Simultaneous NMDA-dependent long-term potentiation of EPSCs and long-term depression of IPSCs in cultured rat hippocampal neurons

Journal of Neuroscience

Volumn 26, Issue 4, 2006, Pages 1199-1210

  Ivenshitz, Miriam ^a   Segal, Menahem ^a  

^a WEIZMANN INSTITUTE OF SCIENCE   (Israel)

Author keywords

Activity dependent plasticity; Conditioning; Culture; LTD; LTP; NMDA

Indexed keywords

4 AMINOBUTYRIC ACID B RECEPTOR; BENZYL[3 [[1 (3,4 DICHLOROPHENYL)ETHYL]AMINO] 2 HYDROXYPROPYL]PHOSPHINIC ACID; CALCIUM ION; CYCLIC AMP DERIVATIVE; N METHYL DEXTRO ASPARTIC ACID; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; NITRIC OXIDE SYNTHASE INHIBITOR; PRESYNAPTIC RECEPTOR; SACLOFEN;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BRAIN NERVE CELL; CELL ACTIVITY; CONDITIONING; CONTROLLED STUDY; EXCITATORY POSTSYNAPTIC POTENTIAL; HIPPOCAMPUS; INHIBITORY POSTSYNAPTIC POTENTIAL; LONG TERM DEPRESSION; LONG TERM POTENTIATION; NERVE CELL CULTURE; NERVE CELL NETWORK; NERVE CELL PLASTICITY; NEUROTRANSMISSION; NONHUMAN; POSTSYNAPTIC POTENTIAL; PRIORITY JOURNAL; RAT; RECEPTOR BLOCKING; SYNAPSE;

2-AMINO-5-PHOSPHONOVALERATE; ANIMALS; BACLOFEN; CALCIUM; CELLS, CULTURED; CYCLIC AMP; EVOKED POTENTIALS; FORSKOLIN; HIPPOCAMPUS; LONG-TERM DEPRESSION (PHYSIOLOGY); LONG-TERM POTENTIATION; NEURONAL PLASTICITY; NEURONS; NITRIC OXIDE; NITRIC OXIDE SYNTHASE; NITROARGININE; PATCH-CLAMP TECHNIQUES; PHOSPHINIC ACIDS; PROPANOLAMINES; QUINOXALINES; RATS; RECEPTORS, GABA-B; RECEPTORS, N-METHYL-D-ASPARTATE; SYNAPTIC TRANSMISSION; TETRODOTOXIN; THIONUCLEOTIDES; TIME FACTORS;

EID: 32544461585     PISSN: 02706474     EISSN: None     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.2964-05.2006     Document Type: Article

References (66)

1. Abraham WC, Gustafsson B, Wigstrom H (1987) Long-term potentiation involves enhanced synaptic excitation relative to synaptic inhibition in guinea-pig hippocampus. J Physiol (Lond) 394:367-380.
2. Bekkers JM, Stevens CF (1990) Presynaptic mechanism for long-term potentiation in the hippocampus. Nature 346:724-729.
3. Bi G, Poo M (1999) Distributed synaptic modification in neural networks induced by patterned stimulation. Nature 401:792-796.
4. Bliss TV, Lomo T (1973) Long-lasting potentiation of synaptic transmission in the dentate area of the anaesthetized rabbit following stimulation of the perforant path. J Physiol (Lond) 232:331-356.
5. Blitzer RD, Wong T, Nouranifar R, Iyengar R, Landau EM (1995) Postsynaptic cAMP pathway gates early LTP in hippocampal CA1 region. Neuron 15:1403-1414.
6. Bonhoeffer T, Staiger V, Aertsen A (1989) Synaptic plasticity in rat hippocampal slice cultures: local "Hebbian" conjunction of pre- and postsynaptic stimulation leads to distributed synaptic enhancement. Proc Natl Acad Sci USA 86:8113-8117.
7. Bredt DS, Nicoll RA (2003) AMPA receptor trafficking at excitatory synapses. Neuron 40:361-379.
8. Caddick SJ, Stanford IM, Chad JE (1995) 2-Hydroxy-saclofen causes a phaclofen-reversible reduction in population spike amplitude in the rat hippocampal slice. Eur J Pharmacol 274:41-46.
9. Davies CH, Pozza MF, Collingridge GL (1993) CGP 55845A: a potent antagonist of GABAB receptors in the CA1 region of rat hippocampus. Neuropharmacology 32:1071-1073.
10. Emptage NJ, Reid CA, Fine A, Bliss TV (2003) Optical quantal analysis reveals a presynaptic component of LTP at hippocampal Schafferassociational synapses. Neuron 38:797-804.
11. Engert F, Bonhoeffer T (1997) Synapse specificity of long-term potentiation breaks down at short distances. Nature 388:279-284.
12. Engert F, Bonhoeffer T (1999) Dendritic spine changes associated with hippocampal long-term synaptic plasticity. Nature 399:66-70.
13. Frey U, Huang YY, Kandel ER (1993) Effects of cAMP simulate a late stage of LTP in hippocampal CA1 neurons. Science 260:1661-1664.
14. Fujii S, Sasaki H, Mikoshiba K, Kuroda Y, Yamazaki Y, Mostafa Taufiq A, Kato H (2004) A chemical LTP induced by co-activation of metabotropic and N-methyl-D-aspartate glutamate receptors in hippocampal CA1 neurons. Brain Res 999:20-28.
15. + current in voltage-clamped CA3 pyramidal cells in hippocampal cultures. Proc Natl Acad Sci USA 5:1558-1562.
16. Goldin M, Segal M (2003) Protein kinase C and ERK involvement in dendritic spine plasticity in cultured rodent hippocampal neurons. Eur J Neurosci 17:2529-2539.
17. Goldin M, Segal M, Avignone E (2001) Functional plasticity triggers formation and pruning of dendritic spines in cultured hippocampal networks. J Neurosci 21:186-193.
18. Griffith WH, Brown TH, Johnston D (1986) Voltage-clamp analysis of synaptic inhibition during long-term potentiation in hippocampus. J Neurophysiol 55:767-775.
19. Huang YY, Li XC, Kandel ER (1994) cAMP contributes to mossy fiber LTP by initiating both a covalently mediated early phase and macromolecular synthesis-dependent late phase. Cell 79:69-79.
20. Izumi Y, Zorumski CF (1993) Nitric oxide and long-term synaptic depression in the rat hippocampus. NeuroReport 4:1131-1134.
21. 2+ release in CA3 pyramidal neurons via a metabotropic glutamate receptor pathway. Neuroscience 107:59-69.
22. Katz B, Miledi R (1968) The role of calcium in neuromuscular facilitation. J Physiol (Lond) 195:481-492.
23. Kleschevnikov AM, Sokolov MV, Kuhnt U, Dawe GS, Stephenson JD, Voronin LL (1997) Changes in paired-pulse facilitation correlate with induction of long-term potentiation in area CA1 of rat hippocampal slices. Neuroscience 76:829-843.
24. Knight AR, Bowery NG (1996) The pharmacology of adenylyl cyclase modulation by GABAB receptors in rat brain slices. Neuropharmacology 35:703-712.
25. Krieger P, Hellgren-Kotaleski J, Kettunen P, El Manira AJ (2000) Interaction between metabotropic and ionotropic glutamate receptors regulates neuronal network activity. J Neurosci 50:5382-5391.
26. Kullmann DM, Siegelbaum SA (1995) The site of expression of NMDA receptor-dependent LTP: new fuel for an old fire. Neuron 15:997-1002.
27. Lamsa K, Heeroma JH, Kullmann DM (2005) Hebbian LTP in feed-forward inhibitory interneurons and the temporal fidelity of input discrimination. Nat Neurosci 8:916-924.
28. 2+ levels affect plasticity differently: the LTP zone, the LTD zone and no man's land. J Physiol (Lond) 15:285.
29. Lu W, Man H, Ju W, Trimble WS, MacDonald JF, Wang YT (2001) Activation of synaptic NMDA receptors induces membrane insertion of new AMPA receptors and LTP in cultured hippocampal neurons. Neuron 29:243-254.
30. Lu YM, Mansuy IM, Kandel ER, Roder J (2000) Calcineurin-mediated LTD of GABAergic inhibition underlies the increased excitability of CA1 neurons associated with LTP. Neuron 26:197-205.
31. Lynch G, Larson J, Kelso S, Barrionuevo G, Schottler F (1983) Intracellular injections of EGTA block induction of hippocampal long-term potentiation. Nature 305:719-721.
32. Malenka RC, Nicoll RA (1999) Long-term potentiation-a decade of progress? Science 285:1870-1874.
33. Malinow R, Malenka RC (2002) AMPA receptor trafficking and synaptic plasticity. Annu Rev Neurosci 25:103-126.
34. Malinow R, Tsien RW (1990) Presynaptic enhancement shown by wholecell recordings of long-term potentiation in hippocampal slices. Nature 346:177-180.
35. Markram H, Segal M (1990) Electrophysiological characteristics of cholinergic and non-cholinergic neurons in the rat medial septum-diagonal band complex. Brain Res 513:171-174.
36. Markram H, Lubke J, Frotscher M, Sakmann B (1997) Regulation of synaptic efficacy by coincidence of postsynaptic APs and EPSPs. Science 275:213-215.
37. Mellor J, Nicoll RA (2001) Hippocampal mossy fiber LTP is independent of postsynaptic calcium. Nat Neurosci 4:125-126.
38. Misgeld U, Klee MR, Zeise ML (1994) Differences in baclofen-sensitivity between CA3 neurons and granule cells of the guinea pig hippocampus in vitro. Neurosci Lett 47:307-311.
39. Misgeld U, Bijak M, Jarolimek W (1995) A physiological role for GABAB receptors and the effects of baclofen in the mammalian central nervous system. Prog Neurobiol 46:423-462.
40. Mott DD, Lewis DV (1991) Facilitation of the induction of long-term potentiation by GABAB receptors. Science 252:1718-1720.
41. Neuhoff H, Roeper J, Schweizer M (1999) Activity-dependent formation of perforated synapses in cultured hippocampal neurons. Eur J Neurosci 11:4241-4250.
42. Nicoll RA, Malenka RC (1999) Expression mechanisms underlying NMDA receptor-dependent long-term potentiation. Ann NY Acad Sci 868:515-525.
43. Nowicky AV, Bindman LJ (1993) The nitric oxide synthase inhibitor, N-monomethyl-L-arginine blocks induction of a long-term potentiation-like phenomenon in rat medial frontal cortical neurons in vitro. J Neurophysiol 70:1255-1259.
44. Ohno-Shosaku T, Sawada S, Yamamoto C (1998) Properties of depolarization-induced suppression of inhibitory transmission in cultured rat hippocampal neurons. Pflügers Arch 435:273-279.
45. Ohno-Shosaku T, Sawada S, Kano M (2000) Heterosynaptic expression of depolarization-induced suppression of inhibition (DSI) in rat hippocampal cultures. Neurosci Res 36:67-71.
46. Ohno-Shosaku T, Tsubokawa H, Mizushima I, Yoneda N, Zimmer A, Kano M (2002) Presynaptic cannabinoid sensitivity is a major determinant of depolarization-induced retrograde suppression at hippocampal synapses. J Neurosci 22:3864-3872.
47. Papa M, Bundman MC, Greenberger V, Segal M (1995) Morphological analysis of dendritic spine development in primary cultures of hippocampal neurons. J Neurosci 15:1-11.
48. Parker D, Grillner S (1999) Long-lasting substance-P-mediated modulation of NMDA-induced rhythmic activity in the lamprey locomotor network involves separate RNA- and protein-synthesis-dependent stages. Eur J Neurosci 11:1515-1522.
49. Patenaude C, Chapman CA, Bertrand S, Congar P, Lacaille JC (2003) GABAB receptor- and metabotropic glutamate receptor-dependent cooperative long-term potentiation of rat hippocampal GABAA synaptic transmission. J Physiol (Lond) 15:155-167.
50. 2+ in rat olfactory bulb neurons. Eur J Neurosci 13:92-102.
51. Santschi LA, Stanton PK (2003) A paired-pulse facilitation analysis of long-term synaptic depression at excitatory synapses in rat hippocampal CA1 and CA3 regions. Brain Res 962:78-91.
52. Schulz PE, Cook EP, Johnston D (1994) Changes in paired-pulse facilitation suggest presynaptic involvement in long-term potentiation. J Neurosci 14:5325-5337.
53. 2+ flux during uncorrelated activity. Neuron 44:835-849.
54. Stanton PK, Winterer J, Bailey CP, Kyrozis A, Raginov I, Laube G, Veh RW, Nguyen CQ, Muller W (2003) Long-term depression of presynaptic release from the readily releasable vesicle pool induced by NMDA receptor-dependent retrograde nitric oxide. J Neurosci 23:5936-5944.
55. Taccola G, Marchetti C, Nistri A (2003) Effect of metabotropic glutamate receptor activity on rhythmic discharges of the neonatal rat spinal cord in vitro. Exp Brain Res 153:388-393.
56. Than M, Szabo B (2002) Analysis of the function of GABA(B) receptors on inhibitory afferent neurons of Purkinje cells in the cerebellar cortex of the rat. Eur J Neurosci 15:1575-1584.
57. Voronin LL, Altinbaev RS, Bayazitov IT, Gasparini S, Kasyanov AV, Saviane C, Savtchenko L, Cherubini E (2004) Postsynaptic depolarisation enhances transmitter release and causes the appearance of responses at "silent" synapses in rat hippocampus. Neuroscience 126:45-59.
58. Wagner JJ, Alger BE (1995) GABAergic and developmental influences on homosynaptic LTD and depotentiation in rat hippocampus. J Neurosci 15:1577-1586.
59. 2+ can potentiate and depress mossy fiber synaptic responses in rat hippocampal CA3 pyramidal neurons. J Neurophysiol 91:1596-1607.
60. Wang JH, Stelzer A (1996) Shared calcium signaling pathways in the induction of long-term potentiation and synaptic disinhibition in CA1 pyramidal cell dendrites. J Neurophysiol 75:1687-1702.
61. Williams JH, Errington ML, Lynch MA, Bliss TV (1989) Arachidonic acid induces a long-term activity-dependent enhancement of synaptic transmission in the hippocampus. Nature 341:739-742.
62. Yamamoto C, Chujo T (1978) Long-term potentiation in thin hippocampal sections studied by intracellular and extracellular recordings. Exp Neurol 58:242-250.
63. i elevation. J Neurophysiol 81:781-787.
64. Yanovsky Y, Mades S, Misgeld U (2003) Retrograde signaling changes the venue of postsynaptic inhibition in rat substantia nigra. Neuroscience 122:317-328.
65. Yeckel MF, Kapur A, Johnston D (1999) Multiple forms of LTP in hippocampal CA3 neurons use a common postsynaptic mechanism. Nat Neurosci 2:625-633.
66. Zorumski CF, Izumi Y (1998) Modulation of LTP induction by NMDA receptor activation and nitric oxide release. Prog Brain Res 118:173-182.