BDNF is required for the induction of a presynaptic component of the functional conversion of silent synapses

Hippocampus

Volumn 21, Issue 4, 2011, Pages 374-385

  Cabezas, Carolina ^a,b   Buño, Washington ^a  

^a INSTITUTO CAJAL   (Spain)

^b INSERM   (France)

Author keywords

BDNF; Functional conversion; LTP; Silent synapses; Transmitter release

Indexed keywords

AMPA RECEPTOR; BRAIN DERIVED NEUROTROPHIC FACTOR; GLUTAMIC ACID; NEUROTROPHIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRAIN SLICE; CONTROLLED STUDY; DEPOLARIZATION; HIPPOCAMPUS; LONG TERM POTENTIATION; NEUROTRANSMITTER RELEASE; NONHUMAN; POSTSYNAPTIC POTENTIAL; PRESYNAPTIC POTENTIAL; PRIORITY JOURNAL; PYRAMIDAL NERVE CELL; RAT;

ALPHA-AMINO-3-HYDROXY-5-METHYL-4-ISOXAZOLEPROPIONIC ACID; ANIMALS; BRAIN-DERIVED NEUROTROPHIC FACTOR; CA1 REGION, HIPPOCAMPAL; CHOLINERGIC FIBERS; GLUTAMIC ACID; LONG-TERM POTENTIATION; MEMORY; NEURONAL PLASTICITY; PATCH-CLAMP TECHNIQUES; RATS; RATS, WISTAR; RECEPTOR, TRKB; RECEPTORS, AMPA; RECEPTORS, N-METHYL-D-ASPARTATE; RECEPTORS, PRESYNAPTIC; SYNAPSES; SYNAPTIC TRANSMISSION;

EID: 79953056611     PISSN: 10509631     EISSN: 10981063     Source Type: Journal    
DOI: 10.1002/hipo.20754     Document Type: Article

References (90)

1. Atwood HL, Wojtowicz JM. 1999. Silent synapses in neural plasticity: Current evidence. Learn Mem 6: 542-571.
2. Auger C, Marty A. 2000. Quantal currents at single-site central synapses. J Physiol (Lond) 526: 3-11.
3. Bayazitov IT, Richardson RJ, Fricke RG, Zakharenko SS. 2007. Slow presynaptic and fast postsynaptic components of compound long-term potentiation. J Neurosci 27: 11510-11521.
4. Bekkers JM, Stevens CF. 1990. Presynaptic mechanism for long-term potentiation in the hippocampus. Nature 346: 724-729.
5. Berninger B, Poo M. 1996. Fast actions of neurotrophic factors. Curr Opin Neurobiol 6: 324-330.
6. Berretta N, Rossokhin AV, Cherubini E, Astrelin AV, Voronin LL. 1999. Long-term synaptic changes induced by intracellular tetanization of CA3 pyramidal neurons in hippocampal slices from juvenile rats. Neuroscience 93: 469-477.
7. Blundon JA, Zakharenko SS. 2008. Dissecting the components of long-term potentiation. Neuroscientitst 14: 598-608.
8. Bolshakov VY, Siegelbaum SA. 1995. Regulation of hippocampal transmitter release during development and long-term potentiation. Science 269: 1730-1734.
9. Bonansco C, Gonzalez de la Vega A, Gonzalez Alegre P, Borde M, Garcia-Segura LM, Buno W. 2002. Tetanic stimulation of schaffer collaterals induces rhythmic bursts via NMDA receptor activation in rat CA1 pyramidal neurons. Hippocampus 12: 434-446.
10. Bramham CR, Messaoudi E. 2005. BDNF function in adult synaptic plasticity: The synaptic consolidation hypothesis. Prog Neurobiol 76: 99-125.
11. Cabezas C, Buno W. 2006. Distinct transmitter release properties determine differences in short-term plasticity at functional and silent synapses. J Neurophysiol 95: 3024-3034.
12. Cavazzini M, Bliss T, Emptage N. 2005. Ca2+ and synaptic plasticity. Cell Calcium 38: 355-367.
13. Choi S, Klingauf J, Tsien RW. 2000. Postfusional regulation of cleft glutamate concentration during LTP at "silent synapses." Nat Neurosci 3: 330-336.
14. Christie JM, Jahr CE. 2006. Multivesicular release at Schaffer collateral-CA1 hippocampal synapses. J Neurosci 26: 210-216.
15. Clark KA, Randall AD, Collingridge GL. 1994. A comparison of paired-pulsed facilitation of AMPA and NMDA receptor-mediated excitatory postsynaptic currents in the hippocampus. Exp Brain Res 101: 272-278.
16. Colbran RJ, Fong YL, Schworer CM, Soderling TR. 1988. Regulatory interactions of the calmodulin-binding, inhibitory, and autophosphorylation domains of Ca2+/calmodulin-dependent protein kinase II. J Biol Chem 263: 18145-18151.
17. Colley PA, Routtenberg A. 1993. Long-term potentiation as synaptic dialogue. Brain Res Brain Res Rev 18: 115-122.
18. Collin T, Marty A, Llano I. 2005. Presynaptic calcium stores and synaptic transmission. Curr Opin Neurobiol 15: 275-281.
19. Conti R, Lisman J. 2003. The high variance of AMPA receptor- and NMDA receptor-mediated responses at single hippocampal synapses: Evidence for multiquantal release. Proc Natl Acad Sci USA 100: 4885-4890.
20. Creager R, Dunwiddie T, Lynch G. 1980. Paired-pulse and frequency facilitation in the CA1 region of the in vitro rat hippocampus. J Physiol (Lond) 299: 409-424.
21. Debanne D, Guérineau NC, Gahwiler BH, Thompson SM. 1996. Paired-pulse facilitation and dépression at unitary synapses in rat hippocampus: Quantal fluctuation affects subsequent release. J Physiol (Lond) 491: 163-176.
22. Debanne D, Gahwiler BH, Thompson SM. 1997. Bidirectional associative plasticity of unitary CA3-CA1 EPSCs in the rat hippocampus in vitro. J Neurophysiol 77: 2851-2855.
23. Dobrunz LE, Stevens CF. 1997. Heterogeneity of release probability, facilitation, and depletion at central synapses. Neuron 18: 995-1008.
24. Dolphin AC, Errington ML, Bliss TV. 1982. Long-term potentiation of the perforant path in vivo is associated with increased glutamate release. Nature 297: 496-498.
25. Dumas TC. 2005. Late postnatal maturation of excitatory synaptic transmission permits adult-like expression of hippocampal-dependent behaviors. Hippocampus 15: 562-578.
26. Emptage NJ, Reid CA, Fine A. 2001. Calcium stores in hippocampal synaptic boutons mediate short-term plasticity, store-operated Ca2+ entry, and spontaneous transmitter release. Neuron 29: 197-208.
27. Emptage NJ, Reid CA, Fine A, Bliss TV. 2003. Optical quantal analysis reveals a presynaptic component of LTP at hippocampal Schaffer-associational synapses. Neuron 38: 797-804.
28. Faber DS, Lin JW, Korn H. 1991. Silent synaptic connections and their modifiability. Ann N Y Acad Sci 627: 151-164.
29. Feldman DE. 2009. Synaptic mechanisms for plasticity in neocortex. Annu Rev Neurosci 32: 33-55. Review.
30. Fernandez de Sevilla D, Cabezas C, de Prada AN, Sanchez-Jimenez A, Buno W. 2002. Selective muscarinic regulation of functional glutamatergic Schaffer collateral synapses in rat CA1 pyramidal neurons. J Physiol (Lond) 545: 51-63.
31. Fernandez de Sevilla D, Nunez A, Borde M, Malinow R, Buno W. 2008. Cholinergic-mediated IP3-receptor activation induces long-lasting synaptic enhancement in CA1 pyramidal neurons. J Neurosci 28: 1469-1478.
32. Goda Y, Stevens CF. 1996. Long-term depression properties in a simple system. Neuron 16: 103-111.
33. Hanse E, Gustafsson B. 2001. Factors explaining heterogeneity in short-term synaptic dynamics of hippocampal glutamatergic synapses in the neonatal rat. J Physiol (Lond) 537: 141-149.
34. Harris KM, Stevens JK. 1989. Dendritic spines of CA1 pyramidal cells in the rat hippocampus: Serial electron microscopy with reference to their biophysical characteristics. J Neurosci 9: 2982-2997.
35. Hasselmo ME. 2006. The role of acetylcholine in learning and memory. Curr Opin Neurobiol 16: 710-715.
36. He L, Xue L, Xu J, McNeil BD, Bai L, Melicoff E, Adachi R, Wu LG. 2009. Compound vesicle fusion increases quantal size and potentiates synaptic transmission. Nature 459: 93-97.
37. Hsia AY, Malenka RC, Nicoll RA. 1998. Development of excitatory circuitry in the hippocampus. J Neurophysiol 79: 2013-2024.
38. Isaac JT, Nicoll RA, Malenka RC. 1995. Evidence for silent synapses: Implications for the expression of LTP. Neuron 15: 427-434.
39. Isaac JT.Hjelmstad GO, Nicoll RA, Malenka RC. 1996. Long-term potentiation at single fiber inputs to hippocampal CA1 pyramidal cells. Proc Natl Acad Sci USA 93: 8710-8715.
40. Itami C, Kimura F, Kohno T, Matsuoka M, Ichikawa M, Tsumoto T, Nakamura S. 2003. Brain-derived neurotrophic factor-dependent unmasking of "silent" synapses in the developing mouse barrel cortex. Proc Natl Acad Sci USA 100: 13069-13074.
41. Jourdi H, Hsu Y-T, Zhou M, Qin Q, Bi X, Baudry M. 2009. Positive AMPA receptor modulation rapidly stimulates BDNF release and increases dendritic mRNA translation. J Neurosci 29: 8688-8697.
42. Kauer JA, Malenka RC, Nicoll RA. 1988. A persistent postsynaptic modification mediates long-term potentiation in the hippocampus. Neuron 1: 911-917.
43. Kerchner GA, Nicoll RA. 2008. Silent synapses and the emergence of a postsynaptic mechanism for LTP. Nat Rev Neurosci 9: 813-825.
44. Kim JH, Udo H, Li HL, Youn TY, Chen M, Kandel ER, Bailey CH. 2003. Presynaptic activation of silent synapses and growth of new synapses contribute to intermediate and long-term facilitation in Aplysia. Neuron 40: 151-165.
45. Kolarow R, Brigadski T, Lessmann V. 2007. Postsynaptic secretion of BDNF and NT-3 from hippocampal neurons depends on calcium calmodulin kinase II signaling and proceeds via delayed fusion pore opening. J Neurosci 27: 10350-10364.
46. Kullmann DM, Nicoll RA. 1992. Long-term potentiation is associated with increases in quantal content and quantal amplitude. Nature 357: 240-244.
47. Kullmann DM, Erdemli G, Asztély F. 1996. LTP of AMPA and NMDA receptor-mediated signals: Evidence for presynaptic expression and extrasynaptic glutamate spill-over. Neuron 17: 461-474.
48. Lauri SE, Bortolotto ZA, Nistico R, Bleakman D, Ornstein PL, Lodge D, Isaac JT, Collingridge GL. 2003. A role for Ca2+ stores in kainate receptor-dependent synaptic facilitation and LTP at mossy fiber synapses in the hippocampus. Neuron 39: 327-341.
49. Le Magueresse C, Cherubini E. 2007. Presynaptic calcium stores contribute to nicotine-elicited potentiation of evoked synaptic transmission at CA3-CA1 connections in the neonatal rat hippocampus. Hippocampus 17: 316-325.
50. Lessmann V. 1998. Neurotrophin-dependent modulation of glutamatergic synaptic transmission in the mammalian CNS. Gen Pharmacol 31: 667-674.
51. Lessmann V, Gottmann K, Malcangio M. 2003. Neurotrophin secretion: Current facts and future prospects. Prog Neurobiol 69: 341-374.
52. Li GL, Keen E, Andor-Ardó D, Hudspeth AJ, von Gersdorff H. 2009. The unitary event underlying multiquantal EPSCs at a hair cell's ribbon synapse. J Neurosci 29: 7558-7568.
53. Li YX, Zhang Y, Lester HA, Schuman EM, Davidson N. 1998. Enhancement of neurotransmitter release induced by brain-derived neurotrophic factor in cultured hippocampal neurons. J Neurosci 18: 10231-10240.
54. 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.
55. Lisman J, Raghavachari S. 2006. A unified model of the presynaptic and post-synaptic changes during LTP at CA1 synapses. Science STKE 356: rev11.
56. Magby JP, Bi C, Chen ZY, Lee FS, Plummer MR. 2006. Single-cell characterization of retrograde signaling by brain-derived neurotrophic factor. J Neurosci 26: 13531-13536.
57. Malinow R, Tsien RW. 1990. Presynaptic enhancement shown by whole-cell recordings of long-term potentiation in hippocampal slices. Nature 346: 177-180.
58. 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.
59. Martin ED, Buno W. 2003. Caffeine-mediated presynaptic long-term potentiation in hippocampal CA1 pyramidal neurons. J Neurophysiol 89: 3029-3038.
60. Matsuda Y, Nakanishi S, Nagasawa K, Iwahashi K, Kase H. 1988. The effect of K-252a, a potent microbial inhibitor of protein kinase, on activated cyclic nucleotide phosphodiesterase. Biochem J 256: 75-80.
61. Muller D, Joly M, Lynch G. 1988. Contributions of quisqualate and NMDA receptors to the induction and expression of LTP. Science 242: 1694-1697.
62. Nicoll RA. 2003. Expression mechanisms underlying long-term potentiation: A postsynaptic view. Philos Trans R Soc Lond B Biol Sci 358: 721-726.
63. Oertner TG, Sabatini BL, Nimchinsky EA, Svoboda K. 2002. Facilitation at single synapses probed with optical quantal analysis. Nat Neurosci 5: 657-664.
64. Pan B, Zucker RS. 2009. A general model of synaptic transmission and short-term plasticity. Neuron 62: 539-554.
65. Poncer JC, Malinow R. 2001. Postsynaptic conversion of silent synapses during LTP affects synaptic gain and transmission dynamics. Nat Neurosci 4: 989-996.
66. Pozzo-Miller L. 2006. BDNF enhances dendritic Ca2+ signals evoked by coincident EPSCs and back-propagating action potentials in CA1 pyramidal neurons. Brain Res 1104: 45-54.
67. Raghavachari S, Lisman JE. 2004. Properties of quantal transmission at CA1 synapses. J Neurophysiol 92: 2456-2467.
68. Reid CA, Dixon DB, Takahashi M, Bliss TV, Fine A. 2004. Optical quantal analysis indicates that long-term potentiation at single hippocampal mossy fiber synapses is expressed through increased release probability, recruitment of new release sites, and activation of silent synapses. J Neurosci 24: 3618-3626.
69. Ricci-Tersenghi F, Minneci F, Sola E, Cherubini E, Maggi L. 2006. Multivesicular release at developing Schaffer collateral-CA1 synapses: An analytic approach to describe experimental data. J Neurophysiol 96: 15-26.
70. Riebe I, Gustafsson B, Hanse E. 2009. Silent synapses onto interneurons in the rat CA1 stratum radiatum. Eur J Neurosci 29: 1870-1882.
71. Routtenberg A. 1999. Tagging the Hebb synapse. TINS 22: 255-256.
72. Rubio N. 1997. Mouse astrocytes store and deliver brain-derived neurotrophic factor using the non-catalytic gp95trkB receptor. Eur J Neurosci 9: 1847-1853.
73. Schuman EM. 1997. Synapse specificity and long-term information storage. Neuron 18: 339-342.
74. Scott R, Lalic T, Kullmann DM, Capogna M, Rusakov DA.2008.Target-cell specificity of kainate autoreceptor and Ca2+-store-dependent short-term plasticity at hippocampal mossy fiber synapses.J Neurosci28:13139-13149.
75. Shen W, Wu B, Zhang Z, Dou Y, Rao ZR, Chen YR, Duan S. 2006. Activity-induced rapid synaptic maturation mediated by presynaptic cdc42 signaling. Neuron 50: 401-414.
76. Sorra KE, Harris KM. 1993. Occurrence and three-dimensional structure of multiple synapses between individual radiatum axons and their target pyramidal cells in hippocampal area CA1. J Neurosci 13: 3736-3748.
77. Steiner P, Higley MJ, Xu W, Czervionke BL, Malenka RC, Sabatini BL. 2008. Destabilization of the postsynaptic density by PSD-95 serine 73 phosphorylation inhibits spine growth and synaptic plasticity. Neuron 60: 788-802.
78. Tyler WJ, Zhang XL, Hartman K, Winterer J, Muller W, Stanton PK, Pozzo-Miller L. 2006. BDNF increases release probability and the size of a rapidly recycling vesicle pool within rat hippocampal excitatory synapses. J Physiol (Lond) 574: 787-803.
79. Voronin LL, Cherubini E. 2003. "Presynaptic silence" may be golden. Neuropharmacol 45: 439-449.
80. Voronin LL, Altinbaev RS, Bayazitov IT, Gasparini S, Kasyanov AV, Saviane C, Savtchenko L, Cherubini E. 2004. Postsynaptic depolarization enhances transmitter release and causes the appearance of responses at "silent" synapses in rat hippocampus. Neuroscience 126: 45-59.
81. Wadiche JI, Jahr CE. 2001. Multivesicular release at climbing fiber-Purkinje cell synapses. Neuron 32: 301-313.
82. Walz C, Jungling K, Lessmann V, Gottmann K. 2006. Presynaptic plasticity in an immature neocortical network requires NMDA receptor activation and BDNF release. J Neurophysiol 96: 3512-3516.
83. Ward B, McGuinness L, Akerman CJ, Fine A, Bliss TV, Emptage NJ. 2006. State-dependent mechanisms of LTP expression revealed by optical quantal analysis. Neuron 52: 649-661.
84. Wozny C, Maier N, Schmitz D, Behr J. 2008. Two different forms of long-term potentiation at CA1-subiculum synapses. J Physiol (Lond) 586: 2725-2734.
85. Xiao MY, Wasling P, Hanse E, Gustafsson B. 2004. Creation of AMPA-silent synapses in the neonatal hippocampus. Nat Neurosci 7: 236-243.
86. Yanagisawa T, Tsumoto T, Kimura F. 2004. Transiently higher release probability during critical period at thalamocortical synapses in the mouse barrel cortex: Relevance to differential short-term plasticity of AMPA and NMDA EPSCs and possible involvement of silent synapses. Eur J Neurosci 20: 3006-3018.
87. Yuste R, Majewska A, Cash SS, Denk W. 1999. Mechanisms of calcium influx into hippocampal spines: Heterogeneity among spines, coincidence detection by NMDA receptors and optical quantal analysis. J Neurosci 19: 1976-1978.
88. Zakharenko SS, Patterson SL, Dragatsis I, Zeitlin SO, Siegelbaum SA, Kandel ER, Morozov A. 2003. Presynaptic BDNF required for a presynaptic but not postsynaptic component of ltp at hippocampal CA1-CA3 synapses. Neuron 39: 975-990.
89. Zinebi F, Russell RT, McKernan M, Shinnick-Gallagher P. 2001. Comparison of paired-pulse facilitation of AMPA and NMDA synaptic currents in the lateral amygdala. Synapse 42: 115-127.
90. Zucker RS, Regehr WG. 2002. Short-term synaptic plasticity. Annu Rev Physiol 64: 355-405.