Coincidence detection and stress modulation of spike time-dependent long-term depression in the hippocampus

Journal of Neuroscience

Volumn 30, Issue 18, 2010, Pages 6225-6235

  Niehusmann, Pitt ^a,c   Seifert, Gabriel ^a   Clark, Kristin ^a   Atas, Hasan C ^a   Herpfer, Inga ^a   Fiebich, Bernd ^a   Bischofberger, Josef ^a,b   Normann, Claus ^a  

^a UNIVERSITY OF FREIBURG   (Germany)

^b UNIVERSITY OF BASEL   (Switzerland)

^c UNIVERSITY OF BONN   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

AMPA RECEPTOR; INOSITOL 1,4,5 TRISPHOSPHATE; LITHIUM; METABOTROPIC RECEPTOR 1; METABOTROPIC RECEPTOR 5; PHORBOL ESTER; PHOSPHOLIPASE C; PROTEIN INTERACTING WITH PROTEIN KINASE C;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BEHAVIORAL STRESS; CONTROLLED STUDY; ENDOCYTOSIS; ENZYME PHOSPHORYLATION; HIPPOCAMPUS; LONG TERM DEPRESSION; NONHUMAN; PDZ DOMAIN; POSTSYNAPTIC MEMBRANE; PRESYNAPTIC NERVE; PRIORITY JOURNAL; RAT; SPIKE; STRESS; TIME;

ANIMALS; EXCITATORY POSTSYNAPTIC POTENTIALS; HIPPOCAMPUS; INOSITOL 1,4,5-TRISPHOSPHATE; LITHIUM COMPOUNDS; LONG-TERM SYNAPTIC DEPRESSION; MEMBRANE POTENTIALS; PDZ DOMAINS; PHORBOL ESTERS; PHOSPHORYLATION; PROTEIN KINASE C; RATS; RATS, WISTAR; RECEPTORS, METABOTROPIC GLUTAMATE; SIGNAL TRANSDUCTION; STRESS, PSYCHOLOGICAL; TIME FACTORS; TYPE C PHOSPHOLIPASES;

EID: 77951785040     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.6411-09.2010     Document Type: Article

References (67)

1. Bender VA, Bender KJ, Brasier DJ, Feldman DE (2006) Two coincidence detectors for spike timing-dependent plasticity in somatosensory cortex. J Neurosci 26:4166-4177.
2. Berthele A, Laurie DJ, Platzer S, Zieglgänsberger W, Tölle TR, Sommer B (1998) Differential expression of rat and human type I metabotropic glutamate receptor splice variant messenger RNAs. Neuroscience 85:733-749. (Pubitemid 28223636)
3. Birnbaum SG, Yuan PX, Wang M, Vijayraghavan S, Bloom AK, Davis DJ, Gobeske KT, Sweatt JD, Manji HK, Arnsten AF (2004) Protein kinase C overactivity impairs prefrontal cortical regulation of working memory. Science 306:882-884. (Pubitemid 39446999)
4. Bitran JA, Manji HK, Potter WZ, Gusovsky F (1995) Down-regulation of PKC alpha by lithium in vitro. Psychopharmacol Bull 31:449-452.
5. Blümcke I, Behle K, Malitschek B, Kuhn R, Knöpfel T, Wolf HK, Wiestler OD (1996) Immunohistochemical distribution of metabotropic glutamate receptor subtypes mGluR1b, mGluR2/3, mGluR4a and mGluR5 in human hippocampus. Brain Res 736:217-226. (Pubitemid 26356479)
6. Bolshakov VY, Siegelbaum SA (1994) Postsynaptic induction and presynaptic expression of hippocampal long-term depression. Science 264:1148-1152. (Pubitemid 24985536)
7. Bortolotto ZA, Collingridge GL (2000) A role for protein kinase C in a form of metaplasticity that regulates the induction of long-term potentiation at CA1 synapses of the adult rat hippocampus. Eur J Neurosci 12:4055-4062.
8. Bredt DS, Nicoll RA (2003) AMPA receptor trafficking at excitatory synapses. Neuron 40:361-379. (Pubitemid 37244101)
9. Castrén E (2005) Is mood chemistry? Nat Rev Neurosci 6:241-246.
10. Chameau P, Qin Y, Spijker S, Smit G, Joëls M (2007) Glucocorticoids specifically enhance L-type calcium current amplitude and affect calcium channel subunit expression in the mouse hippocampus. J Neurophysiol 97:5-14. (Pubitemid 46143335)
11. Chen G, Rajkowska G, Du F, Seraji-Bozorgzad N, Manji HK (2000) Enhancement of hippocampal neurogenesis by lithium. J Neurochem 75:1729-1734.
12. Dan Y, Poo MM (2006) Spike timing-dependent plasticity: from synapse to perception. Physiol Rev 86:1033-1048. (Pubitemid 44033388)
13. Daw MI, Chittajallu R, Bortolotto ZA, Dev KK, Duprat F, Henley JM, Collingridge GL, Isaac JT (2000) PDZ proteins interacting with C-terminal GluR2/3 are involved in a PKC-dependent regulation of AMPA receptors at hippocampal synapses. Neuron 28:873-886. (Pubitemid 32038078)
14. Faas GC, Adwanikar H, Gereau RW 4th, Saggau P (2002) Modulation of presynaptic calcium transients by metabotropic glutamate receptor activation: a differential role in acute depression of synaptic transmission and long-term depression. J Neurosci 22:6885-6890. (Pubitemid 35379146)
15. Fang X, Yu SX, Lu Y, Bast RC Jr, Woodgett JR, Mills GB (2000) Phosphorylation and inactivation of glycogen synthase kinase 3 by protein kinase A. Proc Natl Acad Sci U S A 97:11960-11965.
16. Ferraguti F, Conquet F, Corti C, Grandes P, Kuhn R, Knopfel T (1998) Immunohistochemical localization of the mGluR1beta metabotropic glutamate receptor in the adult rodent forebrain: evidence for a differential distribution of mGluR1 splice variants. J Comp Neurol 400:391-407. (Pubitemid 28447098)
17. Fotuhi M, Standaert DG, Testa CM, Penney JB Jr, Young AB (1994) Differential expression of metabotropic glutamate receptors in the hippocampus and entorhinal cortex of the rat. Brain Res Mol Brain Res 21:283-292. (Pubitemid 24038496)
18. Goode N, Hughes K, Woodgett JR, Parker PJ (1992) Differential regulation of glycogen synthase kinase-3 beta by protein kinase C isotypes. J Biol Chem 267:16878-16882.
19. Hanley JG, Henley JM (2005) PICK1 is a calcium-sensor for NMDA-induced AMPA receptor trafficking. EMBO J 24:3266-3278. (Pubitemid 41348701)
20. Hernández F, Borrell J, Guaza C, Avila J, Lucas JJ (2002) Spatial learning deficit in transgenic mice that conditionally over-express GSK-3beta in the brain but do not form tau filaments. J Neurochem 83:1529-1533. (Pubitemid 35477491)
21. Higashitani Y, Kudo Y, Ogura A, Kato H (1990) Acute effects of lithium on synaptic transmission in rat hippocampus studied in vitro. Biol Psychiatry 27:174-182. (Pubitemid 20033765)
22. Holderbach R, Clark K, Moreau JL, Bischofberger J, Normann C (2007) Enhanced long-term synaptic depression in an animal model of depression. Biol Psychiatry 62:92-100. (Pubitemid 46898221)
23. Hooper C, Markevich V, Plattner F, Killick R, Schofield E, Engel T, Hernandez F, Anderton B, Rosenblum K, Bliss T, Cooke SF, Avila J, Lucas JJ, Giese KP, Stephenson J, Lovestone S (2007) Glycogen synthase kinase-3 inhibition is integral to long-term potentiation. Eur J Neurosci 25:81-86.
24. Hori T, Takai Y, Takahashi T (1999) Presynaptic mechanism for phorbol ester-induced synaptic potentiation. J Neurosci 19:7262-7267.
25. House C, Kemp BE (1987) Protein kinase C contains a pseudosubstrate prototope in its regulatory domain. Science 238:1726-1728.
26. Huang CC, Hsu KS (2006) Sustained activation of metabotropic glutamate receptor 5 and protein tyrosine phosphatases mediate the expression of (S)-3,5-dihydroxyphenylglycine-induced long-term depression in the hippocampal CA1 region. J Neurochem 96:179-194.
27. Huber KM, Kayser MS, Bear MF (2000) Role for rapid dendritic protein synthesis in hippocampal mGluR-dependent long-term depression. Science 288:1254-1257.
28. Huber KM, Roder JC, Bear MF (2001) Chemical induction of mGluR5-and protein synthesis-dependent long-term depression in hippocampal area CA1. J Neurophysiol 86:321-325.
29. Ireland DR, Abraham WC (2009) Mechanisms of group I mGluR-dependent long-term depression of NMDA receptor-mediated transmission at Schaffer collateral-CA1 synapses. J Neurophysiol 101:1375-1385.
30. Isaac JT, Ashby M, McBain CJ (2007) The role of the GluR2 subunit in AMPA receptor function and synaptic plasticity. Neuron 54:859-871.
31. Jo J, Heon S, Kim MJ, Son GH, Park Y, Henley JM, Weiss JL, Sheng M, Collingridge GL, Cho K (2008) Metabotropic glutamate receptormediated LTD involves two interacting Ca(2+) sensors, NCS-1 and PICK1. Neuron 60:1095-1111.
32. Karmarkar UR, Buonomano DV (2002) A model of spike-timing dependent plasticity: one or two coincidence detectors? J Neurophysiol 88:507-513.
33. Kerner JA, Standaert DG, Penney JB Jr, Young AB, Landwehrmeyer GB (1997) Expression of group one metabotropic glutamate receptor subunit mRNAs in neurochemically identified neurons in the rat neostriatum, neocortex, and hippocampus. Brain Res Mol Brain Res 48:259-269.
34. Kim CH, Chung HJ, Lee HK, Huganir RL (2001) Interaction of the AMPA receptor subunit GluR2/3 with PDZ domains regulates hippocampal long-term depression. Proc Natl Acad Sci U S A 98:11725-11730.
35. Klein PS, Melton DA (1996) A molecular mechanism for the effect of lithium on development. Proc Natl Acad Sci U S A 93:8455-8459.
36. Lisman J (1989) A mechanism for the Hebb and the anti-Hebb processes underlying learning and memory. Proc Natl Acad Sci U S A 86:9574-9578.
37. Lujan R, Nusser Z, Roberts JD, 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.
38. Manji HK, Etcheberrigaray R, Chen G, Olds JL (1993) Lithium decreases membrane-associated protein kinase C in hippocampus: selectivity for the alpha isozyme. J Neurochem 61:2303-2310.
39. Manji HK, Bersudsky Y, Chen G, Belmaker RH, Potter WZ (1996) Modulation of protein kinase C isozymes and substrates by lithium: the role of myo-inositol. Neuropsychopharmacology 15:370-381.
40. Mannaioni G, Marino MJ, Valenti O, Traynelis SF, Conn PJ (2001) Metabotropic glutamate receptors 1 and 5 differentially regulate CA1 pyramidal cell function. J Neurosci 21:5925-5934.
41. Masukawa K, Sakai N, Ohmori S, Shirai Y, Saito N (2006) Spatiotemporal analysis of the molecular interaction between PICK1 and PKC. Acta Histochem Cytochem 39:173-181.
42. 2+ signaling in spike-timing-dependent plasticity. J Neurosci 26:11001-11013.
43. 2+ channels. J Neurosci 20:8290-8297.
44. Normann C, Schmitz D, Fürmaier A, Döing C, Bach M (2007) Long-term plasticity of visually evoked potentials in humans is altered in major depression. Biol Psychiatry 62:373-380.
45. Oliet SH, Malenka RC, Nicoll RA (1997) Two distinct forms of long-term depression coexist in CA1 hippocampal pyramidal cells. Neuron 18:969-982.
46. Peineau S, Taghibiglou C, Bradley C, Wong TP, Liu L, Lu J, Lo E,WuD, Saule E, Bouschet T, Matthews P, Isaac JT, Bortolotto ZA, Wang YT, Collingridge GL (2007) LTP inhibits LTD in the hippocampus via regulation of GSK3beta. Neuron 53:703-717.
47. Peineau S, Bradley C, Taghibiglou C, Doherty A, Bortolotto ZA, Wang YT, Collingridge GL (2008) The role of GSK-3 in synaptic plasticity. Br J Pharmacol 153 [Suppl 1]:S428-S437.
48. Perez JL, Khatri L, Chang C, Srivastava S, Osten P, Ziff EB (2001) PICK1 targets activated protein kinase Calpha to AMPA receptor clusters in spines of hippocampal neurons and reduces surface levels of the AMPA-type glutamate receptor subunit 2. J Neurosci 21:5417-5428.
49. Rhee JS, Betz A, Pyott S, Reim K, Varoqueaux F, Augustin I, Hesse D, Südhof TC, Takahashi M, Rosenmund C, Brose N (2002) Beta phorbol esterand diacylglycerol-induced augmentation of transmitter release is mediated by Munc13s and not by PKCs. Cell 108:121-133.
50. Romano C, Sesma MA, McDonald CT, O'Malley K, Van den Pol AN, Olney JW (1995) Distribution of metabotropic glutamate receptor mGluR5 immunoreactivity in rat brain. J Comp Neurol 355:455-469.
51. Schmidt-Hieber C, Jonas P, Bischofberger J (2004) Enhanced synaptic plasticity in newly generated granule cells of the adult hippocampus. Nature 429:184-187.
52. Seidenman KJ, Steinberg JP, Huganir R, Malinow R (2003) Glutamate receptor subunit 2 Serine 880 phosphorylation modulates synaptic transmission and mediates plasticity in CA1 pyramidal cells. J Neurosci 23:9220-9228.
53. Selig DK, Lee HK, Bear MF, Malenka RC (1995) Reexamination of the effects of MCPG on hippocampal LTP, LTD, and depotentiation. J Neurophysiol 74:1075-1082.
54. Shigemoto R, Nakanishi S, Mizuno N (1992) Distribution of the mRNA for a metabotropic glutamate receptor (mGluR1) in the central nervous system: an in situ hybridization study in adult and developing rat. J Comp Neurol 322:121-135.
55. Shors TJ, Thompson RF (1992) Acute stress impairs (or induces) synaptic long-term potentiation (LTP) but does not affect paired-pulse facilitation in the stratum radiatum of rat hippocampus. Synapse 11:262-265.
56. Shors TJ, Seib TB, Levine S, Thompson RF (1989) Inescapable versus escapable shock modulates long-term potentiation in the rat hippocampus. Science 244:224-226.
57. Stanton PK (1995) Transient protein kinase C activation primes long-term depression and suppresses long-term potentiation of synaptic transmission in hippocampus. Proc Natl Acad Sci U S A 92:1724-1728.
58. Terashima A, Pelkey KA, Rah JC, Suh YH, Roche KW, Collingridge GL, McBain CJ, Isaac JT (2008) An essential role for PICK1 in NMDA receptor-dependent bidirectional synaptic plasticity. Neuron 57:872-882.
59. Valenti O, Conn PJ, Marino MJ (2002) Distinct physiological roles of the Gq-coupled metabotropic glutamate receptors co-expressed in the same neuronal populations. J Cell Physiol 191:125-137.
60. Volk LJ, Daly CA, Huber KM (2006) Differential roles for group 1 mGluR subtypes in induction and expression of chemically induced hippocampal long-term depression. J Neurophysiol 95:2427-2438.
61. Wang HY, Friedman E (1989) Lithium inhibition of protein kinase C activation-induced serotonin release. Psychopharmacology (Berl) 99:213-218.
62. Wang HY, Johnson GP, Friedman E (2001) Lithium treatment inhibits protein kinase C translocation in rat brain cortex. Psychopharmacology (Berl) 158:80-86.
63. Wang JH, Feng DP (1992) Postsynaptic protein kinase C essential to induction and maintenance of long-term potentiation in the hippocampal CA1 region. Proc Natl Acad Sci U S A 89:2576-2580.
64. Wierda KD, Toonen RF, de Wit H, Brussaard AB, VerhageM (2007) Interdependence of PKC-dependent and PKC-independent pathways for presynaptic plasticity. Neuron 54:275-290.
65. Wood GE, Young LT, Reagan LP, Chen B, McEwen BS (2004) Stress-induced structural remodeling in hippocampus: prevention by lithium treatment. Proc Natl Acad Sci U S A 101:3973-3978.
66. Xu L, Holscher C, Anwyl R, Rowan MJ (1998) Glucocorticoid receptor and protein/RNA synthesis-dependent mechanisms underlie the control of synaptic plasticity by stress. Proc Natl Acad Sci U S A 95:3204-3208.
67. Yang CH, Huang CC, Hsu KS (2004) Behavioral stress modifies hippocampal synaptic plasticity through corticosterone-induced sustained extracellular signal-regulated kinase/mitogen-activated protein kinase activation. J Neurosci 24:11029-11034.