Hippocampal synaptic activity, pattern separation and episodic-like memory: Implications for mouse models of Alzheimer's disease pathology

Biochemical Society Transactions

Volumn 39, Issue 4, 2011, Pages 902-909

  Palmer, Alice ^a   Good, Mark ^a  

^a CARDIFF UNIVERSITY   (United Kingdom)

Author keywords

Alzheimer's disease (AD); Amyloid peptide (A ); Dentate gyrus (DG); Episodic like memory; Hippocampal synaptic activity; Pattern separation

Indexed keywords

AMYLOID BETA PROTEIN; AMYLOID PRECURSOR PROTEIN;

ALZHEIMER DISEASE; CONFERENCE PAPER; DENTATE GYRUS; ELECTRONEUROLOGY; ENTORHINAL CORTEX; EPISODIC LIKE MEMORY; EPISODIC MEMORY; FRONTAL CORTEX; HIPPOCAMPAL CA3 REGION; HUMAN; INFORMATION PROCESSING; NEUROPATHOLOGY; NONHUMAN; ORBITAL CORTEX; PARAHIPPOCAMPAL GYRUS; PREDICTION; PRIORITY JOURNAL; SUBICULUM; SYNAPTIC POTENTIAL; TRANSGENIC MOUSE;

ALZHEIMER DISEASE; AMYLOID BETA-PEPTIDES; ANIMALS; DISEASE MODELS, ANIMAL; HIPPOCAMPUS; HUMANS; MENTAL RECALL; MICE; MICE, TRANSGENIC; SYNAPTIC TRANSMISSION;

ANIMALIA; MUS;

EID: 79960874601     PISSN: 03005127     EISSN: 14708752     Source Type: Journal    
DOI: 10.1042/BST0390902     Document Type: Conference Paper

References (56)

1. Braak, H. and Braak, E. (1991) Neuropathological stageing of Alzheimer-related pathology. Acta Neuropathol. 82, 239-259
2. Terry, R.D., Masliah, E., Salmon, D.P., Butters, N., DeTeresa, R., Hill, R., Hansen, L.A. and Katzman, R. (1991) Physical basis of cognitive alterations in Alzheimer's disease: synapse loss is the major correlate of cognitive impairment. Ann. Neurol. 30, 572-580
3. DeKosky, S.T. and Scheff, S.W. (1990) Synapse loss in frontal cortex biopsies in Alzheimer's disease: correlation with cognitive severity. Ann. Neurol. 27, 457-464
4. Kerchner, G.A., Hess, C.P., Hammond-Rosenbluth, K.E., Xu, D., Rabinovici, G.D., Kelley, D.A., Vigneron, D.B., Nelson, S.J. and Miller, B.L. (2010) Hippocampal CA1 apical neuropil atrophy in mild Alzheimer disease visualized with 7-T MRI. Neurology 75, 1381-1387
5. Mueller, S.G., Schuff, N., Yaffe, K., Madison, C., Miller, B. and Weiner, M.W. (2010) Hippocampal atrophy patterns in mild cognitive impairment and Alzheimer's disease. Hum. Brain Mapp. 31, 1339-1347
6. Nimmrich, V. and Ebert, U. (2009) Is Alzheimer's disease a result of presynaptic failure? Synaptic dysfunctions induced by oligomeric β-amyloid. Rev. Neurosci. 20, 1-12
7. Gong, Y. and Lippa, C.F. (2010) Disruption of the postsynaptic density in Alzheimer's disease and other neurodegenerative dementias. Am. J. Alzheimer's Dis. Other Dement. 25, 547-555
8. Hyman, B.T., Van Hoesen, G.W., Kromer, L.J. and Damasio, A.R. (1986) Perforant pathway changes and the memory impairment of Alzheimer's disease. Ann. Neurol. 20, 472-481
9. Witter, M.P. (2007) The perforant path: projections from the entorhinal cortex to the dentate gyrus. Prog. Brain Res. 163, 43-61
10. Amaral, D.G. and Witter, M.P. (1989) The three-dimensional organization of the hippocampal formation: a review of anatomical data. Neuroscience 31, 571-591 (Pubitemid 20032948)
11. Lavenex, P. and Amaral, D.G. (2000) Hippocampal-neocortical interaction: a hierarchy of associativity. Hippocampus 10, 420-430
12. Marr, D. (1971) Simple memory: a theory for archicortex. Philos. Trans. R. Soc. London Ser. B 262, 23-81
13. McNaughton, B.L. and Morris, R.G.M (1987) Hippocampal synaptic enhancement and information storage within a distributed memory system. Trends Neurosci. 10, 408-415 (Pubitemid 17149102)
14. Ceresti, E. and Treves, A. (2010) How informative are aspatial CA3 representations established by the dentate gyrus. PLoS Comput. Biol. 4, 1-16
15. Rolls, E.T. (2010) A computational theory of episodic memory formation in the hippocampus. Behav. Brain Res. 215, 180-196
16. Jung, M.W., Weiner, S.I. and McNaughton, B.L. (1994) Comparison of spatial firing characteristics of units in dorsal and ventral hippocampus of the rat. J. Neurosci. 14, 7347-7356 (Pubitemid 24379745)
17. Terry, R.D. (1996) The pathogenesis of Alzheimer disease: an alternative to the amyloid hypothesis. J. Neuropathol. Exp. Neurol. 55, 1023-1025
18. Lue, L.F., Kuo, Y.M., Roher, A.E., Brachova, L., Shen, Y., Sue, L., Beach, T., Kurth, J.H., Rydel, R.E. and Rogers, J. (1999) Soluble amyloid β peptide concentration as a predictor of synaptic change in Alzheimer's disease. Am. J. Pathol. 155, 853-862
19. Cleary, J.P., Walsh, D.M., Hofmeister, J.J., Shankar, G.M., Kuskowski, M.A., Selkoe, D.J. and Ashe, K.H. (2005) Natural oligomers of the amyloid-β protein specifically disrupt cognitive function. Nat. Neurosci. 8, 79-84
20. Haass, C. and Selkoe, D.J. (2007) Soluble protein oligomers in neurodegeneration: lessons from the Alzheimer's amyloid β-peptide. Nat. Rev. Mol. Cell Biol. 8, 101-112 (Pubitemid 46432529)
21. Aoki, C., Mahadomrongkul, V., Fujisawa, S., Habersat, R. and Shirao, T. (2007) Chemical and morphological alterations of spines within the hippocampus and entorhinal cortex precede the onset of Alzheimer's disease pathology in double knock-in mice. J. Comp. Neurol. 505, 352-362
22. Shankar, G.M. and Walsh, D.M. (2009) Alzheimer's disease: synaptic dysfunction and Aβ. Mol. Neurodegener. 4, 48
23. Ondrejcak, T., Klyubin, I., Hu, N.W., Barry, A.E., Cullen, W.K. and Rowan, M.J. (2010) Alzheimer's disease amyloid β-protein and synaptic function. Neuromol. Med. 12, 13-26
24. 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. (2006) Early-onset behavioral and synaptic deficits in a mouse model of Alzheimer's disease. Proc. Natl. Acad. Sci. U.S.A. 103, 5161-5166
25. Dong, H., Yuede, C.M., Coughlan, C.A., Murphy, K.M. and Csernansky, J.G. (2009) Effects of donepezil on amyloid-β and synapse density in the Tg2576 mouse model of Alzheimer's disease. Brain Res. 1303, 169-178
26. 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.P., Hyman, B.T. et al. (1999) Impaired synaptic plasticity and learning in aged amyloid precursor protein transgenic mice. Nat. Neurosci. 2, 271-276
27. Palop, J.J. and Mucke, L. (2010) Amyloid-β-induced neuronal dysfunction in Alzheimer's disease: from synapses toward neural networks. Nat. Neurosci. 13, 812-818
28. Harris, J.A., Devidze, N., Verret, L., Ho, K., Halabisky, B., Thwin, M.T., Kim, D., Hamto, P., Lo, I., Yu, G.Q. et al. (2010) Transsynaptic progression of amyloid-β-induced neuronal dysfunction within the entorhinal-hippocampal network. Neuron 68, 428-441
29. Leutgeb, J.K., Leutgeb, S., Moser, M.B. and Moser, E.I. (2007) Pattern separation in the dentate gyrus and CA3 of the hippocampus. Science 315, 961-966 (Pubitemid 46281178)
30. McHugh, T.J., Jones, M.W., Quinn, J.J., Balthasar, N., Coppari, R., Elmquist, J.K., Lowell, B.B., Fanselow, M.S., Wilson, M.A. and Tonegawa, S. (2007) Dentate gyrus NMDA receptors mediate rapid pattern separation in the hippocampal network. Science 317, 94-99 (Pubitemid 47056461)
31. Wilson, I.A., Ikonen, S., Gallagher, M., Eichenbaum, H. and Tanila, H. (2005) Age-associated alterations of hippocampal place cells are subregion specific. J. Neurosci. 25, 6877-6886 (Pubitemid 41023155)
32. Poirier, G.L., Amin, E., Good, M.A. and Aggleton, J.P. (2011) Early-onset dysfunction of retrosplenial cortex precedes overt amyloid plaque formation in Tg2576 mice. Neuroscience 174, 71-83
33. Yassa, M.A., Lacy, J.W., Stark, S.M., Albert, M.S., Gallagher, M. and Stark, C.E. (2010) Pattern separation deficits associated with increased hippocampal CA3 and dentate gyrus activity in nondemented older adults. Hippocampus, doi:10.1002/hipo.20808
34. Yassa, M.A., Stark, S.M., Bakker, A., Albert, M.S., Gallagher, M. and Stark, C.E. (2010) High-resolution structural and functional MRI of hippocampal CA3 and dentate gyrus in patients with amnestic mild cognitive impairment. Neuroimage 51, 1242-1252
35. Tulving, E. (1972) Episodic and semantic memory. In Organization of Memory (Tulving, E. and Donaldson, W., eds), pp. 381-403, Academic Press, New York
36. Clayton, N.S. and Dickinson, A. (1998) Episodic-like memory during cache recovery by scrub jays. Nature 395, 272-274 (Pubitemid 28447550)
37. Clayton, N.S., Griffiths, D.P., Emery, N.J. and Dickinson, A. (2001) Elements of episodic-like memory in animals. Philos. Trans. R. Soc. London Ser. B 356, 1483-1491
38. Crystal, J.D. (2010) Episodic-like memory in animals. Behav. Brain Res. 215, 235-243
39. Babb, S.J. and Crystal, J.D. (2006) Episodic-like memory in the rat. Curr. Biol. 16, 1317-1321
40. Crystal, J.D. (2009) Elements of episodic-like memory in animal models. Behav. Proc. 80, 269-277
41. Winters, B.D., Saksida, L.M. and Bussey, T.J. (2008) Object recognition memory: neurobiological mechanisms of encoding, consolidation and retrieval. Neurosci. Biobehav. Rev. 32, 1055-1070
42. Warburton, E.C. and Brown, M.W. (2010) Findings from animals concerning when interactions between perirhinal cortex, hippocampus and medial prefrontal cortex are necessary for recognition memory. Neuropsychologia 48, 2262-2272
43. Dere, E., Huston, J.P. and De Souza Silva, M.A. (2005) Integrated memory for objects, places, and temporal order: evidence for episodic-like memory in mice. Neurobiol. Learn. Mem. 84, 214-221
44. Kart-Teke, E., De Souza Silva, M.A., Huston, J.P. and Dere, E. (2006) Wistar rats show episodic-like memory for unique experiences. Neurobiol. Learn. Mem. 85, 173-182
45. Good, M.A., Barnes, P., Staal, V., McGregor, A. and Honey, R.C. (2007) Context- but not familiarity-dependent forms of object recognition are impaired following excitotoxic hippocampal lesions in rats. Behav. Neurosci. 121, 218-223
46. Good, M.A., Hale, G. and Staal, V. (2007) Impaired 'episodic-like' object memory in adult APPswe transgenic mice. Behav. Neurosci. 121, 443-448
47. Good, M.A. and Hale, G. (2007) The 'Swedish' mutation of the amyloid precursor protein (APPswe) dissociates components of object-location memory in aged Tg2576 mice. Behav. Neurosci. 121, 1180-1191
48. Rescorla, R.A. and Wagner, A.R. (1972) A theory of Pavlovian conditioning; variations in the effectiveness of reinforcement and nonreinforcement. In Classical Conditioning II: Current Research and Theory (Black, A.H. and Prokasy, W.F., eds), pp. 64-99, Appleton Century Crofts, New York
49. Rescorla, R.A. (1972) 'Configural' conditioning in discrete-trial bar pressing. J. Comp. Psychol. 79, 307-317
50. Pearce, J.M. (1994) Similarity and discrimination: a selective review and a connectionist modelPsycholRev. 101, 587-607
51. Rudy, J.W. and Sutherland, R.J. (1989) The hippocampal formation is necessary for rats to learn and remember configural discriminations. Behav. Brain Res. 34, 97-109
52. Rudy, J.W. and Sutherland, R.J. (1995) Configural association theory and the hippocampal formation: an appraisal and reconfiguration. Hippocampus 5, 375-389 (Pubitemid 26088277)
53. Coutureau, E., Killcross, S.A., Good, M., Marshall, V.J., Ward-Robinson, J. and Honey, R.C. (2002) Acquired equivalence and distinctiveness of cues: II. Neural manipulations and their implications. J. Exp. Psychol. Anim. Behav. Proc. 28, 388-396
54. Iordanova, M.D., Good, M.A. and Honey, R.C. (2008) Configural learning without reinforcement: integrated memories for correlates of what, where and when. Q. J. Exp. Psychol. 61, 1785-1792
55. Iordanova, M.D., Burnett, D.J., Aggleton, J.P., Good, M. and Honey, R.C. (2009) The role of the hippocampus in mnemonic integration and retrieval: complementary evidence from lesion and inactivation studies. Eur. J. Neurosci. 30, 2177-2189
56. Mueller, S.G., Chao, L.L., Berman, B. and Weiner, M.W. (2011) Evidence for functional specialization of hippocampal subfields detected by MR subfield volumetry on high resolution images at 4T. Neuroimage 56, 851-857