Dendritic spines and long-term plasticity (original) (raw)

• Cajal, S. R. Histology of the Nervous System of Man and Vertebrate (Oxford Univ. Press, 1995; first published 1899) (trans. Swanson, N & Swanson, L. W.).
  Google Scholar
• Rosenzweig, M. R. & Bennett, E. L. Psychobiology of plasticity: effects of training and experience on brain and behavior. Behav. Brain Res. 78, 57–65 (1996).
  Article CAS PubMed Google Scholar
• Purpura, D. P. Pathobiology of cortical neurons in metabolic and unclassified amentias. Res. Publ. Assoc. Res. Nerv. Ment. Dis. 57, 43–68 (1979).
  CAS PubMed Google Scholar
• Sorra, K. E. & Harris, K. M. Overview on the structure, composition, function, development, and plasticity of hippocampal dendritic spines. Hippocampus 10, 501–511 (2000).
  Article CAS PubMed Google Scholar
• Popov, V. I. et al. Remodelling of synaptic morphology but unchanged synaptic density during late phase long-term potentiation (LTP): a serial section electron micrograph study in the dentate gyrus in the anaesthetised rat. Neuroscience 128, 251–262 (2004).
  Article CAS PubMed Google Scholar
• Yuste, R. & Bonhoeffer, T. Genesis of dendritic spines: insights from ultrastructural and imaging studies. Nature Rev. Neurosci. 5, 24–34 (2004).
  Article CAS Google Scholar
• Trachtenberg, J. T. et al. Long term in vivo imaging of experience-dependent synaptic plasticity in adult cortex. Nature 420, 788–794 (2002). In vivo 2-photon chronic imaging of the barrel field in adult mice, showing that at least half of the dendritic spines in cortical neurons live less than one month, and so questioning the long-held belief that spines are stable structures (but see references 8 and 62 for contradictory observations).
  Article CAS PubMed Google Scholar
• Mizrahi, A. & Katz, L. C. Dendritic stability in the adult olfactory bulb. Nature Neurosci. 6, 1201–1207 (2003).
  Article CAS PubMed Google Scholar
• Jourdain, P., Fukunaga, K. & Muller, D. Calcium/calmodulin-dependent protein kinase II contributes to activity-dependent filopodia growth and spine formation. J. Neurosci. 23, 10645–10649 (2003).
  Article CAS PubMed PubMed Central Google Scholar
• Goldin, M., Segal, M. & Avignone, E. Functional plasticity triggers formation and pruning of dendritic spines in cultured hippocampal networks. J. Neurosci. 21, 186–193 (2001).
  Article CAS PubMed PubMed Central Google Scholar
• Engert, F. & Bonhoeffer, T. Dendritic spine changes associated with hippocampal long-term synaptic plasticity. Nature 399, 66–70 (1999). The first confocal microscopic study to show the formation of new spines after LTP in cultured hippocampal slices. These results were extended by the work described in reference 10, which also showed that the new spines are innervated by presynaptic terminals in cultured hippocampal neurons.
  Article CAS PubMed Google Scholar
• 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
• Dailey, M. E. & Smith, S. J. The dynamics of dendritic structure in developing hippocampal slices. J. Neurosci. 16, 2983–2994 (1996).
  Article CAS PubMed PubMed Central Google Scholar
• El-Husseini, A. E., Schnell, E., Chetkovich, D. M., Nicoll, R. A. & Bredt, D. S. PSD-95 involvement in maturation of excitatory synapses. Science 290, 1364–1368 (2000).
  Article CAS PubMed Google Scholar
• Abe, K., Chisaka, O., Van Roy, F. & Takeichi, M. Stability of dendritic spines and synaptic contacts is controlled by α N-catenin. Nature Neurosci. 7, 357–363 (2004).
  Article CAS PubMed Google Scholar
• Woolley, C. S. & McEwen, B. S. Roles of estradiol and progesterone in regulation of hippocampal dendritic spine density during the estrous cycle in the rat. J. Comp. Neurol. 336, 293–306 (1993). Showed for the first time that dendritic spine density in the hippocampus can vary by as much as 30% across the oestrus cycle in adult female rats, bringing into question the relevance of spine density changes to memory storage.
  Article CAS PubMed Google Scholar
• Star, E. N., Kwiatkowski, D. J. & Murthy, V. N. Rapid turnover of actin in dendritic spines and its regulation by activity. Nature Neurosci. 5, 239–246 (2002).
  Article CAS PubMed Google Scholar
• Bernstein, B. W. & Bamburg, J. R. Actin-ATP hydrolysis is a major energy drain for neurons. J. Neurosci. 23, 1–6 (2003).
  Article CAS PubMed PubMed Central Google Scholar
• Fischer, M., Kaech, S., Knutti, D. & Matus, A. Rapid actin-based plasticity in dendritic spines. Neuron 20, 847–854 (1998). An elegant demonstration that dendritic spines move and change their size and shape continuously. This raises questions about the relevance of a 20% change in spine size after conditioning
  Article CAS PubMed Google Scholar
• Richards, D. A., De Paola, V., Caroni, P., Gahwiler, B. H. & McKinney, R. A. AMPA-receptor activation regulates the diffusion of a membrane marker in parallel with dendritic spine motility in the mouse hippocampus. J. Physiol. (Lond.) 558, 503–512 (2004).
  Article CAS Google Scholar
• Popov, V. I., Bocharova, L. S. & Bragin, A. G. Repeated changes of dendritic morphology in the hippocampus of ground squirrels in the course of hibernation. Neuroscience 48, 45–51 (1992).
  Article CAS PubMed Google Scholar
• Bock, J. & Braun, K. Blockade of _N_-methyl-D-aspartate receptor activation suppresses learning-induced synaptic elimination. Proc. Natl Acad. Sci. USA 96, 2485–2490 (1999).
  Article CAS PubMed PubMed Central Google Scholar
• Hasbani, M. J., Schlief, M. L., Fisher, D. A. & Goldberg, M. P. Dendritic spines lost during glutamate receptor activation reemerge at original sites of synaptic contact. J. Neurosci. 21, 2393–2403 (2001).
  Article CAS PubMed PubMed Central Google Scholar
• Segal, M., Korkotian, E. & Murphy, D. D. Dendritic spine induction and pruning: common cellular mechanisms? Trends Neurosci. 23, 53–57 (2000).
  Article CAS PubMed Google Scholar
• Pilpel, Y. & Segal, M. Activation of PKC induces rapid morphological plasticity in dendrites of hippocampal neurons via Rac and Rho-dependent mechanisms. Eur. J. Neurosci. 19, 3151–3164 (2004). Shows that the removal of dendritic spines from Rho-overexpressing neurons does not deplete their synapses, and that they can produce normal mEPSCs.
  Article PubMed Google Scholar
• Kirov, S. A., Petrak, L. J., Fiala, J. C. & Harris, K. M. Dendritic spines disappear with chilling but proliferate excessively upon rewarming of mature hippocampus. Neuroscience 127, 69–80 (2004).
  Article CAS PubMed Google Scholar
• Roelandse, M. & Matus, A. Hypothermia-associated loss of dendritic spines. J. Neurosci. 24, 7843–7847 (2004).
  Article CAS PubMed PubMed Central Google Scholar
• 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
• Matsuzaki, M. et al. Dendritic spine geometry is critical for AMPA receptor expression in hippocampal CA1 pyramidal neurons. Nature Neurosci. 4, 1086–1092 (2001).
  Article CAS PubMed Google Scholar
• Murphy, D. D., Cole, N. B., Greenberger, V. & Segal, M. Estradiol increases dendritic spine density by reducing GABA neurotransmission in hippocampal neurons. J. Neurosci. 18, 2550–2559 (1998).
  Article CAS PubMed PubMed Central Google Scholar
• Murase, S., Mosser, E. & Schuman, E. M. Depolarization drives β-catenin into neuronal spines promoting changes in synaptic structure and function. Neuron 35, 91–105 (2002).
  Article CAS PubMed Google Scholar
• Zito, K., Knott, G., Shepherd, G. M., Shenolikar, S. & Svoboda, K. Induction of spine growth and synapse formation by regulation of the spine actin cytoskeleton. Neuron 44, 321–334 (2004).
  Article CAS PubMed Google Scholar
• Boda, B. et al. The mental retardation protein PAK3 contributes to synapse formation and plasticity in hippocampus. J. Neurosci. 24, 10816–10825 (2004).
  Article CAS PubMed PubMed Central Google Scholar
• Desmond, N. L. & Levy, W. B. Changes in the postsynaptic density with long-term potentiation in the dentate gyrus. J. Comp. Neurol. 253, 476–482 (1986).
  Article CAS PubMed Google Scholar
• Moser, M. B. Making more synapses: a way to store information? Cell. Mol. Life Sci. 55, 593–600 (1999).
  Article CAS PubMed Google Scholar
• Eyre, M. D., Richter-Levin, G., Avital, A. & Stewart, M. G. Morphological changes in hippocampal dentate gyrus synapses following spatial learning in rats are transient. Eur. J. Neurosci. 17, 1973–1980 (2003).
  Article PubMed Google Scholar
• Geinisman, Y., Berry, R. W., Disterhoft, J. F., Power, J. M. & Van der Zee, E. A. Associative learning elicits the formation of multiple-synapse boutons. J. Neurosci. 21, 5568–5573 (2001).
  Article CAS PubMed PubMed Central Google Scholar
• Geinisman, Y. Structural synaptic modifications associated with hippocampal LTP and behavioral learning. Cereb. Cortex 10, 952–962 (2000).
  Article CAS PubMed Google Scholar
• Knafo, S., Ariav, G., Barkai, E. & Libersat, F. Olfactory learning induced increase in spine density along the apical dendrites of CA1 hippocampal neurons. Hippocampus 14, 819–825 (2004).
  Article PubMed Google Scholar
• Leuner, B., Falduto, J. & Shors, T. J. Associative memory formation increases the observation of dendritic spines in the hippocampus. J. Neurosci. 23, 659–665 (2003).
  Article CAS PubMed PubMed Central Google Scholar
• Matsuzaki, M., Honkura, N., Ellis-Davis, G. C. R. & Kasai, H. Structural basis of long term potentiation in single dendritic spines. Nature 429, 761–766 (2004). The first demonstration that conditioning can change the volume of spine heads and increase the reactivity of the spine to locally uncaged glutamate.
  Article CAS PubMed PubMed Central Google Scholar
• Otmakhov, N. et al. Persistent accumulation of calcium/calmodulin-dependent protein kinase II in dendritic spines after induction of NMDA receptor-dependent chemical long-term potentiation. J. Neurosci. 24, 9324–9331 (2004).
  Article CAS PubMed PubMed Central Google Scholar
• Lang, C. et al. Transient expansion of synaptically connected dendritic spines upon induction of hippocampal long-term potentiation. Proc. Natl Acad. Sci. USA 101, 16665–16670 (2004).
  Article CAS PubMed PubMed Central Google Scholar
• Okamoto, K., Nagai, T., Miyawaki, A. & Hayashi, Y. Rapid and persistent modulation of actin dynamics regulates postsynaptic reorganization underlying bidirectional plasticity. Nature Neurosci. 7, 1104–1112 (2004). Elegant use of FRET to show bidirectional changes in spine volume and the polymeric status of actin in LTP and LTD.
  Article CAS PubMed Google Scholar
• Fukazawa, Y. et al. 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 (2003).
  Article CAS PubMed Google Scholar
• Zhou, Q., Homma, K. J. & Poo, M. M. Shrinkage of dendritic spines associated with long-term depression of hippocampal synapses. Neuron 44, 749–757 (2004).
  Article CAS PubMed Google Scholar
• Fifkova, E. & Anderson, C. L. Stimulation-induced changes in dimensions of stalks of dendritic spines in the dentate molecular layer. Exp. Neurol. 74, 621–627 (1981).
  Article CAS PubMed Google Scholar
• Maletic-Savatic, M., Malinow, R. & Svoboda, K. Rapid dendritic morphogenesis in CA1 hippocampal dendrites induced by synaptic activity. Science 283, 1860–1861 (1999).
  Article Google Scholar
• Goldin, M. & Segal, M. Protein kinase C and ERK involvement in dendritic spine plasticity in cultured rodent hippocampal neurons. Eur. J. Neurosci. 17, 2529–2539 (2003).
  Article PubMed Google Scholar
• Nägerl, U. V., Eberhorn, N., Cambridge, S. B. & Bonhoeffer, T. Bidirectional activity-dependent morphological plasticity in hippocampal neurons. Neuron 44, 759–767 (2004).
  Article PubMed Google Scholar
• Lowndes, M. & Stewart, M. G. Dendritic spine density in the lobus parolfactorius of the domestic chick is increased 24 h after one-trial passive avoidance training. Brain Res. 654, 129–136 (1994).
  Article CAS PubMed Google Scholar
• O'Malley, A., O'Connell, C., Murphy, K. J. & Regan, C. M. Transient spine density increases in the mid-molecular layer of hippocampal dentate gyrus accompany consolidation of a spatial learning task in the rodent. Neuroscience 99, 229–232 (2000).
  Article CAS PubMed Google Scholar
• Moser, M. B., Trommald, M. & Andersen, P. An increase in dendritic spine density on hippocampal CA1 pyramidal cells following spatial learning in adult rats suggests the formation of new synapses. Proc. Natl Acad. Sci. USA 91, 12673–12675 (1994).
  Article CAS PubMed PubMed Central Google Scholar
• Swann, J. W., Al-Noori, S., Jiang, M. & Lee, C. L. Spine loss and other dendritic abnormalities in epilepsy. Hippocampus 10, 617–625 (2000).
  Article CAS PubMed Google Scholar
• Huber, K. M., Roder, J. C. & Bear, M. F. Chemical induction of mGluR5- and protein synthesis-dependent long-term depression in hippocampal area CA1. J. Neurophysiol. 86, 321–325 (2001).
  Article CAS PubMed Google Scholar
• Vanderklish, P. W. & Edelman, G. M. Dendritic spines elongate after stimulation of group 1 metabotropic glutamate receptors in cultured hippocampal neurons. Proc. Natl Acad. Sci. USA 99, 1639–1644 (2002).
  Article CAS PubMed PubMed Central Google Scholar
• Edwards, F. A. Anatomy and electrophysiology of fast central synapses lead to a structural model for long-term potentiation. Physiol. Rev. 75, 759–787 (1995).
  Article CAS PubMed Google Scholar
• Carlin, R. K. & Siekevitz, P. Plasticity in the central nervous system: do synapses divide? Proc. Natl Acad. Sci. USA 80, 3517–3521 (1983).
  Article CAS PubMed PubMed Central Google Scholar
• 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).
  Article CAS PubMed Google Scholar
• Harris, K. M., Fiala, J. C. & Ostroff, L. Structural changes at dendritic spine synapses during long-term potentiation. Phil. Trans. R. Soc. Lond. B 358, 745–748 (2003).
  Article Google Scholar
• Grutzendler, J., Kasthuri, N. & Gan, W. B. Long-term dendritic spine stability in the adult cortex. Nature 420, 812–816 (2002).
  Article CAS PubMed Google Scholar
• Holtmaat, A. J. et al. Transient and persistent dendritic spines in the neocortex in vivo. Neuron 42, 279–291 (2005).
  Article CAS Google Scholar
• Lieshoff, C. & Bischof, H. J. The dynamics of spine density changes. Behav. Brain Res. 140, 87–95 (2003).
  Article PubMed Google Scholar
• Airey, D. C., Kroodsma, D. E. & DeVoogd, T. J. Differences in the complexity of song tutoring cause differences in the amount learned and in dendritic spine density in a songbird telencephalic song control nucleus. Neurobiol. Learn. Mem. 73, 274–281 (2000).
  Article CAS PubMed Google Scholar
• Millesi, E., Prossinger, H., Dittami, J. P. & Fieder, M. Hibernation effects on memory in European ground squirrels (Spermophilus citellus). J. Biol. Rhythms 16, 264–271 (2001).
  Article CAS PubMed Google Scholar
• Segal, M., Greenberger, V. & Korkotian, E. Formation of dendritic spines in cultured striatal neurons depends on excitatory afferent activity. Eur. J. Neurosci. 17, 2573–2585 (2003).
  Article PubMed Google Scholar
• Kossel, A. H., Williams, C. V., Schweizer, M. & Kater, S. B. Afferent innervation influences the development of dendritic branches and spines via both activity-dependent and non-activity-dependent mechanisms. J. Neurosci. 17, 6314–6324 (1997).
  Article CAS PubMed PubMed Central Google Scholar
• Emptage, N. J., Reid, C. A., Fine, A. & Bliss, T. V. Optical quantal analysis reveals a presynaptic component of LTP at hippocampal Schaffer-associational synapses. Neuron 38, 797–804 (2003).
  Article CAS PubMed Google Scholar
• Voronin, L. L. & Cherubini, E. 'Deaf, mute and whispering' silent synapses: their role in synaptic plasticity. J. Physiol. (Lond.) 557 (Pt 1), 3–12 (2004).
  Article CAS Google Scholar
• Deller, T. et al. Synaptopodin-deficient mice lack a spine apparatus and show deficits in synaptic plasticity. Proc. Natl Acad. Sci. USA 100, 10494–10499 (2003).
  Article CAS PubMed PubMed Central Google Scholar
• Frick, A., Magee, J. & Johnston, D. LTP is accompanied by an enhanced local excitability of pyramidal neuron dendrites. Nature Neurosci. 7, 126–135 (2004).
  Article CAS PubMed Google Scholar
• Korkotian, E., Holcman, D. & Segal, M. Dynamic regulation of spine-dendrite coupling in cultured hippocampal neurons. Eur. J. Neurosci. 20, 2649–2663 (2004).
  Article PubMed Google Scholar
• Dunaevsky, A., Blazeski, R., Yuste, R. & Mason, C. Spine motility with synaptic contact. Nature Neurosci. 4, 685–686 (2001).
  Article CAS PubMed Google Scholar
• Korkotian, E. & Segal, M. Regulation of dendritic spine motility in cultured hippocampal neurons. J. Neurosci. 21, 6115–6124 (2001).
  Article CAS PubMed PubMed Central Google Scholar
• Fischer, M., Kaech, S., Wagner, U., Brinkhaus, H. & Matus, A. Glutamate receptors regulate actin-based plasticity in dendritic spines. Nature Neurosci. 3, 887–894 (2000).
  Article CAS PubMed Google Scholar
• Petrozzino, J. J., Pozzo Miller, L. D. & Connor, J. A. Micromolar Ca2+ transients in dendritic spines of hippocampal pyramidal neurons in brain slice. Neuron 14, 1223–1231 (1995).
  Article CAS PubMed Google Scholar
• Yasuda, R., Sabatini, B. L. & Svoboda, K. Plasticity of calcium channels in dendritic spines. Nature Neurosci. 6, 948–955 (2003).
  Article CAS PubMed Google Scholar
• Sala, C. et al. Inhibition of dendritic spine morphogenesis and synaptic transmission by activity-inducible protein Homer1a. J. Neurosci. 23, 6327–6337 (2003).
  Article CAS PubMed PubMed Central Google Scholar
• Vazquez, L. E., Chen, H. -J., Sokolova, I., Knuesel, I. & Kennedy, M. B. SynGAP regulates spine formation. J. Neurosci. 24, 8862–8872 (2004).
  Article CAS PubMed PubMed Central Google Scholar
• Schulz, T. W. et al. Actin/α-actinin-dependent transport of AMPA receptors in dendritic spines: role of the PDZ-LIM protein RIL. J. Neurosci. 24, 8584–8594 (2004).
  Article CAS PubMed PubMed Central Google Scholar
• Meng, Y. et al. Abnormal spine morphology and enhanced LTP in LIMK-1 knockout mice. Neuron 35, 121–133 (2002).
  Article CAS PubMed Google Scholar