AMPA receptors regulate dynamic equilibrium of presynaptic terminals in mature hippocampal networks

Nature Neuroscience

Volumn 6, Issue 5, 2003, Pages 491-500

  De Paola, Vincenzo ^a   Arber, Silvia ^b   Caroni, Pico ^a  

^a FRIEDRICH MIESCHER INSTITUTE FOR BIOMEDICAL RESEARCH   (Switzerland)

^b UNIVERSITY OF BASEL   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

AMPA RECEPTOR; CYCLIC AMP DEPENDENT PROTEIN KINASE; GREEN FLUORESCENT PROTEIN;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRAIN SLICE; CELL MATURATION; CONTROLLED STUDY; ELECTROSTIMULATION; EXPERIENCE; FLUORESCENCE; HIPPOCAMPUS; MOSSY FIBER; MOUSE; NERVE CELL MEMBRANE; NERVE CELL NETWORK; NERVE ENDING; NEUROPIL; NONHUMAN; PRIORITY JOURNAL; PROTEIN SYNTHESIS; SIGNAL TRANSDUCTION; SPINE; SYNAPSE; SYNAPSE VESICLE;

EID: 0242585297     PISSN: 10976256     EISSN: None     Source Type: Journal    
DOI: 10.1038/nn1046     Document Type: Article

References (48)

1. Bailey, C.H. & Kandel, E.R. Structural changes accompanying memory storage. Annu. Rev. Physiol. 55, 397-426 (1993).
2. Ziv, N.E. & Smith, S.J. Evidence for a role of dendritic filopodia in synaptogenesis and spine formation. Neuron 17, 91-102 (1996).
3. Marrs, G.S., Green, S.H. & Dailey, M.E. Rapid formation and remodeling of postsynaptic densities in developing dendrites. Nat. Neurosci. 4, 1006-1013 (2001).
4. Yuste, R. & Bonhoeffer, T. Morphological changes in dendritic spines associated with long-term synaptic plasticity. Annu. Rev. Neurosci, 24, 1071-1089 (2001).
5. Matus, A. Actin-based plasticity in dendritic spines. Science 290, 754-758 (2000).
6. Smart, F.M. & Halpain, S. Regulation of dendritic spine stability. Hippocampus 10, 542-554 (2000).
7. Lendvai, B., Stern, E.A., Chen, B. & Svoboda, K. Experience-dependent plasticity of dendritic spines in the developing rat barrel cortex in vivo. Nature 404, 876-881 (2000).
8. Engert, E & Bonhoeffer, T. Dendritic spine changes associated with hippocampal long-term synaptic plasticity. Nature 399, 66-70 (1999).
9. Toni, N., Buchs, P.A., Nikonenko, I., Bron, C.R. & Muller, D. LTP promotes formation of multiple spine synapses between a single axon terminal and a dendrite. Nature 402, 421-425 (1999).
10. Yankova, M., Hart, S.A. & Woolley, C.S. Estrogen increases synaptic connectivity between single presynaptic inputs and multiple postsynaptic CA1 pyramidal cells: a serial electron-microscopic study. Proc. Natl. Acad. Sci. USA 98, 3525-3530 (2001).
11. Luscher, C., Nicoll, R.A., Malenka, R.C. & Muller, D. Synaptic plasticity and dynamic modulation of the postsynaptic membrane. Nat. Neurosci. 3, 545-550 (2000).
12. Cline, H.T. Dendritic arbor development and synaptogenesis. Curr. Opin. Neurobiol. 11, 118-126 (2001).
13. Stoppini, L., Buchs, P.A. & Muller, D. A simple method for organotypic cultures of nervous tissue. J. Neurosci. Methods 37, 173-182 (1991).
14. Gahwiler, B.H., Capogna, M., Debanne, D., McKinney, R.A. & Thompson, S.M. Organotypic slice cultures: a technique has come of age. Trends Neurosci. 20, 471-477 (1997).
15. Henze, D.A., Urban, N.N. & Barrionuevo, G. The multifarious hippocampal mossy fiber pathway: a review. Neuroscience 98,407-427 (2000).
16. Claiborne, B.J., Amaral, D.G. & Cowan, W.M. A light and electron microscopic analysis of the mossy fibers of the rat dentate gyrus. J. Comp. Neurol. 246, 435-458 (1986).
17. Toth, K. & McBain, C.J. Target-specific expression of pre- and postsynaptic mechanisms. J. Physiol. 525, 41-51 (2000).
18. Acsady, L., Kamondi, A., Sik, A., Freund, T. & Buzsaki, G. GABAergic cells are the major postsynaptic targets of mossy fibers in the rat hippocampus. J. Neurosci. 18, 3386-3403 (1998).
19. Toth, K., Suares, G., Lawrence, J.J., Philips-Tansey, E. & McBain, C.J. Differential mechanisms of transmission at three types of mossy fiber synapse. J. Neurosci. 20, 8279-8289 (2000).
20. Amaral, D.G. Synaptic extensions from the mossy fibers of the fascia dentata. Anat. Embryol. (Berl.) 155, 241-251 (1979).
21. Li, Z. & Murthy, V.N. Visualizing postendocytic traffic of synaptic vesicles at hippocampal synapses. Neuron 31, 593-605 (2001).
22. Ahmari, S.E., Buchanan, J. & Smith, S.J. Assembly of presynaptic active zones from cytoplasmic transport packets. Nat. Neurosci. 3, 445-451 (2000).
23. Davis, G.W. & Bezprozvanny, I. Maintaining the stability of neural function: a homeostatic hypothesis. Annu. Rev. Physiol. 63, 847-869 (2001).
24. Dailey, M.E., Buchanan, J., Bergles, D.E. & Smith, S.J. Mossy fiber growth and synaptogenesis in rat hippocampal slices in vitro. J. Neurosci. 14, 1060-1078 (1994).
25. Ziv, N.E. & Garner, C.C. Principles of glutamatergic synapse formation: seeing the forest for the trees. Curr. Opin. Neurobiol. 11, 536-543 (2001).
26. Friedman, H.V., Bresler, T., Garner, C.C. & Ziv, N.E. Assembly of new individual excitatory synapses: time course and temporal order of synaptic molecule recruitment. Neuron 27, 57-69 (2000).
27. Mizuhashi, S., Nishiyama, N., Matsuki, N. & Ikegaya, Y. Cyclic nucleotide mediated regulation of hippocampal mossy fiber development: a targetspecific guidance. J. Neurosci. 21, 6181-6194 (2001).
28. Baranes, D. et al. Tissue plasminogen activator contributes to the late phase of LTP and to synaptic growth in the hippocampal mossy fiber pathway. Neuron 21, 813-825 (1998).
29. Hatada, Y., Wu, E, Sun, Z.Y., Schacher, S. & Goldberg, D.J. Presynaptic morphological changes associated with long-term synaptic facilitation are triggered by actin polymerization at preexisting varicosities. J. Neurosci. 20, RC82 (2000).
30. Bozdagi, O., Shan, W., Tanaka, H., Benson, D.L. & Huntley, G.W. Increasing numbers of synaptic puncta during late-phase LTP: N-cadherin is synthesized, recruited to synaptic sites, and required for potentiation. Neuron 28, 245-259 (2000).
31. Ma, L., Zablow, L., Kandel, E.R. & Siegelbaum, S.A. Cyclic AMP induces functional presynaptic boutons in hippocampal CA3-CA1 neuronal cultures. Nat. Neurosci. 2, 24-30 (1999).
32. Patterson, S.L. et al. Some forms of cAMP-mediated long-lasting potentiation are associated with release of BDNF and nuclear translocation of phosphoMAP kinase. Neuron 32, 123-140 (2001).
33. Horch, H.W., Kruttgen, A., Portbury, S.D. & Katz, L.C. Destabilization of cortical dendrites and spines by BDNE Neuron 23, 353-364 (1999).
34. Poo, M.M. Neurotrophins as synaptic modulators. Nat. Rev. Neurosci. 2, 24-32 (2001).
35. Castillo, P.E., Schoch, S., Schmitz, F., Sudhof, T.C. & Malenka, R.C. RIM1α is required for presynaptic long-term potentiation. Nature 415, 327-330 (2002).
36. Cremer, H. et al. Inactivation of the N-CAM gene in mice results in size reduction of the olfactory bulb and deficits in spatial learning. Nature 367, 455-459 (1994).
37. Antonova, I. et al. Rapid increase in dusters of presynaptic proteins at onset of long-lasting potentiation. Science 294, 1547-1550 (2001).
38. Nimchinsky, E.A., Sabatini, B.L. & Svoboda, K. Structure and function of dendritic spines. Annu. Rev. Physiol. 64, 313-353 (2002).
39. Dailey, M.E. & Smith, S.J. The dynamics of dendritic structure in developing hippocampal slices. J. Neurosci. 16, 2983-2994 (1996).
40. Bastmeyer, M. & O'Leary, D.D. Dynamics of target recognition by interstitial axon branching along developing cortical axons. J. Neurosci. 16, 1450-1459 (1996).
41. Pennetta, G., Hiesinger, P., Fabian-Fine, R., Meinertzhagen, I. & Bellen, H. Drosophila VAP-33A directs bouton formation at neuromuscular junctions in a dosage-dependent manner. Neuron 35, 291 (2002).
42. Lichtman, J.W. & Colman, H. Synapse elimination and indelible memory. Neuron 25, 269-278 (2000).
43. Shi, S., Hayashi, Y., Esteban, J.A. & Malinow, R. Subunit-specific rules governing AMPA receptor trafficking to synapses in hippocampal pyramidal neurons. Cell 105, 331-343 (2001).
44. Okabe, S., Kim, H.D., Miwa, A., Kuriu, T. & Okado, H. Continual remodeling of postsynaptic density and its regulation by synaptic activity. Nat. Neurosci. 2, 804-811 (1999).
45. Pun, S. et al. An intrinsic distinction in neuromuscular junction assembly and maintenance in different skeletal muscles. Neuron 34, 357-370 (2002).
46. Caroni, P. Overexpression of growth-associated proteins in the neurons of adult transgenic mice. J. Neurosci. Methods 71, 3-9 (1997).
47. Wiederkehr, A., Staple, J. & Caroni, P. The motility-associated proteins GAP-43, MARCKS, and CAP-23 share unique targeting and surface activityinducing properties. Exp. Cell Res. 236, 103-116 (1997).
48. Feng, G. et al. Imaging neuronal subsets in transgenic mice expressing multiple spectral variants of GFP. Neuron 28, 41-51 (2000).