The N-methyl-d-aspartate receptor antagonist CPP alters synapse and spine structure and impairs long-term potentiation and long-term depression induced morphological plasticity in dentate gyrus of the awake rat

Neuroscience

Volumn 165, Issue 4, 2010, Pages 1170-1181

  Medvedev, N I ^a   Popov, V I ^a,b   Rodriguez Arellano, J J ^a,c   Dallerac G ^d,e   Davies, H A ^a   Gabbott, P L ^a   Laroche, S ^d,e   Kraev, I V ^a   Doyere V ^d,e   Stewart, M G ^a  

^a OPEN UNIVERSITY   (United Kingdom)

^b INSTITUTE OF CELL BIOPHYSICS   (Russian Federation)

^c UNIVERSITY OF MANCHESTER   (United Kingdom)

^d CNRS   (France)

^e UNIVERSITÉ PARIS SACLAY   (France)

Author keywords

3 D synaptic ultrastructure; hippocampus; long term potentiation and depression

Indexed keywords

4 (3 PHOSPHONOPROPYL) 2 PIPERAZINECARBOXYLIC ACID; N METHYL DEXTRO ASPARTIC ACID RECEPTOR;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DENTATE GYRUS; LONG TERM DEPRESSION; LONG TERM POTENTIATION; MALE; MEMORY CONSOLIDATION; NERVE CELL PLASTICITY; NEUROPHYSIOLOGY; NONHUMAN; POSTSYNAPTIC MEMBRANE; PRIORITY JOURNAL; RAT;

ANIMALS; DENDRITIC SPINES; DENTATE GYRUS; EXCITATORY AMINO ACID ANTAGONISTS; LONG-TERM POTENTIATION; LONG-TERM SYNAPTIC DEPRESSION; MALE; NEURONAL PLASTICITY; NEURONS; PIPERAZINES; PRESYNAPTIC TERMINALS; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, N-METHYL-D-ASPARTATE; SYNAPSES; WAKEFULNESS;

EID: 74149088399     PISSN: 03064522     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.neuroscience.2009.11.047     Document Type: Article

References (52)

1. Abraham W.C., Christie B.R., Logan B., Lawlor P., and Dragunow M. Immediate early gene expression associated with the persistence of heterosynaptic long-term depression in the hippocampus. Proc Natl Acad Sci U S A 91 (1994) 10049-10053
2. Abraham W.C. How long will long-term potentiation last?. Philos Trans R Soc Lond B 358 (2003) 735-744
3. Abraham W.C., Logan B., Wolff A., and Benuskova L. "Heterosynaptic" LTD in the dentate gyrus of anesthetized rat requires homosynaptic activity. J Neurophysiol 98 (2007) 1048-1051
4. Applegate M.D., and Landfield P.W. Synaptic vesicle redistribution during hippocampal frequency potentiation and depression in young and aged rats. J Neurosci 8 (1988) 1096-1111
5. Bastrikova N., Gardner G.A., Reece J.M., Jeromin A., and Dudek S.M. Synapse elimination accompanies functional plasticity in hippocampal neurons. Proc Natl Acad Sci U S A 105 (2008) 3123-3127
6. Becker N., Wierenga C.J., Fonseca R., Bonhoeffer T., and Nägerl U.V. LTD induction causes morphological changes of presynaptic boutons and reduces their contacts with spines. Neuron 60 (2008) 590-597
7. Bourne J., and Harris K.M. Do thin spines learn to be mushroom spines that remember?. Curr Opin Neurobiol 17 (2007) 381-386
8. Bourne J., and Harris K.M. Balancing structure and function at hippocampal dendritic spines. Annu Rev Neurosci 31 (2008) 47-67
9. Christie B.R., and Abraham W.C. Priming of associative long-term depression in the dentate gyrus by theta frequency synaptic activity. Neuron 9 1 (1992) 79-84
10. De Roo M., Klauster P., and Muller D. LTP promotes a selective long-term stabilization and clustering of dendritic spines. PLoS Biol 6 (2008) 1850-1860
11. Doyère V., Burette F., Negro C.R., and Laroche S. Long-term potentiation of hippocampal afferents and efferents to prefrontal cortex: implications for associative learning. Neuropsychologia 31 (1993) 1031-1053
12. Doyère V., Srebro B., and Laroche S. Heterosynaptic LTD and depotentiation in the medial perforant path of the dentate gyrus in the freely moving rat. J Neurophysiol 77 (1997) 571-578
13. Engert F., and Bonhoeffer T. Dendritic spine changes associated with hippocampal long-term synaptic plasticity. Nature 399 (1999) 66-70
14. Fiala J.C., Feinberg M., Popov V., and Harris K.M. Synaptogenesis via dendritic filopodia in developing hippocampal area CA1. J Neurosci 18 (1998) 8900-8911
15. Fiala J.C., and Harris K.M. Extending unbiased stereology of brain ultrastructure to three-dimensional volumes. J Am Med Inform Assoc 8 (2001) 1-16
16. Ganeshina O., Berry R.W., Petralia R.S., Nicholson D.A., and Geinisman Y. Synapses with a segmented, completely partitioned postsynaptic density express more AMPA receptors than other axospinous synaptic junctions. Neuroscience 125 (2004) 615-623
17. Ganeshina O., Berry R.W., Petralia R.S., Nicholson D.A., and Geinisman Y. Differences in the expression of AMPA and NMDA receptors between axospinous perforated and nonperforated synapses are related to the configuration and size of postsynaptic densities. J Comp Neurol 468 (2004) 86-95
18. Garci{dotless}a-Lopez P., Garci{dotless}a-Mari{dotless}n V., and Freire M. Three-dimensional reconstruction and quantitative study of a pyramidal cell of a Cajal histological preparation. J Neurosci 26 (2006) 11249-11252
19. Geinisman Y., de Toledo-Morrell L., Morrell F., Heller R.E., Rossi M., and Parshall R.F. Structural synaptic correlate of long-term potentiation: formation of axospinous synapses with multiple, completely partitioned transmission zones. Hippocampus 3 (1993) 435-445
20. Geinisman Y. Structural synaptic modifications associated with hippocampal LTP and behavioural learning. Cereb Cortex 10 (2000) 952-962
21. Harris K.M. Serial electron microscopy as an alternative or compliment to confocal microscopy for the study of synapses and dendritic spines in the central nervous system. In: Stevens J.K., Mills L.R., and Trogadis J.E. (Eds). Three-dimensional confocal microscopy, volume investigation of biological specimens (1994), Academic Press, New York 421-445
22. Harris K.M., Jensen F.E., and Tsao B. 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 (1992) 2685-2705
23. Holtmat A.J., Trachtenberg J.T., Wilbrecht L., Shepherd G.M., Zhang X., Knott G., and Svodoba K. Transient and persistent dendritic spines in the neocortex in vivo. Neuron 45 (2005) 279-291
24. Kemp A., and Manahan-Vaughan D. Hippocampal long-term depression: master or minion in declarative memory processes?. Trends Neurosci 30 (2007) 111-118
25. Kirov S.A., and Harris K.M. Dendrites are more spiny on mature hippocampal neurons when synapses are inactivated. Nat Neurosci 2 (1999) 878-883
26. Kosub K.A., Do V.H., and Derrick B.E. NMDA receptor antagonists block heterosynaptic long-term depression (LTD) but not long-term potentiation (LTP) in the CA3 region following lateral perforant path stimulation. Neurosci Lett 374 1 (2005) 29-34
27. Malenka R.C., and Bear M.F. LTP and LTD: an embarrassment of riches. Neuron 44 (2004) 5-21
28. Manahan-Vaughan D., von Haebler D., Winter C., Juckel G., and Heinemann U. A single application of MK801 causes symptoms of acute psychosis, deficits in spatial memory, and impairment of synaptic plasticity in rats. Hippocampus 18 (2008) 125-134
29. Matus A. Actin-based plasticity in dendritic spines. Science 290 (2000) 754-758
30. Matus A. Growth of dendritic spines: a continuing story. Curr Opin Neurobiol 15 (2005) 67-72
31. Mezey S., Doyère V., De Souza I., Harrison E., Cambon C., Kendal C.E., Davies H.A., Laroche S., and Stewart M.G. 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
32. Nicholson D.A., Yoshida R., Berry R.W., Gallagher M., and Geinisman Y. Reduction in size of perforated postsynaptic densities in hippocampal axospinous synapses and age-related spatial learning impairments. J Neurosci 24 (2004) 7648-7653
33. Nicholson D.A., Trana R., Katz Y., Kath W.L., Spruston N., and Geinisman Y. Distance-dependent differences in synapse number and AMPA receptor expression in hippocampal CA1 pyramidal neurons. Neuron 50 (2006) 431-442
34. Nicholson D.A., and Geinisman Y. Axospinous synaptic subtype-specific differences in structure, size, ionotropic receptor expression, and connectivity in apical dendritic regions of rat hippocampal CA1 pyramidal neurons. J Comp Neurol 512 (2009) 399-418
35. Ostroff L.E., Fiala J.C., Allwardt B., and Harris K.M. Polyribosomes redistribute from dendritic shafts into spines with enlarged synapses during LTP in developing rat hippocampal slices. Neuron 35 (2002) 535-545
36. Peters A., and Kaiserman-Abramof I.R. The small pyramidal neuron of the rat cerebral cortex: the perikaryon, dendrites and spines. Am J Anat 127 (1970) 321-356
37. Popov V., Medvedev N.I., Davies H.A., and Stewart M.G. Mitochondria form a filamentous reticular network in hippocampal dendrites but are present as discrete bodies in axons: a three-dimensional ultrastructural study. J Comp Neurol 492 (2005) 50-65
38. Popov V.I., Davies H.A., Rogachevsky V.V., Patrushev I.V., Errington M.L., Gabbott P.L., Bliss T.V., and Stewart M.G. 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 (2004) 251-262
39. Popov V.I., Medvedev N.I., Kraev I.V., Gabbott P.L., Davies H.A., Lynch M., Cowley T.R., Berezin V., Bock E., and Stewart M.G. A cell adhesion molecule mimetic, FGL peptide, induces alterations in synapse and dendritic spine structure in the dentate gyrus of aged rats: a three-dimensional ultrastructural study. Eur J Neurosci 2 (2008) 301-314
40. Schuster T., Krug M., and Wenzel J. Spinules in axospinous synapses of the rat dentate gyrus: changes in density following long-term potentiation. Brain Res 523 (1990) 171-174
41. Sorra K.E., and Harris K.M. Stability in synapse number and size at 2 hr after long-term potentiation in hippocampal area CA1. J Neurosci 18 (1998) 658-671
42. Spacek J., and Harris K.M. Three-dimensional organization of smooth endoplasmic reticulum in hippocampal CA1 dendrites and dendritic spines of the immature and mature rat. J Neurosci 17 (1997) 190-203
43. Spacek J., and Harris K.M. Trans-endocytosis via spinules in adult rat hippocampus. J Neurosci 24 (2004) 4233-4241
44. Staubli U., and Lynch G. Stable hippocampal long-term potentiation elicited by "theta" pattern stimulation. Brain Res 435 (1987) 227-234
45. Stewart M.G., Medvedev N.I., Popov V.I., Schoepfer R., Davies H.A., Murphy K., Dallérac G.M., Kraev I.V., and Rodríguez J.J. 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 (2005) 3368-3378
46. Stewart M.G., Davies H.A., Sandi C., Kraev I.V., Rogachevsky V.V., Peddie C.J., Rodriguez J.J., Cordero M.I., Donohue H.S., Gabbott P.L., and Popov V.I. Stress suppresses and learning induces plasticity in CA3 of rat hippocampus: a three-dimensional ultrastructural study of thorny excrescences and their postsynaptic densities. Neuroscience 131 (2005) 43-54
47. Tao-Cheng J.H., Dosemeci A., Gallant P.E., Miller S., Galbraith J.A., Winters C.A., Azzam R., and Reese T.S. Rapid turnover of spinules at synaptic terminals. Neuroscience 160 1 (2009) 42-50
48. Toni N., Buchs P.A., Nikonenko I., Bron C.R., and Muller D. LTP promotes formation of multiple spine synapses between a single axon terminal and a dendrite. Nature 402 (1999) 421-425
49. Toni N., Buchs P.-A., Nikonenko I., Povilaitite P., Parisi P., and Muller D. Remodeling of synaptic membranes after induction of long-term potentiation. J Neurosci 21 (2001) 6245-6251
50. Wang X.B., Yang Y., and Zhou Q. Independent expression of synaptic and morphological plasticity associated with long-term depression. J Neurosci 27 (2007) 12419-12429
51. Yuste R., and Bonhoeffer T. Morphological changes in dendritic spines associated with long-term synaptic plasticity. Annu Rev Neurosci 24 (2001) 1071-1089
52. Zhou Q., Homma K.J., and Poo M.M. Shrinkage of dendritic spines associated with long-term depression of hippocampal synapses. Neuron 44 (2004) 749-757