Pathological remodeling of dendritic spines

Dendritic Spines: Biochemistry, Modeling and Properties

Volumn , Issue , 2009, Pages 45-65

  Campbell, John N ^a,b   Kurz, Jonathon E ^a,b   Churn, Severn B ^a,b  

^a VIRGINIA COMMONWEALTH UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b VIRGINIA COMMONWEALTH UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

EID: 84856449958     PISSN: None     EISSN: None     Source Type: Book    
DOI: None     Document Type: Chapter

References (131)

1. McIntosh, T.K., et al., Traumatic brain injury in the rat: characterization of a lateral fluid-percussion model. Neuroscience, 1989. 28(1): p. 233-44.
2. Kurz, J.E., Anderson, A. L., Churn, S. B., Calcineurin-Mediated Cofilin Dephosphorylation and Actin Depolymerization in the Pilocarpine Model of Status Epilepticus (Abstract 3.052). Epilepsia, 2006. 47(s4 (Suppl. 4)): p. 204-289.
3. Kurz, J.E., et al., A cellular mechanism for dendritic spine loss in the pilocarpine model of status epilepticus. Epilepsia, 2008. 49(10): p. 1696-710.
4. Farkas, O. and J.T. Povlishock, Cellular and subcellular change evoked by diffuse traumatic brain injury: a complex web of change extending far beyond focal damage. Prog Brain Res, 2007. 161: p. 43-59.
5. Choi, D.W., Ionic dependence of glutamate neurotoxicity. J Neurosci, 1987. 7(2): p. 369-79.
6. Zipfel, G.J., et al., Neuronal apoptosis after CNS injury: the roles of glutamate and calcium. J Neurotrauma, 2000. 17(10): p. 857-69.
7. DeLorenzo, R.J., et al., An in vitro model of stroke-induced epilepsy: elucidation of the roles of glutamate and calcium in the induction and maintenance of stroke-induced epileptogenesis. Int Rev Neurobiol, 2007. 81: p. 59-84.
8. McNamara, J.O., Y.Z. Huang, and A.S. Leonard, Molecular signaling mechanisms underlying epileptogenesis. Sci STKE, 2006. 2006(356): p. re12.
9. Choi, D.W., Excitotoxic cell death. J Neurobiol, 1992. 23(9): p. 1261-76.
10. Nimchinsky, E.A., B.L. Sabatini, and K. Svoboda, Structure and function of dendritic spines. Annu Rev Physiol, 2002. 64: p. 313-53.
11. Cingolani, L.A. and Y. Goda, Actin in action: the interplay between the actin cytoskeleton and synaptic efficacy. Nat Rev Neurosci, 2008. 9(5): p. 344-56.
12. Dillon, C. and Y. Goda, The actin cytoskeleton: integrating form and function at the synapse. Annu Rev Neurosci, 2005. 28: p. 25-55.
13. Buki, A. and J.T. Povlishock, All roads lead to disconnection?--Traumatic axonal injury revisited. Acta Neurochir (Wien), 2006. 148(2): p. 181-93; discussion 193-4.
14. Swann, J.W., et al., Spine loss and other dendritic abnormalities in epilepsy. Hippocampus, 2000. 10(5): p. 617-25.
15. Olney, J.W., R.C. Collins, and R.S. Sloviter, Excitotoxic mechanisms of epileptic brain damage. Adv Neurol, 1986. 44: p. 857-77.
16. Olney, J.W., T. Fuller, and T. de Gubareff, Acute dendrotoxic changes in the hippocampus of kainate treated rats. Brain Res, 1979. 176(1): p. 91-100.
17. Greenwood, S.M. and C.N. Connolly, Dendritic and mitochondrial changes during glutamate excitotoxicity. Neuropharmacology, 2007. 53(8): p. 891-8.
18. Hori, N. and D.O. Carpenter, Functional and morphological changes induced by transient in vivo ischemia. Exp Neurol, 1994. 129(2): p. 279-89.
19. Park, J.S., M.C. Bateman, and M.P. Goldberg, Rapid alterations in dendrite morphology during sublethal hypoxia or glutamate receptor activation. Neurobiol Dis, 1996. 3(3): p. 215-27.
20. Katayama, Y., et al., Early cellular swelling in experimental traumatic brain injury: a phenomenon mediated by excitatory amino acids. Acta Neurochir Suppl (Wien), 1990. 51: p. 271-3.
21. Folkerts, M.M., et al., Disruption of MAP-2 immunostaining in rat hippocampus after traumatic brain injury. J Neurotrauma, 1998. 15(5): p. 349-63.
22. Unterberg, A.W., et al., Edema and brain trauma. Neuroscience, 2004. 129(4): p. 1021-9.
23. Hasbani, M.J., et al., Dendritic spines lost during glutamate receptor activation reemerge at original sites of synaptic contact. J Neurosci, 2001. 21(7): p. 2393-403.
24. Hasbani, M.J., et al., Distinct roles for sodium, chloride, and calcium in excitotoxic dendritic injury and recovery. Exp Neurol, 1998. 154(1): p. 241-58.
25. Ikegaya, Y., et al., Rapid and reversible changes in dendrite morphology and synaptic efficacy following NMDA receptor activation: implication for a cellular defense against excitotoxicity. J Cell Sci, 2001. 114(Pt 22): p. 4083-93.
26. Sattler, R. and M. Tymianski, Molecular mechanisms of glutamate receptor-mediated excitotoxic neuronal cell death. Mol Neurobiol, 2001. 24(1-3): p. 107-29.
27. Ikonomidou, C., et al., Hypobaric-ischemic conditions produce glutamate-like cytopathology in infant rat brain. J Neurosci, 1989. 9(5): p. 1693-700.
28. Zhang, S., et al., Rapid reversible changes in dendritic spine structure in vivo gated by the degree of ischemia. J Neurosci, 2005. 25(22): p. 5333-8.
29. Andrew, R.D., et al., Physiological evidence that pyramidal neurons lack functional water channels. Cereb Cortex, 2007. 17(4): p. 787-802.
30. Hasbani, M.J., N.M. Viquez, and M.P. Goldberg, NMDA receptors mediate hypoxic spine loss in cultured neurons. Neuroreport, 2001. 12(12): p. 2731-5.
31. Takeuchi, H., et al., Neuritic beading induced by activated microglia is an early feature of neuronal dysfunction toward neuronal death by inhibition of mitochondrial respiration and axonal transport. J Biol Chem, 2005. 280(11): p. 10444-54.
32. Emery, D.G. and J.H. Lucas, Ultrastructural damage and neuritic beading in coldstressed spinal neurons with comparisons to NMDA and A23187 toxicity. Brain Res, 1995. 692(1-2): p. 161-73.
33. Kirov, S.A., et al., Dendritic spines disappear with chilling but proliferate excessively upon rewarming of mature hippocampus. Neuroscience, 2004. 127(1): p. 69-80.
34. Inoue, H. and Y. Okada, Roles of volume-sensitive chloride channel in excitotoxic neuronal injury. J Neurosci, 2007. 27(6): p. 1445-55.
35. LoPachin, R.M., et al., Effects of ion channel blockade on the distribution of Na, K, Ca and other elements in oxygen-glucose deprived CA1 hippocampal neurons. Neuroscience, 2001. 103(4): p. 971-83.
36. Arias, C., et al., Neuronal damage and MAP2 changes induced by the glutamate transport inhibitor dihydrokainate and by kainate in rat hippocampus in vivo. Exp Brain Res, 1997. 116(3): p. 467-76.
37. Bindokas, V.P. and R.J. Miller, Excitotoxic degeneration is initiated at non-random sites in cultured rat cerebellar neurons. J Neurosci, 1995. 15(11): p. 6999-7011.
38. Olney, J.W., et al., MK-801 prevents hypobaric-ischemic neuronal degeneration in infant rat brain. J Neurosci, 1989. 9(5): p. 1701-4.
39. Al-Noori, S. and J.W. Swann, A role for sodium and chloride in kainic acid-induced beading of inhibitory interneuron dendrites. Neuroscience, 2000. 101(2): p. 337-48.
40. Oliva, A.A., Jr., T.T. Lam, and J.W. Swann, Distally directed dendrotoxicity induced by kainic Acid in hippocampal interneurons of green fluorescent protein-expressing transgenic mice. J Neurosci, 2002. 22(18): p. 8052-62.
41. Greenwood, S.M., et al., Mitochondrial dysfunction and dendritic beading during neuronal toxicity. J Biol Chem, 2007. 282(36): p. 26235-44.
42. Rothman, S.M., The neurotoxicity of excitatory amino acids is produced by passive chloride influx. J Neurosci, 1985. 5(6): p. 1483-9.
43. Agre, P., et al., Aquaporin water channels--from atomic structure to clinical medicine. J Physiol, 2002. 542(Pt 1): p. 3-16.
44. Hoskison, M.M. and C.W. Shuttleworth, Microtubule disruption, not calpain-dependent loss of MAP2, contributes to enduring NMDA-induced dendritic dysfunction in acute hippocampal slices. Exp Neurol, 2006. 202(2): p. 302-12.
45. Sanchez, C., J. Diaz-Nido, and J. Avila, Phosphorylation of microtubule-associated protein 2 (MAP2) and its relevance for the regulation of the neuronal cytoskeleton function. Prog Neurobiol, 2000. 61(2): p. 133-68.
46. Dehmelt, L. and S. Halpain, The MAP2/Tau family of microtubule-associated proteins. Genome Biol, 2005. 6(1): p. 204.
47. Hoskison, M.M., et al., Calcium-dependent NMDA-induced dendritic injury and MAP2 loss in acute hippocampal slices. Neuroscience, 2007. 145(1): p. 66-79.
48. Halpain, S. and P. Greengard, Activation of NMDA receptors induces rapid dephosphorylation of the cytoskeletal protein MAP2. Neuron, 1990. 5(3): p. 237-46.
49. Quinlan, E.M. and S. Halpain, Emergence of activity-dependent, bidirectional control of microtubule-associated protein MAP2 phosphorylation during postnatal development. J Neurosci, 1996. 16(23): p. 7627-37.
50. Quinlan, E.M. and S. Halpain, Postsynaptic mechanisms for bidirectional control of MAP2 phosphorylation by glutamate receptors. Neuron, 1996. 16(2): p. 357-68.
51. Gong, C.X., et al., Regulation of phosphorylation of neuronal microtubule-associated proteins MAP1b and MAP2 by protein phosphatase-2A and -2B in rat brain. Brain Res, 2000. 853(2): p. 299-309.
52. McNeil, R.S., et al., Neuronal cytoskeletal alterations evoked by a platelet-activating factor (PAF) analogue. Cell Motil Cytoskeleton, 1999. 43(2): p. 99-113.
53. Slemmer, J.E., C.I. De Zeeuw, and J.T. Weber, Don't get too excited: mechanisms of glutamate-mediated Purkinje cell death. Prog Brain Res, 2005. 148: p. 367-90.
54. Bardo, S., M.G. Cavazzini, and N. Emptage, The role of the endoplasmic reticulum Ca2+ store in the plasticity of central neurons. Trends Pharmacol Sci, 2006. 27(2): p. 78-84.
55. Cavazzini, M., T. Bliss, and N. Emptage, Ca2+ and synaptic plasticity. Cell Calcium, 2005. 38(3-4): p. 355-67.
56. Bloodgood, B.L. and B.L. Sabatini, Ca(2+) signaling in dendritic spines. Curr Opin Neurobiol, 2007. 17(3): p. 345-51.
57. Blackstone, C. and M. Sheng, Postsynaptic calcium signaling microdomains in neurons. Front Biosci, 2002. 7: p. d872-85.
58. Oertner, T.G. and A. Matus, Calcium regulation of actin dynamics in dendritic spines. Cell Calcium, 2005. 37(5): p. 477-82.
59. Ethell, I.M. and E.B. Pasquale, Molecular mechanisms of dendritic spine development and remodeling. Prog Neurobiol, 2005. 75(3): p. 161-205.
60. Fifkova, E. and R.J. Delay, Cytoplasmic actin in neuronal processes as a possible mediator of synaptic plasticity. J Cell Biol, 1982. 95(1): p. 345-50.
61. Cohen, R.S., S.K. Chung, and D.W. Pfaff, Immunocytochemical localization of actin in dendritic spines of the cerebral cortex using colloidal gold as a probe. Cell Mol Neurobiol, 1985. 5(3): p. 271-84.
62. Honkura, N., et al., The subspine organization of actin fibers regulates the structure and plasticity of dendritic spines. Neuron, 2008. 57(5): p. 719-29.
63. Sekino, Y., N. Kojima, and T. Shirao, Role of actin cytoskeleton in dendritic spine morphogenesis. Neurochem Int, 2007. 51(2-4): p. 92-104.
64. Huang, T.Y., C. DerMardirossian, and G.M. Bokoch, Cofilin phosphatases and regulation of actin dynamics. Curr Opin Cell Biol, 2006. 18(1): p. 26-31.
65. Sarmiere, P.D. and J.R. Bamburg, Regulation of the neuronal actin cytoskeleton by ADF/cofilin. J Neurobiol, 2004. 58(1): p. 103-17.
66. Bamburg, J.R., H.E. Harris, and A.G. Weeds, Partial purification and characterization of an actin depolymerizing factor from brain. FEBS Lett, 1980. 121(1): p. 178-82.
67. Nishida, E., S. Maekawa, and H. Sakai, Cofilin, a protein in porcine brain that binds to actin filaments and inhibits their interactions with myosin and tropomyosin. Biochemistry, 1984. 23(22): p. 5307-13.
68. Bobkov, A.A., et al., Cooperative effects of cofilin (ADF) on actin structure suggest allosteric mechanism of cofilin function. J Mol Biol, 2006. 356(2): p. 325-34.
69. Niwa, R., et al., Control of actin reorganization by Slingshot, a family of phosphatases that dephosphorylate ADF/cofilin. Cell, 2002. 108(2): p. 233-46.
70. Ohta, Y., et al., Differential activities, subcellular distribution and tissue expression patterns of three members of Slingshot family phosphatases that dephosphorylate cofilin. Genes Cells, 2003. 8(10): p. 811-24.
71. Kurita, S., et al., Molecular dissection of the mechanisms of substrate recognition and F-actin-mediated activation of cofilin-phosphatase slingshot-1. J Biol Chem, 2008.
72. Meng, Y., et al., Abnormal spine morphology and enhanced LTP in LIMK-1 knockout mice. Neuron, 2002. 35(1): p. 121-33.
73. Meng, Y., et al., Regulation of spine morphology and synaptic function by LIMK and the actin cytoskeleton. Rev Neurosci, 2003. 14(3): p. 233-40.
74. Meng, Y., et al., Regulation of ADF/cofilin phosphorylation and synaptic function by LIM-kinase. Neuropharmacology, 2004. 47(5): p. 746-54.
75. Mizuno, K., et al., Identification of a human cDNA encoding a novel protein kinase with two repeats of the LIM/double zinc finger motif. Oncogene, 1994. 9(6): p. 1605-12.
76. Ohashi, K., et al., Molecular cloning of a chicken lung cDNA encoding a novel protein kinase with N-terminal two LIM/double zinc finger motifs. J Biochem, 1994. 116(3): p. 636-42.
77. Scott, R.W. and M.F. Olson, LIM kinases: function, regulation and association with human disease. J Mol Med, 2007. 85(6): p. 555-68.
78. Bernard, O., Lim kinases, regulators of actin dynamics. Int J Biochem Cell Biol, 2007. 39(6): p. 1071-6.
79. Wang, Y., F. Shibasaki, and K. Mizuno, Calcium signal-induced cofilin dephosphorylation is mediated by Slingshot via calcineurin. J Biol Chem, 2005. 280(13): p. 12683-9.
80. Racz, B. and R.J. Weinberg, Spatial organization of cofilin in dendritic spines. Neuroscience, 2006. 138(2): p. 447-56.
81. Rusnak, F. and P. Mertz, Calcineurin: form and function. Physiol Rev, 2000. 80(4): p. 1483-521.
82. Aramburu, J., A. Rao, and C.B. Klee, Calcineurin: from structure to function. Curr Top Cell Regul, 2000. 36: p. 237-95.
83. Klee, C.B., H. Ren, and X. Wang, Regulation of the calmodulin-stimulated protein phosphatase, calcineurin. J Biol Chem, 1998. 273(22): p. 13367-70.
84. Groth, R.D., R.L. Dunbar, and P.G. Mermelstein, Calcineurin regulation of neuronal plasticity. Biochem Biophys Res Commun, 2003. 311(4): p. 1159-71.
85. Zhou, Q., K.J. Homma, and M.M. Poo, Shrinkage of dendritic spines associated with long-term depression of hippocampal synapses. Neuron, 2004. 44(5): p. 749-57.
86. Halpain, S., A. Hipolito, and L. Saffer, Regulation of F-actin stability in dendritic spines by glutamate receptors and calcineurin. J Neurosci, 1998. 18(23): p. 9835-44.
87. Chang, F.L. and W.T. Greenough, Transient and enduring morphological correlates of synaptic activity and efficacy change in the rat hippocampal slice. Brain Res, 1984. 309(1): p. 35-46.
88. 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, 2003. 38(3): p. 447-60.
89. Zeng, L.H., et al., Kainate seizures cause acute dendritic injury and actin depolymerization in vivo. J Neurosci, 2007. 27(43): p. 11604-13.
90. Kurz, J.E., et al., A significant increase in both basal and maximal calcineurin activity in the rat pilocarpine model of status epilepticus. J Neurochem, 2001. 78(2): p. 304-15.
91. Kurz, J.E., et al., Status epilepticus-induced changes in the subcellular distribution and activity of calcineurin in rat forebrain. Neurobiol Dis, 2003. 14(3): p. 483-93.
92. Isokawa, M., Remodeling dendritic spines in the rat pilocarpine model of temporal lobe epilepsy. Neurosci Lett, 1998. 258(2): p. 73-6.
93. Kurz, J.E., et al., A persistent change in subcellular distribution of calcineurin following fluid percussion injury in the rat. Brain Res, 2005. 1048(1-2): p. 153-60.
94. Kurz, J.E., et al., A significant increase in both basal and maximal calcineurin activity following fluid percussion injury in the rat. J Neurotrauma, 2005. 22(4): p. 476-90.
95. Dubreuil, C.I., et al., Activation of Rho after traumatic brain injury and seizure in rats. Exp Neurol, 2006. 198(2): p. 361-9.
96. Schubert, V., J.S. Da Silva, and C.G. Dotti, Localized recruitment and activation of RhoA underlies dendritic spine morphology in a glutamate receptor-dependent manner. J Cell Biol, 2006. 172(3): p. 453-67.
97. Allison, D.W., et al., Role of actin in anchoring postsynaptic receptors in cultured hippocampal neurons: differential attachment of NMDA versus AMPA receptors. J Neurosci, 1998. 18(7): p. 2423-36.
98. Zhang, W. and D.L. Benson, Stages of synapse development defined by dependence on F-actin. J Neurosci, 2001. 21(14): p. 5169-81.
99. Graber, S., S. Maiti, and S. Halpain, Cathepsin B-like proteolysis and MARCKS degradation in sub-lethal NMDA-induced collapse of dendritic spines. Neuropharmacology, 2004. 47(5): p. 706-13.
100. Pak, D.T., et al., Regulation of dendritic spine morphology by SPAR, a PSD-95-associated RapGAP. Neuron, 2001. 31(2): p. 289-303.
101. Pak, D.T. and M. Sheng, Targeted protein degradation and synapse remodeling by an inducible protein kinase. Science, 2003. 302(5649): p. 1368-73.
102. Wu, L.X., et al., Involvement of the Snk-SPAR pathway in glutamate-induced excitotoxicity in cultured hippocampal neurons. Brain Res, 2007. 1168: p. 38-45.
103. Fu, Z., et al., Differential roles of Rap1 and Rap2 small GTPases in neurite retraction and synapse elimination in hippocampal spiny neurons. J Neurochem, 2007. 100(1): p. 118-31.
104. Ponimaskin, E., et al., Morphogenic signaling in neurons via neurotransmitter receptors and small GTPases. Mol Neurobiol, 2007. 35(3): p. 278-87.
105. Seeburg, D.P., et al., Critical role of CDK5 and Polo-like kinase 2 in homeostatic synaptic plasticity during elevated activity. Neuron, 2008. 58(4): p. 571-83.
106. Ang, X.L., et al., Regulation of Postsynaptic RapGAP SPAR by Polo-like Kinase 2 and the SCF{beta}-TRCP Ubiquitin Ligase in Hippocampal Neurons. J Biol Chem, 2008. 283(43): p. 29424-29432.
107. Bingol, B. and E.M. Schuman, Activity-dependent dynamics and sequestration of proteasomes in dendritic spines. Nature, 2006. 441(7097): p. 1144-8.
108. Ouimet, C.C., et al., Localization of the MARCKS (87 kDa) protein, a major specific substrate for protein kinase C, in rat brain. J Neurosci, 1990. 10(5): p. 1683-98.
109. Calabrese, B. and S. Halpain, Essential role for the PKC target MARCKS in maintaining dendritic spine morphology. Neuron, 2005. 48(1): p. 77-90.
110. Meller, R., et al., Ubiquitin proteasome-mediated synaptic reorganization: a novel mechanism underlying rapid ischemic tolerance. J Neurosci, 2008. 28(1): p. 50-9.
111. Solomonia, R.O., et al., Different forms of MARCKS protein are involved in memory formation in the learning process of imprinting. Exp Brain Res, 2008. 188(2): p. 323-30.
112. Hussain, R.J., et al., Myristoylated alanine rich C kinase substrate (MARCKS) heterozygous mutant mice exhibit deficits in hippocampal mossy fiber-CA3 long-term potentiation. Hippocampus, 2006. 16(5): p. 495-503.
113. Chakravarthy, B., P. Morley, and J. Whitfield, Ca2+-calmodulin and protein kinase Cs: a hypothetical synthesis of their conflicting convergences on shared substrate domains. Trends Neurosci, 1999. 22(1): p. 12-6.
114. Arbuzova, A., A.A. Schmitz, and G. Vergeres, Cross-talk unfolded: MARCKS proteins. Biochem J, 2002. 362(Pt 1): p. 1-12.
115. Hartwig, J.H., et al., MARCKS is an actin filament crosslinking protein regulated by protein kinase C and calcium-calmodulin. Nature, 1992. 356(6370): p. 618-22.
116. Scholz, W.K. and H.C. Palfrey, Glutamate-stimulated protein phosphorylation in cultured hippocampal pyramidal neurons. J Neurosci, 1991. 11(8): p. 2422-32.
117. Ohmitsu, M., et al., Phosphorylation of myristoylated alanine-rich protein kinase C substrate by mitogen-activated protein kinase in cultured rat hippocampal neurons following stimulation of glutamate receptors. J Biol Chem, 1999. 274(1): p. 408-17.
118. Durkin, J.P., et al., An early loss in membrane protein kinase C activity precedes the excitatory amino acid-induced death of primary cortical neurons. J Neurochem, 1996. 66(3): p. 951-62.
119. Spizz, G. and P.J. Blackshear, Identification and characterization of cathepsin B as the cellular MARCKS cleaving enzyme. J Biol Chem, 1997. 272(38): p. 23833-42.
120. Curia, G., et al., The pilocarpine model of temporal lobe epilepsy. J Neurosci Methods, 2008. 172(2): p. 143-57.
121. Pitkanen, A. and T.K. McIntosh, Animal models of post-traumatic epilepsy. J Neurotrauma, 2006. 23(2): p. 241-61.
122. Morimoto, K., M. Fahnestock, and R.J. Racine, Kindling and status epilepticus models of epilepsy: rewiring the brain. Prog Neurobiol, 2004. 73(1): p. 1-60.
123. Velazquez, J.L. and P.L. Carlen, Synchronization of GABAergic interneuronal networks during seizure-like activity in the rat horizontal hippocampal slice. Eur J Neurosci, 1999. 11(11): p. 4110-8.
124. Isomura, Y., Y. Fujiwara-Tsukamoto, and M. Takada, A network mechanism underlying hippocampal seizure-like synchronous oscillations. Neurosci Res, 2008. 61(3): p. 227-33.
125. Chen, L.S., et al., Kainic acid-induced focal cortical seizure is associated with an increase of synaptophysin immunoreactivity in the cortex. Exp Neurol, 1996. 141(1): p. 25-31.
126. Kirov, S.A. and K.M. Harris, Dendrites are more spiny on mature hippocampal neurons when synapses are inactivated. Nat Neurosci, 1999. 2(10): p. 878-83.
127. Petrak, L.J., K.M. Harris, and S.A. Kirov, Synaptogenesis on mature hippocampal dendrites occurs via filopodia and immature spines during blocked synaptic transmission. J Comp Neurol, 2005. 484(2): p. 183-90.
128. Leite, J.P., et al., Plasticity, synaptic strength, and epilepsy: what can we learn from ultrastructural data? Epilepsia, 2005. 46 Suppl 5: p. 134-41.
129. Morgan, R.J. and I. Soltesz, Nonrandom connectivity of the epileptic dentate gyrus predicts a major role for neuronal hubs in seizures. Proc Natl Acad Sci U S A, 2008. 105(16): p. 6179-84.
130. Bragin, A., C.L. Wilson, and J. Engel, Jr., Chronic epileptogenesis requires development of a network of pathologically interconnected neuron clusters: a hypothesis. Epilepsia, 2000. 41 Suppl 6: p. S144-52.
131. Wong, M., Stabilizing dendritic structure as a novel therapeutic approach for epilepsy. Expert Rev Neurother, 2008. 8(6): p. 907-15.