Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

  • Review Article
  • Published:

From form to function: calcium compartmentalization in dendritic spines

Abstract

Dendritic spines compartmentalize calcium, and this could be their main function. We review experimental work on spine calcium dynamics. Calcium influx into spines is mediated by calcium channels and by NMDA and AMPA receptors and is followed by fast diffusional equilibration within the spine head. Calcium decay kinetics are controlled by slower diffusion through the spine neck and by spine calcium pumps. Calcium release occurs in spines, although its role is controversial. Finally, the endogenous calcium buffers in spines remain unknown. Thus, spines are calcium compartments because of their morphologies and local influx and extrusion mechanisms. These studies highlight the richness and heterogeneity of pathways that regulate calcium accumulations in spines and the close relationship between the morphology and function of the spine.

This is a preview of subscription content, access via your institution

Access options

Rent or buy this article

Prices vary by article type

from$1.95

to$39.95

Prices may be subject to local taxes which are calculated during checkout

Figure 1: Two-photon imaging of spines.
Figure 2: Calcium dynamics in spines.
Figure 3: Optical quantal analysis of two neighboring spines.
Figure 4: Model of a spine.

Similar content being viewed by others

References

  1. Ramón y Cajal, S. Estructura de los centros nerviosos de las aves. Rev. Trim. Histol. Norm. Pat. 1, 1–10 (1888).

    Google Scholar 

  2. Ramón y Cajal, S. Significación fisiológica de las expansiones protoplásmicas y nerviosas de la sustancia gris. Congreso Médico 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).

    Article  CAS  Google Scholar 

  5. Palay, S. L. Synapses in the central nervous system. J Biophys. Biochem. Cytol. 2, 193–201 (1956).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  6. Gray, E. G. Electron microscopy of synaptic contacts on dendritic spines of the cerebral cortex. Nature 183, 1592–1594 (1959).

    Article  CAS  PubMed  Google Scholar 

  7. Shepherd, G. M. The Synaptic Organization of the Brain (Oxford Univ. Press, Oxford, 1990).

    Google Scholar 

  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).

    Google Scholar 

  9. Rall, W. & Segev, I. in Computer Simulation in Brain Science (ed. Cotterill, R. M. J.) 26–43 (Cambridge Univ. Press, Cambridge, UK, 1988).

    Book  Google Scholar 

  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).

    Article  CAS  PubMed  Google Scholar 

  11. Shepherd, G. The dendritic spine: a multifunctional integrative unit. J. Neurophysiol. 75, 2197–2210 (1996).

    Article  CAS  PubMed  Google Scholar 

  12. Koch, K. in Biophysics of Computation (ed. Koch, C.) 280–308 (Oxford Univ. Press, New York, 1999).

    Google Scholar 

  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).

    Article  CAS  PubMed  Google Scholar 

  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).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  15. Holmes, W. Is the function of dendritic spines to concentrate calcium? Brain Res. 519, 338–342 (1990).

    Article  CAS  PubMed  Google Scholar 

  16. Koch, C. & Zador, A. The function of dendritic spines—devices subserving biochemical rather than electrical compartmentalization. J. Neurosci. 13, 413–422 (1993).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  17. Miller, S. & Kennedy, M. Distinct forebrain and cerebellar isozymes of type II Ca2+/calmodulin-dependent protein kinase associate differently with the postsynaptic density fraction. J. Biol. Chem. 260, 9039–9046 (1985).

    CAS  PubMed  Google Scholar 

  18. Miller, S. G. & Kennedy, M. B. Regulation of brain type II Ca2+/calmodulin-dependent protein kinase by autophosphorylation: a Ca2+-triggered molecular switch. Cell 44, 861–870 (1986).

    Article  CAS  PubMed  Google Scholar 

  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).

    Article  CAS  PubMed  Google Scholar 

  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).

    Article  CAS  PubMed  Google Scholar 

  21. Tsien, R. Y. Fluorescent probes of cell signaling. Annu. Rev. Neurosci. 12, 227–253 (1989).

    Article  CAS  PubMed  Google Scholar 

  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).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  23. Fine, A., Amos, W. B., Durbin, R. M. & McNaughton, P. A. Confocal microscopy: applications in neurobiology. Trends Neurosci. 11, 345–351 (1988).

    Article  Google Scholar 

  24. Denk, W., Strickler, J. H. & Webb, W. W. Two-photon laser scanning fluorescence microscopy. Science 248, 73–76 (1990).

    Article  CAS  PubMed  Google Scholar 

  25. Neher, E. & Augustine, G. J. Calcium gradients and buffers in bovine chromaffin cells. J. Physiol.(Lond.) 450, 273–301 (1992).

    Article  CAS  Google Scholar 

  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).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  27. Neher, E. Usefulness and limitations of linear approximations to the understanding of Ca++ signals. Cell Calcium 24, 345–375 (1998).

    Article  CAS  PubMed  Google Scholar 

  28. Regehr, W. & Tank, D. Dendritic calcium dynamics. Curr. Opin. Neurobiol. 4, 373–382 (1994).

    Article  CAS  PubMed  Google Scholar 

  29. Helmchen, F. in Dendrites (eds. Stuart, G., Spruston, N. & Hausser, M.) 161–192 (Oxford Univ. Press, Oxford, 1999).

    Google Scholar 

  30. Gamble, E. & Koch, C. The dynamics of free calcium in dendritic spines in response to repetitive input. Science 236, 1311–1315 (1987).

    Article  CAS  PubMed  Google Scholar 

  31. Müller, W. & Connor, J. A. Dendritic spines as individual neuronal compartments for synaptic Ca2+ responses. Nature 354, 73–76 (1991).

    Article  PubMed  Google Scholar 

  32. Guthrie, P. B., Segal, M. & Kater, S. B. Independent regulation of calcium revealed by imaging dendritic spines. Nature 354, 76–80 (1991).

    Article  CAS  PubMed  Google Scholar 

  33. Alford, S., Frenguelli, B. G., Schofield, J. G. & Collingridge, G. L. Characterization of the Ca2+ signals induced in hippocampal CA1 neurons by the synaptic activation of NMDA receptors. J. Physiol. (Lond.) 469, 693–716 (1993).

    Article  CAS  Google Scholar 

  34. Jaffe, D., Fisher, S. & Brown, T. Confocal laser scanning microscopy reveals voltage-gated calcium signals within hippocampal dendritic spines. J. Neurobiol. 25, 220–233 (1994).

    Article  CAS  PubMed  Google Scholar 

  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).

    CAS  Google Scholar 

  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).

    Article  CAS  PubMed  Google Scholar 

  37. Denk, W. et al. Anatomical and functional imaging of neurons using 2-photon laser scanning microscopy. J. Neurosci. Methods 54, 151–162 (1994).

    Article  CAS  PubMed  Google Scholar 

  38. Yuste, R. & Denk, W. Dendritic spines as basic units of synaptic integration. Nature 375, 682–684 (1995).

    Article  CAS  PubMed  Google Scholar 

  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).

    Google Scholar 

  40. Hebb, D. O. The Organization of Behaviour (Wiley, New York, 1949).

    Google Scholar 

  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. Acta. Physiol. Scand. 126, 317–319 (1986).

    Article  CAS  PubMed  Google Scholar 

  42. Magee, J. C. & Johnston, D. A synaptically controlled, associative signal for hebbian plasticity in hippocampal neurons. Science 275, 209–212 (1997).

    Article  CAS  PubMed  Google Scholar 

  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).

    Article  CAS  PubMed  Google Scholar 

  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).

    Article  CAS  PubMed  Google Scholar 

  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).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  46. Petrozzino, J., Pozzo Miller, L. & Connor, J. Micromolar Ca2+ transients in dendritic spines of hippocampal pyramidal neurons in brain slice. Neuron 14, 1223–1231 (1995).

    Article  CAS  PubMed  Google Scholar 

  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).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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).

    Article  CAS  PubMed  Google Scholar 

  49. Pozzo-Miller, L., Inoue, T. & Murphy, D. Estradiol increases spine density and NMDA-dependent Ca2+ transients in spines of CA1 pyramidal neurons from hippocampal slices. J. Neurophysiol. 81, 1404–1411 (1999).

    Article  CAS  PubMed  Google Scholar 

  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).

    Article  CAS  PubMed  Google Scholar 

  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).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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).

    Article  CAS  PubMed  Google Scholar 

  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).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  55. Furuichi, T. et al. Multiple types of ryanodine receptor/Ca2+ release channels are differentially expressed in rabbit brain. J. Neurosci. 14, 4794–4805 (1994).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  56. Berridge, M. J. Neuronal calcium signaling. Neuron 21, 13–26 (1998).

    Article  CAS  PubMed  Google Scholar 

  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).

    Article  CAS  PubMed  Google Scholar 

  58. Furuichi, T., Kohda, K., Miyawaki, A. & Mikoshiba, K. Intracellular channels. Curr. Opin. Neurobiol. 4, 294–303 (1994).

    Article  CAS  PubMed  Google Scholar 

  59. Korkotian, E. & Segal, M. Fast confocal imaging of calcium released from stores in dendritic spines. Eur. J. Neurosci. 10, 2076–2084 (1998).

    Article  CAS  PubMed  Google Scholar 

  60. Györke, I. & Györke, S. Regulation of the cardiac ryanodine receptor channel by luminal Ca2+ involves luminal Ca2+ sensing sites. Biophys. J. 75, 2801–2810 (1998).

    Article  PubMed  PubMed Central  Google Scholar 

  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).

    Article  CAS  PubMed  Google Scholar 

  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).

    Article  CAS  PubMed  Google Scholar 

  63. Takechi, H., Eilers, J. & Konnerth, A. A new class of synaptic response involving calcium release in dendritic spines. Nature 396, 757–760 (1998).

    Article  CAS  PubMed  Google Scholar 

  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).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  65. Markram, H., Roth, A. & Helmchen, F. Competitive calcium binding: Implications for dendritic calcium signaling. J. Comput. Neurosci. 5, 331–348 (1998).

    Article  CAS  PubMed  Google Scholar 

  66. Gabso, M., Neher, E. & Spira, M. E. Low mobility of the Ca2+ buffers in axons of cultured Aplysia neurons. Neuron 18, 473–481 (1997).

    Article  CAS  PubMed  Google Scholar 

  67. Helmchen, F., Imoto, K. & Sakmann, B. Ca2+ buffering and action potential-evoked Ca2+ signalling in dendrites of pyramidal neurons. Biophys. J. 70, 1069–1081 (1996).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  69. Fierro, L. & Llano, I. High endogenous calcium buffering in Purkinje cells from rat cerebellar slices. J. Physiol. (Lond.) 496, 617–625 (1996).

    Article  CAS  Google Scholar 

  70. Maeda, H., Ellis-Davis, G. C. R., It, O. K., Miyashita, Y. & Kasai, H. Supralinear Ca2+ signaling by cooperative and mobile Ca2+ buffering in Purkinje neurons. Neuron 24, 989–1002 (1999).

    Article  CAS  PubMed  Google Scholar 

  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).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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).

    Article  CAS  PubMed  Google Scholar 

  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).

    Article  CAS  PubMed  Google Scholar 

  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).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  75. Llinás, R., Sugimori, M. & Silver, R. B. Microdomains of high calcium concentration in a presynaptic terminal. Science 256, 677–679 (1992).

    Article  PubMed  Google Scholar 

  76. Naraghi, M. & Neher, E. Linearized buffered Ca2+ diffusion in microdomains and its implications for calculation of [Ca2+] at the mouth of a calcium channel. J. Neurosci. 17, 6961–6973 (1997).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  77. Svoboda, K., Tank, D. W. & Denk, W. Direct measurement of coupling between dendritic spines and shafts. Science 272, 716–719 (1996).

    Article  CAS  PubMed  Google Scholar 

  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).

    Article  CAS  PubMed  Google Scholar 

  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).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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).

    Article  CAS  Google Scholar 

  81. Stauffer, T. P., Guerini, D. & Carafoli, E. Tissue distribution of the four gene products of the plasma membrane Ca2+ pump. A study using specific antibodies. J. Biol. Chem. 270, 12184–12190 (1995).

    Article  CAS  PubMed  Google Scholar 

  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).

    Article  CAS  PubMed  Google Scholar 

  83. Guerini, D. et al. The expression of plasma membrane Ca2+ pump isoforms in cerebellar granule neurons is modulated by Ca2+. J. Biol. Chem. 274, 1667–1676 (1999).

    Article  CAS  PubMed  Google Scholar 

  84. Schikorski, T. & Stevens, C. Quantitative fine-structural analysis of olfactory cortical synapses. Proc. Natl. Acad. Sci. USA 96, 4107–4112 (1999).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  85. Sobel, E. C. & Tank, D. W. In vivo Ca2+ dynamics in a cricket auditory neuron: an example of chemical computation. Science 263, 823–826 (1994).

    Article  CAS  PubMed  Google Scholar 

  86. Hopfield, J. J. Neural networks and physical systems with emergent collective computational abilities. Proc. Natl. Acad. Sci. USA 79, 2554–2558 (1982).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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).

    Article  PubMed  PubMed Central  Google Scholar 

  89. Siegel, M. S. & Isacoff, E. Y. A genetically encoded optical probe of membrane voltage. Neuron 19, 735–741 (1997).

    Article  CAS  PubMed  Google Scholar 

  90. Rose, C., Kovalchuk, Y., Eilers, J. & Konnerth, A. Two-photon Na+ imaging in spines and fine dendrites of central neurons. Pflugers Arch. 439, 201–207 (1999).

    CAS  PubMed  Google Scholar 

  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).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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).

    Article  CAS  PubMed  Google Scholar 

  93. Fischer, M., Kaech, S., Knutti, D. & Matus, A. Rapid actin-based plasticity in dendritic spine. Neuron 20, 847–854 (1998).

    Article  CAS  PubMed  Google Scholar 

  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).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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).

    Article  CAS  PubMed  Google Scholar 

  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).

    Article  CAS  PubMed  Google Scholar 

  97. Kubota, Y. & Kawaguchi, Y. Dependence of GABAergic synaptic areas on the interneuron type and target size. J. Neurosci. 20, 375–386 (2000).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  98. Maletic-Savatic, M., Malinow, R. & Svoboda, K. Rapid dendritic morphogenesis in CA1 hippocampal dendrites induced by synaptic activity. Science 283, 1923–1927 (1999).

    Article  CAS  PubMed  Google Scholar 

  99. Engert, F. & Bonhoeffer, T. Dendritic spine changes associated with hippocampal long-term synaptic plasticity. Nature 399, 66–70 (1999).

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

We thank A. Tashiro for Fig. 1, E. Brown, J. Goldberg and J. Kozloski for comments, and M. Kennedy, A. Marks, G. Shepherd, S. Siegelbaum, P. Somogyi, C. Stevens and G. Tamas for discussions. Our laboratory is funded by the National Eye Institute (EY 111787) and the Human Frontier Science Program.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Rafael Yuste.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Yuste, R., Majewska, A. & Holthoff, K. From form to function: calcium compartmentalization in dendritic spines. Nat Neurosci 3, 653–659 (2000). https://doi.org/10.1038/76609

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1038/76609

This article is cited by

Search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing