An in vitro and in vivo study of early deficits in associative learning in transgenic mice that over-express a mutant form of human APP associated with Alzheimer's disease

European Journal of Neuroscience

Volumn 20, Issue 7, 2004, Pages 1945-1952

  Domínguez Del Toro, Eduardo ^a   Rodríguez Moreno, Antonio ^a   Porras García, Elena ^a   Sánchez Campusano, Raudel ^a   Blanchard, Véronique ^b   Laville, Michel ^b   Böhme, Georg A ^b   Benavides, Jesús ^b   Delgado García, José M ^a  

^a UNIVERSIDAD PABLO DE OLAVIDE   (Spain)

^b SANOFI   (France)

Author keywords

APPLd2 mice; Classical conditioning; Eyeblink; Hippocampus; Long term potentiation; Transgenic mice

Indexed keywords

AMYLOID PRECURSOR PROTEIN; MUTANT PROTEIN;

ALZHEIMER DISEASE; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONDITIONING; CONTROLLED STUDY; DIAGNOSTIC VALUE; EYELID REFLEX; FACILITATION; GENE MUTATION; GENE OVEREXPRESSION; HIPPOCAMPUS; HUMAN; IN VITRO STUDY; IN VIVO STUDY; LEARNING; LONG TERM POTENTIATION; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PYRAMIDAL NERVE CELL; SENILE PLAQUE; STATE DEPENDENT LEARNING; SYNAPSE; TRANSGENIC MOUSE;

ALZHEIMER DISEASE; AMYLOID BETA-PROTEIN PRECURSOR; ANIMALS; ASSOCIATION LEARNING; CONDITIONING, CLASSICAL; DISEASE MODELS, ANIMAL; EVOKED POTENTIALS; EYELIDS; HUMANS; MALE; MICE; MICE, TRANSGENIC; MUTATION; REACTION TIME;

EID: 8144231283     PISSN: 0953816X     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.1460-9568.2004.03643.x     Document Type: Article

References (43)

1. Bao, S., Chen, L., Kim, J.J. & Thompson, R.F. (2002) Cerebellar cortical inhibition and classical eyeblink conditioning. Proc. Natl. Acad. Sci. USA, 99, 1592-1597.
2. Blanchard, V., Moussaoui, S., Czech, C., Touchet, N., Bonici, B., Planche, M., Canton, T., Jedidi, I., Gohin, M., Wirths, O., Bayer, T.A., Langui, D., Duyckaerts, C., Tremp, G. & Pradier, L. (2003) Time sequence of maturation of dystrophic neuntes associated with Aβ deposits in APP/PS1 transgenic mice. Exp. Neurol., 184, 247-263.
3. Bliss, TV. & Collingridge, G.L. (1993) A synaptic model of memory: long-term potentiation in the hippocampus. Nature, 361, 31-39.
4. Buttini, M., Yu, G.-Q., Shockley, K., Huang, Y., Jones, B., Masliah, E., Mallory, M., Yeo, T., Longo, P.M. & Mucke, L. (2002) Modulation of Alzheimer-like synaptic and cholinergic deficits in transgenic mice by human apolipoprotein E depends on isoform, aging, and overexpression of amyloid β peptides but not on plaque formation. J. Neurosci., 22, 10539-10548.
5. Capocchi, G., Zampolini, M. & Larson, J. (1992) Theta burst stimulation is optimal for induction of LTP at both apical and basal dendritic synapses on hippocampal CA neurons. Brain Res., 591, 332-339.
6. Chapman, P.P., 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.O. & Hsiao, K.K. (1999) Impaired synaptic plasticity and learning in aged amyloid precursor protein transgenic mice. Nat. Neurosci., 2, 271-276.
7. Chen, G., Chen, K.S., Knox, J., Inglis, J., Bernard, A., Martin, S.J., Justice, A., McConlogue, L., Games, D., Freeman, S.B. & Morris, R.G.M. (2000) A learning deficit related to age and β-amyloid plaques in a mouse model of Alzheimer's disease. Nature, 408, 975-979.
8. Christian, K.M., Polos, A.M., Lavond, D.O. & Thompson, R.F. (2004) Comment on 'Cerebellar LTD and learning-dependent timing of conditioned eyelid responses'. Science, 304, 211b.
9. De Zeeuw, C.I., Elgersma, Y, Hulscher, H.C., Dortland, B.R., Hensbroek, R.A., Ruigrok, T.J.H. & Koekkoek, S.K.E. (2004) Response to comment on 'Cerebellar LTD and learning-dependent timing of conditioned eyelid responses'. Science, 304, 211c.
10. Dewachter, I., Reverse, D., Caluwaerts, N., Ris, L., Kuiperi, C., Van den Haute, C., Spittaels, K., Umans, L., Serneels, L., Thiry, E., Moechars, D., Mercken, M., Godaux, E. & Van Leuven, F. (2002) Neuronal deficiency of presenilin 1 inhibits amyloid plaque formation and corrects hippocampal long-term potentiation but not a cognitive defect of amyloid precursor protein [V7171] transgenic mice. J. Neurosci., 22, 3445-3453.
11. Dewachter, I., van Dorpe, J., Spittaels, K., Tesseur, I., Van Den Haute, C., Moechars, D. & Van Leuven, F. (2000) Modeling Alzheimer's disease in transgenic mice: effect of age and of presenilin 1 on amyloid biochemistry and pathology in APP/London mice. Exp. Gerontol., 35, 831-841.
12. Domínguez-del-Toro, E., Rodríguez-Moreno, A., Porras-García, E., Sánchez-Campusano, R., Böhme, O.A., Benavides, J. & Delgado-García, J.M. (2003) An in vitro and in vivo study of learning capabilities in wild-type and transgenic mice with Alzheimer-like deficits. Soc. Neurosci. Abstr., 842, 3.
13. Evinger, C., Manning, K.A. & Sibony, P.A. (1991) Eyelid movements. Mechanisms and normal data. Invest. Ophthalmol. Visual. Sci., 32, 387-400.
14. Fernández de Sevilla, D., Cabezas, C., Oshima de Prada, A.N., Sánchez-Jiménez, A. & Buno, W. (2002) Selective muscarinic regulation of functional glutamatergic Schaffer collateral synapses in rat CA1 pyramidal neurons. J. Physiol. (Lond.), 545, 51-63.
15. Fitzjohn, S.M., Morton, R.A., Kuenzi, F., Rosahl, T.W., Shearman, M., Lewis, H., Smith, D., Reynolds, D.S., Davies, C.H., Collingridge, G.L. & Seabrook, G.R. (2001) 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. J. Neurosci., 21, 4691-4698.
16. Gruart, A., Blázquez, P. & Delgado-García, J.M. (1995) Kinematics of unconditioned and conditioned eyelid movements in the alert cat. J. Neurophysiol., 74, 226-248.
17. Gruart, A., Schreurs, B.C., Domínguez-del-Toro, E. & Delgado-García, J.M. (2000) Kinetic and frequency-domain properties of reflex and conditioned eyelid responses in the rabbit. J. Neurophysiol., 83, 836-852.
18. Kamenetz, F., Tomita, T., Hsieh, H., Seabrook, G., Borchelt, D., Iwatsubo, T., Sisodia, S. & Malinow, R. (2003) APP processing and synaptic function. Neuron, 37, 925-937.
19. Kelly, PH., Bondoli, L., Hunziker, D., Schlecht, H.-P., Carver, K., Maguir, E., Abramowski, D., Wiederhold, K.-H., Sturchler-Pierrat, C., Jucker, M., Bergman, R., Staufenbiel, M. & Sommer, B. (2003) Progressive age-related impairment of cognitive behavior in APP23 transgenic mice. Neurobiol. Aging, 24, 365-378.
20. Koekkoek, S.K., Den Ouden, W.L., Perry, G., Highstein, S.M. & De Zeeuw, C.I. (2002) Monitoring kinetic and frequency-domain properties of eyelid responses in mice with magnetic distance measurement technique. J. Neurophysiol., 88, 2124-2133.
21. Koekkoek, S.K., Hulscher, H.C., Dortland, B.R., Hensbroek, R.A., Elgersma, Y., Ruigrok, T.J. & De Zeeuw, C.I. (2003) Cerebellar LTD and learning-dependent timing of conditioned eyelid responses. Science, 301, 1736-1739.
22. Kugelberg, E. (1952) Facial reflexes. Brain, 75, 385-396.
23. Liu, L., Ikonen, S., Heikkinen, T., Heikkilä, M., Puoliväli, J., van Groen, T. & Tanila, H. (2002) Effects of fimbria-fornix ilesion and amyloid pathology on spatial learning and memory in transgenic APP + PS1 mice. Behav. Brain Res., 134, 433-445.
24. Marshall-Goodell, B., Kehoe, E.J. & Gormezano, I. (1992) Laws of the unconditioned reflex and rabbit nictitating membrane preparation. Psychobiology, 20, 229-237.
25. Moechars, D., Dewachter, I., Lorent, K., Reversé, D., Baekeladt, V., Naidu, A., Tesseur, I., Spittaels, K., Van Dern Haute, C., Checler, F., Godaux, E., Cordell, B. & Van Leuven, F. (1999) Early phenotypic changes in transgenic mice that overexpress different mutants of amyloid precursor protein in brain. J. Biol. Chem., 274, 6483-6492.
26. Múnera, A., Gruart, A., Muñoz, M.D. & Delgado-García, J.M. (2000) Scopolamine impairs information processing in the hippocampus and performance of a learned eyeblink response. Neurosci. Lett., 292, 33-36.
27. Múnera, A., Gruart, A., Muñoz, M.D., Fernández-Mas, R. & Delgado-García, J.M. (2001) Hippocampal pyramidal cells activity encodes conditioned stimulus predictive value during classical conditioning in alert cats. J. Neurophysiol., 86, 2571-2582.
28. Ohno, M., Sametsky, E.A., Youkin, L.H., Oakley, H., Younkin, S.G., Citron, M., Vassar, R. & Disterhoft, J.F. (2004) BACE1 deficiency rescues memory deficits and cholinergic dysfunction in a mouse model of Alzheimer's disease. Neuron, 41, 27-33.
29. Selkoe, D.J. (2002) Alzheimer's disease is a synaptic failure. Science, 298, 789-791.
30. Takatsuki, K., Kawahara, S., Kotani, S., Fukunaga, S., Mori, H., Mishina, M. & Kirino, Y. (2003) The hippocampus plays an important role in eyeblink conditioning with a short trace interval in glutamate receptor subunit 52 mutant mice. J. Neurosci., 23, 17-22.
31. Terry, A.V. Jr & Buccafusco, J.J. (2003) The cholinergic hypothesis of age and Alzheimer's disease-related cognitive deficits: recent challenges and their implications for novel drug development. J. Pharmacol. Exp. Ther., 306, 821-827.
32. Terwel, D., Dewachter, L. & Van Leuven, F. (2002) Axonal transport, tau protein, and neurodegeneration in Alzheimer's disease. Neuromol. Med., 2, 151-165.
33. Thompson, R.F. & Krupa, D.J. (1994) Organization of memory traces in the mammalian brain. Annu. Rev. Neurosci., 17, 519-549.
34. Trinchese, F., Liu, S., Battaglia, F., Walter, S., Mathews, P.M. & Arancio, O. (2004) Progressive age-related development of Alzheimer-like pathology in APP/PS1 mice. Ann. Neurol., 455, 801-814.
35. Trinh, N.H., Hoblyn, J., Mohanty, S. & Yaffe, K. (2003) Efficacy of cholinesterase inhibitors in the treatment of neuropsychiatric symptoms and functional impairment in Alzheimer disease: a meta-analysis. JAMA, 289, 210-216.
36. Van Dam, D., D'Hooge, R., Staufenbiel, M., Van Ginneken, C, Van Meir, F. & De Dyen, P.P. (2003) Age-dependent cognitive decline in the APP23 model precedes amyloid deposition. Eur. J. Neurosci., 17, 388-396.
37. Vogel, R.W., Ewers, M., Ross, C., Gould, T.J. & Woodruff-Pak, D.S. (2002) Age-related impairment in the 250-millisecond delay eyeblink classical conditioning procedure in C57BL/6 mice. Learn. Mem., 9, 321-336.
38. Weiss, C., Knuttinen, M.G., Powe, R.J.M., Patel, R.I., O'Connor, M.S. & Disterhoft, J.F. (1999) Trace eyeblink conditioning in the freely moving rat: optimizing the conditioning parameters. Behav. Neurosci., 113, 1100-1105.
39. Weiss, C., Venkatasubramanian, P.N., Aguado, A.S., Poer, J.M., Tom, B.C., Li, L., Chen, K.S., Disterhoft, J.F. & Wyrwicz, A.M. (2002) Impaired eyeblink conditioning and decreased hippocampal volume in PDAPP V717F mice. Neurobiol. Dis., 11, 425-433.
40. Wong, T.P., Debeir, T., Duff, K. & Cuello, A.C. (1999) Reorganization of cholinergic terminals in the cerebral cortex and hippocampus in transgenic mice carrying mutated presenilin-1 and amyloid precursor protein transgenes. J. Neurosci., 19, 2706-2716.
41. Woodruff-Pak, D.S., Finkbiner, R.G. & Sasse, DX. (1990) Eyeblink conditioning discriminates Alzheimer's patients from non-demented aged. Neuroreport, 1, 45-48.
42. Woodruff-Pak, D.S. & Santos, I.S. (2000) Nicotinic modulation in an animal model of a form of associative learning impaired in Alzheimer's disease. Behav. Brain. Res., 113, 11-19.
43. Zucker, R.S. (1989) Short-term synaptic plasticity. Annu. Rev. Neurosci., 12, 13-31.