The older rabbit as an animal model: Implications for Alzheimer's disease

Neurobiology of Aging

Volumn 17, Issue 2, 1996, Pages 283-290

  Woodruff Pak, Diana S ^a,b   Trojanowski, John Q ^c  

^a POLISHER RESEARCH INSTITUTE   (United States)

^b TEMPLE UNIVERSITY   (United States)

^c UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

Classical conditioning; Cognition enhancing; Diagnosis; Eyeblink; Learning; Memory; Nictitating membrane

Indexed keywords

TAU PROTEIN;

AGING; ALZHEIMER DISEASE; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; COGNITION; CONDITIONING; CONTROLLED STUDY; HIPPOCAMPUS; IMMUNOHISTOCHEMISTRY; MEMORY; NEUROPATHOLOGY; NONHUMAN; PRIORITY JOURNAL; RABBIT;

EID: 0029891416     PISSN: 01974580     EISSN: None     Source Type: Journal    
DOI: 10.1016/0197-4580(95)02064-0     Document Type: Article

References (87)

1. Arai, H.; Lee, V. M.-Y.; Messinger, M. L.; Greenberg, B. D.; Lowery, D. E.; Trojanowski, J. Q. Expression patterns of amyloid precursor protein (APP) in neural and nonneural human tissue from Alzheimer disease and control subjects. Ann. Neurol. 30:686-693; 1991.
2. Arai, H.; Lee, V. M.-Y.; Otvos, L., Jr.; Greenberg, B.; Lowery, D. E.; Sharma, S. K.; Schmidt, M. L.; Trojanowski, J. Q. Relative abundance of tau and neurofilament epitopes in hippocampal neurofibrillary tangles. Am. J. Pathol. 136:1069-1075; 1990.
3. Bahro, M.; Schreurs, B. G.; Sunderland, T.; and Molchan, S. E. The effects of scopolamine, lorazepam, and glycopyrrolate on classical conditioning of the human eyeblink response. Psychopharmacology (Berlin) (in press).
4. Berger, T. W. Long-term potentiation of hippocampal synaptic transmission affects rate of behavioral learning. Science 224:627-630; 1984.
5. Berger, T. W.; Rinaldi, P.; Weisz, D. J.; Thompson, R. F. Single unit analysis of different hippocampal cell types during classical conditioning of the rabbit NM response. J. Neurophysiol. 59:1197-1219; 1983.
6. Berger, T. W.; Thompson, R. F. Identification of pyramidal cells as the critical elements in hippocampal neuronal plasticity during learning. Proc. Natl. Acad. Sci. USA 75:1572-57; 1978.
7. Berry, S. D.; Thompson, R. F. Medial septal lesions retard classical conditioning of the nictitating membrane response in rabbits. Science 205:209-211; 1979.
8. Berthier, N. E.; Moore, J, W. Cerebellar Purkinje cell activity related to the classically conditioned nictitating membrane response. Exp. Brain Res. 63:341-350; 1986.
9. Berthier, N. E.; Moore, J. W. Activity of deep cerebellar nuclei during classical conditioning of nictitating membrane extension in rabbit nictitating response. Exp. Brain Res. 83:44-54; 1990.
10. Brizzee, K. R.; Ordy, J. M. Age pigments, cell loss and hippocampal function. Mech. Aging Dev. 9:143-162; 1979.
11. Brizzee, K. R.; Ordy, J. M.; Bartus, R. T. Localization of cellular changes within multimodal sensory regions in aged monkey brain: Possible implications for age-related cognitive loss. Neurobiol. Aging 1:45-52; 1980.
12. Coffin, J. M.; Trojanowski, J. Q.; Woodruff-Pak, D.S. Age-related cell loss and eyeblink classical conditioning in rabbits aged 3 to 85 months. (submitted).
13. Coffin, J. M.; Woodruff-Pak, D.S. Delay classical conditioning in young and older rabbits: Acquisition and retention at 12 and 18 months. Behav. Neurosci. 107:63-71; 1993.
14. Cordell, B. β-Amyloid formation as a potential therapeutic target for Alzheimer's disease. Annu. Rev. Pharmacol. Toxicol. 34:69-89; 1994.
15. Cork, L. C.; Powers, R. E.; Selkoe, D. J.; Davies, P.; Geyer, J. J.; Price, D. L. Neurofibrillary tangles and senile plaques in aged bears. J. Neuropathol. Exp. Neurol. 47:629-641; 1988.
16. Daum, I.; Channon, S.; Canavan, A. G. M. Classical conditioning in patients with severe memory problems. J. Neurol. Neurosurg. Psychiatry 52:47-51; 1989.
17. Daum, I.; Channon, S.; Polkey, C. E.; Gray, J. A. Classical conditioning after temporal lobe lesions in man: Impairment in conditional discrimination. Behav. Neurosci. 105:396-408; 1991.
18. Daum, I.; Schugens, M. M.; Ackermann, H.; Lutzenberger, W.; Dichgans, J.; Birbaumer, N. Classical conditioning after cerebellar lesions in humans. Behav. Neurosci. 107:748-756; 1993.
19. Ferrante, L. S.; Woodruff-Pak, D. S. Longitudinal investigation of eyeblink classical conditioning in elderly human subjects. J. Gerontol. Psychol. Sci. 50B:42-50; 1995.
20. Flood, D. G.; Coleman, P. D. Neuron numbers and sizes in aging brain: Comparisons of human, monkey, and rodent data. Neurobiol. Aging 9:453-463; 1988.
21. Games, D.; Adams, D.; Alessandrini, R.; Barbour, R.; Bethelette, P.; Blackwell, C.; Carr, T.; et al. Alzheimer-type neuropathology in transgenic mice overexpressing V717F β-amyloid precursor protein. Nature 373:523-527; 1995.
22. Giaccone, G.; Verga, L.; Finazzi, M.; Pollo, B.; Tagliavini, F.; Fragione, B.; Bugiani, O. Cerebral preamyloid deposits and congophilic angiopathy in aged dogs. Neurosci. Lett. 114:178-183:1990.
23. Goedert, M. Tau protein and the neurofibrillary pathology of Alzheimer's disease. Trends Neurosci. 6:460-465; 1993.
24. Gould, T. J.; Sears, L. L.; Steinmetz, J. E. Possible CS and US pathways for rabbit classical eyelid conditioning: Electrophysiological evidence for projections from the pontine nuclei and inferior olive to cerebellar cortex and nuclei. Behav. Neural Biol. 60:172-85; 1993.
25. Gould, T. J.; Steinmetz, J.E. Multiple-unit activity from rabbit cerebellar cortex and interpositus nucleus during classical discrimination/ reversal eyelid conditioning. Brain Res. 652:98-106; 1994.
26. Hall T. C.; Miller K. H.; Corsellis J. A. N. Variations in the human Purkinje cell population according to age and sex. Neuropathol. Appl. Neurobiol. 1:267-292; 1975.
27. Hyman, B. T.; Mann, D. M. A. Alzheimer-type pathologic changes in Down's syndrome individuals of various ages. In: Iqbal, K.; McLachlan, D. R. C; Winblad, B.; Wisniewski, H. M., eds. Alzheimer's disease basic mechanisms, diagnosis and therapeutic strategies. New York: Wiley; 1991:105-113.
28. Knox, C. A. Effects of aging and chronic arterial hypertension of the cell populations in the neocortex and archicortex of the rat. Acta Neuropathol. 56:139-145; 1982.
29. Larsell, O. Rabbit, In: Jansen, J., ed. The comparative anatomy and history of the cerebellum from monotremes through apes. Minneapolis: University of Minnesota Press; 1970:116-123.
30. Lavond, D. G.; Steinmetz, J. E. Acquisition of classical conditioning without cerebellar cortex. Behav. Brain Res. 33:113-164; 1989.
31. Lee, V. M.-Y.; Balin, B. J.; Otvos, L., Jr.; Trojanowski, J. Q. A68: A major subunit of paired helical filaments and derivatized forms of normal tau. Science 251:675-678; 1991.
32. Lee, V. M.-Y.; Otvos, L., Jr.; Schmidt, M. L.; Trojanowski, J. Q. Alzheimer's neurofibrillary tangles share immunological homologies with multiphosphorylation domains in the 2 layer neurofilament proteins. Proc. Natl. Acad. Sci. USA 85:7384-7388; 1988.
33. Lee, V. M.-Y.; Page, C. D.; Wu, H. L.; Schlaepfer, W. W. Monoclonal antibodies to gel excised glial filament protein and their reactivity with other intermediate filaments. J. Neurochem. 42:25-32; 1984.
34. Li, Y.-T.; Woodruff-Pak, D. S.; Trojanowski, J. Q. Amyloid plaques in cerebellar cortex and the integrity of Purkinje cell dendrites. Neurobiol. Aging 15:1-9; 1994.
35. Logan, C. G.; Grafton, S. T. Functional anatomy of human eyeblink conditioning determined with regional cerebral glucose metabolism and positron emission tomography. Proc. Natl. Acad. Sci. USA 92:7500-7504;1995.
36. Lye, R. H.; O'Boyle, D. J.; Ramsden, R. T.; Schady, W. Effects of a unilateral cerebellar lesion on the acquisition of eye-blink conditioning in man. J. Physiol. (Lond.) 403:58P; 1988.
37. Mani, R. B.; Lohr, J. B.; Jeste, D. V. Hippocampal pyramidal cells and aging in the human: A quantitative study of neuronal loss in sectors CA1 to CA4. Exp. Neurol. 94:29-40; 1986.
38. Mann, D. M. A.; Esiri, M. M. The pattern of acquisition of plaques and tangles in the brains of patients under 50 years of age with Down's syndrome. J. Neurol. Sci. 89:169-179; 1989.
39. Mann D. M. A.; Jones, D.; Prinja, D.; Purkiss, M. S. The prevalence of amyloid (A4) protein deposits in cerebral and cerebellar cortex in Down's syndrome and Alzheimer's disease. Acta Neuropathol. 80: 318-327; 1990.
40. Matsuo, E. S.; Shin, R.-W.; Billingsley, M. L.; Van de Voorde, J.; O'Connor, M.; Trojanowski, J. Q.; Lee, V. M.-Y. Biopsy-derived adult human brain tau is phosphorylated at many of the same sites as Alzheimer's disease paired helical filament tau. Neuron 13:989-1002; 1994.
41. McCormick, D. S.; R. F. Thompson. Neuronal responses of the rabbit cerebellum during acquisition and performance of a classically conditioned nictitating membrane/eyelid response. J. Neurosci. 4:2811-2822; 1984.
42. Miller, A. K. H.; Alston, R.; Mountjoy, C.; Corsellis, J. A. N., Automated differential cell counting on a sector of the normal human hippocampus: Influence of age. Neuropathol. Appl. Neurobiol. 10: 123-141; 1984.
43. Molchan, S. E.; Sunderland, T.; McIntosh, A. R.; Herscovitch, P.; Schreurs, B. G. A functional anatomical study of associative learning in humans. Proc. Natl. Acad. Sci. USA 91:8122-8126; 1994.
44. Mouritzen, D. A. The density of neurons in the human hippocampus. Neuropathol. Appl. Neurobiol. 5:249-264; 1979.
45. Moyer, J. R.; Disterhoft, J. D. Increased calcium action potentials in aging rabbit CA1 neurons are reduced by low concentrations of nimodipine. Hippocampus 4:11-18; 1994.
46. Moyer, J. R.; Thompson, L. F.; Black; Disterhoft, J. F., Nimodipine increases excitability of rabbit CA1 pyramidal neurons in an age- and concentration-dependent manner. J. Neurophysiol. 68:2100-2109; 1992.
47. Mullan, M.; Crawford, F. Genetic and molecular advances in Alzheimer's disease. Trends Neurosci. 16:398-403; 1993.
48. Nabeshima, T. Ameliorating effects of nefiracetam (DM-9384) on brain dysfunction. Drugs Today 30:357-379; 1994.
49. Nelson, P. T.; Saper, C. B. Alz-50 and PHF-1 immunoreactivity near β-AP injections in the cerebral cortex of sheep. Soc. Neurosci. Abstr. 20:1036; 1994.
50. Salvatierra, A. T.; Berry, S. D. Scopolamine disruption of septo-hippocampal activity and classical conditioning. Behav. Neurosci. 103:715-721; 1989.
51. Selkoe, D. J. Physiological production of the A protein and the mechanisms of Alzheimer's disease. Trends Neurosci. 16:403-409; 1993.
52. Selkoe, D. J.; Bell, D. S.; Podlisny, M. B.; Price, D. L.; Cork, L. C. Conservation of brain amyloid proteins in aged mammals and humans with Alzheimer's disease. Science 235:873-877; 1987.
53. Solomon, P. R.; Brett, M.; Groccia-Ellison, M.; Oyler, C.; Tomasi, M.; Pendlebury, W. W. Classical conditioning in patients with Alzheimer's disease: A multiday study. Psychol. Aging 10:248-254; 1995.
54. Solomon, P. R.; Groccia-Ellison, M.; Flynn, D.; Mirak, J.; Edwards, K. R.; Dunehew, A.; Stanton, M. E. Disruption of human eyeblink conditioning after central cholinergic blocade with scopolamine. Behav. Neurosci. 107:271-279; 1993.
55. Solomon, P. R.; Levine, E.; Bein, T.; Pendlebury, W. W. Disruption of classical conditioning in patients with Alzheimer's disease. Neurobiol. Aging 12:283-287; 1991.
56. Solomon, P. R.; Solomon, S. D.; Vander Schaaf, E.; Perry, H. E. Altered activity in the hippocampus is more detrimental to classical conditioning than removing the structure. Science 220:329-331; 1983.
57. Solomon, P. R.; Stowe, G. T.; Pendlebeury, W. W. Disrupted eyelid conditioning in a patient with damage to cerebellar afferents. Behav. Neurosci. 103:898-902; 1989.
58. Steinmetz, J. E.; Lavond, D. G.; Ivkovich, D.; Logan, C. G.; Thompson, R. F. Disruption of classical eyelid conditioning after cerebellar lesions: Damage to a memory trace system or a simple performance deficit? J. Neurosci. 12:4403-4426; 1992.
59. Stern, R. A.; Otvos, L., Jr.; Trojanowski, J. Q.; Lee, V. M.-Y. Monoclonal antibodies to a synthetic peptide homologous with the first 28 amino acids of Alzheimer's disease β-protein to recognize amyloid and diverse glial and neuronal cell types in the central nervous system. Am. J. Pathol. 134:973-978; 1989.
60. Thompson, L. T., Deyo, R. A., and Disterhoft, J. F., Nimodipine enhances spontaneous activity of hippocampal pyramidal neurons in aging rabbits at a dose that facilitates associative learning. Brain Res. 535:119-130; 1990.
61. Thompson, L. T.; Moyer, J. R., Jr.; Black, J.; and Disterhoft, J. F. Cellular mechanisms for nimodipine's reduction of aging-related learning deficits. In: Meyer, E. M., ed. Treatment of dementias. New York: Plenum Press; 1992:241-256.
62. Thompson, R. F. The neurobiology of learning. Science 233:941-947; 1986.
63. Topka, H.; Valls-Sole, J.; Massaquoi, S. G.; Hallett, M. Deficit in classical conditioning in patients with cerebellar degeneration. Brain 116:961-969; 1993.
64. Trojanowski, J. Q.; Lee, V. M.-Y. Paired helical filament tau in Alzheimer's disease: The kinase connection. Am. J. Pathol. 144:449-453; 1994.
65. Trojanowski, J. Q.; Schmidt, M. L.; Shin, R.-W.; Bramblett, G. T.; Goedert, M.; Lee, V. M.-Y. PHF tau (A68): From pathologic marker to potential mediator of neuronal dysfunction and degeneration in Alzheimer's disease. Clin. Neurosci. 1:184-191; 1993.
66. Trojanowski, J. Q.; Schuck, T.; Schmidt, M. L.; Lee, V. M.-Y. The distribution of tau in the normal human nervous system. Histochem. Cytochem. 37:209-215; 1989.
67. Watabe, S.; Yamaguchi, H.; Ashida, S. DM-9384, a new cognition-enhancing agent, increases the turnover of components of the GAB-Aergic system in the rat cerebral cortex. Eur. Pharmacol. 238:303-309; 1993.
68. Weiskrantz, L.; Warrington, E. K. Conditioning in amnesic patients. Neuropsychologia 17:187-194; 1979.
69. Wisniewski, T.; Ghiso, J.; Frangione, B. Alzheimer's disease and soluble Aβ. Neurobiol. Aging 15:143-152; 1994.
70. Woodruff-Pak, D. S. Eyeblink classical conditioning in H.M.: Delay and trace paradigms. Behav. Neurosci. 107:911-925; 1993.
71. Woodruff-Pak, D. S.; Cronholm, J. F.; Sheffield, J. B. Purkinje cell number related to rate of eyeblink classical conditioning. Neuroreport 1:165-168; 1990.
72. Woodruff-Pak, D. S.; Finkbiner, R. G.; Katz, I. R. A model system demonstrating parallels in animal and human aging: Extension to Alzheimer's disease. In: Meyer, E. M.; Simpkins, J. W.; Yamamoto, J., eds. Novel approaches to the treatment of Alzheimer's disease. New York: Plenum; 1989:355-371.
73. Woodruff-Pak, D. S.; Finkbiner, R. G.; Sasse, D. K. Eyeblink conditioning discriminates Alzheimer's patients from nondemented aged. Neuroreport 1:45-48; 1990.
74. Woodruff-Pak, D. S.; Lavond, D. G., Logan, C. G.; Steinmetz, J. E.; Thompson, R. F. Cerebellar cortical lesions and reacquisition in classical conditioning of the nictitating membrane response in rabbits. Brain Res. 608:67-77; 1993.
75. Woodruff-Pak, D. S.; Lavond, D. G.; Logan, C. G.; Thompson, R. F. Classical conditioning in 3-, 30-, and 45 month-old rabbits: Behavioral learning and hippocampal unit activity. Neurobiol. Aging 8:101-108; 1987.
76. Woodruff-Pak, D. S.; Li. Y.-T. Hippocampus: Possible site of amelioration of eyeblink classical conditioning by Nefiracetam. Soc. Neurosci. Abstr. 20:1764; 1994a.
77. Woodruff-Pak, D. S.; Li, Y.-T. Nefiracetam (DM-9384): Effect on eyeblink classical conditioning in older rabbits. Psychopharmacology (Berlin) 114:200-208; 1994.
78. Woodruff-Pak, D. S.; Li. Y.-T.; Kazmi, A.; Kern, W. R. Nicotinic cholinergic system involvement in eyeblink classical conditioning in rabbits. Behav. Neurosci. 108:486-493; 1994.
79. Woodruff-Pak, D. S.; Papka, M. Probable Alzheimer's disease patients are impaired less in the trace than in the delay eyeblink classical conditioning paradigm. Neurobiol. Aging (in press).
80. Woodruff-Pak, D. S.; Papka, M.; Ivry, R. Cerebellar involvement in eyeblink classical conditioning in humans. Neuropsych. (in press).
81. Woodruff-Pak, D. S.; Papka, M.; Romano, S.; Li, Y.-T. Eyeblink classical conditioning in Alzheimer's disease and cerebrovascular dementia. Neurobiol. Aging (in press).
82. Woodruff-Pak, D. S.; Papka, M.; Simon, E. W. Down's Syndrome adults aged 35 and older show eyeblink classical conditioning profiles comparable to Alzheimer's disease patients. Neuropsychology 8:1-11; 1994.
83. Woodruff-Pak, D. S.; Romano, S.; Papka, M. Training to criterion in eyeblink classical conditioning in Alzheimer's disease, Down's Syndrome with Alzheimer's disease, and normal age-matched elderly. Behav. Neurosci. (in press).
84. Woodruff-Pak, D. S.; Thompson, R. F. Cerebellar correlates of classical conditioning across the life span. In: Baltes, P. B.; Featherman, D. M.; Lerner, R. M., eds. Life-span development and behavior, vol. 9. Hillsdale, NJ: Erlbaum; 1988:1-37.
85. Yankner, B. A.; Dawes, L. R.; Fisher, S.; Villa-Komaroff, L.; Oster-Granite, M. L.; Neve, R. L. Neurotoxicity of a fragment of the amyloid precursor associated with Alzheimer's disease. Science 245:417-420; 1989.
86. Yankner, B. A.; Duffy, L. K.; Kirschner, D. A. Neurotropic and neurotoxic effects of amyloid protein: Reversal by tachykinin neuropeptides. Science 250:279-281; 1990.
87. Yoshi, M.; Watabe, S. Enhancement of neuronal calcium channel currents by the nootropic agent, nefiracetam (DM-9384), in NG108-15 cells. Brain Res. 642:123-131; 1994.