The expression of long-term potentiation: Reconciling the preists and the postivists

Philosophical Transactions of the Royal Society B: Biological Sciences

Volumn 369, Issue 1633, 2014, Pages

  MacDougall, Matthew J ^a   Fine, Alan ^a  

^a DALHOUSIE UNIVERSITY   (Canada)

Author keywords

Hippocampus; Optical quantal analysis; Presynaptic; Release probability; Silent synapse; Synaptic plasticity

Indexed keywords

BRAIN; COGNITION; ENZYME ACTIVITY; PROBABILITY;

AGENTS INTERACTING WITH TRANSMITTER, HORMONE OR DRUG RECEPTORS; GLUTAMIC ACID;

BIOLOGICAL MODEL; CYTOLOGY; EXCITATORY POSTSYNAPTIC POTENTIAL; HIPPOCAMPUS; HUMAN; LONG TERM POTENTIATION; METABOLISM; NERVE CELL PLASTICITY; OPTICAL QUANTAL ANALYSIS; PHYSIOLOGY; PRESYNAPTIC; RELEASE PROBABILITY; REVIEW; SILENT SYNAPSE; SYNAPTOSOME;

HIPPOCAMPUS; OPTICAL QUANTAL ANALYSIS; PRESYNAPTIC; RELEASE PROBABILITY; SILENT SYNAPSE; SYNAPTIC PLASTICITY;

EXCITATORY POSTSYNAPTIC POTENTIALS; GLUTAMIC ACID; HIPPOCAMPUS; HUMANS; LONG-TERM POTENTIATION; MODELS, NEUROLOGICAL; NEUROTRANSMITTER AGENTS; PRESYNAPTIC TERMINALS;

EID: 84888796179     PISSN: 09628436     EISSN: 14712970     Source Type: Journal    
DOI: 10.1098/rstb.2013.0135     Document Type: Review

References (87)

1. Nicoll RA, Roche KW. 2013 Long-term potentiation: peeling the onion. Neuropharmacology 74, 18-22. (doi:10.1016/j.neuropharm.2013.02.010)
2. Bliss TV, Lømo T. 1973 Long-lasting potentiation of synaptic transmission in the dentate area of the anaesthetized rabbit following stimulation of the perforant path. J. Physiol. 232, 331-356.
3. Bliss TV, Collingridge GL. 2013 Expression of NMDA receptor-dependent LTP in the hippocampus: bridging the divide. Mol. Brain 6, 5. (doi:10.1186/ 1756-6606-6-5)
4. Harvey J, Collingridge GL. 1992 Thapsigargin blocks the induction of long-term potentiation in rat hippocampal slices. Neurosci. Lett. 139, 197-200. (doi:10.1016/0304-3940(92)90551-H)
5. Sanhueza M, Lisman J. 2013 The CaMKII/NMDAR complex as a molecular memory. Mol. Brain 6, 1-8. (doi:10.1186/1756-6606-6-10)
6. Lisman J, Raghavachari S. 2006 A unified model of the presynaptic and postsynaptic changes during LTP at CA1 synapses. Sci. STKE 2006, re11. (doi:10. 1126/stke.3562006re11)
7. Collingridge GL, Isaac JT, Wang YT. 2004 Receptor trafficking and synaptic plasticity. Nat. Rev. Neurosci. 5, 952-962. (doi:10.1038/nrn1556)
8. Malinow R, Malenka RC. 2002 AMPA receptor trafficking and synaptic plasticity. Annu. Rev. Neurosci. 25, 103-126. (doi:10.1146/annurev. neuro.25.112701.142758)
9. Lee VM. 2001 Biomedicine. Tauists and beta-aptists united-well almost! Science 293, 1446-1447. (doi:10.1126/science.1064684)
10. Trojanowski JQ. 2002 Tauists, Baptists, Syners, Apostates, and new data. Ann. Neurol. 52, 263-265. (doi:10.1002/ana.10281)
11. Nicoll RA. 2003 Expression mechanisms underlying long-term potentiation: a postsynaptic view. Phil. Trans. R. Soc. Lond. B 358, 721-726. (doi:10. 1098/rstb.2002.1228)
12. Kerchner GA, Nicoll RA. 2008 Silent synapses and the emergence of a postsynaptic mechanism for LTP. Nat. Rev. Neurosci. 9, 813-825. (doi:10.1038/ nrn2501)
13. Hebb. 1949 The organization of behavior: a neuropsychological theory. New York, NY: Wiley.
14. Kullmann DM. 2012 The mother of all battles 20 years on: is LTP expressed pre-or postsynaptically? J. Physiol. 590, 2213-2216. (doi:10.1113/jphysiol. 2011.221127)
15. Skrede KK, Malthe-Sørenssen D. 1981 Increased resting and evoked release of transmitter following repetitive electrical tetanization in hippocampus: a biochemical correlate to long-lasting synaptic potentiation. Brain Res. 208, 436-441. (doi:10. 1016/0006-8993(81)90573-4)
16. Dolphin AC, Errington ML, Bliss TVP. 1982 Long-term potentiation of the perforant path in vivo is associated with increased glutamate release. Nature 297, 496-497. (doi:10.1038/ 297496a0)
17. 3H] glutamate from rat dentate gyrus three days after induction of long-term potentiation. Neurosci. Lett. 83, 107-112. (doi:10.1016/0304-3940(87)90224-2)
18. 3H] glutamate release from slices of dentate gyrus and hippocampus following classical-conditioning in the rat. Behav. Brain Res. 25, 23-29. (doi:10.1016/0166-4328 (87)90042-8)
19. Errington ML, Galley PT, Bliss TV. 2003 Long-term potentiation in the dentate gyrus of the anaesthetized rat is accompanied by an increase in extracellular glutamate: real-time measurements using a novel dialysis electrode. Phil. Trans. R. Soc. Lond. B 358, 675-687. (doi:10.1098/rstb. 2002.1251)
20. Diamond JS, Bergles DE, Jahr CE. 1998 Glutamate release monitored with astrocyte transporter currents during LTP. Neuron 21, 425-433. (doi:10. 1016/S0896-6273(00)80551-6)
21. Luscher C, Malenka RC, Nicoll RA. 1998 Monitoring glutamate release during LTP with glial transporter currents. Neuron 21, 435-441. (doi:10.1016/S0896-6273(00)80552-8)
22. Manabe T, Nicoll RA. 1994 Long-term potentiation: evidence against an increase in transmitter release probability in the CA1 region of the hippocampus. Science 265, 1888-1892. (doi:10.1126/Science. 7916483)
23. Mainen ZF, Jia Z, Roder J, Malinow R. 1998 Usedependent AMPA receptor block in mice lacking GluR2 suggests postsynaptic site for LTP expression. Nat. Neurosci. 1, 579-586. (doi:10.1038/2812)
24. Betz WJ, Bewick GS. 1992 Optical analysis of synaptic vesicle recycling at the frog neuromuscularjunction. Science 255, 200-203. (doi:10.1126/ Science.1553547)
25. 2+channels during LTP enhances low release efficacy of hippocampal CA1 perforant path synapses. Neuron 63, 372-385. (doi:10.1016/j. neuron.2009.07.013)
26. Zakharenko SS, Zablow L, Siegelbaum SA. 2001 Visualization of changes in presynaptic function during long-term synaptic plasticity. Nat. Neurosci. 4, 711-717. (doi:10.1038/89498)
27. Kauer JA, Malenka RC, Nicoll RA. 1988 A persistent postsynaptic modification mediates long-term potentiation in the hippocampus. Neuron 1, 911-917. (doi:10.1016/0896-6273(88)90148-1)
28. Muller D, Lynch G. 1988 Long-term potentiation differentially affects two components of synaptic responses in hippocampus. Proc. Natl Acad. Sci. USA 85, 9346-9350. (doi:10.1073/ pnas.85.23.9346)
29. Lynch G, Baudry M. 1984 The biochemistry of memory: a new and specific hypothesis. Science 224, 1057-1063. (doi:10.1126/science.6144182)
30. Bashir ZI, Alford S, Davies SN, Randall AD, Collingridge GL. 1991 Long-term potentiation of NMDA receptor-mediated synaptic transmission in the hippocampus. Nature 349, 156-158. (doi:10. 1038/349156a0)
31. Clark KA, Collingridge GL. 1995 Synaptic potentiation of dual-component excitatory postsynaptic currents in the rat hippocampus. J. Physiol. 482, 39-52.
32. Kullmann DM, Erdemli G, Asztely F. 1996 LTP of AMPA and NMDA receptor-mediated signals: evidence for presynaptic expression and extrasynaptic glutamate spill-over. Neuron 17, 461-474. (doi:10.1016/S0896-6273(00)80178-6)
33. Grosshans DR, Clayton DA, Coultrap SJ, Browning MD. 2002 LTP leads to rapid surface expression of NMDA but not AMPA receptors in adult rat CA1. Nat. Neurosci. 5, 27-33. (doi:10.1038/nn779)
34. Hayashi Y, Shi SH, Esteban JA, Piccini A, Poncer JC, Malinow R. 2000 Driving AMPA receptors into synapses by LTP and CaMKII: requirement for GluR1 and PDZ domain interaction. Science 287, 2262-2267. (doi:10.1126/Science.287.5461.2262)
35. Shi SH, Hayashi Y, Petralia RS, Zaman SH, Wenthold RJ, Svoboda K, Malinow R. 1999 Rapid spine delivery and redistribution of AMPA receptors after synaptic NMDA receptor activation. Science 284, 1811-1816. (doi:10.1126/science.284.5421.1811)
36. Makino H, Malinow R. 2009 AMPA receptor incorporation into synapses during LTP: the role of lateral movement and exocytosis. Neuron 64, 381-390. (doi:10.1016/j.neuron.2009.08.035)
37. Kessels HW, Kopec CD, Klein ME, Malinow R. 2009 Roles of stargazin and phosphorylation in the control of AMPA receptor subcellular distribution. Nat. Neurosci. 12, 888-896. (doi:10.1038/nn.2340)
38. Kessels HW, Malinow R. 2009 Synaptic AMPA receptor plasticity and behavior. Neuron 61, 340-350. (doi:10.1016/j.neuron.2009.01.015)
39. Granger AJ, Shi Y, Lu W, Cerpas M, Nicoll RA. 2013 LTP requires a reserve pool of glutamate receptors independent of subunit type. Nature 493, 495-500. (doi:10.1038/nature11775)
40. Bekkers JM, Stevens CF. 1990 Presynaptic mechanism for long-term potentiation in the hippocampus. Nature 346, 724-729. (doi:10. 1038/346724a0)
41. Malinow R. 1991 Transmission between pairs of hippocampal slice neurons: quantal levels, oscillations, and LTP. Science 252, 722-724. (doi:10.1126/Science.1850871)
42. Malinow R, Tsien RW. 1990 Presynaptic enhancement shown by whole-cell recordings of long-term potentiation in hippocampal slices. Nature 346, 177-180. (doi:10.1038/346177a0)
43. Bolshakov VY, Siegelbaum SA. 1995 Regulation of hippocampal transmitter release during development and long-term potentiation. Science 269, 1730-1734. (doi:10.1126/science.7569903)
44. Del Castillo J, Katz B. 1954 Quantal components of the end-plate potential. J. Physiol. 124, 560-573.
45. Faber DS, Korn H. 1991 Applicability of the coefficient of variation method for analyzing synaptic plasticity. Biophys. J. 60, 1288-1294. (doi:10.1016/S0006-3495(91)82162-2)
46. Korn H, Faber DS. 1991 Quantal analysis and synaptic efficacy in the CNS. Trends Neurosci. 14, 439-445. (doi:10.1016/0166-2236(91)90042-S)
47. Larkman A, Stratford K, Jack J. 1991 Quantal analysis of excitatory synaptic action and depression in hippocampal slices. Nature 350, 344-347. (doi:10.1038/350344a0)
48. Edwards F. 1991 Neurobiology: LTP is a long-term problem. Nature 350, 271-272. (doi:10.1038/ 350271a0)
49. Kullmann DM. 1994 Amplitude fluctuations of dualcomponent EPSCs in hippocampal pyramidal cells: implications for long-term potentiation. Neuron 12, 1111-1120. (doi:10.1016/0896-6273(94)90318-2)
50. Liao D, Hessler NA, Malinow R. 1995 Activation of postsynaptically silent synapses during pairinginduced LTP in CA1 region of hippocampal slices. Nature 375, 400-404. (doi:10.1038/375400a0)
51. Isaac JT, Nicoll RA, Malenka RC. 1995 Evidence for silent synapses: implications for the expression of LTP. Neuron 15, 427-434. (doi:10.1016/0896-6273(95)90046-2)
52. Durand GM, Kovalchuk Y, Konnerth A. 1996 Longterm potentiation and functional synapse induction in developing hippocampus. Nature 381, 71-75. (doi:10.1038/381071a0)
53. Emptage N, Bliss TV, Fine A. 1999 Single synaptic events evoke NMDA receptor-mediated release of calcium from internal stores in hippocampal dendritic spines. Neuron 22, 115-124. (doi:10. 1016/S0896-6273(00)80683-2)
54. 2+entry through the N-methyl-Daspartate channel. Proc. Natl Acad. Sci. USA 91, 8170-8174. (doi:10.1073/pnas.91.17.8170)
55. Yuste R, Denk W. 1995 Dendritic spines as basic functional units of neural integration. Nature 375, 682-684. (doi:10.1038/375682a0)
56. Emptage NJ, Reid CA, Fine A, Bliss TVP. 2003 Optical quantal analysis reveals a presynaptic component of LTP at hippocampal Schaffer-associational synapses. Neuron 38, 797-804. (doi:10.1016/S0896-6273(03)00325-8)
57. Reid CA, Dixon DB, Takahashi M, Bliss TV, Fine A. 2004 Optical quantal analysis indicates that longterm 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. (doi:10.1523/JNEUROSCI.3567-03.2004)
58. Enoki R, Hu YL, Hamilton D, Fine A. 2009 Expression of long-term plasticity at individual synapses in hippocampus is graded, bidirectional, and mainly presynaptic: optical quantal analysis. Neuron 62, 242-253. (doi:10.1016/j.neuron.2009.02.026)
59. Nicoll RA, Schmitz D. 2005 Synaptic plasticity at hippocampal mossy fibre synapses. Nat. Rev. Neurosci. 6, 863-876. (doi:10.1038/nrn1786)
60. Stevens CF, Wang YY. 1994 Changes in reliability of synaptic function as a mechanism for plasticity. Nature 371, 704-707. (doi:10.1038/371704a0)
61. Busetto G, Higley MJ, Sabatini BL. 2008 Developmental presence and disappearance of postsynaptically silent synapses on dendritic spines of rat layer 2/3 pyramidal neurons. J. Physiol. 586, 1519-1527. (doi:10.1113/jphysiol.2007.149336)
62. 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. (doi:10.1016/j.neuron.2006. 10.007)
63. Ehrlich I, Malinow R. 2004 Postsynaptic density 95 controls AMPA receptor incorporation during longterm potentiation and experience-driven synaptic plasticity. J. Neurosci. 24, 916-927. (doi:10.1523/ JNEUROSCI.4733-03.2004)
64. Schnell E, Sizemore M, Karimzadegan S, Chen L, Bredt DS, Nicoll RA. 2002 Direct interactions between PSD-95 and stargazin control synaptic AMPA receptor number. Proc. Natl Acad. Sci. USA 99, 13 902-13 907. (doi:10.1073/pnas.172511199)
65. Kim E, Sheng M. 2004 PDZ domain proteins of synapses. Nat. Rev. Neurosci. 5, 771-781. (doi:10. 1038/nrn1517)
66. Chen L, Chetkovich DM, Petralia RS, Sweeney NT, Kawasaki Y, Wenthold RJ, Bredt DS, Nicoll RA. 2000 Stargazin regulates synaptic targeting of AMPA receptors by two distinct mechanisms. Nature 408, 936-943. (doi:10.1038/35046031)
67. Tomita S, Adesnik H, Sekiguchi M, Zhang W, Wada K, Howe JR, Nicoll RA, Bredt DS. 2005 Stargazin modulates AMPA receptor gating and trafficking by distinct domains. Nature 435, 1052-1058. (doi:10. 1038/nature03624)
68. Xu W, Schluter OM, Steiner P, Czervionke BL, Sabatini B, Malenka RC. 2008 Molecular dissociation of the role of PSD-95 in regulating synaptic strength and LTD. Neuron 57, 248-262. (doi:10.1016/j. neuron.2007.11.027)
69. Dean C, Scholl FG, Choih J, DeMaria S, Berger J, Isacoff E, Scheiffele P. 2003 Neurexin mediates the assembly of presynaptic terminals. Nat. Neurosci. 6, 708-716. (doi:10.1038/nn1074)
70. El-Husseini AE, Schnell E, Chetkovich DM, Nicoll RA, Bredt DS. 2000 PSD-95 involvement in maturation of excitatory synapses. Science 290, 1364-1368. (doi:10.1126/science.290.5495.1364)
71. Beique JC, Andrade R. 2002 PSD-95 regulates synaptic transmission and plasticity in rat cerebral cortex. J. Physiol. 546, 859-867. (doi:10.1113/ jphysiol.2002.031369)
72. Stein V, House DR, Bredt DS, Nicoll RA. 2003 Postsynaptic density-95 mimics and occludes hippocampal long-term potentiation and enhances long-term depression. J. Neurosci. 23, 5503-5506.
73. Ehrlich I, Klein M, Rumpel S, Malinow R. 2007 PSD-95 is required for activity-driven synapse stabilization. Proc. Natl Acad. Sci. USA 104, 4176-4181. (doi:10.1073/pnas.0609307104)
74. Sturgill JF, Steiner P, Czervionke BL, Sabatini BL. 2009 Distinct domains within PSD-95 mediate synaptic incorporation, stabilization, and activity-dependent trafficking. J. Neurosci. 29, 12 845-12 854. (doi:10. 1523/JNEUROSCI.1841-09.2009)
75. Kopec CD, Real E, Kessels HW, Malinow R. 2007 GluR1 links structural and functional plasticity at excitatory synapses. J. Neurosci. 27, 13 706-13 718. (doi:10.1523/JNEUROSCI.3503-07.2007)
76. Ehlers MD, Heine M, Groc L, Lee MC, Choquet D. 2007 Diffusional trapping of GluR1 AMPA receptors by input-specific synaptic activity. Neuron 54, 447-460. (doi:10.1016/j.neuron.2007.04.010)
77. Plant K, Pelkey KA, Bortolotto ZA, Morita D, Terashima A, McBain CJ, Collingridge GL, Isaac JT. 2006 Transient incorporation of native GluR2-lacking AMPA receptors during hippocampal long-term potentiation. Nat. Neurosci. 9, 602-604. (doi:10. 1038/nn1678)
78. Chen X et al. 2011 PSD-95 is required to sustain the molecular organization of the postsynaptic density. J. Neurosci. 31, 6329-6338. (doi:10.1523/ JNEUROSCI.5968-10.2011)
79. Harris KM, Jensen FE, Tsao B. 1992 Threedimensional structure of dendritic spines and synapses in rat hippocampus (CA1) at postnatal day 15 and adult ages: implications for the maturation of synaptic physiology and long-term potentiation. J. Neurosci. 12, 2685-2705.
80. Chen X, Winters C, Azzam R, Li X, Galbraith JA, Leapman RD, Reese TS. 2008 Organization of the core structure of the postsynaptic density. Proc. Natl Acad. Sci. USA 105, 4453-4458. (doi:10.1073/pnas. 0800897105)
81. Takumi Y, Ramirez-Leon V, Laake P, Rinvik E, Ottersen OP. 1999 Different modes of expression of AMPA and NMDA receptors in hippocampal synapses. Nat. Neurosci. 2, 618-624. (doi:10. 1038/10172)
82. Rusakov DA, Kullmann DM. 1998 Extrasynaptic glutamate diffusion in the hippocampus: ultrastructural constraints, uptake, and receptor activation. J. Neurosci. 18, 3158-3170.
83. Raghavachari S, Lisman JE. 2004 Properties of quantal transmission at CA1 synapses. J. Neurophysiol. 92, 2456-2467. (doi:10.1152/jn.00258.2004)
84. Heine M, Groc L, Frischknecht R, Beique JC, Lounis B, Rumbaugh G, Huganir RL, Cognet L, Choquet D. 2008 Surface mobility of postsynaptic AMPARs tunes synaptic transmission. Science 320, 201-205. (doi:10.1126/science.1152089)
85. Regehr WG, Carey MR, Best AR. 2009 Activitydependent regulation of synapses by retrograde messengers. Neuron 63, 154-170. (doi:10.1016/j. neuron.2009.06.021)
86. Shepherd GM, Harris KM. 1998 Three-dimensional structure and composition of CA3!CA1 axons in rat hippocampal slices: implications for presynaptic connectivity and compartmentalization. J. Neurosci. 18, 8300-8310.
87. Schikorski T, Stevens CF. 1997 Quantitative ultrastructural analysis of hippocampal excitatory synapses. J. Neurosci. 17, 5858-5867.