Neocortical LTD via coincident activation of presynaptic NMDA and cannabinoid receptors

Neuron

Volumn 39, Issue 4, 2003, Pages 641-654

  Sjöström, Per Jesper ^a   Turrigiano, Gina G ^a   Nelson, Sacha B ^a  

^a BRANDEIS UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CANNABINOID 1 RECEPTOR; CANNABINOID RECEPTOR; N METHYL DEXTRO ASPARTIC ACID;

ARTICLE; CALCIUM TRANSPORT; DEPRESSION; NEOCORTEX; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; SYNAPSE; SYNAPTIC TRANSMISSION;

EID: 0042163180     PISSN: 08966273     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0896-6273(03)00476-8     Document Type: Article

References (84)

1. Abbott L.F., Varela J.A., Sen K., Nelson S.B. Synaptic depression and cortical gain control. Science. 275:1997;220-224.
2. Abbott L.F., Nelson S.B. Synaptic plasticity. taming the beast Nat. Neurosci. 3:2000;1178-1183.
3. Aoki C., Venkatesan C., Go C.G., Mong J.A., Dawson T.M. Cellular and subcellular localization of NMDA-R1 subunit immunoreactivity in the visual cortex of adult and neonatal rats. J. Neurosci. 14:1994;5202-5222.
4. Artola A., Bröcher S., Singer W. Different voltage-dependent thresholds for inducing long-term depression and long-term potentiation in slices of rat visual cortex. Nature. 347:1990;69-72.
5. Auclair N., Otani S., Soubrie P., Crepel F. Cannabinoids modulate synaptic strength and plasticity at glutamatergic synapses of rat prefrontal cortex pyramidal neurons. J. Neurophysiol. 83:2000;3287-3293.
6. Beltramo M., Stella N., Calignano A., Lin S.Y., Makriyannis A., Piomelli D. Functional role of high-affinity anandamide transport, as revealed by selective inhibition. Science. 277:1997;1094-1097.
7. Berretta N., Jones R.S. Tonic facilitation of glutamate release by presynaptic N-methyl-D-aspartate autoreceptors in the entorhinal cortex. Neuroscience. 75:1996;339-344.
8. Bi G.Q., Poo M.M. Synaptic modifications in cultured hippocampal neurons. dependence on spike timing, synaptic strength, and postsynaptic cell type J. Neurosci. 18:1998;10464-10472.
9. Bi G.Q., Poo M.M. Synaptic modification by correlated activity. Hebb's postulate revisited. Annu. Rev. Neurosci. 24:2001;139-166.
10. Bisogno T., Melck D., De Petrocellis L., Bobrov M.Y., Gretskaya N.M., Bezuglov V.V., Sitachitta N., Gerwick W.H., Di Marzo V. Arachidonoylserotonin and other novel inhibitors of fatty acid amide hydrolase. Biochem. Biophys. Res. Commun. 248:1998;515-522.
11. Buonomano D.V. Distinct functional types of associative long-term potentiation in neocortical and hippocampal pyramidal neurons. J. Neurosci. 19:1999;6748-6754.
12. Calabresi P., Maj R., Pisani A., Mercuri N.B., Bernardi G. Long-term synaptic depression in the striatum. physiological and pharmacological characterization J. Neurosci. 12:1992;4224-4233.
13. Carlson G., Wang Y., Alger B.E. Endocannabinoids facilitate the induction of LTP in the hippocampus. Nat. Neurosci. 5:2002;723-724.
14. Casado M., Isope P., Ascher P. Involvement of presynaptic N-methyl-D-aspartate receptors in cerebellar long-term depression. Neuron. 33:2002;123-130.
15. Charton J.P., Herkert M., Becker C.M., Schröder H. Cellular and subcellular localization of the 2B-subunit of the NMDA receptor in the adult rat telencephalon. Brain Res. 816:1999;609-617.
16. Chevaleyre V., Castillo P.E. Heterosynaptic LTD of hippocampal GABAergic synapses. a novel role of endocannabinoids in regulating excitability Neuron. 38:2003;461-472.
17. Cline H.T. Topographic maps. developing roles of synaptic plasticity Curr. Biol. 8:1998;R836-R839.
18. Debanne D., Gähwiler B.H., Thompson S.M. Asynchronous pre- and postsynaptic activity induces associative long-term depression in area CA1 of the rat hippocampus in vitro. Proc. Natl. Acad. Sci. USA. 91:1994;1148-1152.
19. Debanne D., Gähwiler B.H., Thompson S.M. Long-term synaptic plasticity between pairs of individual CA3 pyramidal cells in rat hippocampal slice cultures. J. Physiol. 507:1998;237-247.
20. DeBiasi S., Minelli A., Melone M., Conti F. Presynaptic NMDA receptors in the neocortex are both auto- and heteroreceptors. Neuroreport. 7:1996;2773-2776.
21. Di Marzo V., Fontana A., Cadas H., Schinelli S., Cimino G., Schwartz J.C., Piomelli D. Formation and inactivation of endogenous cannabinoid anandamide in central neurons. Nature. 372:1994;686-691.
22. Dittman J.S., Regehr W.G. Calcium dependence and recovery kinetics of presynaptic depression at the climbing fiber to Purkinje cell synapse. J. Neurosci. 18:1998;6147-6162.
23. Dudek S.M., Bear M.F. Homosynaptic long-term depression in area CA1 of hippocampus and effects of N-methyl-D-aspartate receptor blockade. Proc. Natl. Acad. Sci. USA. 89:1992;4363-4367.
24. Egger V., Feldmeyer D., Sakmann B. Coincidence detection and changes of synaptic efficacy in spiny stellate neurons in rat barrel cortex. Nat. Neurosci. 2:1999;1098-1105.
25. Engert F., Bonhoeffer T. Synapse specificity of long-term potentiation breaks down at short distances. Nature. 388:1997;279-284.
26. Faber D.S., Korn H. Applicability of the coefficient of variation method for analyzing synaptic plasticity. Biophys. J. 60:1991;1288-1294.
27. Feldman D.E. Timing-based LTP and LTD at vertical inputs to layer II/III pyramidal cells in rat barrel cortex. Neuron. 27:2000;45-56.
28. 1 receptors Eur. J. Pharmacol. 307:1996;331-338.
29. Gerdeman G.L., Ronesi J., Lovinger D.M. Postsynaptic endocannabinoid release is critical to long-term depression in the striatum. Nat. Neurosci. 5:2002;446-451.
30. Glitsch M., Marty A. Presynaptic effects of NMDA in cerebellar Purkinje cells and interneurons. J. Neurosci. 19:1999;511-519.
31. Hillard C.J. Biochemistry and pharmacology of the endocannabinoids arachidonylethanolamide and 2-arachidonylglycerol. Prostaglandins Other Lipid Mediat. 61:2000;3-18.
32. Hillard C.J., Manna S., Greenberg M.J., DiCamelli R., Ross R.A., Stevenson L.A., Murphy V., Pertwee R.G., Campbell W.B. Synthesis and characterization of potent and selective agonists of the neuronal cannabinoid receptor (CB1). J. Pharmacol. Exp. Ther. 289:1999;1427-1433.
33. Kemp N., McQueen J., Faulkes S., Bashir Z.I. Different forms of LTD in the CA1 region of the hippocampus. role of age and stimulus protocol Eur. J. Neurosci. 12:2000;360-366.
34. Klingauf J., Kavalali E.T., Tsien R.W. Kinetics and regulation of fast endocytosis at hippocampal synapses. Nature. 394:1998;581-585.
35. Koester H.J., Sakmann B. Calcium dynamics in single spines during coincident pre- and postsynaptic activity depend on relative timing of back-propagating action potentials and subthreshold excitatory postsynaptic potentials. Proc. Natl. Acad. Sci. USA. 95:1998;9596-9601.
36. Kreitzer A.C., Regehr W.G. Retrograde inhibition of presynaptic calcium influx by endogenous cannabinoids at excitatory synapses onto Purkinje cells. Neuron. 29:2001;717-727.
37. Kreitzer A.C., Regehr W.G. Retrograde signaling by endocannabinoids. Curr. Opin. Neurobiol. 12:2002;324-330.
38. Kreitzer A.C., Carter A.G., Regehr W.G. Inhibition of interneuron firing extends the spread of endocannabinoid signaling in the cerebellum. Neuron. 34:2002;787-796.
39. Larkman A., Hannay T., Stratford K., Jack J. Presynaptic release probability influences the locus of long-term potentiation. Nature. 360:1992;70-73.
40. Legendre P., Rosenmund C., Westbrook G.L. Inactivation of NMDA channels in cultured hippocampal neurons by intracellular calcium. J. Neurosci. 13:1993;674-684.
41. Levy W.B., Steward O. Temporal contiguity requirements for long-term associative potentiation/depression in the hippocampus. Neuroscience. 8:1983;791-797.
42. Linden D.J., Connor J.A. Long-term synaptic depression. Annu. Rev. Neurosci. 18:1995;319-357.
43. Liu H., Mantyh P.W., Basbaum A.I. NMDA-receptor regulation of substance P release from primary afferent nociceptors. Nature. 386:1997;721-724.
44. MacDermott A.B., Role L.W., Siegelbaum S.A. Presynaptic ionotropic receptors and the control of transmitter release. Annu. Rev. Neurosci. 22:1999;443-485.
45. Magee J.C., Johnston D. A synaptically controlled, associative signal for Hebbian plasticity in hippocampal neurons. Science. 275:1997;209-213.
46. Malenka R.C., Nicoll R.A. Long-term potentiation - a decade of progress? Science. 285:1999;1870-1874.
47. Markram H., Tsodyks M. Redistribution of synaptic efficacy between neocortical pyramidal neurons. Nature. 382:1996;807-810.
48. Markram H., Lübke J., Frotscher M., Roth A., Sakmann B. Physiology and anatomy of synaptic connections between thick tufted pyramidal neurones in the developing rat neocortex. J. Physiol. 500:1997;409-440. a.
49. Markram H., Lübke J., Frotscher M., Sakmann B. Regulation of synaptic efficacy by coincidence of postsynaptic APs and EPSPs. Science. 275:1997;213-215. b.
50. Marsicano G., Wotjak C.T., Azad S.C., Bisogno T., Rammes G., Cascio M.G., Hermann H., Tang J., Hofmann C., Zieglgänsberger W.et al. The endogenous cannabinoid system controls extinction of aversive memories. Nature. 418:2002;530-534.
51. Medina I., Filippova N., Bakhramov A., Bregestovski P. Calcium-induced inactivation of NMDA receptor-channels evolves independently of run-down in cultured rat brain neurons. J. Physiol. 495:1996;411-427.
52. Misner D.L., Sullivan J.M. Mechanism of cannabinoid effects on long-term potentiation and depression in hippocampal CA1 neurons. J. Neurosci. 19:1999;6795-6805.
53. Mulkey R.M., Malenka R.C. Mechanisms underlying induction of homosynaptic long-term depression in area CA1 of the hippocampus. Neuron. 9:1992;967-975.
54. Nedergaard M., Takano T., Hansen A.J. Beyond the role of glutamate as a neurotransmitter. Nat. Rev. Neurosci. 3:2002;748-755.
55. Nishiyama M., Hong K., Mikoshiba K., Poo M.M., Kato K. Calcium stores regulate the polarity and input specificity of synaptic modification. Nature. 408:2000;584-588.
56. Oliet S.H., Malenka R.C., Nicoll R.A. Two distinct forms of long-term depression coexist in CA1 hippocampal pyramidal cells. Neuron. 18:1997;969-982.
57. Ong W.Y., Mackie K. A light and electron microscopic study of the CB1 cannabinoid receptor in primate brain. Neuroscience. 92:1999;1177-1191.
58. Otmakhov N., Shirke A.M., Malinow R. Measuring the impact of probabilistic transmission on neuronal output. Neuron. 10:1993;1101-1111.
59. Pananceau M., Chen H., Gustafsson B. Short-term facilitation evoked during brief afferent tetani is not altered by long-term potentiation in the guinea-pig hippocampal CA1 region. J. Physiol. 508:1998;503-514.
60. Partridge J.G., Tang K.C., Lovinger D.M. Regional and postnatal heterogeneity of activity-dependent long-term changes in synaptic efficacy in the dorsal striatum. J. Neurophysiol. 84:2000;1422-1429.
61. A responses in hippocampal pyramidal cells. J. Neurosci. 12:1992;4122-4132.
62. Poncer J.C., Malinow R. Postsynaptic conversion of silent synapses during LTP affects synaptic gain and transmission dynamics. Nat. Neurosci. 4:2001;989-996.
63. Robbe D., Kopf M., Remaury A., Bockaert J., Manzoni O.J. Endogenous cannabinoids mediate long-term synaptic depression in the nucleus accumbens. Proc. Natl. Acad. Sci. USA. 99:2002;8384-8388.
64. Sawtell N.B., Huber K.M., Roder J.C., Bear M.F. Induction of NMDA receptor-dependent long-term depression in visual cortex does not require metabotropic glutamate receptors. J. Neurophysiol. 82:1999;3594-3597.
65. Schuman E.M., Madison D.V. Locally distributed synaptic potentiation in the hippocampus. Science. 263:1994;532-536.
66. Selig D.K., Nicoll R.A., Malenka R.C. Hippocampal long-term potentiation preserves the fidelity of postsynaptic responses to presynaptic bursts. J. Neurosci. 19:1999;1236-1246.
67. Sheng M., Cummings J., Roldan L.A., Jan Y.N., Jan L.Y. Changing subunit composition of heteromeric NMDA receptors during development of rat cortex. Nature. 368:1994;144-147.
68. Sjöström P.J., Turrigiano G.G., Nelson S.B. Rate, timing, and cooperativity jointly determine cortical synaptic plasticity. Neuron. 32:2001;1149-1164.
69. Solowij N. Cannabis and Cognitive Functioning. 1998;Cambridge University Press, London.
70. Stocca G., Vicini S. Increased contribution of NR2A subunit to synaptic NMDA receptors in developing rat cortical neurons. J. Physiol. 507:1998;13-24.
71. Sullivan J.M. Mechanisms of cannabinoid-receptor-mediated inhibition of synaptic transmission in cultured hippocampal pyramidal neurons. J. Neurophysiol. 82:1999;1286-1294.
72. Tao H.W., Poo M. Retrograde signaling at central synapses. Proc. Natl. Acad. Sci. USA. 98:2001;11009-11015.
73. Trettel J., Levine E.S. Endocannabinoids mediate rapid retrograde signaling at interneuron right-arrow pyramidal neuron synapses of the neocortex. J. Neurophysiol. 89:2003;2334-2338.
74. Tsodyks M.V., Markram H. The neural code between neocortical pyramidal neurons depends on neurotransmitter release probability. Proc. Natl. Acad. Sci. USA. 94:1997;719-723.
75. Turrigiano G.G., Leslie K.R., Desai N.S., Rutherford L.C., Nelson S.B. Activity-dependent scaling of quantal amplitude in neocortical neurons. Nature. 391:1998;892-896.
76. Wang Y.T., Linden D.J. Expression of cerebellar long-term depression requires postsynaptic clathrin-mediated endocytosis. Neuron. 25:2000;635-647.
77. Williams K. Ifenprodil discriminates subtypes of the N-methyl-D-aspartate receptor. selectivity and mechanisms at recombinant heteromeric receptors Mol. Pharmacol. 44:1993;851-859.
78. Williams K., Russell S.L., Shen Y.M., Molinoff P.B. Developmental switch in the expression of NMDA receptors occurs in vivo and in vitro. Neuron. 10:1993;267-278.
79. Wilson R.I., Nicoll R.A. Endogenous cannabinoids mediate retrograde signalling at hippocampal synapses. Nature. 410:2001;588-592.
80. Wilson R.I., Nicoll R.A. Endocannabinoid signaling in the brain. Science. 296:2002;678-682.
81. Woodhall G., Evans D.I., Cunningham M.O., Jones R.S. NR2B-containing NMDA autoreceptors at synapses on entorhinal cortical neurons. J. Neurophysiol. 86:2001;1644-1651.
82. Zakharenko S., Zablow L., Siegelbaum S. Altered presynaptic vesicle release and cycling during mGluR-dependent LTD. Neuron. 35:2002;1099-1100.
83. Zhang L.I., Tao H.W., Holt C.E., Harris W.A., Poo M. A critical window for cooperation and competition among developing retinotectal synapses. Nature. 395:1998;37-44.
84. Zucker R.S., Regehr W.G. Short-term synaptic plasticity. Annu. Rev. Physiol. 64:2002;355-405.