Complexity of calcium signaling in synaptic spines

BioEssays

Volumn 24, Issue 12, 2002, Pages 1130-1144

  Franks, Kevin M ^a   Sejnowski, Terrence J ^b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b SALK INSTITUTE FOR BIOLOGICAL STUDIES   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CALCIUM;

ANIMAL; BIOLOGICAL MODEL; DENDRITE; FLUORESCENCE MICROSCOPY; HUMAN; LEARNING; MEMORY; METABOLISM; MONTE CARLO METHOD; NERVE CELL; PHYSIOLOGY; REVIEW; SIGNAL TRANSDUCTION; SYNAPSE; TIME;

ANIMALS; CALCIUM; DENDRITES; HUMANS; LEARNING; MEMORY; MICROSCOPY, FLUORESCENCE; MODELS, BIOLOGICAL; MONTE CARLO METHOD; NEURONS; SIGNAL TRANSDUCTION; SYNAPSES; TIME FACTORS;

EID: 0036906215     PISSN: 02659247     EISSN: None     Source Type: Journal    
DOI: 10.1002/bies.10193     Document Type: Review

References (90)

1. Churchland PS, Sejnowski TJ. The Computational Brain. Cambridge, Mass: MIT Press; 1992.
2. Bliss TV, Collingridge GL. A synaptic model of memory: Long-term potentiation in the hippocampus. Nature 1993;361:31-39.
3. Bliss TV, Lomo T. Long-lasting potentiation of synaptic transmission in the dentate area of the anaesthetized rabbit following stimulation of the perforant path. J Physiol (Lond) 1973;232:331-356.
4. Sejnowski TJ. Statistical constraints on synaptic plasticity. J Theor Biol 1977;69:385-389.
5. Bienenstock EL, Cooper LN, Munro PW. Theory for the development of neuron selectivity: Orientation specificity and binocular interaction in visual cortex. J Neurosci 1982;2:32-48.
6. Dunwiddie T, Lynch G. Long-term potentiation and depression of synaptic responses in the rat hippocampus: Localization and frequency dependency. J Physiol 1978;276:353-367.
7. Levy WB, Steward O. Temporal contiguity requirements for long-term associative potentiation/depression in the hippocampus. Neuroscience 1983;8:791-797.
8. Dudek SM, Bear MF. Homosynaptic long-term depression in area CA1 of hippocampus and effects of N-methyl-D-aspartate receptor blockade. Proc Natl Acad Sci USA 1992;89:4363-4367.
9. Malenka RC, Nicoll RA. Long-term potentiation - A decade of progress? Science 1999;285:1870-1874.
10. Bekkers JM, Stevens CF. NMDA and non-NMDA receptors are colocalized at individual excitatory synapses in cultured rat hippocampus. Nature 1989;341:230-233.
11. Isaac JT, Nicoll RA, Malenka RC. Evidence for silent synapses: Implications for the expression of LTP. Neuron 1995;15:427-434.
12. Takumi Y, Ramirez-Leon V, Laake P, Rinvik E, Ottersen OP. Different modes of expression of AMPA and NMDA receptors in hippocampal synapses. Nat Neurosci 1999;2:618-624.
13. Artola A, Singer W. Long-term depression of excitatory synaptic transmission and its relationship to long-term potentiation. Trends Neurosci 1993;16:480-487.
14. Lisman J. The CaM kinase II hypothesis for the storage of synaptic memory. Trends Neurosci 1994;17:406-412.
15. Lynch G, Larson J, Kelso S, Barrionuevo G, Schottler F. Intracellular injections of EGTA block induction of hippocampal long-term potentiation. Nature 1983;305:719-721.
16. Malenka RC, Kauer JA, Zucker RS, Nicoll RA. Postsynaptic calcium is sufficient for potentiation of hippocampal synaptic transmission. Science 1988;242:81-84
17. Mulkey RM, Malenka RC. Mechanisms underlying induction of homosynaptic long-term depression in area CA1 of the hippocampus. Neuron 1992;9:967-975.
18. Malinow R, Schulman H, Tsien RW. Inhibition of postsynaptic PKC or CaMKII blocks induction but not expression of LTP. Science 1989;245:862-866.
19. Silva AJ, Wang Y, Paylor R, Wehner JM, Stevens CF, Tonegawa S. Alpha calcium/calmodulin kinase II mutant mice: Deficient long-term potentiation and impaired spatial learning. Cold Spring Harb Symp Quant Biol 1992;57:527-539.
20. Mulkey RM, Herron CE, Malenka RC. An essential role for protein phosphatases in hippocampal long-term depression. Science 1993;261:1051-1055.
21. Mulkey RM, Endo S, Shenolikar S, Malenka RC. Involvement of a calcineurin/inhibitor-1 phosphatase cascade in hippocampal long-term depression. Nature 1994;369:486-488.
22. 2+ signaling requirements for long-term depression in the hippocampus. Neuron 1996;16:825-833.
23. Nishiyama M, Hong K, Mikoshiba K, Poo MM, Kato K. Calcium stores regulate the polarity and input specificity of synaptic modification. Nature 2000;408:584-588.
24. 2+ channels to homosynaptic long-term depression in the CA1 region in vitro. J Neurophysiol 1997;77:1651-1655.
25. Tang YP, Shimizu E, Dube GR, Rampon C, Kerchner GA, Zhuo M, Liu G, Tsien JZ. Genetic enhancement of learning and memory in mice. Nature 1999;401:63-69.
26. Malenka RC, Lancaster B, Zucker RS. Temporal limits on the rise in postsynaptic calcium required for the induction of long-term potentiation. Neuron 1992;9:121-128.
27. i needed to trigger LTD and LTP. Neuron 1996;16:619-629.
28. i elevation. J Neurophysiol 1999;81:781-787.
29. Wigstrom H, Gustafsson B, Huang YY, Abraham WC. Hippocampal long-term potentiation is induced by pairing single afferent volleys with intracellularly injected depolarizing current pulses. Acta Physiol Scand 1986;126:317-319.
30. Stuart GJ, Sakmann B. Active propagation of somatic action potentials into neocortical pyramidal cell dendrites. Nature 1994;367:69-72.
31. Debanne D, Gahwiler BH, Thompson SM. Long-term synaptic plasticity between pairs of individual CA3 pyramidal cells in rat hippocampal slice cultures. J Physiol 1998;507(Pt 1):237-247.
32. Bi GQ, Poo MM. Synaptic modifications in cultured hippocampal neurons: Dependence on spike timing, synaptic strength, and postsynaptic cell type. J Neurosci 1998;18:10464-10472.
33. Markram H, Lubke J, Frotscher M, Sakmann B. Regulation of synaptic efficacy by coincidence of postsynaptic APs and EPSPs. Science 1997;275:213-215.
34. Sjostrom PJ, Turrigiano GG, Nelson SB. Rate, timing, and cooperativity jointly determine cortical synaptic plasticity. Neuron 2001;32:1149-1164
35. Feldman DE. Timing-based LTP and LTD at vertical inputs to layer II/III pyramidal cells in rat barrel cortex. Neuron 2000;27:45-56.
36. Schuett S, Bonhoeffer T, Hubener M. Pairing-induced changes of orientation maps in cat visual cortex. Neuron 2001;32:325-337.
37. Yao H, Dan Y. Stimulus timing-dependent plasticity in cortical processing of orientation. Neuron 2001;32:315-323.
38. Zhang LI, Tao HW, Holt CE, Harris WA, Poo M. A critical window for cooperation and competition among developing retinotectal synapses. Nature 1998;395:37-44.
39. Yuste R, Denk W. Dendritic spines as basic functional units of neuronal integration. Nature 1995;375:682-684.
40. Magee JC, Johnston D. A synaptically controlled, associative signal for Hebbian plasticity in hippocampal neurons. Science 1997;275:209-213.
41. Koester HJ, Sakmann B. Calcium dynamics in single spines during coincident pre- and postsynaptic activity depend on relative timing of back-propagating action potentials and subthreshold excitatory postsynaptic potentials. Proc Natl Acad Sci USA 1998;95:9596-9601.
42. Yuste R, Majewska A, Cash SS, Denk W. Mechanisms of calcium influx into hippocampal spines: Heterogeneity among spines, coincidence detection by NMDA receptors, and optical quantal analysis. J Neurosci 1999;19:1976-1987.
43. 2+ ions in dendritic spines. Neuron 2002;33:439-452.
44. Denk W, Yuste R, Svoboda K, Tank DW. Imaging calcium dynamics in dendritic spines. Curr Opin Neurobiol 1996;6:372-378.
45. Zacharias DA, Baird GS, Tsien RY. Recent advances in technology for measuring and manipulating cell signals. Curr Opin Neurobiol 2000;10:416-421.
46. Yuste R, Majewska A, Holthoff K. From form to function: Calcium compartmentalization in dendritic spines. Nat Neurosci 2000;3:653-659.
47. Nimchinsky EA, Sabatini BL, Svoboda K. Structure and function of dendritic spines. Annu Rev Physiol 2002;64:313-353.
48. Mainen ZF, Malinow R, Svoboda K. Synaptic calcium transients in single spines indicate that NMDA receptors are not saturated. Nature 1999;399:151-155.
49. Sabatini BL, Svoboda K. Analysis of calcium channels in single spines using optical fluctuation analysis. Nature 2000;408:589-593.
50. Llinas R, Sugimori M, Silver RB. Microdomains of high calcium concentration in a presynaptic terminal. Science 1992;256:677-679.
51. Shaywitz AJ, Greenberg ME. CREB: A stimulus-induced transcription factor activated by a diverse array of extracellular signals. Annu Rev Biochem 1999;68:821-861.
52. Deisseroth K, Bito H, Tsien RW. Signaling from synapse to nucleus: Postsynaptic CREB phosphorylation during multiple forms of hippocampal synaptic plasticity. Neuron 1996;16:89-101.
53. Dolmetsch RE, Pajvani U, Fife K, Spotts JM, Greenberg ME. Signaling to the nucleus by an L-type calcium channel-calmodulin complex through the MAP kinase pathway. Science 2001;294:333-339.
54. Hardingham GE, Arnold FJ, Bading H. A calcium microdomain near NMDA receptors: On switch for ERK-dependent synapse-to-nucleus communication. Nat Neurosci 2001;4:565-566.
55. Takasu MA, Dalva MB, Zigmond RE, Greenberg ME. Modulation of NMDA receptor-dependent calcium influx and gene expression through EphB receptors. Science 2002;295:491-495.
56. Walikonis RS, Jensen ON, Mann M, Provance DW Jr, Mercer JA, Kennedy MB. Identification of proteins in the postsynaptic density fraction by mass spectrometry. J Neurosci 2000;20:4069-4080.
57. Husi H, Ward MA, Choudhary JS, Blackstock WP, Grant SG. Proteomic analysis of NMDA receptor-adhesion protein signaling complexes. Nat Neurosci 2000;3:661-669.
58. Valtschanoff JG, Weinberg RJ. Laminar organization of the NMDA receptor complex within the postsynaptic density. J Neurosci 2001;21:1211-1217.
59. Sheng M, Lee SH. Growth of the NMDA receptor industrial complex. Nat Neurosci 2000;3:633-635.
60. Kennedy MB. Signal-processing machines at the postsynaptic density. Science 2000;290:750-754.
61. Hayashi Y, Shi SH, Esteban JA, Piccini A, Poncer JC, Malinow R. Driving AMPA receptors into synapses by LTP and CaMKII: Requirement for GluR1 and PDZ domain interaction. Science 2000;287:2262-2267.
62. Wu J, Wang Y, Rowan MJ, Anwyl R. Evidence for involvement of the neuronal isoform of nitric oxide synthase during induction of long-term potentiation and long-term depression in the rat dentate gyrus in vitro. Neuroscience 1997;78:393-398.
63. English JD, Sweatt JD. A requirement for the mitogen-activated protein kinase cascade in hippocampal long term potentiation. J Biol Chem 1997;272:19103-19106.
64. Cho KO, Hunt CA, Kennedy MB. The rat brain postsynaptic density fraction contains a homolog of the Drosophila discs-large tumor suppressor protein. Neuron 1992;9:929-942.
65. Kornau HC, Seeburg PH, Kennedy MB. Interaction of ion channels and receptors with PDZ domain proteins. Curr Opin Neurobiol 1997;7:368-373.
66. Komau HC, Schenker LT, Kennedy MB, Seeburg PH. Domain interaction between NMDA receptor subunits and the postsynaptic density protein PSD-95. Science 1995;269:1737-1740.
67. Niethammer M, Kim E, Sheng M. Interaction between the C terminus of NMDA receptor subunits and multiple members of the PSD-95 family of membrane-associated guanylate kinases. J Neurosci 1996;16:2157-2163.
68. Kim E, Che KO, Rothschild A, Sheng M. Heteromultimerization and NMDA receptor-clustering activity of Chapsyn-110, a member of the PSD-95 family of proteins. Neuron 1996;17:103-113.
69. + channels in vivo. J Neurosci 1997;17:152-159.
70. Migaud M, Charlesworth P, Dempster M, Webster LC, Watabe AM, Makhinson M, He Y, Ramsay MF, Morris RG, Morrison JH, O'Dell TJ, Grant SG. Enhanced long-term potentiation and impaired learning in mice with mutant postsynaptic density-95 protein. Nature 1998;396:433-439.
71. Malenka RC. Synaptic plasticity in the hippocampus: LTP and LTD. Cell 1994;78:535-538.
72. Lee HK, Barbarosie M, Kameyama K, Bear MF, Huganir RL. Regulation of distinct AMPA receptor phosphorylation sites during bidirectional synaptic plasticity. Nature 2000;405:955-959.
73. Sanes JR, Lichtman JW. Can molecules explain long-term potentiation? Nat Neurosci 1999;2:597-604.
74. Stiles JR, Bartol TM Jr. Monte Carlo methods for simulating realistic synaptic microphysiology. In: de Schutter E, editor. Computational Neuroscience: Realistic Modeling for Experimentalists Boca Raton CRC Press; 2001. 87-127.
75. Stiles JR, Bartol TM Jr, Salpeter EE, Salpeter MM, Sejnowski TJ. Synaptic variability: New insights from reconstructions and Monte Carlo simulations with MCell. In: Cowan WM, Sudhof TC, Stevens CF, editors. Synapses Baltimore Johns Hopkins University Press; 2001. 681-731.
76. Bartol TM Jr, Land BR, Salpeter EE, Salpeter MM. Monte Carlo simulation of miniature endplate current generation in the vertebrate neuromuscular junction. Biophys J 1991;59:1290-1307.
77. Anglister L, Stiles JR, Salpeter MM. Acetylcholinesterase density and turnover number at frog neuromuscular junctions, with modeling of their role in synaptic function. Neuron 1994;12:783-794.
78. Stiles JR, Van Hefden D, Bartol TM Jr, Salpeter EE, Salpeter MM. Miniature endplate current rise times less than 100 microseconds from improved dual recordings can be modeled with passive acetylcholine diffusion from a synaptic vesicle. Proc Natl Acad Sci USA 1996;93:5747-5752.
79. Faber DS, Young WS, Legendre P, Korn H. Intrinsic quantal variability due to stochastic properties of receptor-transmitter interactions. Science 1992;258:1494-1498.
80. Wahl LM, Pouzat C, Stratford KJ. Monte Carlo simulation of fast excitatory synaptic transmission at a hippocampal synapse. J Neurophysiol 1996;75:597-608.
81. Franks KM, Bartol TM Jr, Sejnowski TJ. A Monte Carlo model reveals independent signaling at central glutamatergic synapses. Biophys J 2002;
82. Hines ML, Carnevale NT. The NEURON simulation environment. Neural Comput 1997;9:1179-1209.
83. Emptage N, Bliss TV, Fine A. Single synaptic events evoke NMDA receptor-mediated release of calcium from internal stores in hippocampal dendritic spines. Neuron 1999;22:115-124.
84. 2+ signals in spines of hippocampal neurons. J Neurosci 2000;20:1791-1799.
85. 2+ buffering in Purkinje neurons. Neuron 1999;24:989-1002.
86. Franks KM, Bartol TM Jr, Sejnowski TJ. An MCell model of calcium dynamics and frequency-dependence of calmodulin activation in dendritic spines. Neurocomput 2001;38-40:9-16.
87. Schiller J, Major G, Koester HJ, Schiller Y. NMDA spikes in basal dendrites of cortical pyramidal neurons. Nature 2000;404:285-289.
88. Wei DS, Mei YA, Bagal A, Kao JP, Thompson SM, Tang CM. Compartmentalized and binary behavior of terminal dendrites in hippocampal pyramidal neurons. Science 2001;293:2272-2275.
89. Svoboda K, Tank DW, Denk W. Direct measurement of coupling between dendritic spines and shafts. Science 1996;272:716-719.
90. Majewska A, Tashiro A, Yuste R. Regulation of spine calcium dynamics by rapid spine motility. J Neurosci 2000;20:8262-8268.