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

Volumn 128, Issue 2, 2004, Pages 251-262

  Popov, V I ^a,b   Davies, H A ^a   Rogachevsky, V V ^b   Patrushev, I V ^b   Errington, M L ^c   Gabbott, P L A ^a   Bliss, T V P ^c   Stewart, M G ^a  

^a OPEN UNIVERSITY   (United Kingdom)

^b RUSSIAN ACADEMY OF SCIENCES   (Russian Federation)

^c NATIONAL INSTITUTE FOR MEDICAL RESEARCH   (United Kingdom)

Author keywords

long term potentiation; postsynaptic densities; thin sections; three dimensional reconstructions

Indexed keywords

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRAIN DEPTH STIMULATION; BRAIN SIZE; CONTROLLED STUDY; DENDRITIC SPINE; DENSITY; DENTATE GYRUS; ELECTRON MICROSCOPY; HEMISPHERE; HIPPOCAMPUS; IN VIVO STUDY; LONG TERM POTENTIATION; MALE; MUSHROOM BODY; NEUROANATOMY; NEUROCHEMISTRY; NONHUMAN; POSTSYNAPTIC POTENTIAL; PRIORITY JOURNAL; RAT; STEREOMETRY; SYNAPSE; THREE DIMENSIONAL IMAGING;

ANIMALS; DENDRITIC SPINES; DENTATE GYRUS; IMAGE PROCESSING, COMPUTER-ASSISTED; IMAGING, THREE-DIMENSIONAL; LONG-TERM POTENTIATION; MALE; MICROSCOPY, ELECTRON; NEURONAL PLASTICITY; RATS; RATS, SPRAGUE-DAWLEY; SYNAPSES;

EID: 4444310172     PISSN: 03064522     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.neuroscience.2004.06.029     Document Type: Article

References (66)

1. W.C. Abraham, B. Logan, J.M. Greenwood, M. Dragunow Induction and experience dependent consolidation of stable long-term potentiation lasting months in the hippocampus J Neurosci 22 2002 9626 9634
2. T.V.P. Bliss, G.L. Collingridge A synaptic model of memory: long-term potentiation in the hippocampus Nature 361 1993 31 39
3. T.V.P. Bliss, T. Lømo Long-lasting potentiation of synaptic transmission in the dentate area of the anaesthetized rabbit following stimulation of the perforant path J Physiol (Lond) 232 1973 331 356
4. Bradshaw, KD, Emptage, NJ, Bliss, TVP (2003) A role for local protein synthesis is required for hippocampal late LTP. Eur J Neurosci 11:3150-3152.
5. F.L. Chang, W.T. Greenough Transient and enduring morphological correlates of synaptic activity and efficacy change in the rat hippocampal slice Brain Res 309 1984 35 46
6. R.E. Coggeshall, H.A. Lekan Methods for determining numbers of cells and synapses: a case for more uniform standards of review J Comp Neurol 364 1996 6 15
7. N. Desmond, W.B. Levy Synaptic correlates of associative potentiation/depression: an ultrastructural study in the hippocampus Brain Res 265 1983 21 30
8. N. Desmond, W.B. Levy Changes in the numerical density of synaptic contacts with long-term potentiation in the hippocampal dentate gyrus J Comp Neurol 253 1986 466 475
9. N. Desmond, W.B. Levy Changes in the postsynaptic density with long-term potentiation in the dentate gyrus J Comp Neurol 253 1986 476 482
10. N. Desmond, W.B. Levy Synaptic interface surface area increases with long-term potentiation in the hippocampal dentate gyrus Brain Res 453 1988 308 314
11. N. Desmond, W.B. Levy Morphological correlates of long-term potentiation imply the modification of existing synapses, not synaptogenesis, in the hippocampal dentate gyrus Synapse 5 1990 139 143
12. Dhanrajan TM, Lynch MA, Kelly A, Popov VI, Rusakov DA, Stewart MG (2003) Expression of long term potentiation in aged rats involves perforated synapses but dendritic spine branching results from high frequency stimulation alone. Hippocampus 14:255-264.
13. A. Dunaevsky, C.A. Mason Spine motility: a means towards an end? Trends Neurosci 26 2003 155 160
14. N.J. Emptage, C.A. Reid, A. Fine, T.V.P. Bliss Optical quantal analysis reveals a presynaptic component of LTP at hippocampal Schaffer-associational synapses Neuron 38 2003 797 804
15. F. Engert, T. Bonhoeffer Dendritic spine changes associated with hippocampal long-term synaptic plasticity Nature 399 1999 66 70
16. J.C. Fiala, K.M. Harris Extending unbiased stereology of brain ultrastructure to three-dimensional volumes J Am Med Inform Assoc 8 2001 1 16
17. J.C. Fiala, K.M. Harris Cylindrical diameters method for calibrating section thickness in serial electron microscopy J Microsc 202 2001 468 472
18. J.C. Fiala, M. Feinberg, V. Popov, K.M. Harris Synaptogenesis via dendritic filopodia in developing hippocampal area CA1 J Neurosci 18 1998 8900 8911
19. U. Frey, M. Krug, K.G. Reymann, H. Matthies Anisomycin, an inhibitor of protein synthesis, blocks late phases of LTP phenomena in the hippocampal CA1 region in vitro Brain Res 452 1988 57 65
20. U. Frey, R.G.M. Morris Synaptic tagging and long-term potentiation Nature 385 1997 533 536
21. Y. Fukazawa, Y. Saitoh, F. Ozawa, Y. Ohta, K. Mizuno, K. Inokuchi Hippocampal LTP is accompanied by enhanced F-actin content within the dendritic spine that is essential for late LTP maintenance in vivo Neuron 38 2003 447 460
22. Y. Geinisman, L. DeToledo-Morrell, F. Morrell, I.S. Persina, M. Rossi Structural synaptic plasticity associated with the induction of long-term potentiation is preserved in the dentate gyrus of aged rats Hippocampus 2 1992 445 456
23. Y. Geinisman, L. DeToledo-Morrell, F. Morrell Induction of long-term potentiation is associated with an increase in the number of axospinous synapses with segmented postsynaptic densities Brain Res 566 1991 77 88
24. Y. Geinisman, L. DeToledo-Morrell, F. Morrell Comparison of structural synaptic modifications induced by long-term potentiation in the hippocampal dentate gyrus of young and aged rats Ann NY Acad Sci 747 1994 452 466
25. Y. Geinisman, R.W. Berry, J.F. Disterhoft, J.M. Power, E.A. Van der Zee Associative learning elicits the formation of multiple-synapse boutons J Neurosci 21 2001 5568 5573
26. M. Goldin, M. Segal, E. Avignone Functional plasticity triggers formation and pruning of dendritic spines in cultured hippocampal networks J Neurosci 21 2001 186 193
27. M. Goldin, M. Segal Protein kinase C and ERK involvement in dendritic spine plasticity in cultured rodent hippocampal neurons Eur J Neurosci 17 2003 2529 2539
28. S. Halpain, A. Hipolito, L. Saffer Regulation of F-actin stability in dendritic spines by glutamate receptors and calcineurin J Neurosci 18 1998 9835 9844
29. K.M. Harris Serial electron microscopy as an alternative or complement to confocal microscopy for the study of synapses and dendritic spines in the central nervous system J.K. Stevens L.R. Mills J.E. Trogadis Three-dimensional confocal microscopy; volume investigation of biological specimens 1994 Academic Press New York 421 445
30. K.M. Harris Calcium from internal stores modifies dendritic spine shape Proc Natl Acad Sci USA 96 1999 12213 12215
31. K.M. Harris Structure, development, and plasticity of dendritic spines Curr Opin Neurobiol 9 1999 343 348
32. K.M. Harris, J.C. Fiala, L. Ostroff Structural changes at dendritic spine synapses during long-term potentiation Philos Trans R Soc Lond B Biol Sci 358 2003 745 748
33. T. Hosokawa, D.A. Rusakov, T.V. Bliss, A. Fine Repeated confocal imaging of individual dendritic spines in the living hippocampal slice: evidence for changes in length and orientation associated with chemically induced LTP J Neurosci 15 1995 5560 5573
34. S.A. Kirov, K.M. Harris Dendrites are more spiny on mature hippocampal neurons when synapses are inactivated Nat Neurosci 2 1999 878 883
35. E. Korkotian, M. Segal Regulation of dendritic spine motility in cultured hippocampal neurons J Neurosci 21 2001 6115 6124
36. R.C. Malenka, R.A. Nicoll Long-term potentiation: a decade of progress? Science 285 1999 1870 1874
37. M. Maletic-Savatic, R. Malinow, K. Svoboda Rapid dendritic morphogenesis in CA1 hippocampal dendrites induced by synaptic activity Science 283 1999 1923 1927
38. D.F. Marrone, T.L. Petit The role of synaptic morphology in neural plasticity: structural interactions underlying synaptic power Brain Res Rev 38 2002 291 308
39. S. Mezey, V. Doỳre, I. Souza, E. Harrison, C. Cambon, C.E. Kendal, H.A. Davies, S. Laroche, M.G. Stewart Long-term synaptic morphometry changes after induction of LTP and LTD in the dentate gyrus of awake rats are not simply mirror phenomena Eur J Neurosci 19 2004 2310 2318
40. M.B. Moser, M. Trommald, T. Egeland, P. Andersen Spatial training in a complex environment and isolation alter the spine distribution differently in rat CA1 pyramidal cells J Comp Neurol 380 1997 373 381
41. D. Muller, N. Toni, P.-A. Buchs Spine changes associated with long-term potentiation Hippocampus 10 2000 596 604
42. I. Nikonenko, P. Jourdain, S. Alberi, N. Toni, D. Muller Activity-induced changes of spine morphology Hippocampus 12 2002 585 591
43. L.E. Ostroff, J.C. Fiala, B. Allwardt, K.M. Harris Polyribosomes redistribute from dendritic shafts into spines with enlarged synapses during LTP in developing rat hippocampal slices Neuron 35 2002 535 545
44. B. Pakkenberg, H.J. Gundersen Neocortical neuron number in humans: effect of sex and age J Comp Neurol 384 1997 312 320
45. A. Peters, I.R. Kaiserman-Abramof The small pyramidal neuron of the rat cerebral cortex: the perikaryon, dendrites, and spines J Anat 127 1970 321 356
46. V.V. Petukhov, V.I. Popov Quantitative analysis of ultrastructural changes in synapses of the rat hippocampal field CA3 in vitro in different functional states Neuroscience 18 1986 823 835
47. V.I. Popov, L.S. Bocharova Hibernation-induced structural changes in synaptic contacts between mossy fibres and hippocampal pyramidal neurons Neuroscience 48 1992 53 62
48. V.I. Popov, L.S. Bocharova, A.G. Bragin Repeated changes of dendritic morphology in the hippocampus of ground squirrels in the course of hibernation Neuroscience 48 1992 45 51
49. V.I. Popov, N.I. Medvedev, V.V. Rogachevskii, D.A. Ignat'ev, M.G. Stewart, E.E. Fesenko Three-dimensional organization of synapses and astroglia in the hippocampus of rats and ground squirrels: new structural and functional paradigms of the synapse function Biofizika 48 2003 289 308
50. D.A. Rusakov, G. Richter-Levin, M.G. Stewart, T. Bliss Reduction in spine density associated with long-term potentiation in the dentate gyrus suggests a spine fusion-and-branching model of potentiation Hippocampus 7 1997 489 500
51. M. Segal Rapid plasticity of dendritic spine: hints to possible functions? Prog Neurobiol 63 2001 61 70
52. M. Segal, P. Andersen Dendritic spines shaped by synaptic activity Curr Opin Neurobiol 10 2001 582 586
53. K.E. Sorra, K.M. Harris Stability in synapse number and size at 2 h after long-term potentiation in hippocampal area CA1 J Neurosci 15 1998 658 671
54. K.E. Sorra, J.C. Fiala, K.M. Harris Critical assessment of the involvement of perforations, spinules, and spine branching in hippocampal synapse formation J Comp Neurol 398 1998 225 240
55. O. Steward, E.M. Schuman Protein synthesis at synaptic sites on dendrites Ann Rev Neurosci 24 2001 299 325
56. M.G. Stewart, E. Harrison, D.A. Rusakov, G. Richter-Levin, M. Maroun Re-structuring of synapses 24 hours after induction of long-term potentiation in the dentate gyrus of the rat hippocampus in vivo Neuroscience 100 2000 221 227
57. D.A. Stuart, D.E. Oorschot Embedding, sectioning, immunocytochemical and stereological methods that optimise research on the lesioned adult rat spinal cord J Neurosci Methods 61 1995 5 14
58. L.W. Swanson Brain maps: structure of the rat brain. 1998 Elsevier Amsterdam
59. N. Toni, P.-A. Buchs, I. Nikonenko, C.R. Bron, D. Muller LTP promotes formation of multiple spine synapses between a single axon terminal and a dendrite Nature 402 1999 421 425
60. N. Toni, P.-A. Buchs, I. Nikonenko, P. Povilaitite, L. Parisi, D. Muller Remodelling of synaptic membranes after induction of long-term potentiation J Neurosci 15 2001 6245 6251
61. A.C. Weeks, T.L. Ivanco, J.C. Leboutillier, R.J. Racine, T.L. Petit Sequential changes in the synaptic structural profile following long-term potentiation in the rat dentate gyrus: I. The intermediate maintenance phase Synapse 31 1999 97 9107
62. A. Weeks, T. Ivanco, J. LeBoutillier, R. Racine, T. Petit Sequential changes in the synaptic structural profile following long-term potentiation in the rat dentate gyrus. II. Induction/early maintenance phase Synapse 36 2000 286 296
63. A. Weeks, T. Ivanco, J. LeBoutillier, R. Racine, T. Petit Sequential changes in the synaptic structural profile following long-term potentiation in the rat dentate gyrus. III. Long-term maintenance phase Synapse 40 2001 74 84
64. A.C. Weeks, T.L. Ivanco, J.C. Leboutillier, D.F. Marrone, R.J. Racine, T.L. Petit Unique changes in synaptic morphology following tetanization under pharmacological blockade Synapse 47 2003 77 86
65. R. Yuste, T. Bonhoeffer Morphological changes in dendritic spines associated with long-term synaptic plasticity Annu Rev Neurosci 24 2001 1071 1089
66. S.S. Zakharenko, L. Zablow, S.A. Siegelbaum Visualization of changes in presynaptic function during long-term synaptic plasticity Nat Neurosci 4 2001 711 717