyramid to horizontal oriens-alveus interneurone inputs: dual intracellular recordings in slices of rat hippocampus. J Physiol 507, 185-199.
2. Alle H, Jonas P & Geiger JR (2001). PTP and LTP at a hippocampal mossy fiber-interneuron synapse. Proc Natl Acad Sci U S A 98, 14708-14713.
3. Baude A, Nusser Z, Roberts JD, Mulvihill E, McIlhinney RA & Somogyi P (1993). The metabotropic glutamate receptor (mGluR1 alpha) is concentrated at the perisynaptic membrane of neuronal subpopulations as detected by immunogold reaction. Neuron 11, 771-787.
4. Bibbig A, Faulkner HJ, Whittington MA & Traub RD (2001). Self-organized synaptic plasticity contributes to the shaping of γ and β oscillations In Vitro. J Neurosci 21, 9053-9067.
5. Blasco-Ibanez JM & Freund TF (1995). 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.
6. Bliss TVP & Collingridge GL (1993). A synaptic model of memory: long-term potentiation in the hippocampus. Nature 361, 31-39.
7. Buzsáki G & Chrobak JJ (1995). Temporal structure in spatially organized neuronal ensembles: a role for interneuronal networks. Curr Opin Neurobiol 5, 504-510.
8. Conquet F, Bashir ZI, Davies CH, Daniel H, Ferraguti F, Bordi F, Franz-Bacon K, Reggiani A, Matarese V, Condé F, Collingridge GL & Crépel F (1994). Motor deficit and impairment of synaptic plasticity in mice lacking mGluR1. Nature 372, 237-243.
9. Cowan AI, Stricker C, Reece LJ & Redman SJ (1998). Long-term plasticity at excitatory synapses on aspinous interneurons in area CA1 lacks synaptic specificity. J Neurophysiol 79, 13-20.
10. Evans DI, Jones RS & Woodhall G (2001). Differential actions of PKA and PKC in the regulation of glutamate release by group III mGluRs in the entorhinal cortex. J Neurophysiol 85, 571-579.
11. Freund TF & Buzsáki G (1996). Interneurons of the hippocampus. Hippocampus 6, 347-470.
12. Gee CE, Woodhall G & Lacaille J-C (2001). Synaptically activated calcium responses in dendrites of hippocampal oriens-alveus interneurons. J Neurophysiol 85, 1603-1613.
13. Grunze HC, Rainnie DG, Hasselmo ME, Barkai E, Hearn EF, McCarley RW & Greene RW (1996). NMDA-dependent modulation of CA1 local circuit inhibition. J Neurosci 16, 2034-2043.
14. Isaac JTR, Nicoll RA & Malenka RC (1995). Evidence for silent synapses: implications for the expression of LTP. Neuron 15, 427-434.
15. Kamiya H, Shinozaki H & Yamamoto C (1996). Activation of metabotropic glutamate receptor type 2/3 suppresses transmission at rat hippocampal mossy fiber synapses. J Physiol 493, 447-455.
16. Lacaille J-C, Muller A, Kunkel DD & Schwartzkroin PA (1987). Local circuit interactions between oriens/alveus interneurons and CA1 pyramidal cells in hippocampal slices: electrophysiology and morphology. J Neurosci 7, 1979-1993.
17. Laezza F, Doherty JJ & Dingledine R (1999). Long-term depression in hippocampal interneurons: Joint requirement for pre- and postsynaptic events. Science 285, 1411-1414.
18. Liao D, Hessler NA & Malinow R (1995). Activation of postsynaptically silent synapses during pairing-induced LTP in CA1 region of hippocampal slice. Nature 375, 400-404.
19. Luján R, Nusser Z, Roberts JDB, Shigemoto R & Somogyi P (1996). Perisynaptic location of metabotropic glutamate receptors mGluR1 and mGluR5 on dendrites and dendritic spines in the rat hippocampus. Eur J Neurosci 8, 1488-1500.
20. McBain CJ, Freund TF & Mody I (1999). Glutamatergic synapses onto hippocampal interneurons: precision timing without lasting plasticity. Trends Neurosci 22, 228-235.
21. Macek TA, Winder DG, Gereau RW, Ladd CO & Conn PJ (1996). Differential involvement of group II and group III mGluRs as autoreceptors at lateral and medial perforant path synapses. J Neurosci 76, 3798-3806.
22. McMahon LL & Kauer JA (1997). Hippocampal interneurons express a novel form of synaptic plasticity. Neuron 18, 295-305.
23. Malenka RC & Nicoll RA (1999). Long-term potentiation: a decade of progress? Science 285, 1870-1874.
24. 2+-dependent protein kinases with subsequent presynaptic enhancement. Prog Brain Res 89, 271-289.
25. Manabe T, Wyllie DJ, Perkel DJ & Nicoll RA (1993). Modulation of synaptic transmission and long-term potentiation: effects on paired-pulse facilitation and EPSC variance in the CA1 region of the hippocampus. J Neurophysiol 70, 1451-1459.
26. Manzoni OJ, Castillo PE & Nicoll RA (1995). Pharmacology of metabotropic glutamate receptors at the mossy fiber synapses of the guinea pig hippocampus. Neuropharmacol 34, 965-971.
27. Nicoll RA & Malenka RC (1995). Contrasting properties of two forms of long-term potentiation in the hippocampus. Nature 377, 115-118.
28. Ouardouz M & Lacaille J-C (1995). Mechanisms of selective long-term potentiation of excitatory synapses in stratum oriens/alveus interneurons of rat hippocampal slices. J Neurophysiol 73, 810-819.
29. Perez Y, Morin F & Lacaille J-C (2001). A hebbian form of long-term potentiation dependent on mGluR1a in hippocampal inhibitory interneurons. Proc Natl Acad Sci U S A 98, 9401-9406.
30. Petralia RS, Wang Y-X, Niedzielski AS & Wenthold RJ (1996). The metabotropic glutamate receptors mGluR2 and mGluR3, show unique postsynaptic, presynaptic and glial localizations. Neuroscience 71, 949-976.
31. Raastad M (1995). Extracellular activation of unitary excitatory synapses between hippocampal CA3 and CA1 pyramidal cells. Eur J Neurosci 7, 1882-1888.
32. Ross ST & Soltesz I (2001). Long-term plasticity in interneurons of the dentate gyrus. Proc Natl Acad Sci U S A 98, 8874-8879.
33. Shigemoto R, Kinoshita A, Wada E, Nomura S, Ohishi H, Takada M, Flor PJ, Neki A, Abe T, Nakanishi S & Mizuno N (1997). Differential presynaptic localization of metabotropic glutamate receptor subtypes in the rat hippocampus. J Neurosci 17, 7503-7522.
34. Sokolov MV, Rossokhin AV, Behnisch T, Reymann KG & Voronin LL (1998). Interaction between paired-pulse facilitation and long-term potentiation of minimal excitatory postsynaptic potentials in rat hippocampal slices: a patch-damp study. Neuroscience 85, 1-13.
35. Stevens CF & Wang Y (1994). Changes in reliability of synaptic function as a mechanism for plasticity. Nature 371, 704-707.
36. Tóth K & McBain CJ (1998). Afferent-specific innervation of two distinct AMPA receptor subtypes on single hippocampal interneurons. Nature Neurosci 1, 572-578.
37. Tóth K & McBain CJ (2000). Target-specific expression of pre- and postsynaptic mechanisms. J Physiol 525, 41-51.
38. Tóth K, Suares G, Lawrence JJ, Philips-Tansey E & McBain CJ (2000). Differential mechanisms of transmission at three types of mossy fiber synapse. J Neurosci 20, 8279-8289.
39. Whittington MA, Traub RD & Jefferys JGR (1995). Synchronized oscillations in interneuron networks driven by metabotropic glutamate receptor activation. Nature 373, 612-615.
40. 2+ oscillations activated by mGluRs in hippocampal stratum oriens/alveus interneurons. J Neurophysiol 81, 371-382.
41. Ylinen A, Bragin A, Nadasdy Z, Jando G, Szabo I, Sík A & Buzsáki G (1995). Sharp wave-associated high-frequency oscillation (200Hz) in the intact hippocampus: network and intracellular mechanisms. J Neurosci 15, 30-46.