Anatomical and physiological plasticity of dendritic spines

Annual Review of Neuroscience

Volumn 30, Issue , 2007, Pages 79-97

  Alvarez, Veronica A ^a   Sabatini, Bernardo L ^a  

^a HARVARD MEDICAL SCHOOL   (United States)

Author keywords

2 photon time lapse imaging; Environmental enrichment; Experience induced structural plasticity; Glutamate uncaging; Spine remodeling

Indexed keywords

CELL SURVIVAL; DENDRITIC SPINE; HUMAN; MORPHOLOGY; NERVE CELL NETWORK; NERVE CELL PLASTICITY; NEUROANATOMY; NEUROPHYSIOLOGY; NONHUMAN; PRIORITY JOURNAL; REVIEW;

AGING; ANIMALS; BRAIN; DENDRITIC SPINES; HUMANS; MEMBRANE POTENTIALS; NEURAL PATHWAYS; NEURONAL PLASTICITY; SENSATION; SYNAPSES; SYNAPTIC TRANSMISSION;

EID: 34249933552     PISSN: 0147006X     EISSN: None     Source Type: Book Series    
DOI: 10.1146/annurev.neuro.30.051606.094222     Document Type: Review

References (85)

1. Altman J, Das GD. 1964. Autoradiographic examination of the effects of enriched environment on the rate of glial multiplication in the adult rat brain. Nature 204:1161-63
2. Altschuler RA. 1979. Morphometry of the effect of increased experience and training on synaptic density in area CA3 of the rat hippocampus. J. Histochem. Cytochem. 27(11):1548-50
3. Bloodgood BL, Sabatini BL. 2005. Neuronal activity regulates diffusion across the neck of dendritic spines. Science 310(5749):866-69
4. Briones TL, Klintsova AY, Greenough WT. 2004. Stability of synaptic plasticity in the adult rat visual cortex induced by complex environment exposure. Brain Res. 1018(1):130-35
5. Brown RT. 1968. Early experience and problem-solving ability. J. Comp. Physiol. Psychol. 65(3):433-40
6. Carter AG, Sabatini BL. 2004. State-dependent calcium signaling in dendritic spines of striatal medium spiny neurons. Neuron 44(3):483-93
7. Davalos D, Grutzendler J, Yang G, Kim JV, Zuo Y, et al. 2005. ATP mediates rapid microglial response to local brain injury in vivo. Nat. Neurosci. 8(6):752-58
8. Denk W, Strickler JH, Webb WW. 1990. Two-photon laser scanning fluorescence microscopy. Science 248(4951):73-76
9. De Paola V, Holtmaat A, Knott G, Song S, Wilbrecht, et al. 2006. Cell type-specific structural plasticity of axonal branches and boutons in the adult neocortex. Neuron 49(6):861-75
10. Diamond MC, Lindner B, Johnson R, Bennett EL, Rosenzweig MR. 1975. Differences in occipital cortical synapses from environmentally enriched, impoverished, and standard colony rats. J. Neurosci. Res. 1(2):109-19
11. Diamond ME, Huang W, Ebner FF. 1994. Laminar comparison of somatosensory cortical plasticity. Science 265(5180):1885-88
12. Duffy SN, Craddock KJ, Abel T, Nguyen PV. 2001. Environmental enrichment modifies the PKA-dependence of hippocampal LTP and improves hippocampus- dependent memory. Learn Mem. 8(1):26-34
13. Engert F, Bonhoeffer T. 1999. Dendritic spine changes associated with hippocampal long-term synaptic plasticity. Nature 399(6731):66-70
14. Feng G, Mellor RH, Bernstein M, Keller-Peck C, Nguyen QT, et al. 2000. Imaging neuronal subsets in transgenic mice expressing multiple spectral variants of GFP. Neuron 28(1):41-51
15. Fiala JC, Allwardt B, Harris KM. 2002. Dendritic spines do not split during hippocampal LTP or maturation. Nat. Neurosci. 5(4):297-98
16. Gardner EB, Boitano JJ, Mancino NS, D'Amico DP. 1975. Environmental enrichment and deprivation: effects on learning, memory and exploration. Physiol. Behav. 14(3):321-7
17. Glazewski S, McKenna M, Jacquin M, Fox K. 1998. Experience-dependent depression of vibrissae responses in adolescent rat barrel cortex. Eur. J. Neurosci. 10(6):2107-16
18. Globus A, Rosenzweig MR, Bennett EL, Diamond MC. 1973. Effects of differential experience on dendritic spine counts in rat cerebral cortex. J. Comp. Physiol. Psychol. 82(2):175-81
19. Greenough WT, Hwang HM, Gorman C. 1985. Evidence for active synapse formation or altered postsynaptic metabolism in visual cortex of rats reared in complex environments. Proc. Natl. Acad. Sci. USA 82(13):4549-52
20. Greenough WT, West RW, DeVoogd TJ. 1978. Subsynaptic plate perforations: changes with age and experience in the rat. Science 202(4372):1096-98
21. Grutzendler J, Kasthuri N, Gan WB. 2002. Long-term dendritic spine stability in the adult cortex. Nature 420(6917):812-16
22. Harris KM, Jensen FE, Tsao B. 1992. Three-dimensional structure of dendritic spines and synapses in rat hippocampus (CA1) at postnatal day 15 and adult ages: implications for the maturation of synaptic physiology and long-term potentiation. J. Neurosci. 12(7):2685-705
23. Harris KM, Stevens JK. 1989. Dendritic spines of CA pyramidal cells in the rat hippocampus: serial electron microscopy with reference to their biophysical characteristics. J. Neurosci. 9(8):2982-97
24. Hebb D. 1949. The Organization of Behavior. New York: Wiley
25. Holtmaat A, Wilbrecht L, Knott GW, Welker E, Svoboda K. 2006. Experience-dependent and cell-type-specific spine growth in the neocortex. Nature 441(7096):979-83
26. Holtmaat AJ, Trachtenberg JT, Wilbrecht L, Shepherd GM, Zhang X, et al. 2005. Transient and persistent dendritic spines in the neocortex in vivo. Neuron 45(2):279-91
27. Hymovitch B. 1952. The effects of experimental variations on problem solving in the rat. J. Comp. Physiol. Psychol. 45(4):313-21
28. Knott GW, Holtmaat A, Wilbrecht L, Welker E, Svoboda K. 2006. Spine growth precedes synapse formation in the adult neocortex in vivo. Nat. Neurosci. 9(9):1117-24
29. Koch C, Zador A. 1993. The function of dendritic spines: devices subserving biochemical rather than electrical compartmentalization. J. Neurosci. 13(2):413-22
30. Koo JW, Park CH, Choi SH, Kim NJ, Kim HS, et al. 2003. The postnatal environment can counteract prenatal effects on cognitive ability, cell proliferation, and synaptic protein expression. FASEB J. 17(11):1556-58
31. Kopec CD, Li B, Boehm J, Malinow R. 2006. Glutamate receptor exocytosis and spine enlargement during chemically induced long-term potentiation. J. Neurosci. 26(7):2000-9
32. Korkotian E, Holcman D, Segal M. 2004. Dynamic regulation of spine-dendrite coupling in cultured hippocampal neurons. Eur. J. Neurosci. 20(10):2649-63
33. Kozorovitskiy Y, Gross CG, Kopil C, Battaglia L, McBreen M, et al. 2005. Experience induces structural and biochemical changes in the adult primate brain. Proc. Natl. Acad. Sci. USA 102(48):17478-82
34. Lang C, Barco A, Zablow L, Kandel ER, Siegelbaum SA, Zakharenko SS. 2004. Transient expansion of synaptically connected dendritic spines upon induction of hippocampal long-term potentiation. Proc. Natl. Acad. Sci. USA 101(47):16665-70
35. Lazarov O, Robinson J, Tang YP, Hairston IS, Korade-Mirnics Z, et al. 2005. Environmental enrichment reduces Abeta levels and amyloid deposition in transgenic mice. Cell 120(5):701-13
36. Lee WC, Huang H, Feng G, Sanes JR, Brown EN, et al. 2006. Dynamic remodeling of dendritic arbors in GABAergic interneurons of adult visual cortex. PLOS Biol. 4(2):e29
37. Leggio MG, Mandolesi L, Federico F, Spirito F, Ricci B, et al. 2005. Environmental enrichment promotes improved spatial abilities and enhanced dendritic growth in the rat. Behav. Brain Res. 163(1):78-90
38. Lewis MH. 2004. Environmental complexity and central nervous system development and function. Ment. Retard. Dev. Disabil. Res. Rev. 10(2):91-95
39. Lissin DV, Carroll RC, Nicoll RA, Malenka RC, von Zastrow M. 1999. Rapid, activation-induced redistribution of ionotropic glutamate receptors in cultured hippocampal neurons. J. Neurosci. 19(4):1263-72
40. Losonczy A, Magee JC. 2006. Integrative properties of radial oblique dendrites in hippocampal CA1 pyramidal neurons. Neuron 50(2):291-307
41. Majewska A, Sur M. 2003. Motility of dendritic spines in visual cortex in vivo: changes during the critical period and effects of visual deprivation. Proc. Natl. Acad. Sci. USA 100(26):16024-29
42. Majewska A, Tashiro A, Yuste R. 2000. Regulation of spine calcium dynamics by rapid spine motility. J. Neurosci. 20(22):8262-68
43. Majewska AK, Newton JR, Sur M. 2006. Remodeling of synaptic structure in sensory cortical areas in vivo. J. Neurosci. 26(11):3021-29
44. Maletic-Savatic M, Malinow R, Svoboda K. 1999. Rapid dendritic morphogenesis in CA1 hippocampal dendrites induced by synaptic activity. Science 283(5409):1923-27
45. Malinow R, Malenka RC. 2002. AMPA receptor trafficking and synaptic plasticity. Annu. Rev. Neurosci. 25:103-26
46. Matsuzaki M, Ellis-Davies GC, Nemoto T, Miyashita Y, Iino M, Kasai H. 2001. Dendritic spine geometry is critical for AMPA receptor expression in hippocampal CA1 pyramidal neurons. Nat. Neurosci. 4(11):1086-92
47. Matsuzaki M, Honkura N, Ellis-Davies GC, Kasai H. 2004. Structural basis of long-term potentiation in single dendritic spines. Nature 429(6993):761-66
48. Mizrahi A, Katz LC. 2003. Dendritic stability in the adult olfactory bulb. Nat. Neurosci. 6(11):1201-7
49. Nicoll RA, Malenka RC. 1999. Expression mechanisms underlying NMDA receptor-dependent long-term potentiation. Ann. N.Y.Acad. Sci. 868:515-25
50. Nikonenko I, Jourdain P, Alberi S, Toni N, Muller D. 2002. Activity-induced changes of spine morphology. Hippocampus 12(5):585-91
51. Nimchinsky EA, Yasuda R, Oertner TG, Svoboda K. 2004. The number of glutamate receptors opened by synaptic stimulation in single hippocampal spines. J. Neurosci. 24(8):2054-64
52. Nimmerjahn A, Kirchhoff F, Helmchen F. 2005. Resting microglial cells are highly dynamic surveillants of brain parenchyma in vivo. Science 308(5726):1314-18
53. Noguchi J, Matsuzaki M, Ellis-Davies GC, Kasai H. 2005. Spine-neck geometry determines NMDA receptor-dependent Ca2+ signaling in dendrites. Neuron 46(4):609-22
54. Oray S, Majewska A, Sur M. 2004. Dendritic spine dynamics are regulated by monocular deprivation and extracellular matrix degradation. Neuron 44(6):1021-30
55. Oray S, Majewska A, Sur M. 2006. Effects of synaptic activity on dendritic spine motility of developing cortical layer v pyramidal neurons. Cereb. Cortex 16(5):730-41
56. Patterson GH, Lippincott-Schwartz J. 2002. A photoactivatable GFP for selective photolabeling of proteins and cells. Science 297(5588):1873-77
57. Rampon C, Jiang CH, Dong H, Tang YP, Lockhart DJ, et al. 2000. Effects of environmental enrichment on gene expression in the brain. Proc. Natl. Acad. Sci. USA 97(23):12880-84
58. Rampon C, Tang YP, Goodhouse J, Shimizu E, Kyin M, Tsien JZ. 2000. Enrichment induces structural changes and recovery from nonspatial memory deficits in CA1 NMDAR1-knockout mice. Nat. Neurosci. 3(3):238-44
59. Rema V, Armstrong-James M, Jenkinson N, Ebner FF. 2006. Short exposure to an enriched environment accelerates plasticity in the barrel cortex of adult rats. Neuroscience 140(2):659-72
60. Restivo L, Ferrari F, Passino E, Sgobio C, Bock J, et al. 2005. Enriched environment promotes behavioral and morphological recovery in a mouse model for the fragile X syndrome. Proc. Natl. Acad. Sci. USA 102(32):11557-62
61. Sabatini BL, Maravall M, Svoboda K. 2001. Ca(2+) signaling in dendritic spines. Curr. Opin. Neurobiol. 11(3):349-56
62. Sabatini BL, Oertner TG, Svoboda K. 2002. The life cycle of Ca(2+) ions in dendritic spines. Neuron 33(3):439-52
63. Sabatini BL, Svoboda K. 2000. Analysis of calcium channels in single spines using optical fluctuation analysis. Nature 408(6812):589-93
64. Saito S, Kobayashi S, Ohashi Y, Igarashi M, Komiya Y, Ando S. 1994. Decreased synaptic density in aged brains and its prevention by rearing under enriched environment as revealed by synaptophysin contents. J. Neurosci. Res. 39(1):57-62
65. Sawtell NB, Frenkel MY, Philpot BD, Nakazawa K, Tonegawa S, Bear MF. 2003. NMDA receptor-dependent ocular dominance plasticity in adult visual cortex. Neuron 38(6):977-85
66. Schapiro S, Vukovich KR. 1970. Early experience effects upon cortical dendrites: a proposed model for development. Science 167(916):292-94
67. Scheuss V, Yasuda R, Sobczyk A, Svoboda K. 2006. Nonlinear [Ca2+] signaling in dendrites and spines caused by activity-dependent depression of Ca2+ extrusion. J. Neurosci. 26(31):8183-94
68. Schikorski T, Stevens CF. 1997. Quantitative ultrastructural analysis of hippocampal excitatory synapses. J. Neurosci. 17(15):5858-67
69. Segev I, Rall W. 1988. Computational study of an excitable dendritic spine. J. Neurophysiol. 60(2):499-523
70. Shi SH, Hayashi Y, Petralia RS, Zaman SH, Wenthold RJ, et al. 1999. Rapid spine delivery and redistribution of AMPA receptors after synaptic NMDA receptor activation. Science 284(5421):1811-16
71. Shipley MT, Fu L, Ennis M, Liu WL, Aston-Jones G. 1996. Dendrites of locus coeruleus neurons extend preferentially into two pericoerulear zones. J. Comp. Neurol. 365(1):56-68
72. Sobczyk A, Scheuss V, Svoboda K. 2005. NMDA receptor subunit-dependent [Ca2+] signaling in individual hippocampal dendritic spines. J. Neurosci. 25(26):6037-46
73. Sorra KE, Harris KM. 2000. Overview on the structure, composition, function, development, and plasticity of hippocampal dendritic spines. Hippocampus 10(5):501-11
74. Stewart MG, Medvedev NI, Popov VI, Schoepfer R, Davies HA, et al. 2005. Chemically induced long-term potentiation increases the number of perforated and complex postsynaptic densities but does not alter dendritic spine volume in CA1 of adult mouse hippocampal slices. Eur. J. Neurosci. 21(12):3368-78
75. Svoboda K, Tank DW, Denk W. 1996. Direct measurement of coupling between dendritic spines and shafts. Science 272(5262):716-19
76. Szeligo F, Leblond CP. 1977. Response of the three main types of glial cells of cortex and corpus callosum in rats handled during suckling or exposed to enriched, control and impoverished environments following weaning. J. Comp. Neurol. 172(2):247-63
77. Takumi Y, Ramirez-Leon V, Laake P, Rinvik E, Ottersen OP. 1999. Different modes of expression of AMPA and NMDA receptors in hippocampal synapses. Nat. Neurosci. 2(7):618-24
78. Toni N, Buchs PA, Nikonenko I, Povilaitite P, Parisi L, Muller D. 2001. Remodeling of synaptic membranes after induction of long-term potentiation. J. Neurosci. 21(16):6245-51
79. Trachtenberg JT, Chen BE, Knott GW, Feng G, Sanes JR. 2002. Long-term in vivo imaging of experience-dependent synaptic plasticity in adult cortex. Nature 420(6917):788-94
80. van Praag H, Kempermann G, Gage FH. 1999. Running increases cell proliferation and neurogenesis in the adult mouse dentate gyrus. Nat. Neurosci. 2(3):266-70
81. Volkmar FR, Greenough WT. 1972. Rearing complexity affects branching of dendrites in the visual cortex of the rat. Science 176(42):1445-47
82. Zakharenko SS, Zablow L, Siegelbaum SA. 2001. Visualization of changes in presynaptic function during long-term synaptic plasticity. Nat. Neurosci. 4(7):711-17
83. Zhou Q, Homma KJ, Poo MM. 2004. Shrinkage of dendritic spines associated with long-term depression of hippocampal synapses. Neuron 44(5):749-57
84. Zuo Y, Lin A, Chang P, Gan W-B. 2005. Development of long-term dendritic spine stability in diverse regions of cerebral cortex. Neuron 46(2):181-89
85. Zuo Y, Yang G, Kwon E, Gan W-B. 2005. Long-term sensory deprivation prevents dendritic spine loss in primary somatosensory cortex. Nature 436(7048):261-65