Spine expansion and stabilization associated with long-term potentiation

Journal of Neuroscience

Volumn 28, Issue 22, 2008, Pages 5740-5751

  Yang, Yunlei ^a   Wang, Xiao Bin ^a   Frerking, Matthew ^b   Zhou, Qiang ^a  

^a MOUNT SINAI SCHOOL OF MEDICINE   (United States)

^b OREGON HEALTH AND SCIENCE UNIVERSITY   (United States)

Author keywords

Actin; Ampa receptors; Dendritic spines; Depotentiation; LTP; Two photon imaging

Indexed keywords

CYCLIC AMP DEPENDENT PROTEIN KINASE; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; 8 BROMO CYCLIC AMP; AMINO ACID RECEPTOR BLOCKING AGENT; ENZYME INHIBITOR;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DENDRITIC SPINE; EXOCYTOSIS; HIPPOCAMPUS; LEARNING; LONG TERM POTENTIATION; MEMORY; NERVE CELL PLASTICITY; NERVE STIMULATION; NONHUMAN; PATCH CLAMP; PRIORITY JOURNAL; PYRAMIDAL NERVE CELL; RAT; SPINE; SPINE STABILIZATION; ANIMAL; CYTOLOGY; DRUG EFFECT; ELECTROSTIMULATION; EXCITATORY POSTSYNAPTIC POTENTIAL; IN VITRO STUDY; METHODOLOGY; NERVE CELL INHIBITION; NEWBORN; NONPARAMETRIC TEST; PHYSIOLOGY; RADIATION EXPOSURE; RADIATION RESPONSE; SIGNAL TRANSDUCTION; SPRAGUE DAWLEY RAT; ULTRASTRUCTURE;

8-BROMO CYCLIC ADENOSINE MONOPHOSPHATE; ANIMALS; ANIMALS, NEWBORN; CYCLIC AMP-DEPENDENT PROTEIN KINASES; DENDRITIC SPINES; DOSE-RESPONSE RELATIONSHIP, RADIATION; ELECTRIC STIMULATION; ENZYME INHIBITORS; EXCITATORY AMINO ACID ANTAGONISTS; EXCITATORY POSTSYNAPTIC POTENTIALS; HIPPOCAMPUS; LONG-TERM POTENTIATION; NEURAL INHIBITION; PATCH-CLAMP TECHNIQUES; PYRAMIDAL CELLS; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, N-METHYL-D-ASPARTATE; SIGNAL TRANSDUCTION; STATISTICS, NONPARAMETRIC;

EID: 45949085855     PISSN: 02706474     EISSN: 02706474     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.3998-07.2008     Document Type: Article

References (81)

1. Ambros-Ingerson J, Holmes WR (2005) Analysis and comparison of morphological reconstructions of hippocampal field CA1 pyramidal cells. Hippocampus 15:302-315.
2. Ashby MC, Maier SR, Nishimune A, Henley JM (2006) Lateral diffusion drives constitutive exchange of AMPA receptors at dendritic spines and is regulated by spine morphology. J Neurosci 26:7046-7055.
3. Bagal AA, Kao JP, Tang CM, Thompson SM (2005) Long-term potentiation of exogenous glutamate responses at single dendritic spines. Proc Natl Acad Sci USA 102:14434-14439.
4. Baliga BS, Pronczuk AW, Munro HN (1969) Mechanism of cycloheximide inhibition of protein synthesis in a cell-free system prepared from rat liver. J Biol Chem 244:4480-4489.
5. Banke TG, Bowie D, Lee H, Huganir RL, Schousboe A, Traynelis FF (2000) Control of GluR1 AMPA receptor function by cAMP-dependent protein kinase. J Neurosci 20:89-102.
6. Bliss TV, Collingridge GL (1993) A synaptic model of memory: long-term potentiation in the hippocampus. Nature 361:31-39.
7. Blitzer RD, Wong T, Nouranifar R, Iyenger R, Landau EM (1995) Postsynaptic cAMP pathway gates early LTP in hippocampal CA1 region. Neuron 15:1403-1414.
8. Blitzer RD, Connor JH, Brown GP, Wong T, Shenolikar S, Iyengar R, Landau EM (1998) Gating of CaMKII by cAMP-regulated protein phosphatase activity during LTP. Science 280:1940-1942.
9. Bloodgood BL, Sabatini BL (2005) Neuronal activity regulates diffusion across the neck of dendritic spines. Science 310:866-869.
10. Brown GP, Blitzer RD, Connor JH, Wong T, Shenolikar S, Iyebgar R, Landau EM (2000) Long-term potentiation induced by theta frequency stimulation is regulated by a protein phosphatase-1-operated gate. J Neurosci 20:7880-7887.
11. Chen LY, Rex CS, Casale MS, Gall CM, Lynch G (2007) Changes in synaptic morphology accompany actin signaling during LTP. J Neurosci 27:5363-5372.
12. Desmond NL, Levy WB (1983) Synaptic correlates of associative potentiation/depression: an ultrastructural study in the hippocampus. Brain Res 265:21-30.
13. Desmond NL, Levy WB (1986) Changes in the numerical density of synaptic contacts with long-term potentiation in the hippocampal dentate gyrus. J Comp Neurol 253:466-475.
14. Dinman JD, Ruiz-Echevarria MJ, Czaplinski K, Peltz SW (1997) Peptidyl-transferase inhibitors have antiviral properties by altering programmed-1 ribosomal frameshifting efficiencies: development of model systems. Proc Natl Acad Sci USA 94:6606-6611.
15. Duffy SN, Nguyen PV (2003) Postsynaptic application of a peptide inhibitor of cAMP-dependent protein kinase blocks expression of long-lasting synaptic potentiation in hippocampal neurons. J Neurosci 23:1142-1150.
16. Edwards FA (1995) Anatomy and electrophysiology of fast central synapses lead to a structural model of long-term potentiation. Physiol Rev 75:759-787.
17. 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.
18. Engert F, Bonhoeffer T (1999) Dendritic spine changes associated with hippocampal long-term synaptic plasticity. Nature 399:66-70.
19. Esteban JA, Shi SH, Wilson C, Nuriya M, Huganir RL, Malinow R (2003) PKA phosphorylation of AMPA receptor subunits controls synaptic trafficking underlying plasticity. Nat Neurosci 6:136-143.
20. Fifkova E, Morales M (1992) Actin matrix of dendritic spines, synaptic plasticity, and long-term potentiation. Int Rev Cytol 139:267-307.
21. Fifkova E, Van Harreveld A (1977) Long-lasting morphological changes in dendritic spines of dentate granular cells following stimulation of the entorhinal area. J Neurocytol 6:211-230.
22. Frey U, Huang YY, Kandel ER (1993) Effects of cAMP simulate a late stage of LTP in hippocampal CA1 neurons. Science 260:1661-1664.
23. Fukazawa Y, Saitoh Y, Ozawa F, Ohta Y, Mizuno K, Inokuchi K (2003) Hippocampal LTP is accompanied by enhanced F-actin content within the dendritic spine that is essential for late LTP maintenance in vivo. Neuron 38:447-460.
24. Golding NL, Staff NP, Spruston N (2002) Dendritic spikes as a mechanism for cooperative long-term potentiation. Nature 418:326-331.
25. Harris KM (1999) Structure, development, and plasticity of dendritic spines. Curr Opin Neurobiol 9:343-348.
26. Hayashi Y, Majewska AK (2005) Dendritic spine geometry: functional implication and regulation. Neuron 46:529-532.
27. Holtmaat AJ, Trachtenberg JT, Wilbrecht L, Shepherd GM, Zhang X, Knott GW, Svoboda K (2005) Transient and persistent dendritic spines in the neocortex in vivo. Neuron 45:279-291.
28. Hsieh H, Boehm J, Sato C, Iwatsubo T, Tomita T, Sisodia S, Malinow R (2006) AMPAR removal underlies Abeta-induced synaptic depression and dendritic spine loss. Neuron 52:831-843.
29. Huang YY, Kandel ER (2005) Theta frequency stimulation up-regulates the synaptic strength of the pathway from CA1 to subiculum region of hippocampus. Proc Natl Acad Sci USA 102:9365-9370.
30. Huang YY, Nguyen PV, Kandel ER (1996) Long-lasting forms of synaptic potentiation in the mammalian hippocampus. Learn Mem 3:74-85.
31. Huang YY, Pittenger C, Kandel ER (2004) A form of long-lasting, learning-related synaptic plasticity in the hippocampus induced by heterosynaptic low-frequency pairing. Proc Natl Acad Sci USA 101:859-864.
32. Kang-Park MH, Sarda MA, Jones KH, Moore SD, Shenolikar S, Clark S, Wilson WA (2003) Protein phosphatases mediate depotentiation induced by high-intensity theta-burst stimulation. J Neurophysiol 89:684-690.
33. Kasai H, Matsuzaki M, Noguchi J, Yasumatsu N, Nakahara H (2003) Structure-stability-function relationships of dendritic spines. Trends Neurosci 26:360-368.
34. Kopec CD, Li B, Wei W, Boehm J, Malinow R (2006) Glutamate receptor exocytosis and spine enlargement during chemically induced long-term potentiation. J Neurosci 26:2000-2009.
35. Kopec CD, Real E, Kessels HW, Malinow R (2007) GluR1 links structural and functional plasticity at excitatory synapses. J Neurosci 27:13706-13718.
36. Korkotian E, Segal M (2006) Spatially confined diffusion of calcium in dendrites of hippocampal neurons revealed by flash photolysis of caged calcium. Cell Calcium 40:441-449.
37. Kramar EA, Lin B, Rex CS, Gall CM, Lynch G (2006) Integrin-driven actin polymerization consolidates long-term potentiation. Proc Natl Acad Sci USA 103:5579-5584.
38. Lang C, Barco A, Zablow L, Kandel ER, Siegelbaum SA, Zakharenko SS (2004) Transient expansion of synaptically connected dendritic spines upon induction of hippocampal long-term potentiation. Proc Natl Acad Sci USA 101:16665-16670.
39. Larson J, Xiao P, Lynch G (1993) Reversal of LTP by theta frequency stimulation. Brain Res 600:97-102.
40. Lin B, Kramar EA, Bi X, Brucher FA, Gall CM, Lynch G (2005) Theta stimulation polymerizes actin in dendritic spines of hippocampus. J Neurosci 25:2062-2069.
41. Lisman J, Raghavachari S (2006) A unified model of the presynaptic and postsynaptic changes during LTP at CA1 synapses. Sci STKE 356:re11.
42. Lledo PM, Zhang X, Sudhof TC, Malenka RC, Nicoll RA (1998) Postsynaptic membrane fusion and long-term potentiation. Science 279:399-403.
43. Lüscher C, Xia H, Beattie EC, Carroll RC, von Zastrow M, Malenka RC, Nicoll RA (1999) Role of AMPA receptor cycling in synaptic transmission and plasticity. Neuron 24:649-658.
44. Lüscher C, Nicoll RA, Malenka RC, Muller D (2000) Synaptic plasticity and dynamic modulation of the postsynaptic membrane. Nat Neurosci 3:545-550.
45. Magee JC, Johnston D (1997) A synaptically controlled, associative signal for Hebbian plasticity in hippocampal neurons. Science 275:209-213.
46. Makhinson M, Opazo P, Carlisle HJ, Godsil B, Grant GN, O'Dell TJ (2006) A novel role for cyclic guanosine 3′,5′ monophosphate signaling in synaptic plasticity: a selective suppressor of protein kinase A-dependent forms of long-term potentiation. Neuroscience 140:415-431.
47. Maletic-Savatic M, Malinow R, Svoboda K (1999) Rapid dendritic morphogenesis in CA1 hippocampal dendrites induced by synaptic activity. Science 283:1923-1927.
48. Malinow R, Malenka RC (2002) AMPA receptor trafficking and synaptic plasticity. Annu Rev Neurosci 25:103-126.
49. Matsuzaki M, Honkura N, Ellis-Davies GC, Kasai H (2004) Structural basis of long-term potentiation in single dendritic spines. Nature 429:761-766.
50. Nguyen PV, Woo NH (2003) Regulation of hippocampal synaptic plasticity by cyclic AMP-dependent protein kinases. Prog Neurobiol 71:401-437.
51. Nimchinsky EA, Sabatini BL, Svoboda K (2002) Structure and function of dendritic spines. Annu Rev Physiol 64:313-353.
52. Nosyreva ED, Huber KM (2006) Metabotropic receptor-dependent long-term depression persists in the absence of protein synthesis in the mouse model of fragile X syndrome. J Neurophysiol 95:3291-3295.
53. Obrig TG, Culp WJ, McKeehan WL, Hardesty B (1971) The mechanism by which cycloheximide and related glutarimide antibiotics inhibit peptide synthesis on reticulocyte ribosomes. J Biol Chem 246:174-181.
54. O'Dell TJ, Kandel ER (1994) Low-frequency stimulation erases LTP through an NMDA receptor-mediated activation of protein phosphatases. Learn Mem 1:129-139.
55. Oh MC, Derkach VA, Guire ES, Soderling TR (2006) Extrasynaptic membrane trafficking regulated by GluR1 serine 845 phosphorylation primes AMPA receptors for long-term potentiation. J Biol Chem 281:752-758.
56. Okamoto K, Nagai T, Miyawaki A, Hayashi Y (2004) Rapid and persistent modulation of actin dynamics regulates postsynaptic reorganization underlying bidirectional plasticity. Nat Neurosci 7:1104-1112.
57. Ostroff LE, Fiala JC, Allwardt B, Harris KM (2002) Polyribosomes redistribute from dendritic shafts into spines with enlarged synapses during LTP in developing rat hippocampal slices. Neuron 35:535-545.
58. Otmakhova NA, Otmakhov N, Mortenson LH, Lisman JE (2000) Inhibition of the cAMP pathway decreases early long-term potentiation at CA1 hippocampal synapses. J Neurosci 20:4446-4451.
59. Otto T, Eichenbaum H, Wiener SI, Wibble CG (1991) Learning-related patterns of CA1 spike trains parallel stimulation parameters optimal for inducing hippocampal long-term potentiation. Hippocampus 1:181-192.
60. 2+/calmodulin- dependent protein kinase II via dendritic protein synthesis in hipocampal neurons. J Neurosci 19:7823-7833.
61. Park M, Penick EC, Edwards JG, Kauer JA, Ehlers MD (2004) Recycling endosomes supply AMPA receptors for LTP. Science 305:1972-1975.
62. Park M, Salgado JM, Ostroff L, Helton TD, Robinson CG, Harris KM, Ehlers MD (2006) Plasticity-induced growth of dendritic spines by exocytic trafficking from recycling endosomes. Neuron 52:817-830.
63. Pfeiffer BE, Huber KM (2006) Current advances in local protein synthesis and synaptic plasticity. J Neurosci 26:7147-7150.
64. Pike FG, Meredith RM, Olding AW, Paulsen O (1999) Rapid report: postsynaptic bursting is essential for "Hebbian" induction of associative long-term potentiation at excitatory synapses in rat hippocampus. J Physiol (Lond) 518:571-576.
65. Rao SS, Grollman AP (1967) Cycloheximide resistance in yeast: a property of the 60S ribosomal subunit. Biochem Biophys Res Commun 29:696-704.
66. Rodriguez A, Ehlenberger DB, Hof PR, Wearne SL (2006) Rayburst sampling, an algorithm for automated three-dimensional shape analysis from laser scanning microscopy images. Nat Protoc 1:2152-2161.
67. Rodriguez-Fonseca C, Amils R, Garrett RA (1995) Fine structure of the peptidyl transferase center on 23 S-like rRNAs deduced from chemical probing of antibiotic-ribosome complexes. J Mol Biol 247:224-235.
68. Segal M (2005) Dendritic spines and long-term plasticity. Nat Rev Neurosci 6:277-284.
69. 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.
70. Stewart MG, Medvedev NI, Popov VI, Schoepfer R, Davies HA, Murphy K, Dallerac GM, Kraev IV, Rodriguez JJ (2005) Chemically induced long-term potentiation increases the number of perforated and complex postsynaptic densities but does not alter dendritic spine volume in CA1 of adult mouse hippocampal slices. Eur J Neurosci 21:3368-3378.
71. Toni N, Buchs PA, Nikonenko I, Bron CR, Muller D (1999) LTP promotes formation of multiple spine synapses between a single axon terminal and a dendrite. Nature 402:421-425.
72. Toni N, Buchs PA, Nikonenko I, Povilaitite P, Parisi L, Muller D (2001) Remodeling of synaptic membranes after induction of long-term potentiation. J Neurosci 21:6245-62551.
73. Tsokas P, Grace EA, Chan P, Ma T, Sealfon SC, Iyengar R, Landau EM, Blitzer RD (2005) Local protein synthesis mediates a rapid increase in dendritic elongation factor 1A after induction of late long-term potentiation. J Neurosci 25:5833-5843.
74. van Praag H, Christie BR, Sejnowski TJ, Gage FH (1999) Running enhances neurogenesis, learning, and long-term potentiation in mice. Proc Natl Acad Sci USA 96:13427-13431.
75. Wang XB, Yang Y, Zhou Q (2007) Independent expression of synaptic and morphological plasticity associated with long-term depression. J Neurosci 27:12419-12429.
76. + channels contribute to spike-timing dependent long-term potentiation in hippocampal pyramidal neurons. Proc Natl Acad Sci USA 99:8366-8371.
77. Wearne SL, Rodriguez A, Ehlenberger DB, Rocher AB, Henderson SC, Hof PR (2005) New techniques for imaging, digitization and analysis of three-dimensional neural morphology on multiple scales. Neuroscience 136:661-680.
78. Yin HH, Davis MI, Ronesi JA, Lovinger DM (2006) The role of protein synthesis in striatal long-term depression. J Neurosci 26:11811-11820.
79. Yuste R, Bonhoeffer T (2001) Morphological changes in dendritic spines associated with long-term synaptic plasticity. Annu Rev Neurosci 24:1071-1089.
80. Zhou Q, Tao HW, Poo MM (2003) Reversal and stabilization of synaptic modifications in a developing visual system. Science 300:1953-1957.
81. Zhou Q, Homma KJ, Poo MM (2004) Shrinkage of dendritic spines associated with long-term depression of hippocampal synapses. Neuron 44:749-757.