Deficits of neuronal density in CA1 and synaptic density in the dentate gyrus, CA3 and CA1, in a mouse model of Down syndrome

Brain Research

Volumn 1022, Issue 1-2, 2004, Pages 101-109

  Ayberk Kurt, M ^a   Ilker Kafa, M ^a   Dierssen, Mara ^b   Ceri Davies, D ^c  

^a ULUDAG UNIVERSITY   (Turkey)

^b CENTRE FOR GENOMIC REGULATION CRG   (Spain)

^c ST GEORGE'S UNIVERSITY OF LONDON   (United Kingdom)

Author keywords

Down syndrome; Hippocampus; Neuron density; Stereology; Synapse density; Ts65Dn mouse

Indexed keywords

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN REGION; BRIGHT FIELD MICROSCOPY; CELL COMMUNICATION; CELL DENSITY; COGNITIVE DEFECT; CONTROLLED STUDY; DENTATE GYRUS; DIPLOIDY; DOWN SYNDROME; ELECTRON MICROSCOPY; FEMALE; HIPPOCAMPUS; MALE; MOUSE; MOUSE STRAIN; NEUROPATHOLOGY; NONHUMAN; PRIORITY JOURNAL; PYRAMIDAL NERVE CELL; SPECIES COMPARISON; SYNAPSE VESICLE; TEMPORAL CORTEX;

ANIMALS; CELL COUNT; DENTATE GYRUS; DIPLOIDY; DISEASE MODELS, ANIMAL; DOWN SYNDROME; HIPPOCAMPUS; MALE; MICE; MICROSCOPY, ELECTRON, TRANSMISSION; NEURONS; SYNAPSES; TRISOMY;

EID: 4444336568     PISSN: 00068993     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.brainres.2004.06.075     Document Type: Article

References (72)

1. J. Altman, and S.A. Bayer Migration and distribution of two populations of hippocampal granule cell precursors during the perinatal and postnatal periods J. Comp. Neurol. 301 1990 365 381
2. P. Andersen, J.C. Eccles, and P.E. Voorhoeve Inhibitory synapses on somas of purkinje cells in the cerebellum Nature (Lond.) 199 1963 655 656
3. L.L. Baxter, T.H. Moran, J.T. Richtsmeier, J. Troncoso, and R.H. Reeves Discovery and genetic localization of Down syndrome cerebellar phenotypes using the Ts65Dn mouse Hum. Mol. Genet. 9 2000 195 202
4. P.V. Belichenko, A.M. Kleschevnikov, E. Masliah, A.J. Vilar, C.J. Epstein, and W.C. Mobley Excitatory-inhibitory relationship in fascia dentata in Ts65Dn mice Abstr.-Soc. Neurosci. 715 2002 5
5. J.L. Bizon, and M. Gallagher Production of new cells in the rat dentate gyrus over the lifespan: relation to cognitive decline Eur. J. Neurosci. 18 2003 215 219
6. R.K. Calverley, K.S. Bedi, and D.G. Jones Estimation of the numerical density of synapses in rat neocortex. Comparison of the 'dissector' with an 'unfolding' method J. Neurosci. Methods 23 1988 195 205
7. M.F. Casanova, L.C. Walker, P.J. Whitehouse, and D.L. Price Abnormalities of the nucleus basal is in Down's syndrome Ann. Neurol. 18 1985 310 313
8. M. Colonnier Synaptic patterns on different cell types in the different laminae of the cat visual cortex; An electron microscope study Brain Res. 9 1968 268 287
9. P. Corsi, and J.T. Coyle Nerve growth factor corrects developmental impairments of basal forebrain cholinergic neurons in the trisomy 16 mouse Proc. Natl. Acad. Sci. U. S. A. 88 1991 1793 1797
10. J.T. Coyle, M.L. Oster-Granite, R.H. Reeves, and J.D. Gearhart Down syndrome, Alzheimer's disease and the trisomy 16 mouse Trends Neurosci. 11 1988 390 394
11. M.T. Davisson, and A.C. Costa Mouse models of Down syndrome B. Popko Mouse Models of Human Genetic Neurological Disease 1998 Plenum Publishing Corporation New York 127 163
12. M.T. Davisson, C. Schmidt, R.H. Reeves, N.G. Irving, E.C. Akeson, B.S. Harris, and R.T. Bronson Segmental trisomy as a mouse model for Down syndrome C.J. Epstein The Phenotypic Mapping of Down Syndrome and Other Aneuploid Conditions 1993 Wiley-Liss New York 117 133
13. D.M. De Groot, and E.P.B. Bierman Numerical changes in rat hippocampal synapses. An effect of 'aging'? Acta Stereol. 6 1987 53 58
14. S.T. DeKosky, and S.W. Scheff Synapse loss in frontal cortex biopsies in Alzheimer's disease: correlation with cognitive severity Ann. Neurol. 27 1990 457 464
15. S.T. DeKosky, S.W. Scheff, and S.C. Styren Structural correlates of cognition in dementia: quantification and assessment of synapse change Neurodegeneration 5 1996 417 421
16. G.E. Demas, R.J. Nelson, B.K. Krueger, and P.J. Yarowsky Spatial memory deficits in segmental trisomic Ts65Dn mice Behav. Brain Res. 82 1996 85 92
17. G.E. Demas, R.J. Nelson, B.K. Krueger, and P.J. Yarowsky Impaired spatial working and reference memory in segmental trisomy (Ts65Dn mice) Behav. Brain Res. 90 1998 199 201
18. M. Dierssen, R. Benavides-Piccione, C. Martí-nez-Cué, X. Estivill, J. Flórez, G.N. Elston, and J. DeFelipe Alterations of neocortical pyramidal cell phenotype in the Ts65Dn mouse model of Down syndrome: effects of environmental enrichment Cereb. Cortex 13 2003 758 764
19. J.C. Eccles The Physiology of Synapses 1964 Springer-Verlag Berlin 125 143
20. C.J. Epstein Trisomy 21 and the nervous system: from cause to cure C.J. Epstein The Neurobiology of Down Syndrome 1986 Raven Press New York 1 15
21. C.J. Epstein, D.R. Cox, and L.B. Epstein Mouse trisomy 16: an animal model of human trisomy 21 (Down Syndrome) Ann. N.Y. Acad. Sci. 450 1985 157 168
22. R.M. Escorihuela, A. Fernandez-Teruel, I.F. Vallina, C. Baamonde, M.A. Lumbreras, M. Dierssen, A. Tobena, and J. Flórez A behavioral assessment of Ts65Dn mice: a putative Down syndrome model Neurosci. Lett. 199 1995 143 146
23. R.M. Escorihuela, C. Martínez-Cué, I.F. Vallina, C. Baamonde, M. Dierssen, A. Tobeña, J. Flórez, and A. Fernàndez-Teruel Impaired short- and long-term memory in Ts65Dn mice Neurosci. Lett. 247 1998 171 174
24. Y. Geinisman, L. De Toledo-Morrell, and F. Morrel Loss of perforated synapses in the dentate gyrus: morphological substrate of memory deficit in aged rats Proc. Natl. Acad. Sci. U. S. A. 83 1986 3027 3031
25. A.C. Granholm, L.S. Sanders, and L.S. Crnic Loss of cholinergic phenotype in basal forebrain coincides with cognitive decline in a mouse model of Down's syndrome Exp. Neurol. 161 2000 647 663
26. A.C. Granholm, K.A. Ford, L.A. Hyde, H.A. Bimonte, C.L. Hunter, M. Nelson, D. Albeck, L.A. Sanders, E.J. Mufson, and L.S. Crnic Estrogen restores cognition and cholinergic phenotype in an animal model of Down syndrome Physiol. Behav. 77 2002 371 385
27. S. Greber, G. Lubec, N. Cairns, and M. Fountoulakis Decreased levels of synaptosomal associated protein 25 in the brain of patients with Down syndrome and Alzheimer's disease Electrophoresis 20 1999 928 934
28. M. Hattori, A. Fujiyama, T.D. Taylor, H. Watanabe, T. Yada, H.-S. Park, A. Toyoda, K. Ishii, Y. Totoki, D.-K. Choi, E. Soeda, M. Ohki, T. Takagi, Y. Sakaki, S. Taudien, K. Blechschmidt, A. Polley, U. Menzel, J. Delabar, K. Kumpf, R. Lehmann, D. Patterson, K. Reichwald, A. Rump, M. Schillhabel, A. Schudy, W. Zimmermann, A. Rosenthal, J. Kudoh, K. Shibuya, K. Kawasaki, S. Asakawa, A. Shintani, T. Sasaki, K. Nagamine, S. Mitsuyama, S.E. Antonarakis, S. Minoshima, N. Shimizu, G. Nordsiek, K. Hornischer, P. Brandt, M. Scharfe, O. Schon, A. Desario, J. Reichelt, G. Kauer, H. Blocker, J. Ramser, A. Beck, S. Klages, S. Hennig, L. Riesselmann, E. Dagand, S. Wehrmeyer, K. Borzym, K. Gardiner, D. Nizetic, F. Francis, H. Lehrach, R. Reinhardt, and M.-L. Yaspo The DNA sequence of human chromosome 21 Nature 405 2000 311 319
29. D.E. Hillman, and S. Chen Reciprocal relationship between size of postsynaptic densities and their number: constancy in contact area Brain Res. 295 1984 325 343
30. D.M. Holtzman, Y. Li, K. Chen, F.H. Gage, C.J. Epstein, and W.C. Mobley Nerve growth factor reverses neuronal atrophy in a Down syndrome model of age-related neurodegeneration Neurology 43 1993 2668 2673
31. D.M. Holtzman, D. Santucci, J. Kilbridge, J. Chua-Couzens, D.J. Fontana, S.E. Daniels, R.M. Johnson, K. Chen, Y. Sun, E. Carlson, E. Alleva, C.J Epstein, and W.C. Mobley Developmental abnormalities and age-related neurodegeneration in a mouse model of Down syndrome Proc. Natl. Acad. Sci. U. S. A. 93 1996 13333 13338
32. C.L. Hunter, H.A. Bimonte, and A.C. Granholm Behavioral comparison of 4 and 6 month-old Ts65Dn mice: age related impairments in working and reference memory Behav. Brain Res. 138 2003 121 131
33. C.L. Hunter, O. Isacson, M. Nelson, H. Bimonte-Nelson, H. Seo, L. Lin, K. Ford, M.S. Kindy, and A.C. Granholm Regional alterations in amyloid precursor protein and nerve growth factor across age in a mouse model of Down's syndrome Neurosci. Res. 45 2003 437 445
34. L.A. Hyde, and L.S. Crnic Age-related deficits in context discrimination learning in Ts65Dn mice that model Down Syndrome and Alzheimer's disease Behav. Neurosci. 115 2001 1239 1246
35. L.A. Hyde, D.F. Frisone, and L.S. Crnic Ts65Dn mice, a model for Down Syndrome, have deficits in context discrimination learning suggesting impaired hippocampal function Behav. Neurosci. 118 2001 53 60
36. A.M. Insausti, M. Megias, D. Crespo, L.M. Cruz-Orive, M. Dierssen, T.F. Vallina, R. Insausti, and J. Flórez Hippocampal volume and neuronal number in Ts65Dn mice: a murine model of Down syndrome Neurosci. Lett. 253 1998 175 178
37. S. Kish, H. Karlinsky, L. Becker, J. Gilbert, M. Rebbetoy, L.J. Chang, L. Di Stefano, and O. Hornykiewicz Down's syndrome individuals begin life with normal levels of brain cholinergic markers J. Neurochem. 52 1989 1183 1187
38. J.A. Kleim, E. Lussnig, E.R. Schwarz, T.A. Comery, and W.T. Greenough Synaptogenesis and fos expression in the motor cortex of the adult rat after motor skill learning J. Neurosci. 16 1996 4529 4535
39. S.L. Klein, L.J. Kriegsfeld, J.E. Hairston, V. Rau, R.J. Nelson, and P.J. Yarowsky Characterization of sensorimotor performance, reproductive and aggressive behaviors in segmental trisomic 16 (Ts65Dn) mice Physiol. Behav. 60 1996 1159 1164
40. A.M. Kleschevnikov, P.V. Belichenko, S.B. Basu, C.J. Epstein, A.J. Vilar, R.C. Malenka, and W.C. Mobley Increased inhibition as a cause of suppresses plasticity in dentate gyrus of Ts65Dn mice, an animal model of Down Syndrome Abstr.-Soc. Neurosci. 751 2002 4
41. M.A. Kurt, D.C. Davies, M. Kidd, M. Dierssen, and J. Florez Synaptic deficit in the temporal cortex of partial trisomy 16 (Ts65Dn) mice Brain Res. 858 2000 191 197
42. E.A. Ling, J.A. Paterson, A. Privat, S. Mori, and C.P. Leblond Investigation of glial cells in semithin sections: I. Identification of glial cells in the brain of young rats J. Comp. Neurol. 149 1973 43 71
43. T.M. Mayhew Stereological approach to the study of synapse morphology with particular regard to estimating number in a volume and on a surface J. Neurocytol. 8 1979 121 138
44. T.M. Mayhew A review of recent advances in stereology for quantifying neural structure J. Neurocytol. 21 1992 313 328
45. T. Miki, Y. Fukui, Y. Takeuchi, and M. Itoh A quantitative study of the effects of prenatal X-irradiation on the development of cerebral cortex in rats Neurosci. Res. 23 1995 241 247
46. T. Miki, Y. Fukui, M. Itoh, S. Hisano, Q. Xie, and Y. Takeuchi Estimation of the numerical densities of neurons and synapses in cerebral cortex Brain Res. Protoc. 2 1997 9 16
47. R.G.M. Morris Developments of a water-maze procedure for studying spatial learning in the rat J. Neurosci. Methods 1 1984 47 60
48. R.G. Morris, P. Garrud, J.N. Rawlins, and J. O'Keefe Place navigation impaired in rats with hippocampal lesions Nature 297 1982 681 683
49. R.G.M. Morris, F. Schenk, F. Tweedie, and L.E. Jarrard Ibotenate lesions hippocampus and/or subiculum-dissociating components of allocentric spatial-learning Eur. J. Neurosci. 2 1990 1016 1028
50. E. Moser, M.B. Moser, and P. Andersen Spatial learning impairment parallels the magnitude of dorsal hippocampal-lesions, but is hardly present following ventral lesions J. Neurosci. 13 1993 3916 3925
51. M.A. Packer, Y. Stasiv, A. Benraiss, E. Chmielnicki, A. Grinberg, H. Westphal, S.A. Goldman, and G. Enikolopov Nitric oxide negatively regulates mammalian adult neurogenesis Proc. Natl. Acad. Sci. U. S. A. 100 2003 9566 9571
52. T.L. Petit, J.C. LeBoutillier, D.P. Alfano, and L.E. Becker Synaptic development in the human fetus: a morphometric analysis of normal and Down syndrome neocortex Exp. Neurol. 83 1984 13 23
53. J. Raisman, W.M. Cowan, and T.P.S. Powell The extrinsic efferent, commissural and association fibres of the hippocampus Brain 88 1965 963 996
54. R.H. Reeves, N.G. Irving, T.H. Moran, A. Wohn, C. Kitt, S.S. Sisodia, C. Schmidt, R.T. Bronson, and M.T. Davisson A mouse model for Down syndrome exhibits learning and behaviour deficits Nat. Med. 11 1995 177 184
55. D. Risser, G. Lubec, N. Cairns, and M. Herrera-Marschitz Excitatory amino acids and monoamines in parahippocampal gyrus and frontal cortical pole of adults with Down syndrome Life Sci. 60 1997 1231 1237
56. E.T. Rolls Memory systems in the brain Annu. Rev. Psychol. 51 2000 599 630
57. H. Sago, E.J. Carlson, D.J. Smith, J. Kilbridge, E.M. Rubin, W.C. Mobley, C.J. Epstein, and T.T. Huang Ts1Cje, a partial trisomy 16 mouse model for Down syndrome, exhibits learning and behavioural abnormalities Proc. Natl. Acad. Sci. U. S. A. 95 1998 6256 6261
58. H. Sago, E.J. Carlson, D.J. Smith, J. Kilbridge, L.S. Crnic, E.M. Rubin, W.C. Mobley, T.T. Huang, and C.J. Epstein Genetic dissection of the region associated with behavioural abnormalities in mouse models for Down syndrome Pediatr. Res. 48 2000 606 613
59. S.W. Scheff, S.T. DeKosky, and D.A. Price Quantitative assessment of cortical synaptic density in Alzheimer's disease Neurobiol. Aging 11 1990 29 37
60. K.S. Shim, and G. Lubec Drebrin, a dendritic spine protein, is manifold decreased in brains of patients with Alzheimer's disease and Down syndrome Neurosci. Lett. 24 2002 209 212
61. R.J. Siarey, J. Stoll, S.I. Rapoport, and Z. Galdzicki Altered long-term potentiation in the young and old Ts65Dn mouse, a model for Down Syndrome Neuropharmacology 36 1997 1549 1554
62. R.J. Siarey, E.J. Carlson, C.J. Epstein, A. Balbo, S.I. Rapoport, and Z. Galdzicki Increased synaptic depression in the Ts65Dn mouse, a model for mental retardation in Down Syndrome Neuropharmacology 38 1999 1917 1920
63. D.C. Sterio The unbiased estimation of number and sizes of arbitrary particles using the dissector J. Microsc. 134 1984 127 136
64. S. Takashima, K. Iida, T. Mito, and M. Arima Dendritic and histochemical development and ageing in patients with Down's syndrome J. Intellect. Disabil. Res. 38 1994 265 273
65. R.D. Terry, E. Masliah, D.P. Salmon, N. Butters, R. DeTeresa, R. Hill, L.A. Hansen, and R. Katzman Physical basis of cognitive alterations in Alzheimer's disease: synapse loss is the major correlate of cognitive impairment Ann. Neurol. 30 1991 572 580
66. A.M. Turner, and W.T. Greenough Differential rearing effects on rat visual cortex synapses: I. Synaptic and neuronal density and synapses per neuron Brain Res. 329 1985 195 203
67. M.A. Warren Simple morphometry of the nervous system M.G. Stewart Quantitative Method in Neuroanatomy 1992 Wiley New York 211 247
68. R. Weitzdoerfer, M. Dierssen, M. Fountoulakis, and G. Lubec Fetal life in Down syndrome starts with normal neuronal density but impaired dendritic spines and synaptosomal structure J. Neural Transm., Suppl. 61 2001 59 70
69. M.J. West Stereological methods for estimating the total number of neurons and synapses: issues of precision and bias Trends Neurosci. 22 1999 51 61
70. K.E. Wisniewski Down syndrome children often have brain maturation delay, retardation of growth and cortical dysgenesis Am. J. Med. Genet., Suppl. 7 1990 274 281
71. K.E. Wisniewski, M. Laure-Kaminowska, and H.M. Wisniewski Evidence of arrest of neurogenesis and synaptogenesis in Down Syndrome Brains N. Engl. J. Med. 311 1984 1187 1188
72. C.M. Yates, J. Simpson, A. Gordon, A.F. Maloney, Y. Allison, I.M. Ritchie, and A. Urquhart Catecholamines and cholinergic enzymes in pre-senile and senile Alzheimer-type dementia and Down's syndrome Brain Res. 280 1983 119 126