Presynaptic Spike Timing-Dependent Long-Term Depression in the Mouse Hippocampus

Cerebral Cortex

Volumn 26, Issue 8, 2016, Pages 3637-3654

  Andrade Talavera, Yuniesky ^a   Duque Feria, Paloma ^a   Paulsen, Ole ^b   Rodríguez Moreno, Antonio ^a  

^a UNIVERSIDAD PABLO DE OLAVIDE   (Spain)

^b UNIVERSITY OF CAMBRIDGE   (United Kingdom)

Author keywords

hippocampus; NMDA receptor; spike timing dependent plasticity; t LTD; t LTP

Indexed keywords

CALCINEURIN; CALCIUM; CANNABINOID 1 RECEPTOR; DIZOCILPINE; ENDOCANNABINOID; GLUTAMATE RECEPTOR; INOSITOL TRISPHOSPHATE; IONOTROPIC RECEPTOR; METABOTROPIC RECEPTOR; N METHYL DEXTRO ASPARTIC ACID RECEPTOR 2A; N METHYL DEXTRO ASPARTIC ACID RECEPTOR 2B; N METHYL DEXTRO ASPARTIC ACID RECEPTOR 2C; N METHYL DEXTRO ASPARTIC ACID RECEPTOR 2D; N METHYL DEXTRO ASPARTIC ACID RECEPTOR BLOCKING AGENT; PHOSPHOLIPASE C; POSTSYNAPTIC RECEPTOR; SERINE; AGENTS INTERACTING WITH TRANSMITTER, HORMONE OR DRUG RECEPTORS; CNR1 PROTEIN, MOUSE; DIVALENT CATION; N METHYL DEXTRO ASPARTIC ACID RECEPTOR;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; ASTROCYTE; CALCIUM TRANSPORT; CONTROLLED STUDY; HIPPOCAMPAL CA1 REGION; HIPPOCAMPAL CA3 REGION; HIPPOCAMPUS; INTRACELLULAR SIGNALING; LONG TERM DEPRESSION; LONG TERM POTENTIATION; MOUSE; NERVE CELL PLASTICITY; NEUROTRANSMITTER RELEASE; NONHUMAN; POSTSYNAPTIC POTENTIAL; PRESYNAPTIC NERVE; PRIORITY JOURNAL; RECEPTOR UPREGULATION; SPIKE; ACTION POTENTIAL; ANIMAL; ANTAGONISTS AND INHIBITORS; C57BL MOUSE; DRUG EFFECTS; METABOLISM; NERVE ENDING; PATCH CLAMP TECHNIQUE; PHYSIOLOGY; TIME FACTOR; TISSUE CULTURE TECHNIQUE;

ACTION POTENTIALS; ANIMALS; ASTROCYTES; CA1 REGION, HIPPOCAMPAL; CA3 REGION, HIPPOCAMPAL; CALCINEURIN; CALCIUM; CATIONS, DIVALENT; ENDOCANNABINOIDS; LONG-TERM POTENTIATION; LONG-TERM SYNAPTIC DEPRESSION; MICE, INBRED C57BL; NEUROTRANSMITTER AGENTS; PATCH-CLAMP TECHNIQUES; PRESYNAPTIC TERMINALS; RECEPTOR, CANNABINOID, CB1; RECEPTORS, N-METHYL-D-ASPARTATE; SERINE; TIME FACTORS; TISSUE CULTURE TECHNIQUES;

EID: 84981275643     PISSN: 10473211     EISSN: 14602199     Source Type: Journal    
DOI: 10.1093/cercor/bhw172     Document Type: Article

References (122)

1. Alger BE. 2002. Retrograde signalling in the regulation of synaptic transmission: focus on endocannabinoids. Prog Neurobiol. 68:247-286.
2. Andersson M, Blomstand F, Hanse E. 2007. Astrocytes play a critical role in transient heterosynaptic depression in the rat hippocampal CA1 region. J Physiol. 585:843-855.
3. Anwyl R. 1999. Metabotropic glutamate receptors: electrophysiological properties and role in plasticity. Brain Res Rev. 29:83-120.
4. Araque A, Carmignoto G, Haydon PG, Oliet SH, Robitaille R, Volterra A. 2014. Gliotransmitters travel in time and space. Neuron. 81:728-739.
5. Auberson YP, Allegier H, Bischoff S, Lingenhoehl K, Moretti R, Schmutz M. 2002. 5-Phosphonomethylquinoxalinediones as competitive NMDA receptor antagonists with a preference for the human 1A/2A, rather 1A/2B receptor composition. Bioorg Med Chem Lett. 12:1099-1102.
6. Auclair N, Otani S, Soubrie P, Crepel F. 2000. Cannabinoids modulate synaptic strength and plasticity at glutamatergic synapses of rat prefrontal cortex pyramidal neurons. J Neurophysiol. 83:3287-3293.
7. Babiec WE, Guglietta R, Jami SA, Morishita W, Malenka RC, O'Dell TJ. 2014. Ionotropic NMDA receptor signaling is required for the induction of long-term depression in the mouse hippocampal CA1 region. J Neurosci. 34:5285-5290.
8. Banerjee A, Larsen RS, Philpot BD, Paulsen O. 2016. Roles of presynaptic NMDA receptors in neurotransmission and plasticity. Trends Neurosci. 39:26-39.
9. Banerjee A, Meredith RM, Rodríguez-Moreno A, Mierau SB, Auberson YP, Paulsen O. 2009. Double dissociation of spike timing-dependent potentiation and depression by subunitpreferring NMDA receptors antagonists in mouse barrel cortex. Cereb Cortex. 19:2959-2969.
10. Bender VA, Bender KJ, Brasier DJ, Feldman DE. 2006. Two coincidence detectors for spike timing-dependent plasticity in somatosensory cortex. J Neurosci. 16:4166-4177.
11. Berberich S, Punnakal P, Jensen V, Pawlak V, Seeburg PH, Hvalby Ø, Köhr G. 2005. Lack of NMD Areceptor subtype selectivity for hippocampal long-term potentiation. J Neurosci. 25:6907-6910.
12. Berridge MJ. 1998. Neuronal calcium signalling. Neuron. 21:13-26.
13. Bi G-Q, Poo M-M. 1998. Synaptic modifications in cultured hippocampal neurons: dependence on spike timing, synaptic strength, and postsynaptic cell type. J Neurosci. 18:10464-10472.
14. Bidoret C, Ayon A, Barbour B, Casado M. 2009. Presynaptic NR2Acontaining NMDA receptors implement a high-pass filter synaptic plasticity rule. Proc Natl Acad Sci USA. 106:14126-14131.
15. Bliss TV, Collingridge GL. 1993. A synaptic model of memory: long-term potentiation in the hippocampus. Nature. 361:31-39.
16. Blum KI, Abbott LF. 1996. A model of spatial map formation in the hippocampus of the rat. Neural Comput. 8:85-93.
17. Brasier DJ, Feldman DE. 2008. Synapse-specific expression of functional presynaptic NMDA receptors in rat somatosensory cortex. J Neurosci. 28:2199-2211.
18. Buchanan KA, Mellor JR. 2007. The development of synaptic plasticity induction rules and the requirement for postsynaptic spikes in rat hippocampal CA1 pyramidal neurones. J Neurosci. 585:429-445.
19. Bush D, Philippides A, Husbands P, O'Shea M. 2010. Spike timingdependent plasticity and the cognitive map. Front Comput Neurosci. 4:142.
20. Bykhovskaia M. 2011. Synapsin regulation of vesicle organization and functional pools. Semin Cell Dev Biol. 22:387-392.
21. Cajal SR. 1894. The Croonian Lecture: La fine structure des centres nerveux. Proc R Soc Lond. 55:444-468.
22. Campanac E, Debanne D. 2008. Spike timing-dependent plasticity: a learning rule for dendritic integration in rat CA1 pyramidal neurons. J Physiol. 586:779-793.
23. Caporale N, Dan Y. 2008. Spike timing-dependent plasticity: a Hebbian learning rule. Annu Rev Neurosci. 31:25-46.
24. Carlisle HJ, Fink AE, Grant SG, O'Dell TJ. 2008. Opposing effects of PSD-93 and PSD-95 on long-term potentiation and spike timing-dependent plasticity. J Physiol. 586:5885-5900.
25. Catterall WA, Few AP. 2008. Calcium channel regulation and presynaptic plasticity. Neuron. 59:882-901.
26. Charton JP, Herkert M, Becker CM, Schroder H. 1999. Cellular and subcellular localization of the 2B-subunit of the NMDA receptor in the adult rat telencephalon. Brain Res. 816:609-617.
27. Chevaleyre V, Takahashi KA, Castillo PE. 2006. Endocannabinoidmediated synaptic plasticity in the CNS. Annu Rev Neurosci. 29:37-76.
28. Chevaliere V, Castillo PE. 2003. Heterosynaptic LTD of hippocampal GABAergic synapses: a novel role of endocannabinoids in regulating excitability. Neuron. 38:461-472.
29. Corlew R, Brasier DJ, Feldman DE, Philpot B. 2008. Presynaptic NMDA receptors: newly appreciated roles in cortical synaptic function and plasticity. Neuroscientist. 14:609-625.
30. Corlew R, Wang Y, Ghermazien H, Erisir A, Philpot BD. 2007. Developmental switch in the contribution of presynaptic and postsynaptic NMDA receptors to long-term depression. J Neurosci. 27:9835-9845.
31. Cull-Candy SG, Leszkiewicz DN. 2004. Role of distinct NMDA receptor subtypes at central synapses. Sci STKE. 2004:re16.
32. Dan Y, Poo MM. 2006. Spike timing-dependent plasticity: from synapse to perception. Physiol Rev. 86:1033-1048.
33. Debanne D, Gahwiler BH, Thompson SM. 1998. Long-term synaptic plasticity between pairs of individual CA3 pyramidal cells in rat hippocampal slice cultures. J Physiol. 507:237-247.
34. Duffy S, Labrie V, Roder JC. 2008. D-serine augments NMDA-NR2B receptor-dependent hippocampal long-term depression and spatial reversal learning. Neuropsychopharmacology. 33:1004-1018.
35. Duguid IC, Sjöström PJ. 2006. Novel presynaptic mechanisms for coincidence detection in synaptic plasticity. Curr Opin Neurobiol. 16:312-322.
36. Egger V, Feldmeyer D, Sakmann B. 1999. Coincidence detection and changes of synaptic efficacy in spiny stellate neurons in rat barrel cortex. Nat Neurosci. 2:1098-1105.
37. Feldman DE. 2012. Spike timing-dependence of plasticity. Neuron. 75:556-571.
38. Feldman DE, Brecht M. 2005. Map plasticity in somatosensory cortex. Science. 310:810-815.
39. Fischer G, Mutel V, Trube G, Malherbe P, Kew JN, Mohacsi E, Heitz MP, Kemp JA. 1997. Ro 25-6981, a highly potent and selective blocker of N-methyl-D-aspartate receptors containing the NR2B subunit. Characterization in vitro. J Pharmacol Exp Ther. 283:1285-1292.
40. Freund TF, Katona I, Piomelli D. 2003. Role of endogenous cannabinoids in synaptic signalling. Physiol Rev. 83: 1017-1066.
41. Gerdeman GL, Ronesi J, Lovinger DM. 2002. Postsynaptic endocannabinoid release is critical to long-term depression in the striatum. Nat Neurosci. 5:446-451.
42. Ghosh TK, Eis PS, Mullane JM, Ebert CL, Gill DL. 1988. Competitive, reversible, and potent antagonism of inositol 1,4,5-triphosphate-activated calcium release by heparin. J Biol Chem. 263:11075-11079.
43. Gómez-Gonzalo M, Navarrete M, Perea G, Covelo A, Martín-Fernández M, Shigemoto R, Luján R, Araque A. 2015. Endocannabinoids induce lateral long-term potentiation of glutamate release by stimulation of gliotransmission. Cereb Cortex. 25:3699-3712.
44. Hebb DO. 1949. The organization of behavior. New York: Wiley.
45. Henneberger C, Papouin T, Oliet SH, Rusakov DA. 2010. Long-term potentiation depends on release of D-serine from astrocytes. Nature. 463:232-236.
46. Hessler NA, Shirke AM, Malinow R. 1993. The probability of transmitter release at a mammalian central synapse. Nature. 366:569-572.
47. Huang YC, Wang SJ, Chiou LC, Gean PW. 2003. Mediation of amphetamine-induced long-term depression of synaptic transmission by CB1 cannabinoid receptors in the rat amygdala. J Neurosci. 23:10311-10320.
48. Jahr CE. 1992. High probability opening of NMDA receptor channels by L-glutamate. Science. 255:470-472.
49. Jourdain P, Bergersen LH, Bhaukaurally K, Bezzi P, Santello M, Domercq M, Matute C, Tonello F, Gundersen U, Volterra A. 2007. Glutamate exocytosis from astrocytes controls synaptic strength. Nat Neurosci. 10:331-339.
50. Kaeser PS, Südhof TC. 2005. RIM function in short and long-term synaptic plasticity. Biochem Soc Trans. 33:1345-1349.
51. Khodakhah K, Armstrong CM. 1997. Induction of long-term depression and rebound potentiation by inositol trisphosphate in cerebellar Purkinje neurons. Proc Natl Acad Sci USA. 94:14009-14014.
52. Kim SH, Ryan TA. 2010. CDK5 serves as a major control point in neurotransmitter release. Neuron. 67:797-809.
53. Kim SH, Ryan TA. 2013. Balance of calcineurin Aα and CDK5 activities sets release probability at nerve terminals. J Neurosci. 33:8937-8950.
54. Kohl MM, Shipton OA, Deacon RM, Rawlins JN, Deisseroth K, Paulsen O. 2011. Hemisphere-specific optogenetic stimulation reveals left-right asymmetry of hippocampal plasticity. Nat Neurosci. 14:1413-1415.
55. Kourrich SK, Glasgow SD, Caruana DA, Chapman CA. 2008. Postsynaptic signals mediating induction of long-term synaptic depression in the entorhinal cortex. Neural Plast. Article ID 840374.
56. Kwag J, Paulsen O. 2009. The timing of external input controls the sign of plasticity at local synapses. Nat Neurosci. 12:1219-1221.
57. Kwag J, Paulsen O. 2012. Gating of NMDA receptor-mediated hippocampal spike timing-dependent potentiation by mGluR5. Neuropharmacology. 63:701-719.
58. Larsen RS, Corlew RJ, Henson MA, Roberts AC, Mishina M, Watanabe M, Lipton SA, Nakanishi N, Pérez-Otaño I, Weinberg RJ, et al. 2011. NR3A-containing NMDARs promote neurotransmitter release and spike timing-dependent plasticity. Nat Neurosci. 14:338-344.
59. Larsen RS, Smith IT, Miriyala J, Han JE, Corlew RJ, Smith SL, Philpot BD. 2014. Synapse-specific control of experiencedependent plasticity by presynaptic NMDA receptors. Neuron. 83:879-893.
60. Leenders AGM, Sheng Z-H. 2005. Modulation of neurotransmitter release by the second messenger-activated protein kinases: implications for presynaptic plasticity. Pharmacol Ther. 105:69-84.
61. Liu L, Wong TP, Pozza MF, Lingenhoehl K, Wang Y, Sheng M, Auberson YP, Wang YT. 2004. Role of NMDA receptor subtypes in governing the direction of hippocampal synaptic plasticity. Science. 304:1021-1024.
62. Llano I, Leresche N, Marty A. 1991. Calcium entry increases the sensitivity of cerebellar Purkinje cells to applied GABA and decreases inhibitory synaptic currents. Neuron. 6:565-574.
63. Malenka RC, Bear MF. 2004. LTP and LTD: an embarrassment of riches. Neuron. 44:5-21.
64. Malinow R, Tsien RW. 1990. Presynaptic enhancement shown by whole-cell recordings of long-term potentiation in hippocampal slices. Nature. 346:177-180.
65. Mameli M, Carta M, Partridge LD, Valenzuela CF. 2005. Neurosteroid-induced plasticity of immature synapses via retrograde modulation of presynaptic NMDA receptors. J Neurosci. 25:2285-2294.
66. Markram H, Lubke J, Frotscher M, Sakmann B. 1997. Regulation of synaptic efficacy by coincidence of postsynaptic APs and EPSPs. Science. 275:213-215.
67. Marsicano G, Wotjak CT, Azad SC, Bisogno T, Ammes G, Cascio MG, Herman H, Tang J, Hofmann C, Zieglgansberger W, et al. 2002. The endogenous cannabinoid system controls extinction of aversive memories. Nature. 418:530-534.
68. Massey PV, Johnson BE, Moult PR, Auberson YP, Brown MW, Molnar E, Collingridge GL, Bashir ZI. 2004. Differential roles of NR2A and NR2B-containing NMDA receptors in cortical long-term potentiation and long-term depression. J Neurosci. 24:7821-7828.
69. McGuinness L, Taylor C, Taylor RD, Yau C, Langenhan T, Hart M, Christian H, Tynan P, Donnelly P, Emptage N. 2010. Presynaptic NMDARs in the hippocampus facilitate transmitter release at theta frequency. Neuron. 68:1109-1127.
70. Mehta MR, Barnes CA, McNaughton BL. 1997. Experiencedependent, asymmetric expansion of hippocampal place fields. Proc Natl Acad Sci USA. 94:8918-8921.
71. Meredith RM, Floyer-Lea AM, Paulsen O. 2003. Maturation of longterm potentiation induction rules in rodent hippocampus: role of GABAergic inhibition. J Neurosci. 23:11142-11146.
72. Min R, Nevian T. 2012. Astrocyte signaling controls spike timingdependent depression at neocortical synapses. Nat Neurosci. 15:746-753.
73. Monyer H, Burnashev N, Laurie DJ, Sakmann B, Seeburg PH. 1994. Developmental and regional expression in the rat brain and functional properties of four NMDA receptors. Neuron. 12:529-540.
74. Morishita W, Lu W, Smith GB, Nicoll RA, Bear MF, Malenka RC. 2007. Activation of NR2B-containing NMDA receptors is not required for NMDA receptor-dependent long-term depression. Neuropharmacology. 52:71-76.
75. 1-substituted piperazine-2,3-dicarboxylic acid derivatives acting as NMDA receptor antagonists. J Med Chem. 48:2627-2637.
76. Mulkey RM, Endo S, Shenolikar S, Malenka RC. 1994. Involvement of a calcineurin/inhibitor-1 phosphatase cascade in hippocampal long-term depression. Nature. 369:486-488.
77. Nabavi S, Kessels HW, Alfonso S, Aow J, Fox R, Malinow R. 2013. Metabotropic NMDA receptor function is required for NMDA receptor-dependent long-term depression. Proc Natl Acad Sci USA. 110:4027-4032.
78. Navarrete M, Araque A. 2008. Endocannabinoids mediate neuron-astrocyte communication. Neuron. 57:883-893.
79. Navarrete M, Araque A. 2010. Endocannabinoids potentiate synaptic transmission through stimulation of astrocytes. Neuron. 68:113-126.
80. 2+ signaling in spike-timingdependent plasticity. J Neurosci. 43:11001-11013.
81. Neyton J, Paoletti P. 2006. Relating NMDA receptor function to receptor subunit composition: limitations of the pharmacological approach. J Neurosci. 26:1331-1336.
82. 2+ channels. J Neurosci. 20:8290-8297.
83. Nosyreva ED, Huber KM. 2005. Developmental switch in synaptic mechanisms of hippocampal metabotropic glutamate receptor-dependent long-term depression. J Neurosci. 25: 2992-3001.
84. Oliet SH, Malenka RC, Nicoll RA. 1997. Two distinct forms of longterm depression coexist in CA1 hippocampal pyramidal cells. Neuron. 18:969-982.
85. 2+ entry and synaptic activation of metabotropic glutamate receptors for the induction of long-term depression in adult rat hippocampus. J Physiol. 511:761-770.
86. Panatier A, Theodosis DT, Mothet JP, Touquet B, Pollegioni L, Poulain D, Oliet SHR. 2006. Glia-derived D-serine controls NMDA receptor activity and memory. Cell. 125:775-784.
87. Paoletti P, Bellone C, Zhou Q. 2013. NMDA receptor subunit diversity: impact on receptor properties, synaptic plasticity and disease. Nat Rev Neurosci. 14:383-400.
88. Parpura V, Zorec R. 2010. Gliotransmission: exocytotic release from astrocytes. Brain Res Rev. 63:83-92.
89. Perea G, Araque A. 2005. Properties of synaptically evoked astrocyte calciumsignal reveal synaptic information processing by astrocytes. J Neurosci. 25:2192-2203.
90. Perea G, Araque A. 2007. Astrocytes potentiate transmitter release at single hippocampal synapses. Science. 317:1083-1086.
91. Pike FG, Meredith RM, Olding AW, Paulsen O. 1999. Postsynaptic bursting is essential for "Hebbian" induction of associative long-term potentiation at excitatory synapses in rat hippocampus. J Physiol. 518:571-576.
92. Pittaluga A, Raiteri M. 1990. Release-enhancing glycinedependent presynaptic NMDA receptors exist on noradrenergic terminal of hippocampus. Eur J Pharmacol. 191:231-234.
93. Pittaluga A, Raiteri M. 1992. N-methyl-D-aspartic acid (NMDA) and non-NMDA receptors regulating hippocampal norepinephrine release. I. Location on axon terminals and pharmacological characterization. J Pharmacol Exp Ther. 260:232-237.
94. Porter JT, McCarthy KD. 1996. Hippocampal astrocytes in situ respond to glutamate released from synaptic terminals. J Neurosci. 16:5073-5081.
95. Reeve JE, Kohl MM, Rodríguez-Moreno A, Paulsen O, Anderson HL. 2012. Caged intracellular NMDA receptor blockers for the study of subcellular ion channel function. Commun Integr Biol. 5:240-242.
96. Robbe D, Kopf M, Remaury A, Bockaert J, Manzoni OJ. 2002. Endogenous cannabinoids mediate long-term synaptic depression in the nucleus accumbens. Proc Natl Acad Sci USA. 99:8384-8388.
97. Rodríguez JJ, Mackie K, Pickel VM. 2001. Ultrastructural localization of the CB1 cannabinoid receptor inmu-opioid receptor patches of the rat caudate putamen nucleus. J Neurosci. 21:823-833.
98. Rodríguez-Moreno A, Banerjee A, Paulsen O. 2010. Presynaptic NMDA receptors and spike timing-dependent depression at cortical synapses. Front Synaptic Neurosci. 2:18.
99. Rodríguez-Moreno A, González-Rueda A, Banerjee A, Upton ML, Craig M, Paulsen O. 2013. Presynaptic self-depression at developing neocortical synapses. Neuron. 77:35-42.
100. Rodríguez-Moreno A, Kohl MM, Reeve J, Eaton TR, Collins HA, Anderson HL, Paulsen O. 2011. Presynaptic induction and expression of timing-dependent long-term depression demonstrated by compartment specific photorelease of a use-dependent NMDA antagonist. J Neurosci. 31:8564-8569.
101. Rodríguez-Moreno A, Paulsen O. 2008. Spike timing-dependent long-term depression requires presynaptic NMDA receptors. Nat Neurosci. 11:744-745.
102. Rodríguez-Moreno A, Sistiaga A, Lerma J, Sánchez-Prieto J. 1998. Switch from facilitation to inhibition of excitatory synaptic transmission by group ImGluR desensitization. Neuron. 21:1477-1486.
103. Rosenmund C, Clements JD, Westbrook GL. 1993. Nonuniform probability of glutamate release at a hippocampal synapse. Science. 262:754-757.
104. Safo PK, Regehr WG. 2005. Endocannabinoids control the induction of cerebellar LTD. Neuron. 48:647-659.
105. Salio C, Doly S, Fisher J, Franzoni MF, Conrath M. 2002. Neuronal and astrocytic localization of the cannabinoid receptor-1 in the dorsal horn of the rat spinal cord. Neurosci Lett. 329:13-16.
106. Serrano A, Haddjeri N, Lacaille JC, Robitaille R. 2006. GABAergic network activation of glial cells underlies hippocampal heterosynaptic depression. J Neurosci. 26:5370-5382.
107. Siegel SJ, Brose N, Janssen WG, Gasic GP, Jahn R, Heinemann SF, Morrison JH. 1994. Regional, cellular, and ultrastructural distribution of N-methyl-D-aspartate receptor subunit 1 in monkey hippocampus. Proc Natl Acad Sci USA. 91:564-568.
108. Sjöström PJ, Turrigiano GG, Nelson SB. 2003. Neocortical LTD via coincident activation of presynaptic NMDA and cannabinoid receptors. Neuron. 39:641-654.
109. Stella N. 2004. Cannabinoid signalling in glial cells. Glia. 48:267-277.
110. Su SC, Seo J, Pan JQ, Samuels BA, Rudenko A, Ericsson M, Neve RL, Yue DT, Tsai L-H. 2012. Regulation of N-type voltage-gated calcium channels and presynaptic function by cyclindependent kinase 5. Neuron. 75:675-687.
111. 2+): intracellular stores spill their guts. Neuron. 22:427-430.
112. Torii N, Kamishita T, Otsu Y, Tsumoto T. 1995. An inhibitor for calcineurin, FK506, blocks induction of long-term depression in rat visual cortex. Neurosci Lett. 185:1-4.
113. Toyoda H, Zhao MG, Zhuo M. 2005. Roles of NMDA receptor NR2A and NR2B subtypes for long-term depression in the anterior cingulate cortex. Eur J Neurosci. 22:485-494.
114. Urban-Ciecko J, Wen JA, Parekh PK, Barth AL. 2014. Experiencedependent regulation of presynaptic NMDARs enhances neurotransmitter release at neocortical synapses. Learn Mem. 22:47-55.
115. Wang JKT, Andrews H, Thkral V. 1992. Presynaptic NMDA receptors regulate noradrenaline release from isolated never terminals. J Neurochem. 58:204-211.
116. Weitlauf C, Honse Y, Auberson YP, Mishina M, Lovinger DM, Winder DG. 2005. Activation of NR2A-containing NMDA receptors is not obligatory for NMDA receptor-dependent long-term potentiation. J Neurosci. 25:8386-8390.
117. Wittenberg GM, Wang SSH. 2006. Malleability of spike timingdependent plasticity at the CA3-CA1 synapse. J Neurosci. 26:6610-6617.
118. Yasuda H, Barth AL, Stellwagen D, Malenka RC. 2003. A developmental switch in the signaling cascades for LTP induction. Nat Neurosci. 6:15-16.
119. Yu X, Shouval HZ, Knierim JJ. 2008. A biophysical model of synaptic plasticity and metaplasticity can account for the dynamics of the backward shift of hippocampal place fields. J Neurophysiol. 100:983-992.
120. Zhang JM, Wang HK, Ye CQ, Ge W, Chen Y, Jiang ZL, Wu CP, Poo MM, Duan S. 2003. ATP released by astrocytes mediates glutamatergic activity-dependent heterosynaptic suppression. Neuron. 40:971-982.
121. Zhang Z, Gong N, Wang W, Xu L, Xu TL. 2008. Bellshaped D-serine actions on hippocampal long-term depression and spatial memory retrieval. Cereb Cortex. 18:2391-2401.
122. Zhuang Z, Yang B, Theus MH, Sick JT, Bethea JR, Sick TJ, Liebl DJ. 2010. EphrinBs regulate D-serine synthesis and release in astrocytes. J Neurosci. 30:16015-16024.