From form to function: Calcium compartmentalization in dendritic spines

Nature Neuroscience

Volumn 3, Issue 7, 2000, Pages 653-659

  Yuste, Rafaël ^a   Majewska, Ania ^a   Holthoff, Knut ^a  

^a Och Spine at New York Presbyterian Hospitals   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMPA RECEPTOR; CALCIUM CHANNEL; CALCIUM ION; N METHYL DEXTRO ASPARTIC ACID RECEPTOR;

CALCIUM CONDUCTANCE; CALCIUM TRANSPORT; CELL COMPARTMENTALIZATION; CELL STRUCTURE; DENDRITIC SPINE; DIFFUSION; ENDOPLASMIC RETICULUM; NONHUMAN; PRIORITY JOURNAL; REVIEW; SYNAPTIC MEMBRANE;

ANIMALS; BRAIN; CALCIUM; CALCIUM SIGNALING; CALCIUM-BINDING PROTEINS; DENDRITES; HUMANS; MODELS, NEUROLOGICAL; NEURONS; RECEPTORS, AMPA; RECEPTORS, N-METHYL-D-ASPARTATE;

EID: 0033947688     PISSN: 10976256     EISSN: None     Source Type: Journal    
DOI: 10.1038/76609     Document Type: Review

References (99)

1. Ramón y Cajal, S. Estructura de los centros nerviosos de las aves. Rev. Trim. Histol. Norm. Pat. I, 1-10 (1888).
2. Ramón y Cajal, S. Significación fisiológica de las expansiones protoplásmicas y nerviosas de la sustancia gris. Congreso Medico Valenciano. June 24 (1891).
3. Ramón y Cajal, S. Neue darstellung vom histologischen bau des centralnervensystem. Arch. Anat. Entwick. 319-428 (1893).
4. DeRobertis, E. D. P. & Bennett, H. S. Some features of the submicroscopic morphology of synapses in frog and earthworm. J. Biophys. Biochem. Cytol. 1, 47-58 (1955).
5. Palay, S. L. Synapses in the central nervous system. J Biophys. Biochem. Cytol. 2, 193-201 (1956).
6. Gray, E. G. Electron microscopy of synaptic contacts on dendritic spines of the cerebral cortex. Nature 183, 1592-1594 (1959).
7. Shepherd, G. M. The Synaptic Organization of the Brain (Oxford Unív. Press, Oxford, 1990).
8. Rall, W. in Cellular Mechanisms Subserving Changes in Neuronal Activity (eds. Woody, C. D., Brown, K. A., Crow, T. J. & Knispel, J. D.) 13-21 (Brain Information Services, Los Angeles, California, 1974).
9. Rail, W. & Segev, I. in Computer Simulation in Brain Science (ed. Cotterill, R. M. J.) 26-43 (Cambridge Univ. Press, Cambridge, UK, 1988).
10. Harris, K. M. & Kater, S. B. Dendritic spines: cellular specializations imparting both stability and flexibility to synaptic function. Annu. Rev. Neurosci. 17, 341-371 (1994).
11. Shepherd, G. The dendritic spine: a multifunctional integrative unit. J. Neurophysiol. 75, 2197-2210 (1996).
12. Koch, K. in Biophysics of Computation (ed. Koch, C.) 280-308 (Oxford Univ. Press, New York, 1999).
13. Wickens, J. Electrically coupled but chemically isolated synapses: dendritic spines and calcium in a rule for synaptic modification. Prog. Neurobiol 31, 507-528 (1988).
14. Lisman, J. A mechanism for the Hebb and anti-Hebb processes underlying learning and memory. Proc. Natl. Acad. Sci. USA 86, 9574-9578 (1989).
15. Holmes, W. Is the function of dendritic spines to concentrate calcium? Brain Res. 519, 338-342 (1990).
16. Koch, C. & Zador, A. The function of dendritic spines - devices subservíng biochemical rather than electrical compartmentalization. J. Neurosci. 13, 413-422 (1993).
17. 2+/calmodulin-dependent protein kinase associate differently with the postsynaptic density fraction. J. Biol. Chem. 260, 9039-9046 (1985).
18. 2+-triggered molecular switch. Cell 44, 861-870 (1986).
19. Lynch, G., Larson, J., Kelso, S., Barrionuevo, G. & Schottler, F. Intracellular injections of EGTA block induction of hippocampal long-term potentiation. Nature 305, 719-721 (1983).
20. Malenka, R. C., Kauer, J. A., Zucker R. S. & Nicoll R. A. Postsynaptic calcium is sufficient for potentiation of hippocampal synaptic transmission. Science 242, 81-84 (1988).
21. Tsien, R. Y. Fluorescent probes of cell signaling. Annu. Rev. Neurosci. 12, 227-253 (1989).
22. Connor, J. A. Digital imaging of free calcium changes and of spatial gradients in growing processes in single, mammalian central nervous system cells. Proc. Natl. Acad. Sci. USA 83, 6179-6183 (1986).
23. Fine, A., Amos, W. B., Durbin, R. M. & McNaughton, P. A. Confocal microscopy: applications in neurobiology. Trends Neurosci. 11, 345-351 (1988).
24. Denk, W., Strickler, J. H. & Webb, W. W. Two-photon laser scanning fluorescence microscopy. Science 248, 73-76 (1990).
25. Neher, E. & Augustine, G. J. Calcium gradients and buffers in bovine chromaffin cells. J. Physiol.(Lond.) 450, 273-301 (1992).
26. Tank, D. W., Delaney, K. D. & Regehr, W. G. The quantitative analysis of presynaptic calcium dynamics that contribute to short-term synaptic enhacement. J. Neurosci. 15, 7940-7952 (1995).
27. ++ signals. Cell Calcium 24, 345-375 (1998).
28. Regehr, W. & Tank, D. Dendritic calcium dynamics. Curr. Opin. Neurobiol. 4, 373-382 (1994).
29. Helmchen, F. in Dendrites (eds. Stuart, G., Spruston, N. & Hausser, M.) 161-192 (Oxford Univ. Press, Oxford, 1999).
30. Gamble, E. & Koch, C. The dynamics of free calcium in dendritic spines in response to repetitive input. Science 236, 1311-1315 (1987).
31. Müller, W. &Connor, J. A. Dendritic spines as individual neuronal compartments for synaptic Ca responses. Nature 354, 73-76 (1991).
32. Guthrie, P. B., Segal, M. &Kater, S. B. Independent regulation of calcium revealed by imaging dendritic spines. Nature 354, 76-80 (1991).
33. Alford, S., Frenguelli, B. G., Schofield, I. G. &Collingridge, G. L Characterization of the Ca signals induced in hippocampal CAl neurons by the synaptic activation of NMDA receptors. /. Physiol. (Land.) 469, 693-716(1993).
34. Jaffe, D., Fisher, S. &Brown, T. Confocal laser scanning microscopy reveals voltage-gated calcium signals within hippocampal dendritic spines. /. Neurobiol. 25, 220-233 (1994).
35. Murphy, T. H., Baraban, J. M., Gil Wier, W. &Blatter, L. A. Visualization of quantal synaptic transmission by dendritic calcium imaging. Nature 263, 529-532(1994).
36. Murphy, T, Baraban, J. &Wier, W. Mapping miniature synaptic currents to single synapses using calcium imaging reveals heterogeneity in postsynaptic output. Neuron 15, 159-168 (1995).
37. Denk, W. et al. Anatomical and functional imaging of neurons using 2-photon laser scanning microscopy. /. Neurosci. Methods 54, 151-162 (1994).
38. Yuste, R. &Denk, W. Dendritic spines as basic units of synaptic integration. Nature 375, 682-684 (1995).
39. Ariens-Kapper, C. U., Huber, G. C. &Crosby, E. C. The Comparative Anatomy of the Nervous System of Vertebrates, Including Man 73-94 (MacMillan, New York, 1936).
40. Hebb, D. O. The Organization of Behaviour (Wiley, New York, 1949).
41. Wigstrom, H., Gustafsson, B., Huang, Y.-Y. &Abraham, W. C. Hippocampal long-term potentiation is induced by pairing single afferent volleys with intracellularly injected depolarizing current pulses. Acts. Physiol. Scand. 126,317-319 (1986).
42. Magee, I. C. &Johnston, D. A synaptically controlled, associative signal for hebbian plasticity in hippocampal neurons. Science 275, 209-212 (1997).
43. Markram, H., Luebke, J-, Frotscher, M. &Sakmann, B. Regulation of synaptic efficacy by coincidence of postsynaptic APs and EPSPs. Science 275, 213-215 (1997).
44. Zhang, L., Tao, H., Holt, C., Harris, W. &Poo, M. A critical window for cooperation and competition among developing retinotectal synapses. Nature 395, 37-44(1998).
45. Denk, W., Sugimori, M. & Llinás, R. Two types of calcium response limited to single spines in cerebellar Purkinje cells. Proc. Natl. Acad. Sci. USA 92, 8279-8282 (1995).
46. 2+ transients in dendritic spines of hippocampal pyramidal neurons in brain slice. Neuron 14, 1223-1231 (1995).
47. Yuste, R., Majewska, A., Cash, S. & Denk, W. Mechanisms of calcium influx into spines: Heterogeneity among spines, coincidence detection by NMDA receptors and optical quantal analysis. J. Neurosci. 19, 1976-1987 (1999).
48. Emptage, N., Bliss, T. V. & Fine, A. Single synaptic events evoke NMDA receptor-mediated release of calcium from internal stores in hippocampal dendritic spines. Neuron 22, 115-124 (1999).
49. 2+ transients in spines of CA1 pyramidal neurons from hippocampal slices. J. Neurophysiol. 81, 1404-1411 (1999).
50. Mainen, Z., Malinow, R. & Svoboda, K. Synaptic calcium transients in single spines indicate that NMDA receptors are not saturated. Nature 399, 151-155 (1999).
51. Kovalchuk, Y., Eilers, J., Lisman, J. & Konnerth, A. NMDA receptor-mediated subthreshold Ca(2+) signals in spines of hippocampal neurons. J. Neurosci. 20, 1791-1799 (2000).
52. Koester, H. J. & 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 95, 9596-9601 (1998).
53. Schiller, J., Schiller, Y. & Clapham, D. NMDA receptors amplify calcium influx into dendritic spines during associative pre- and postsynaptic activation. Nat. Neurosci. 1, 114-118 (1998).
54. Marks, A. et al. Molecular cloning and characterization of the ryanodine receptor/junctional channel complex cDNA from skeletal muscle sarcoplasmic reticulum. Proc. Natl. Acad. Sci. USA 86, 8683-8687 (1989).
55. 2+ release channels are differentially expressed in rabbit brain. J. Neurosci. 14, 4794-4805 (1994).
56. Berridge, M. J. Neuronal calcium signaling. Neuron 21, 13-26 (1998).
57. Nabauer, M., Callewaert, G., Cleemann, L. & Morad, M. Regulation of calcium release is gated by calcium current, not gating charge, in cardiac myocytes. Science 244, 800-803 (1989).
58. Furuichi, T., Kohda, K., Miyawaki, A. & Mikoshiba, K. Intracellular channels. Curr. Opin. Neurobiol. 4, 294-303 (1994).
59. Korkotian, E. & Segal, M. Fast confocal imaging of calcium released from stores in dendritic spines. Eur. J. Neurosci. 10, 2076-2084 (1998).
60. 2+ sensing sites. Biophys. J. 75, 2801-2810 (1998).
61. Colonnier, M. Synaptic patterns on different cell types in the different laminae of the cat visual cortex. An electron microscope study. Brain Res. 9, 268-287 (1968).
62. Finch, E. A. & Augustine, G. J. Local calcium signalling by inositol-1,4,5-trisphosphate in Purkinje cell dendrites. Nature 396, 753-756 (1998).
63. Takechi, H., Eilers, J. & Konnerth, A. A new class of synaptic response involving calcium release in dendritic spines. Nature 396, 757-760 (1998).
64. Petersen, C., Malenka, R., Nicoll, R. & Hopfield, J. All-or-none potentiation at CA3-CA1 synapses. Proc. Natl. Acad. Sci. USA 95, 4732-4737 (1998).
65. Markram, H., Roth, A. & Helmchen, F. Competitive calcium binding: Implications for dendritic calcium signaling. J. Comput. Neurosci. 5, 331-348 (1998).
66. 2+ buffers in axons of cultured Aplysia neurons. Neuron 18, 473-481 (1997).
67. 2+ signalling in dendrites of pyramidal neurons. Biophys. J. 70, 1069-1081 (1996).
68. Murthy, V. N., Sejnowski, T. & Stevens, C. Dynamics of dendritic calcium transients evoked by quantal release at excitatory hippocampal synapses. Proc. Natl. Acad. Sci. USA 97, 901-906 (2000).
69. Fierro, L. & Llano, I. High endogenous calcium buffering in Purkinje cells from rat cerebellar slices. J. Physiol. (Lond.) 496, 617-625 (1996).
70. 2+ buffering in Purkinje neurons. Neuron 24, 989-1002 (1999).
71. Airaksinen, M. S., Eiler, J., Garaschuk, O., Thoenen, H. & Konnerth, A. Ataxia and altered dendritic calcium signaling in mice carrying a targeted null mutation of the calbindin D28k gene. Proc. Natl. Acad. Sci. USA 94, 1488-1493 (1997).
72. Batini, C., Pelstini, M., Thonasset, M. & Vigot, R. Cytoplasmic calcium buffer, calbindin-D28k, is regulated by excitatory amino acids. Neuroreport 4, 927-930 (1993).
73. Allbritton, N. L., Meyer, T. & Stryer, L. Range of messenger action of calcium ion and inositol 1,4,5-trisphosphate. Science 258, 1812-1815 (1992).
74. Eilers, J., Callewaert, G., Armstrong, C. & Konnerth, A. Calcium signaling in a narrow somatic submembrane shell during synaptic activity in cerebellar Purkinje neurons. Proc. Natl. Acad. Sci. USA 92, 10272-10276 (1995).
75. Llinás, R., Sugimori, M. & Silver, R. B. Microdomains of high calcium concentration in a presynaptic terminal. Science 256, 677-679 (1992).
76. 2+] at the mouth of a calcium channel. J. Neurosci. 17, 6961-6973 (1997).
77. Svoboda, K., Tank, D. W. & Denk, W. Direct measurement of coupling between dendritic spines and shafts. Science 272, 716-719 (1996).
78. Volfovsky, N., Parnas, H., Segal, M. & Korkotian, E. Geometry of dendritic spines affects calcium dynamics in hippocampal neurons: theory and experiments. J. Neurophysiol. 82, 450-462 (1999).
79. Majewska, A., Brown, E., Ross, J. & Yuste, R. Mechanisms of calcium decay kinetics in hippocampal spines: role of spine calcium pumps and calcium diffusion through the spine neck in biochemical compartmentalization. J. Neurosci. 20, 1722-1734 (2000).
80. Hunter, T. The Croonian Lecture 1997. The phosphorylation of proteins on tyrosine: its role in cell growth and disease. Phil. Trans. R. Soc. Lond. B Biol. Sci. 353, 583-605 (1998).
81. 2+ pump. A study using specific antibodies. J. Biol. Chem. 270, 12184-12190 (1995).
82. Miller, K. K., Verma, A., Snyder, S. H. & Ross, C. A. Localization of an endoplasmic reticulum calcium ATPase in rat brain by in situ hybridization. Neuroscience 43, 1-9 (1991).
83. 2+. J. Biol. Chem. 274, 1667-1676 (1999).
84. Schikorski, T. & Stevens, C. Quantitative fine-structural analysis of olfactory cortical synapses. Proc. Natl. Acad. Sci. USA 96, 4107-4112 (1999).
85. 2+ dynamics in a cricket auditory neuron: an example of chemical computation. Science 263, 823-826 (1994).
86. Hopfield, J. J. Neural networks and physical systems with emergent collective computational abilities. Proc. Natl. Acad. Sci. USA 79, 2554-2558 (1982).
87. Goodman, M. & Lockery, S. Pressure polishing: a method for re-shaping patch pipettes during fire-polishing. J. Neurosci. Methods (in press).
88. González, J. E. & Tsien, R. Y. Voltage sensing by fluorescence resonance energy transfer in single cells. Biophys. J. 69, 1272-1280 (1995).
89. Siegel, M. S. & Isacoff, E. Y. A genetically encoded optical probe of membrane voltage. Neuron 19, 735-741 (1997).
90. + imaging in spines and fine dendrites of central neurons. Pflugers Arch. 439, 201-207 (1999).
91. Harris, K. M. & Stevens, J. K. Dendritic spines of CA1 pyramidal cells in the rat hippocampus: serial electron microscopy with reference to their biophysical characteristics. J. Neurosci. 9, 2982-2997 (1989).
92. Nusser, Z. et al. Cell type and pathway dependence of synaptic AMPA receptor number and variability in the hippocampus. Neuron 21, 545-559 (1998).
93. Fischer, M., Kaech, S., Knutti, D. & Matus, A. Rapid actin-based plasticity in dendritic spine. Neuron 20, 847-854 (1998).
94. Dunaevsky, A., Tashiro, A., Majewska, A., Mason, C. A. & Yuste, R. Developmental regulation of spine motility in mammalian CNS. Proc. Natl. Acad. Sci. USA 96, 13438-13443 (1999).
95. Somogyi, P., Tamas, G., Lujan, R. & Buhl, E. Salient features of synaptic organisation in the cerebral cortex. Brain Res. Rev. 26, 113-135 (1998).
96. Gupta, A., Wang, Y. & Markram, H. Organizing principles for a diversity of GABAergic interneurons and synapses in the neocortex. Science 287, 273-278 (2000).
97. Kubota, Y. & Kawaguchi, Y. Dependence of GABAergic synaptic areas on the interneuron type and target size. J. Neurosci. 20, 375-386 (2000).
98. Maletic-Savatic, M., Malinow, R. & Svoboda, K. Rapid dendritic morphogenesis in CA1 hippocampal dendrites induced by synaptic activity. Science 283, 1923-1927 (1999).
99. Engert, F. & Bonhoeffer, T. Dendritic spine changes associated with hippocampal long-term synaptic plasticity. Nature 399, 66-70 (1999).