Synaptic transmission is impaired prior to plaque formation in amyloid precursor protein-overexpressing mice without altering behaviorally-correlated sharp wave-ripple complexes

Neuroscience

Volumn 162, Issue 4, 2009, Pages 1081-1090

  Hermann, D ^a   Both, M ^b   Ebert, U ^a   Gross, G ^a   Schoemaker, H ^a   Draguhn, A ^b   Wicke, K ^a   Nimmrich, V ^a  

^a ABBOTT GMBH AND CO KG   (Germany)

^b UNIVERSITY OF HEIDELBERG   (Germany)

Author keywords

Alzheimer's disease; amyloid plaques; amyloid ; sharp wave ripples

Indexed keywords

AMYLOID PRECURSOR PROTEIN; OLIGOMER;

AGING; ANIMAL BEHAVIOR; ANIMAL TISSUE; ARTICLE; BRAIN ELECTROPHYSIOLOGY; BRAIN SLICE; CONTROLLED STUDY; FEMALE; HIPPOCAMPUS; IMMUNOHISTOCHEMISTRY; MEMORY CONSOLIDATION; MOUSE; MUTANT; NEUROTRANSMISSION; NONHUMAN; OSCILLATION; PRIORITY JOURNAL; PROTEIN EXPRESSION; SYNAPTIC TRANSMISSION; WILD TYPE;

AGING; AMYLOID BETA-PROTEIN PRECURSOR; ANIMALS; BEHAVIOR, ANIMAL; EXCITATORY POSTSYNAPTIC POTENTIALS; FEMALE; HIPPOCAMPUS; HUMANS; MEMORY; MICE; MICE, TRANSGENIC; PLAQUE, AMYLOID; SYNAPTIC TRANSMISSION;

EID: 67949104946     PISSN: 03064522     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.neuroscience.2009.05.044     Document Type: Article

References (57)

1. Axmacher N., Mormann F., Fernández G., Elger C.E., and Fell J. Memory formation by neuronal synchronization. Brain Res Rev 52 (2006) 170-182
2. Barghorn S., Nimmrich V., Striebinger A., Krantz C., Keller P., Janson B., Bahr M., Schmidt M., Bitner R.S., Harlan J., Barlow E., Ebert U., and Hillen H. Globular amyloid β-peptide oligomer-a homogenous and stable neuropathological protein in Alzheimer's disease. J Neurochem 95 (2005) 834-847
3. Barnes C.A., Rao G., and McNaughton B.L. Increased electrotonic coupling in aged rat hippocampus: a possible mechanism for cellular excitability changes. J Comp Neurol 259 (1987) 547-558
4. Başar E., Başar-Eroglu C., Karakaş S., and Schürmann M. Gamma, alpha, delta, and theta oscillations govern cognitive processes. Int J Psychophysiol 39 (2001) 241-248
5. Blennow K., Bogdanovic N., Alafuzoff I., Ekman R., and Davidsson P. Synaptic pathology in Alzheimer's disease: relation to severity of dementia, but not to senile plaques, neurofibrillary tangles, or the ApoEIV allele. J Neural Transm 103 (1996) 603-618
6. Born J., Rasch B., and Gais S. Sleep to remember. Neuroscientist 12 (2006) 410-424
7. Buzsáki G., Horváth Z., Urioste R., Hetke J., and Wise K. High-frequency network oscillation in the hippocampus. Science 256 (1992) 1025-1027
8. Buzsáki G. Memory consolidation during sleep: a neurophysiological perspective. J Sleep Res 7 (1998) 17-23
9. Cacucci F., Yi M., Wills T.J., Chapman P., and O'Keefe J. Place cell firing correlates with memory deficits and amyloid plaque burden in Tg2576 Alzheimer mouse model. Proc Natl Acad Sci U S A 105 (2008) 7863-7868
10. Chapman P.F., White G.L., Jones M.W., Cooper-Blacketer D., Marshall V.J., Irizarry M., Younkin L., Good M.A., Bliss T.V., Hyman B.T., Younkin S.G., and Hsiao K.K. Impaired synaptic plasticity and learning in aged amyloid precursor protein transgenic mice. Nat Neurosci 2 (1999) 271-276
11. Cleary J. Natural oligomers of the amyloid-β protein specifically disrupt cognitive function. Nat Neurosci 8 (2005) 79-84
12. Dewachter I., Reversé D., Caluwaerts N., Ris L., Kuipéri C., Van den Haute C., Spittaels K., Umans L., Serneels L., Thiry E., Moechars D., Mercken M., Godaux E., and Van Leuven F. Neuronal deficiency of presenilin 1 inhibits amyloid plaque formation and corrects hippocampal long-term potentiation but not a cognitive defect of amyloid precursor protein [V717I] transgenic mice. J Neurosci 22 (2002) 3445-3453
13. Draguhn A., Traub R.D., Schmitz D., and Jefferys J.G. Electrical coupling underlies high-frequency oscillation in the hippocampus in vitro. Nature 394 (1998) 189-192
14. Driver J.E., Racca C., Cunningham C.C., Towers S.K., Davies C.H., Whittington M.A., and Lebeau F.E. Impairment of hippocampal gamma (γ)-frequency oscillations in vitro in mice overexpressing human amyloid precursor protein (APP). Eur J Neurosci 26 (2007) 1280-1288
15. Engel A.K., Fries P., and Singer W. Dynamic predictions: oscillations and synchrony in top-down processing. Nat Rev Neurosci 2 (2001) 704-716
16. Fitzjohn S., Morton R., Kuenzi F., Rosahl T., Shearman M., Lewis H., Smith D., Reynolds D., Davies C., Collingridge G., and Seabrook G. Age-related impairment of synaptic transmission but normal long-term potentiation in transgenic mice that overexpress the human APP695SWE mutant form of amyloid precursor protein. Trends Genet 21 (2001) 4691-4698
17. Fukuda T., and Kosaka T. Gap junctions linking the dendritic network of GABAergic interneurons in the hippocampus. J Neurosci 20 (2000) 1519-1528
18. Holcomb L., Gordon M.N., McGowan E., Yu X., Benkovic S., Jantzen P., Wright K., Saad I., Mueller R., Morgan D., Sanders S., Zehr C., O'Campo K., Hardy J., Prada C.M., Eckman C., Younkin S., Hsiao K., and Duff K. Accelerated Alzheimer-type phenotype in transgenic mice carrying both mutant amyloid precursor protein and presenilin 1 transgenes. Nat Med 4 (1998) 97-100
19. Hsia A., Masliah E., Mcconlogue L., Yu G.Q., Tatsuno G., Hu K., Kholodenko D., Malenka R., Nicoll R., and Mucke L. Plaque-independent disruption of neural circuits in Alzheimer's disease mouse models. Proc Natl Acad Sci U S A 96 (1999) 3228-3233
20. Hsiao K., Chapman P., Nilsen S., Eckman C., Harigaya Y., Younkin S., Yang F., and Cole G. Correlative memory deficits, Aβ elevation, and amyloid plaques in transgenic mice. Science 274 (1996) 99-102
21. Ishibashi K., Tomiyama T., Nishitsuji K., Hara M., and Mori H. Absence of synaptophysin near cortical neurons containing oligomer Aβ in Alzheimer's disease brain. J Neurosci Res 84 (2006) 632-636
22. Jacobsen J.S., Wu C.C., Redwine J.M., Comery T.A., Arias R., Bowlby M., Martone R., Morrison J.H., Pangalos M.N., Reinhart P.H., and Bloom F.E. Early-onset behavioral and synaptic deficits in a mouse model of Alzheimer's disease. Proc Natl Acad Sci U S A 103 (2006) 5161-5166
23. Kawarabayashi T., Younkin L.H., Saido T.C., Shoji M., Ashe K.H., and Younkin S.G. Age-dependent changes in brain, CSF, and plasma amyloid (beta) protein in the Tg2576 transgenic mouse model of Alzheimer's disease. J Neurosci 21 (2001) 372-381
24. Kelly B.L., Vassar R., and Ferreira A. β-Amyloid-induced dynamin 1 depletion in hippocampal neurons. A potential mechanism for early cognitive decline in Alzheimer disease. J Biol Chem 280 (2005) 31746-31753
25. Kelly B.L., and Ferreira A. β-Amyloid disrupted synaptic vesicle endocytosis in cultured hippocampal neurons. Neuroscience 147 (2007) 60-70
26. King D.L., Arendash G.W., Crawford F., Sterk T., Menendez J., and Mullan M.J. Progressive and gender-dependent cognitive impairment in the APP(SW) transgenic mouse model for Alzheimer's disease. Behav Brain Res 103 (1999) 145-162
27. Kokubo H., Kayed R., Glabe C.G., and Yamaguchi H. Soluble Aβ oligomers ultrastructurally localize to cell processes and might be related to synaptic dysfunction in Alzheimer's disease brain. Brain Res 1031 (2005) 222-228
28. Kubota D., Colgin L.L., Casale M., Brucher F.A., and Lynch G. Endogenous waves in hippocampal slices. J Neurophysiol 89 (2003) 81-89
29. Lacor P.N., Buniel M.C., Furlow P.W., Clemente A.S., Velasco P.T., Wood M., Viola K.L., and Klein W.L. Abeta oligomer-induced aberrations in synapse composition, shape, and density provide a molecular basis for loss of connectivity in Alzheimer's disease. J Neurosci 27 (2007) 796-807
30. LeBeau F.E., Towers S.K., Traub R.D., Whittington M.A., and Buhl E.H. Fast network oscillations induced by potassium transients in the rat hippocampus in vitro. J Physiol 542 (2002) 167-179
31. Lesné S., Koh M.T., Kotilinek L., Kayed R., Glabe C.G., Yang A., Gallagher M., and Ashe K.H. A specific amyloid-β protein assembly in the brain impairs memory. Nature 440 (2006) 352-357
32. Lesné S., Kotilinek L., and Ashe K.H. Plaque-bearing mice with reduced levels of oligomeric amyloid-β assemblies have intact memory function. Neuroscience 151 (2008) 745-749
33. Magnusson K.R., Nelson S.E., and Young A.B. Age-related changes in the protein expression of subunits of the NMDA receptor. Mol Brain Res 99 (2002) 40-45
34. Maier N., Güldenagel M., Söhl G., Siegmund H., Willecke K., and Draguhn A. Reduction of high-frequency network oscillations (ripples) and pathological network discharges in hippocampal slices from connexin 36-deficient mice. J Physiol 541 (2002) 521-528
35. Maier N., Nimmrich V., and Draguhn A. Cellular and network mechanisms underlying spontaneous sharp wave-ripple complexes in mouse hippocampal slices. J Physiol 550 (2003) 873-887
36. Miller D.B., and O'Callaghan J.P. Aging, stress and the hippocampus. Ageing Res Rev 4 (2005) 123-140
37. Moechars D., Dewachter I., Lorent K., Reverse D., Baekelandt V., Naidu A., Tesseur I., Spittaels K., Haute C., Checleri F., Godaux E., Cordell B., and Leuven F. Early phenotypic changes in transgenic mice that overexpress different mutants of amyloid precursor protein in brain. J Biol Chem 274 (1999) 6483-6492
38. Mölle M., Yeshenko O., Marshall L., Sara S.J., and Born J. Hippocampal sharp wave-ripples linked to slow oscillations in rat slow-wave sleep. J Neurophysiol 96 (2006) 62-70
39. Nimmrich V., Maier N., Schmitz D., and Draguhn A. Induced sharp wave-ripple complexes in the absence of synaptic inhibition in mouse hippocampal slices. J Physiol 563 (2005) 663-670
40. Nimmrich V., Grimm C., Draguhn A., Barghorn S., Lehmann A., Schoemaker H., Hillen H., Gross G., Ebert U., and Bruehl C. Amyloid β oligomers (Aβ 1-42 globulomer) suppress spontaneous synaptic activity by inhibition of P/Q calcium currents. J Neurosci 28 (2008) 788-797
41. Pais I., Hormuzdi S.G., Monyer H., Traub R.D., Wood I.C., Buhl E.H., Whittington M.A., and LeBeau F.E. Sharp wave-like activity in the hippocampus in vitro in mice lacking the gap junction protein connexin 36. J Neurophysiol 89 (2003) 2046-2054
42. Rocher A.B., Kinson M.S., and Luebke J.I. Significant structural but not physiological changes in cortical neurons of 12-month-old Tg2576 mice. Neurobiol Dis 32 (2008) 309-318
43. Roder S., Danober L., Pozza M.F., Lingenhoehl K., Wiederhold K.H., and Olpe H.R. Electrophysiological studies on the hippocampus and prefrontal cortex assessing the effects of amyloidosis in amyloid precursor protein 23 transgenic mice. Neuroscience 120 (2003) 705-720
44. Selkoe D.J. Alzheimer's disease is a synaptic failure. Science 298 (2002) 789-791
45. Shankar G.M., Bloodgood B.L., Townsend M., Walsh D.M., Selkoe D.J., and Sabatini B.L. Natural oligomers of the Alzheimer amyloid-β protein induce reversible synapse loss by modulating an NMDA-type glutamate receptor-dependent signalling pathway. J Neurosci 27 (2007) 2866-2875
46. Shankar G.M., Li S., Mehta T.H., Garcia-Munoz A., Shepardson N.E., Smith I., Brett F.M., Farrell M.A., Rowan M.J., Lemere C.A., Regan C.M., Walsh D.M., Sabatini B.L., and Selkoe D.J. Amyloid-β protein dimers isolated directly from Alzheimer's brain impairs synaptic plasticity and memory. Nat Med 14 (2008) 837-842
47. Siapas A.G., and Wilson M.A. Coordinated interactions between hippocampal ripples and cortical spindles during slow-wave sleep. Neuron 21 (1998) 1123-1128
48. Stern E.A., Bacskai B.J., Hickey G.A., Attenello F.J., Lombardo J.A., and Hyman B.T. Cortical synaptic integration in vivo is disrupted by amyloid-β plaques. J Neurosci 24 (2004) 4535-4540
49. Tomiyama T., Nagata T., Shimada H., Teraoka R., Fukushima A., Kanemitsu H., Takuma H., Kuwano R., Imagawa M., Ataka S., Wada Y., Yoshioka E., Nishizaki T., Watanabe Y., and Mori H. A new amyloid β variant favoring oligomerization in Alzheimer's-type dementia. Ann Neurol 63 (2008) 377-387
50. Townsend M., Shankar G.M., Mehta T., Walsh D.M., and Selkoe D.J. Effects of secreted oligomers of amyloid β-protein on hippocampal synaptic plasticity: a potent role for trimers. J Physiol 572 (2006) 477-492
51. Traub R.D., Draguhn A., Whittington M.A., Baldeweg T., Bibbig A., Buhl E.H., and Schmitz D. Axonal gap junctions between principal neurons: a novel source of network oscillations, and perhaps epileptogenesis. Rev Neurosci 13 (2002) 1-30
52. Vloeberghs E., Van Dam D., D'Hooge R., Staufenbiel M., and De Deyn P.P. APP23 mice display working memory impairment in the plus-shaped water maze. Neurosci Lett 407 (2006) 6-10
53. Walsh D.M., Klyubin I., Fadeeva J.V., Cullen W.K., Anwyl R., Wolfe M.S., Rowan M.J., and Selkoe D.J. Naturally secreted oligomers of amyloid β protein potently inhibit hippocampal long-term potentiation in vivo. Nature 416 (2002) 535-539
54. Walsh D.M., and Selkoe D.J. Aβ oligomers-a decade of discovery. J Neurochem 101 (2007) 1172-1184
55. Wang Q., Wu J., Rowan M.J., and Anwyl R. β-Amyloid inhibition of long-term potentiation is mediated via tumor necrosis factor. Eur J Neurosci 22 (2005) 2827-2832
56. Watanabe T., Yamagata N., Takasaki K., Sano K., Hayakawa K., Katsurabayashi S., Egashira N., Mishima K., Iwasaki K., and Fujiwara M. Decreased acetylcholine release is correlated to memory impairment in the Tg2576 transgenic mouse model of Alzheimer's disease. Brain Res 1249 (2009) 222-228
57. Westerman M.A., Cooper-Blacketer D., Mariash A., Kotilinek L., Kawarabayashi T., Younkin L.H., Carlson G.A., Younkin S.G., and Ashe K.H. The relationship between Aβ and memory in the Tg2576 mouse model of Alzheimer's disease. J Neurosci 22 (2002) 1858-1867