Present imperfect: A critical review of animal models of the mnemonic impairments in Alzheimer's disease

Neuroscience and Biobehavioral Reviews

Volumn 22, Issue 1, 1997, Pages 99-120

  McDonald, Michael P ^a   Overmier, J Bruce ^a  

^a UNIVERSITY OF MINNESOTA   (United States)

Author keywords

Alzheimer's disease; Animal models; Fimbria fornix; Hippocampus; Medial septum; Memory; Nucleus basalis magnocellularis; Scopolamine

Indexed keywords

AMYLOID BETA PROTEIN; ATROPINE; MUSCARINIC RECEPTOR BLOCKING AGENT; NEUROPEPTIDE; NEUROTOXIN; PUROMYCIN; SCOPOLAMINE;

ALZHEIMER DISEASE; AMNESIA; ANIMAL EXPERIMENT; ANIMAL MODEL; AVOIDANCE BEHAVIOR; BEHAVIOR DISORDER; BRAIN FORNIX; BRAIN INJURY; HIPPOCAMPUS; INSTRUMENTAL CONDITIONING; LEARNING; NONHUMAN; OLIVARY NUCLEUS; PERCEPTIVE DISCRIMINATION; PRIORITY JOURNAL; REVIEW; SEPTUM NUCLEUS; TASK PERFORMANCE; TRANSGENIC MOUSE;

EID: 0344701087     PISSN: 01497634     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0149-7634(97)00024-9     Document Type: Article

References (315)

1. Abas M. A., Sahakian B. J., Levy R. Neuropsychological deficits and CT scan changes in elderly depressives. Psychological Medicine. 20:1990;507-520.
2. Abe E., Murai S., Masuda Y., Saito H., Itoh T. Alpha-sialyl cholesterol reverses AF64A-induced deficit in passive avoidance response and depletion of hippocampal acetylcholine in mice. British Journal of Pharmacology. 108:1993;387-392.
3. Abe E., Murai S., Saito H., Masuda Y., Takasu Y., Shoitani T., Tachizawa H., Itoh T. Effects of nefiracetam on deficits in active avoidance response and hippocampal cholinergic and monoaminergic dysfunctions induced by AF64A in mice. Journal of Neural Transmission, General Section. 95:1994;179-193.
4. Adelstein T. B., Kesner R. P., Strassberg D. S. Spatial recognition and spatial order memory in patients with dementia of the Alzheimer's type. Neuropsychologia. 30:1992;59-67.
5. Aggleton J. P., Hunt P. R., Rawlins J. N. P. The effects of hippocampal lesions upon spatial and non-spatial tests of working memory. Behavioural Brain Research. 19:1986;133-136.
6. Aggleton J. P., Keith A. B., Rawlins J. N. P., Hunt P. R., Sahgal A. Removal of the hippocampus and transection of the fornix produce comparable deficits on delayed non-matching to position by rats. Behavioural Brain Research. 52:1992;61-71.
7. Aggleton J. P., Keith A. B., Sahgal A. Both fornix and anterior thalamic, but not mammillary, lesions disrupt delayed non-matching-to-position memory in rats. Behavioural Brain Research. 44:1991;151-161.
8. Aggleton J. P., Neave N., Nagle S., Sahgal A. A comparison of the effects of medial prefrontal, cingulate cortex, and cingulum bundle lesions on tests of spatial memory: Evidence of a double dissociation between frontal and cingulum bundle contributions. Journal of Neuroscience. 15:1995;7270-7281.
9. Aigner T. G., Mitchell S. J., Aggleton J. P., DeLong M. R., Struble R. G., Price D. L., Wenk G. L., Mishkin M. Effects of scopolamine and physostigmine on recognition memory in monkeys with ibotenic-acid lesions of the nucleus basalis of Meynert. Psychopharmacology (Berlin). 92:1987;292-300.
10. Aigner T. G., Mitchell S. J., Aggleton J. P., DeLong M. R., Struble R. G., Price D. L., Wenk G. L., Pettigrew K. D., Mishkin M. Transient impairment of recognition memory following ibotenic-acid lesions of the basal forebrain in macaques. Experimental Brain Research. 86:1991;18-26.
11. Albert M. S. Special behavioral paradigms in animals to study age-related changes in memory. Neurobiology of Aging. 9:1988;507-509.
12. Alvarez P., Zola-Morgan S., Squire L. R. The animal model of human amnesia: Long-term memory impaired and short-term memory intact. Proceedings of the National Academy of Sciences of the United States of America. 91:1994;5637-5641.
13. Amaral D. G., Kurz J. An analysis of the origins of the cholinergic and noncholinergic septal projections to the hippocampal formation of the rat. Journal of Comparative Neurology. 240:1985;37-59.
14. Auchus A. P., Green R. C., Nemeroff C. B. Cortical and subcortical neuropeptides in Alzheimer's disease. Neurobiology of Aging. 15:1994;589-595.
15. Bachevalier J., Parkinson J. K., Mishkin M. Visual recognition in monkeys: Effects of separate vs. combined transection of fornix and amygdalofugal pathways. Experimental Brain Research. 57:1985;554-561.
16. Bachevalier J., Saunders R. C., Mishkin M. Visual recognition in monkeys: Effects of transection of fornix. Experimental Brain Research. 57:1985;547-553.
17. Bahro M., Schreurs B. G., Sunderland T., Molchan S. E. The effects of scopolamine, lorazepam, and glycopyrrolate on classical conditioning of the human eyeblink response. Psychopharmacology (Berlin). 122:1995;395-400.
18. Bailey E. L., Overstreet D. H., Crocker A. D. Effects of intrahippocampal injections of the cholinergic neurotoxin AF64A on open-field activity and avoidance learning in the rat. Behavioral and Neural Biology. 45:1986;263-274.
19. Ball M. J. Topographic distribution of neurofibrillary tangles and granulovacuolar degeneration in hippocampal cortex of aging and demented patients. A quantitative study. Acta Neuropathologica. 42:1978;73-80.
20. Bartus R. T. The need for common perspectives in the development and use of animal models for age-related cognitive and neurodegenerative disorders. Neurobiology of Aging. 9:1988;445-451.
21. Bartus R. T., Dean R. L., Beer B., Lippa A. S. The cholinergic hypothesis of geriatric memory dysfunction. Science. 217:1982;408-414.
22. Bartus R. T., Flicker C., Dean R. L., Pontecorvo M., Figueiredo J. C., Fisher S. K. Selective memory loss following nucleus basalis lesions: Long term behavioral recovery despite persistent cholinergic deficiencies. Pharmacology, Biochemistry and Behavior. 23:1985;125-135.
23. Bartus R. T., Johnson H. R. Short-term memory in the rhesus monkey: Disruption from the anticholinergic scopolamine. Pharmacology, Biochemistry and Behavior. 23:1976;1-6.
24. Beal M. F., Growdon J. H. CSF neurotransmitter markers in Alzheimer's disease. Progress in Neuropsychopharmacology and Biological Psychiatry. 10:1986;259-270.
25. Beatty W. W., Winn P., Adams R. L., Allen E. W., Wilson D. A., Prince J. R., Olson K. A., Dean K., Littleford D. Preserved cognitive skills in dementia of the Alzheimer type. Archives of Neurology. 51:1994;1040-1046.
26. Bemelmans K. J., Goekoop J. G. The contribution of list length to the absence of the primacy effect in word recall in dementia of the Alzheimer type. Psychological Medicine. 21:1991;1047-1050.
27. Beninger R. J., Jhamandas K., Boegman R. J., El-Defrawy S. R. Effects of scopolamine and unilateral lesions of the basal forebrain on T-maze discrimination and alternation in rats. Pharmacology, Biochemistry and Behavior. 24:1986;1353-1360.
28. Berger-Sweeney J., Heckers S., Mesulam M.-M., Wiley R. G., Lappi D. A., Sharma M. Differential effects on spatial navigation of immunotoxin-induced cholinergic lesions of the medial septal area and nucleus basalis magnocellularis. Journal of Neuroscience. 14:1994;4506-4519.
29. Berry S. D., Thompson R. F. Medial septal lesions retard classical conditioning of the nictitating membrane response in rabbits. Science. 205:1979;209-211.
30. Bouffard J. P., Jarrard L. E. Acquisition of a complex place task in rats with selective ibotenate lesions of hippocampal formation: Combined lesions of subiculum and entorhinal cortex versus hippocampus. Behavioral Neuroscience. 102:1988;828-834.
31. Braak H., Braak E. Neuropathological staging of Alzheimer-related changes. Acta Neuropathologica. 82:1991;239-259.
32. Brandeis, R., Pittel, Z., Lachman, C., Heldman, E., Luz, S., Dachir, S., Levy, A., Hanin, I. and Fisher, A., AF64A-induced cholinotoxicity: Behavioral and biochemical correlates. In Alzheimer's and Parkinson's Disease: Strategies for Research and Development, ed. A. Fisher, I. Hanin and C. Lachman. Plenum Press, New York, 1986, pp. 469-478.
33. Bratt A. M., Cassel J. C., Neufang B., Greene P. L., Jackisch R., Herting G., Will B. E. Behavioural and neurochemical effects of superior cervical ganglionectomy in rats with septo-hippocampal lesions. Experimental Brain Research. 102:1995;429-444.
34. Brown J. Some tests of the decay theory of immediate memory. Quarterly Journal of Experimental Psychology. 10:1958;12-21.
35. Buresova O., Bolthius J., Bures J. Differential effects of cholinergic blockade on performance of rats in the water tank navigation task and in a radial maze. Behavioral Neuroscience. 100:1986;476-482.
36. Buschke H., Fuld P. A. Evaluating, storage, retention, and retrieval in disordered memory and learning. Neurology. 24:1974;1019-1025.
37. Buxton A., Callan O. A., Blatt E. J., Wong E. H. F., Fontana D. J. Cholinergic agents and delay-dependent performance in the rat. Pharmacology, Biochemistry and Behavior. 49:1994;1067-1073.
38. Bymaster F. P., Heath I., Hendrix J. C., Shannon H. E. Comparative behavioral and neurochemical activities of cholinergic antagonists in rats. Journal of Pharmacology and Experimental Therapeutics. 267:1993;16-24.
39. Cassel J. C., Kelche C., Peterson G. M., Ballough G. P., Goepp I., Will B. Graft-induced behavioral recovery from subcallosal septohippocampal damage in rats depends on maturity stage of donor tissue. Neuroscience. 45:1991;571-586.
40. Christiansen B. A., Schmajuk N. A. Hippocampectomy disrupts the topography of the rat eyeblink response during acquisition and extinction of classical conditioning. Brain Research. 595:1992;206-214.
41. Chrobak J. J., Hanin I., Schmechel D. E., Walsh T. J. AF64A-induced working memory impairment: Behavioral, neurochemical and histological correlates. Brain Research. 463:1988;107-117.
42. Choi D. W. Excitotoxic cell death. Journal of Neurobiology. 23:1992;1261-1276.
43. Cleary J., Hittner J. M., Semotuk M., Mantyh P., O'Hare E. β-amyloid (1-40) effects on behavior and memory. Brain Research. 682:1995;69-74.
44. Cleary J. P., O'Hare E., Weldon D. T., Esler W. P., Ghilardi J. R., Rogers S., Maggio J. E., Mantyh P. W. Distribution, stability and ultimate fate of aggregated β-amyloid injected into the rat brain. Abstracts of the Society for Neuroscience. 21:1995;475.
45. Coffin J. M., Ferrante L. S., Woodruff-Pak D. S. Delay classical conditioning has a higher sensitivity for Alzheimer's disease than trace. Abstracts of the Society for Neuroscience. 18:1992;736.
46. Connor D. J., Langlais P. J., Thal L. J. Behavioral impairments after lesions of the nucleus basalis by ibotenic acid and quisqualic acid. Brain Research. 555:1991;84-90.
47. Corkin, S., Some relationships between global amnesias and the memory impairments in Alzheimer's disease. In Alzheimer's Disease: A Report of Research in Progress, ed. S. Corkin, K. L. Davis, J. H. Growdon, E. Usdin and R. J. Wurtman. Raven Press, New York, 1982, pp. 149-164.
48. Coyle J. T. Neurotoxic action of kainic acid. Journal of Neurochemistry. 41:1983;1-11.
49. Coyle J. T., Bird S. J., Evans R. H., Gulley R. L., Nadler J. V., Nicklas W. J., Olney J. W. Excitatory amino acid neurotoxins: Selectivity and mechanisms of action. Neuroscience Research Progress Bulletin. 19:1981;331-427.
50. Crawley J. N. Functional interactions of galanin and acetylcholine: Relevance to memory and Alzheimer's disease. Behavioural Brain Research. 57:1993;133-141.
51. Dalrymple-Alford J. C., Kelche C., Cassel J. C., Toniolo G., Pallage V., Will B. E. Behavioral deficits after intrahippocampal fetal septal grafts in rats with selective fimbria-fornix lesions. Experimental Brain Research. 69:1988;545-558.
52. Decker M. W., Curzon P., Brioni J. D. Influence of separate and combined septal and amygdala lesions on memory, acoustic startle, anxiety, and locomotor activity in rats. Neurobiology of Learning and Memory. 64:1995;156-168.
53. Decker M. W., McGaugh J. L. The role of interactions between the cholinergic system and other neuromodulatory systems in learning and memory. Synapse. 7:1991;151-168.
54. de Leon M. J., Golomb J., George A. E., Convit A., Tarshish C. Y., McRai T., DeSanti S., Smith G., Ferris S. H., Noz M., Rusinek H. The radiologic prediction of Alzheimer's disease: The atrophic hippocampal formation. American Journal of Neuroradiology. 14:1993;897-906.
55. Diamond A. S., Zola-Morgan S., Squire L. Successful performance by monkeys with lesions of the hippocampal formation on AB and object retrieval, two tasks that mark developmental changes in human infants. Behavioral Neuroscience. 103:1989;526-537.
56. Diesfeldt H. F. A. The distinction between long-term and short-term memory in senile dementia: An analysis of free recall and delayed recognition. Neuropsychologia. 16:1978;115-119.
57. Dubois B., Mayo W., Agid Y., LeMoal M., Simon H. Profound disturbances of spontaneous and learned behaviors following lesions of the nucleus basalis magnocellularis in the rat. Brain Research. 338:1985;249-258.
58. Dunnett S. B. Comparative effects of cholinergic drugs and lesions of nucleus basalis or fimbria-fornix on delayed matching in rats. Psychopharmacology (Berlin). 87:1985;357-363.
59. Dunnett S. B., Everitt B. J., Robbins T. W. The basal forebrain-cortical cholinergic system: Interpreting the functional consequences of excitotoxic lesions. Trends in Neuroscience. 14:1991;494-501.
60. Dunnett S. B., Low W. C., Iversen S. D., Stenevi U., Bjorklund A. Septal transplants restore maze learning in rats with fimbria-fornix lesions. Brain Research. 251:1982;335-348.
61. Dunnett S. B., Rogers D. C., Jones G. H. Effects of nucleus basalis magnocellularis lesions in rats on delayed matching and non-matching to position tasks. European Journal of Neuroscience. 1:1989;395-405.
62. Dunnett S. B., Toniolo G., Fine A., Ryan C. N., Björklund A., Iversen S. D. Transplantation of embryonic ventral forebrain neurons to the neocortex of rats with lesions of nucleus basalis magnocellularis. II. Sensorimotor and learning impairments. Neuroscience. 16:1985;787-797.
63. Dunnett S. B., Whishaw I. Q., Jones G. H., Bunch S. T. Behavioural, biochemical and histochemical effects of different neurotoxic amino acids injected into the nucleus basalis magnocellularis of rats. Neuroscience. 20:1987;653-669.
64. Dutar P., Bassant M. H., Senut M. C., Lamour Y. The septohippocampal pathway: Structure and function of a central cholinergic system. Physiological Reviews. 75:1995;393-427.
65. Ellison D. W., Beal M. F., Mazurek M. F., Bird E. D., Martin J. B. A postmortem study of amino acid neurotransmitters in Alzheimer's disease. Annals of Neurology. 20:1986;616-621.
66. Etherington R., Mittelman G., Robbins T. W. Comparative effects of nucleus basalis and fimbria fornix lesions on delayed matching and alternation tests of memory. Neuroscience Research Communication. 1:1987;135-143.
67. Eva C., Fabrazzo M., Costa E. Changes of cholinergic, noradrenergic and serotonergic synaptic transmission indices by ethylcholine aziridinium ion (AF64A) infused intraventricularly. Journal of Pharmacology and Experimental Therapeutics. 222:1987;181-186.
68. Ferris, S. H., Flicker, C., Kluger, A., de Leon, M. J., Mittelman, M., Sinaiko, E. and Reisberg, B., Early clinical prediction of Alzheimer's disease in mildly impaired elderly. Paper presented at the Third International Conference on Alzheimer's Disease and Related Disorders, 1992.
69. Fibiger H. Cholinergic mechanisms in learning, memory, and dementia: A review of recent evidence. Trends in Neuroscience. 14(6):1991;220-223.
70. Fibiger, H., Damsma, G. and Day, J. C., Behavioral pharmacology and biochemistry of central cholinergic neurotransmission. In The Basal Forebrain, ed. T. C. Napier, P. W. Kalivas and I. Hanin. Plenum Press, New York, 1991.
71. Fisher A., Hanin I. Potential animal models for senile dementia of Alzheimer's type, with emphasis on AF64A-induced cholinotoxicity. Annual Review of Pharmacology and Toxicology. 26:1986;161-181.
72. Flicker C., Bartus R. T., Crook T. H., Ferris S. H. Effects of aging and dementia upon recent visuospatial memory. Neurobiology of Aging. 5:1984;275-283.
73. Flicker C., Dean R., Bartus R. T., Ferris S. H., Crook T. Animal and human memory dysfunctions associated with aging, cholinergic lesions, and senile dementia. Annals of the New York Academy of Sciences. 444:1985;515-517.
74. Flicker C., Dean R. L., Watkins D. L., Fisher S. K., Bartus R. T. Behavioral and neurochemical effects following neurotoxic lesions of a major cholinergic input to the cerebral cortex in the rat. Pharmacology, Biochemistry and Behaviour. 18:1983;973-981.
75. Flicker C., Ferris S. H., Kalkstein D., Serby M. A double-blind, placebo-controlled crossover study of ganglioside GM1 treatment for Alzheimer's disease. American Journal of Psychiatry. 151:1994;126-129.
76. Flicker C., Ferris S. H., Reisberg B. Mild cognitive impairment in the elderly: Predictors of dementia. Neurology. 41:1991;1006-1009.
77. Flicker C., Ferris S. H., Reisberg B. A two-year longitudinal study of cognitive function in normal aging and Alzheimer's disease. Journal of Geriatric Psychiatry and Neurology. 6:1993;84-96.
78. Flood J. F., Cherkin A. Scopolamine effects on memory retention in mice: A model of dementia? Behavioral and Neural Biology. 45:1986;169-184.
79. Flood J. F., Morley J. E., Roberts E. Amnesic effects in mice of four synthetic peptides homologous to amyloid β protein from patients with Alzheimer disease. Proceedings of the National Academy of Sciences of the United States of America. 88:1991;3363-3366.
80. Flood J. F., Morley J. E., Roberts E. An amyloid β-protein fragment, Aβ[12-28], equipotently impairs post-training memory processing when injected into different limbic system structures. Brain Research. 663:1994;271-276.
81. Folstein M. F., Folstein S. E., McHugh P. R. 'Mini-Mental state', a practical method for grading the cognitive state of patients for the clinician. Journal of Psychiatric Research. 12:1975;189-198.
82. Folstein M. F., Whitehouse P. J. Cognitive impairment of Alzheimer disease. Neurobehavioral Toxicology and Teratology. 5:1983;631-634.
83. Freedman M., Oscar-Berman M. Selective delayed response deficits in Parkinson's and Alzheimer's disease. Archives of Neurology. 43:1986;886-890.
84. Gage F. H., Bjorklund A., Stenevi U., Dunnett S. B. Functional correlates of compensatory collateral sprouting by aminergic and cholinergic afferents in the hippocampal formation. Brain Research. 268:1983;39-47.
85. Games D., Adams D., Allesandrini R., Bardour R., Berthelette P., Blackwell C., Carr T., Clemens J., Donaldson T., Gillespie F., Guido T., Hagopian S., Johnson-Wood K., Khan K., Lee M., Leibowitz P., Lieberburg I., Little S., Masliah E., McConlogue L., Montoya-Zavala M., Mucke L., Paganini L., Penniman E., Pom M., Schenk D., Seubert P., Snyder B., Soriano F., Tan H., Vitale S., Wadsworth S., Wolozin B., Zhao J. Alzheimer-like neuropathology in transgenic mice overexpressing V717F β-amyloid precursor protein. Nature. 373:1995;523-527.
86. Gibson A. J. A further analysis of memory loss in dementia and depression in the elderly. British Journal of Clinical Psychology. 20:1981;179-185.
87. Ginn S. R., Powell D. A. Nucleus basalis lesions attenuate acquisition, but not retention, of Pavlovian heart rate conditioning and have no effect on eyeblink conditioning. Experimental Brain Research. 89:1992;501-510.
88. Gray J. A., McNaughton N. Comparison between the behavioural effects of septal and hippocampal lesions: A review. Neuroscience & Biobehavioral Reviews. 7:1983;119-188.
89. Hagan J. J., Tweedie F., Morris R. G.M. Lack of task specificity and absence of posttraining effects of atropine on learning. Behavioral Neuroscience. 100:1986;483-493.
90. Hall M. E., Stewart J. M. The amnesic effects of β-amyloid fragments on passive avoidance responding in mice are blocked by substance P. Abstracts of the Society for Neuroscience. 18:1992;164.
91. Hampson R. E., Byrd D. R., Konstantopoulos J. K., Bunn T., Jarrard L. E., Deadwyler S. A. Proactive interference and short-term memory during performance of a DNMS task in normal rats and rats with hippocampus removed. Abstracts of the Society for Neuroscience. 21:1995;1215.
92. Harper D. N., Dalrymple-Alford J. C., McLean A. P. The effect of medial septal and mammillary body lesions on the serial position curve in rats. Psychobiology. 21:1993;130-138.
93. Harper D. N., McLean A. P., Dalrymple-Alford J. C. List item memory in rats: Effects of delay and delay task. Journal of Experimental Psychology: Animal Behavior Processes. 19:1993;307-316.
94. Harper D. N., McLean A. P., Dalrymple-Alford J. C. Forgetting in rats following medial septum or mammillary body damage. Behavioral Neuroscience. 108:1994;691-702.
95. Harvey J. A., Gormezano I., Cool-Hauser V. A. Effects of scopolamine and methyl scopolamine on classical conditioning of the rabbit nictitating membrane response. Journal of Pharmacology and Experimental Therapeutics. 225:1983;42-49.
96. Harvey J. A., Gormezano I., Cool-Hauser V. A. Relationship between heterosynaptic reflex facilitation and acquisition of the nictitating membrane response in control and scopolamine-injected rabbits. Journal of Neuroscience. 5:1985;596-602.
97. Hepler D. J., Olton D. S., Wenk G. L., Coyle J. T. Lesions in nucleus basalis magnocellularis and medial septal area of rats produce qualitatively similar memory impairments. Journal of Neuroscience. 5:1985;866-873.
98. Hepler D. J., Wenk G. L., Cribbs B. L., Olton D. S., Coyle J. T. Memory impairments following basal forebrain lesions. Brain Research. 346:1985;8-14.
99. Herndon R. M., Coyle J. T. Selective destruction of neurons by a transmitter agonist. Science. 198:1977;71-72.
100. Herremans A. H. J., Hijzen T. H., Slangen J. L. Validity of a delayed conditional discrimination task as a model for working memory in the rat. Physiology and Behavior. 56:1994;869-875.
101. Hesse, M. B., Models and Analogies in Science. University of Notre Dame Press, South Bend, IN, 1966.
102. Higgins L. S., Holtzman D. M., Rabin J., Mobley W. C., Cordell B. Transgenic mouse brain histopathology resembles early Alzheimer's disease. Annals of Neurology. 35:1994;598-607.
103. Hironaka N., Miyata H., Ando K. Effects of psychoactive drugs on short-term memory in rats and rhesus monkeys. Japanese Journal of Pharmacology. 59:1992;113-120.
104. Hsiao K. K., Borchelt D. R., Olson K., Johannsdottir R. R., Kitt Cheryl, Yunis W., Xu S., Eckman C., Younkin S., Price D., Iadecola C., Clark H. B., Carlson G. Age-related CNS disorder and early death in transgenic FVB/N mice overexpressing Alzheimer amyloid precursor proteins. Neuron. 15:1995;1203-1218.
105. Hsiao K., Chapman P., Nilsen S., Eckman C., Harigaya Y., Younkin S., Yang F., Cole G. Correlative memory deficits, Aβ elevation, and amyloid plaques in transgenic mice. Science. 274:1996;99-102.
106. Hudzik T. J., Wenger G. R. Effects of drugs of abuse and cholinergic agents on delayed matching-to-sample responding in the squirrel monkey. Journal of Pharmacology and Experimental Therapeutics. 265:1993;120-127.
107. Hunt P. R., Neave N., Shaw C., Aggleton J. P. The effects of lesions to the fornix and dorsomedial thalamus on concurrent discrimination learning by rats. Behavioural Brain Research. 62:1994;195-205.
108. Husain M. M., Nemeroff C. B. Neuropeptides and Alzheimer's disease. Journal of the American Geriatric Society. 38:1990;918-925.
109. Hyman B. T., Van Hoesen G. W., Damasio A. R., Barnes C. L. Alzheimer's disease: Cell-specific pathology isolates the hippocampal formation. Science. 225:1984;1168-1170.
110. Irle E., Markowitsch H. J. Functional recovery after limbic lesions in monkeys. Brain Research Bulletin. 25:1990;79-92.
111. Janis L. S., Bishop T. W., Dunbar G. L. Medial septal lesions in rats produce permanent deficits for strategy selection in a spatial memory task. Behavioral Neuroscience. 108:1994;892-898.
112. Janis L. S., Glasier M. M., Martin G., Stackman R. W., Walsh T. J., Stein D. G. A single intraseptal injection of nerve growth factor facilitates radial maze performance following damage to the medial septum in rats. Brain Research. 679:1995;99-109.
113. Jarrard L. E. On the use of ibotenic acid to lesion selectively different components of the hippocampal formation. Journal of Neuroscience Methods. 29:1989;251-259.
114. Jarrard L. E. On the role of the hippocampus in learning and memory in the rat. Behavioral and Neural Biology. 60:1993;9-26.
115. Jarrard L. E., Kant G. J., Meyerhoff J. L., Levy A. Behavioral and neurochemical effects of intraventricular AF64A administration in rats. Pharmacology, Biochemistry and Behavior. 21:1984;273-280.
116. Jarrard L. E., Levy A., Meyerhoff J. L., Kant G. J. Intracerebral injections of AF64A: An animal model of Alzheimer's disease? Annals of the New York Academy of Sciences. 444:1985;520-522.
117. Jarrard L. E., Ringland J. M., Johnson L. S. Increased rate of forgetting of spatial information in rats with ibotenate lesions of hippocampus. Abstracts of the Society for Neuroscience. 13:1987;802.
118. Jeltsch H., Cassel J. C., Neufant B., Kelche C., Hertting G., Jackisch R., Will B. The effects of intrahippocampal raphe and/or septal grafts in rats with fimbria-fornix lesions depend on the origin of the grafted tissue and the behavioural task used. Neuroscience. 63:1994;19-39.
119. Jesberger J. A., Richardson J. R. Animal models of depression: Parallels and correlates to severe depression in humans. Biological Psychiatry. 20:1985;764-784.
120. Kakihana M., Kato K., Fukumoto H., Fujiwara E., Iwane M., Suno M. Detailed characterization of the biological activities of recombinant human nerve growth factor expressed in Chinese hamster ovary cells. Molecular Chemistry and Neuropathology. 18:1993;51-83.
121. Kametani H., Bresnahan E. L., Chachich M. E., Spangler E. L., Ingram D. K. Comparison of retention performance between young rats with fimbria-fornix lesions and aged rats in a 14-unit T-maze. Behavioural Brain Research. 35:1989;253-263.
122. Kelche C., Dalrymple-Alford J., Will B. Effects of postoperative environment on recovery of function after fimbria-fornix transection in the rat. Physiology and Behavior. 40:1987;731-736.
123. Kelsey J. E., Vargas H. Medial septal lesions disrupt spatial, but not nonspatial, working memory in rats. Behavioral Neuroscience. 107:1993;565-574.
124. Kesner R. P., Adelstein T., Crutcher K. A. Rats with nucleus basalis magnocellularis lesions mimic mnemonic symptomatology observed in patients with dementia of the Alzheimer type. Behavioral Neuroscience. 101:1987;451-456.
125. Kesner R. P., Adelstein T., Crutcher K. A. Equivalent spatial location memory deficits in rats with medial septum or hippocampal formation lesions and patients with dementia of the Alzheimer's type. Brain and Cognition. 9:1989;289-300.
126. Kesner R. P., Crutcher K., Beers D. R. Serial position curves for item (spatial location) information: Role of the dorsal hippocampal formation and medial septum. Brain Research. 454:1988;219-226.
127. Kesner R. P., Crutcher K., Measom M. Medial septal and nucleus basalis magnocellularis lesions produce order memory deficits in rats which mimic symptomatology of Alzheimer's disease. Neurobiology of Aging. 7:1986;287-295.
128. Kesner R. P., Novak J. M. Serial position curve in rats: Role of the dorsal hippocampus. Science. 218:1982;173-175.
129. Koda L. Y., Bloom F. E. A light and electron microscopic study of noradrenergic terminals in the rat dentate gyrus. Brain Research. 120:1957;325-335.
130. Köhler C., Chan-Palay V., Wu J. Y. Septal neurons containing glutamic acid decarboxylase immunoreactivity project to the hippocampal region in the rat brain. Anatomy and Embryology. 169:1984;41-44.
131. Köhler C., Schwarcz R. Comparison of ibotenate and kainate neurotoxicity in rat brain: A histological study. Neuroscience. 8:1983;819-835.
132. Kordower J. H., Gash D. M. Animals and experimentation: An evaluation of animal models of Alzheimer's and Parkinson's disease. Integrated Psychiatry. 4:1986;64-80.
133. Kordower J. H., Gash D. M. Animal models of age- and disease-related cognitive decline: Perspectives on the models and therapeutic strategies. Neurobiology of Aging. 9:1988;685-689.
134. Kwo-On-Yuen P. F., Mandel R., Chen A. D., Thal L. J. Tetrahydroaminoacridine improves the spatial acquisition deficit produced by nucleus basalis lesions in rats. Experimental Neurology. 108:1990;221-228.
135. La Rue, A., Aging and Neuropsychological Assessment. Plenum Press, New York, 1992.
136. Lachman R. The model in theory construction. Psychological Review. 67:1960;113-129.
137. Lamour Y., Senut M. C., Dutar P., Bassant M. H. Neuropeptides and septo-hippocampal neurons: Electrophysiological effects and distributions of immunoreactivity. Peptides. 9:1989;1351-1359.
138. 192IgG -saporin: Behavioural, biochemical and stereological studies in the rat European Journal of Neuroscience. 7:1995;329-343.
139. Lerer B., Warner J., Friedman E., Incent G., Gamu E. Cortical cholinergic impairment and behavioral deficits produced by kainic acid lesions of rat magnocellular basal forebrain. Behavioral Neuroscience. 99:1985;661-667.
140. Lewis P. R., Shute C. C. D. The cholinergic limbic system: Projections to hippocampal formation, medial cortex, nuclei of the ascending cholinergic reticular system and the subfornical organ and supra-optic crest. Brain. 90:1967;521-537.
141. Lister R. G., Weingartner H. J. Neuropharmacological strategies for understanding psychobiological determinants of cognition. Human Neurobiology. 6:1987;119-127.
142. Mahut H., Zola-Morgan S., Moss M. Hippocampal resections impair associative learning and recognition memory in the monkey. Journal of Neuroscience. 2:1982;1214-1229.
143. Maier D. L., Ryan J. P., Isaacson R. The residual spatial abilities of hippocampally lesioned rats can be enhanced by peripheral sympathetic-adrenal interventions. Behavioral and Neural Biology. 53:1990;123-132.
144. Mandel R. J., Chen A. D., Connor D. J., Thal L. J. Continuous physostigmine infusion in rats with excitotoxic lesions of the nucleus basalis magnocellularis: Effects on performance in the water maze task and cortical cholinergic markers. Journal of Pharmacology and Experimental Therapeutics. 251:1989;612-619.
145. Mandel R. J., Gage F. H., Thal L. J. Spatial learning in rats: Correlation with cortical choline acetyltransferase and improvement with NGF following NBM damage. Experimental Neurology. 104:1989;208-217.
146. Mandel R. J., Gage F. H., Thal L. J. Enhanced detection of nucleus basalis magnocellularis lesion-induced spatial learning deficit in rats by modification of training regimen. Behavioural Brain Research. 31:1989;221-229.
147. Mandel R. J., Thal L. J. Physostigmine improves water maze performance following nucleus basalis magnocellularis lesions in rats. Psychopharmacology. 96:1988;421-425.
148. Mannisto P. T., Tuomainen P., Kutepova O., Borisenko S. A., Zolotov N., Voronina T. Effects of bilateral cholinotoxin infusions on the behavior and brain biochemistry of the rats. Pharmacology, Biochemistry and Behavior. 49:1994;33-40.
149. Mantione C. R., Fisher A., Hanin I. The AF64A-treated mouse: Possible model for central cholinergic hypofunction. Science. 213:1981;579-580.
150. Mantyh P. W., Ghilardi J. R., Rogers S., Demaster E., Allen C. J., Stimson E. R., Maggio J. E. Aluminum, iron, and zinc ions promote aggregation of physiological concentrations of β-amyloid peptide. Journal of Neurochemistry. 61:1993;1171-1174.
151. Markowska A. L., Wenk G. L., Olton D. S. Nucleus basalis magnocellularis and memory: Differential effects of two neurotoxins. Behavioral and Neural Biology. 54:1990;13-26.
152. Matsuoka N., Maeda N., Ohkubo Y., Yamaguchi I. Differential effects of physostigmine and pilocarpine on the spatial memory deficits produced by two septo-hippocampal deafferentations in rats. Brain Research. 559:1991;233-240.
153. Matsuoka N., Maeda N., Yamazaki M., Ohkubo Y., Yamaguchi I. Effect of FR121196: A novel cognitive enhancer, on the memory impairments of rats in passive avoidance and radial arm maze tasks. Journal of Pharmacology and Experimental Therapeutics. 263:1992;436-444.
154. Matsuoka N., Yamazaki M., Yamaguchi I. Changes in brain somatostatin in memory-deficient rats: Comparison with cholinergic markers. Neuroscience. 66:1995;617-626.
155. McAlonan G. M., Wilkinson L. S., Robbins T. W., Everitt B. J. The effects of AMPA-induced lesions of the septo-hippocampal cholinergic projection on aversive conditioning to explicit and contextual cues and spatial learning in the water maze. European Journal of Neuroscience. 7:1995;281-292.
156. McDonald M. P., Dahl E. E., Overmier J. B., Mantyh P., Cleary J. Effects of an exogenous β-amyloid peptide on retention for spatial learning. Behavioral and Neural Biology. 62:1994;60-67.
157. McDonald M. P., Overmier J. B., Bandyopadhyay S., Babcock D., Cleary J. Reversal of β-amyloid-induced retention deficit after exposure to training and state cues. Neurobiology of Learning and Memory. 65:1996;35-47.
158. McGaugh J. L. Time-dependent processes in memory storage. Science. 153:1966;1351-1358.
159. McKinney M., Coyle J. T., Hedreen J. C. Topographic analysis of the innervation of the rat neocortex and hippocampus by the basal forebrain cholinergic system. Journal of Comparative Neurology. 217:1983;103-121.
160. Messer W. S., Thomas G. J., Hoss W. P. Selectivity of pirenzepine in the central nervous system. II. Differential effects of pirenzepine and scopolamine on performance of a representational memory task. Brain Research. 407:1987;37-45.
161. Miller E. On the nature of the memory disorder in presenile dementia. Neuropsychologia. 9:1971;75-81.
162. Miller E. K., Desimone R. Scopolamine affects short-term memory but not inferior temporal neurons. Neuroreport. 4:1993;81-84.
163. Mishkin M. Memory in monkeys severely impaired by combined but not by separate removal of amygdala and hippocampus. Nature. 273:1978;297-298.
164. Miyamoto M., Hirai K., Takahashi H., Kato K., Nishiyama M., Okada H., Nagaoka A. Effects of sustained release formulation of thyrotropin-releasing hormone on learning impairments caused by scopolamine and AF64A in rodents. European Journal of Pharmacology. 238:1993;181-189.
165. Miyamoto M., Kato J., Narumi S., Nagaoka A. Characteristic of memory impairment following lesioning of the basal forebrain and medial septal nucleus in rats. Brain Research. 419:1987;19-31.
166. Miyamoto M., Shintani M., Nagaoka A., Nagawa Y. Lesioning of the rat basal forebrain leads to memory impairments in passive and active avoidance tasks. Brain Research. 328:1985;97-104.
167. Mizumori S. J., Perez G. M., Alvarado M. C., Barnes C. A., McNaughton B. L. Reversible inactivation of the medial septum differentially affects two forms of learning in rats. Brain Research. 528:1990;12-20.
168. Mohs R. C. Memory impairment in amnesia and dementia: Implications for the use of animal models. Neurobiology of Aging. 9:1988;465-468.
169. 3H -L-glutamate binding sites Nature. 306:1983;176-179.
170. Money E. A., Kirk R. C., McNaughton N. Alzheimer's dementia produces a loss of discrimination but no increase in rate of memory decay in delayed matching to sample. Neuropsychologia. 30:1992;133-143.
171. Moore R. Y., Halaras A. E. Hippocampal innervation by serotonin neurons if the midbrain raphe in the rat. Journal of Comparative Neurology. 164:1975;171-183.
172. Moran P. M., Higgins L. S., Cordell B., Moser P. C. Age-related learning deficits in transgenic mice expressing the 751-amino acid isoform of human β-amyloid precursor protein. Proceedings of the National Academy of Sciences of the United States of America. 92:1995;5341-5345.
173. Morris R. G., Kopelman M. D. The memory deficits in Alzheimer-type dementia: A review. Quarterly Journal of Experimental Psychology. 38A:1986;575-602.
174. Moss M., Mahut H., Zola-Morgan S. Concurrent discrimination learning of monkeys after hippocampal, entorhinal, or fornix lesions. Journal of Neuroscience. 1:1981;227-240.
175. Mowrer, O. H., Learning Theory and Behavior. Wiley, New York, 1960.
176. Muir J. L., Dunnett S. B., Robbins T. W., Everitt B. J. Attentional functions of the forebrain cholinergic systems: Effects of intraventricular hemicholinium, physostigmine, basal forebrain lesions and intracortical grafts on a multiple-choice serial reaction time task. Experimental Brain Research. 89:1992;611-622.
177. Muir J. L., Everitt B. J., Robbins T. W. Reversal of visual attentional dysfunction following lesions of the cholinergic basal forebrain by physostigmine and nicotine but not by the 5-HT3 receptor antagonist, ondansetron. Psychopharmacology (Berlin). 118:1995;82-92.
178. Muir J. L., Page K. J., Sirinathsinghji D. J., Robbins T. W., Everitt B. J. Excitotoxic lesions of basal forebrain cholinergic neurons: Effects on learning, memory, and attention. Behavioural Brain Research. 57:1993;123-131.
179. Muir J. L., Robbins T. W., Everitt B. J. Disruptive effects of muscimol infused into the basal forebrain on conditional discrimination and visual attention: Differential interactions with cholinergic mechanisms. Psychopharmacology (Berlin). 107:1992;541-550.
180. Mumby D. G., Pinel J. P. J. Rhinal cortex lesions and object recognition in rats. Behavioural Neuroscience. 108:1994;11-18.
181. Mumby D. G., Pinel J. P. J., Kornecook T. J., Shen M. J., Redila V. A. Memory deficits following lesions of hippocampus or amygdala in rat: Assessment by an object-memory test battery. Psychobiology. 23:1995;26-36.
182. Muñoz C., Grossman S. P. Spatial discrimination, reversal and active or passive avoidance learning in rats with KA-induced neuronal depletions in dorsal hippocampus. Brain Research Bulletin. 6:1981;399-406.
183. Murray C. L., Fibiger H. C. Learning and memory deficits after lesions of the nucleus basalis magnocellularis: Reversal by physostigmine. Neuroscience. 14:1985;1025-1032.
184. Murray E. A., Bachevalier J., Mishkin M. Effects of rhinal cortical lesions on visual recognition memory in rhesus monkeys. Abstracts of the Society for Neuroscience. 15:1989;342.
185. Murtha S. J. E., Pappas B. A. Neurochemical, histopathological and mnemonic effects of combined lesions of the medial septal and serotonin afferents to the hippocampus. Brain Research. 651:1994;16-26.
186. Nabeshima T., Nitta A. Memory impairment and neuronal dysfunction induced by β-amyloid protein in rats. Tohoku Journal of Experimental Medicine. 174:1994;241-249.
187. Nadler J. V., Perry B. W., Cotman C. W. Intraventricular kainic acid preferentially destroys hippocampal pyramidal cells. Nature. 271:1978;676-677.
188. Nagahara A. H., McGaugh J. L. Muscimol infused into the medial septal area impairs long-term memory but not short-term memory in inhibitory avoidance, water maze place learning and rewarded alternation tasks. Brain Research. 591:1992;54-61.
189. Neave N., Lloyd S., Sahgal A., Aggleton J. P. Lack of effect of lesions in the anterior cingulate cortex and retrosplenial cortex on certain tests of spatial memory in the rat. Behavioural Brain Research. 65:1994;89-101.
190. Nilsson O. G., Shapiro M. L., Gage F. H., Olton D. S., Bjorklund A. Spatial learning and memory following fimbria-fornix transection and grafting of fetal septal neurons to the hippocampus. Experimental Brain Research. 67:1987;195-215.
191. Nitta A., Itoh A., Hasegawa T., Nabeshima T. β-amyloid protein-induced Alzheimer's disease animal model. Neuroscience Letters. 28:1994;63-66.
192. Numan R., Klis D. Effects of medial septal lesions on an operant delayed go/no-go discrimination in rats. Brain Research Bulletin. 29:1992;643-650.
193. Numan R., Quaranta J. R. Effects of medial septal lesions on operant delayed alternation in rats. Brain Research. 531:1990;232-241.
194. O'Boyle V. J., Murray E. A., Mishkin M. Effects of excitotoxic amygdalo-hippocampal lesions on visual recognition in rhesus monkeys. Abstracts of the Society for Neuroscience. 19:1993;438.
195. Okaichi H., Oshima Y. Choice behavior of hippocampectomized rats in the radial arm maze. Psychobiology. 18:1990;416-421.
196. Okaichi H., Oshima Y., Jarrard L. E. Scopolamine impairs both working and reference memory in rats: A replication and extension. Pharmacology, Biochemistry and Behaviour. 34:1989;599-602.
197. Okaichi Y., Okaichi H. Effects of fimbria-fornix lesions on avoidance tasks with temporal elements in rats. Physiology and Behavior. 56:1994;759-765.
198. Olton D. S. Dementia: Animal models of the cognitive impairments following damage to the basal forebrain cholinergic system. Brain Research Bulletin. 25:1991;499-502.
199. Olton D. S. Shock-motivated avoidance and the analysis of behavior. Psychological Bulletin. 4:1973;243-251.
200. Olton D. S. Strategies for the development of animal models of human memory impairments. Annals of the New York Academy of Science. 444:1985;113-121.
201. Olton D. S., Becker J. T., Handelmann G. E. Hippocampus, space, and memory. Behavioral and Brain Science. 2:1979;313-365.
202. Olton D. S., Papas B. C. Spatial memory and hippocampal function. Neuropsychologia. 17:1979;669-682.
203. Olton, D. S. and Wenk, G. L., Dementia: Animal models of the cognitive impairments produced by degeneration of the basal forebrain cholinergic system. In Psychopharmacology: The Third Generation of Progress, ed. H. Y. Meltzer. Raven Press, New York, 1987.
204. Opello K. D., Stackman R. W., Ackerman S., Walsh T. J. AF64A (ethylcholine mustard aziridinium) impairs acquisition and performance of a spatial, but not a cued water maze task. Physiology and Behavior. 54:1993;1227-1233.
205. Ordy J. M., Thomas G. J., Volpe B. T., Dunlap W. P., Colombo P. M. An animal model of human-type memory loss based on aging, lesion, forebrain ischemia, and drug studies with the rat. Neurobiology of Aging. 9:1988;667-683.
206. Overmier, J. B. and Patterson, J., Animal models of human psychopathology. In Selected Models of Anxiety, Depression and Psychosis. Animal Models of Psychiatric Disorders, Vol. 1, ed. P. Simon, P. Soubrié and D. Widlocher. S. Karger, Basel, Switzerland, 1988, pp. 1-35.
207. Owen M. J., Butler S. R. Amnesia after transection of the fornix in monkeys: Long-term memory impaired, short-term memory intact. Behavioural Brain Research. 3:1981;115-123.
208. Owen M. J., Butler S. R. Does amnesia after transection of the fornix in monkeys reflect abnormal sensitivity to proactive interference? Behavioural Brain Research. 14:1984;183-192.
209. Page K. J., Everitt B. J., Robbins T. W., Marston H. M., Wilkinson L. S. Dissociable effects on spatial maze and passive avoidance acquisition and retention following AMPA- and ibotenic acid-induced excitotoxic lesions of the basal forebrain in rats: Differential dependence on cholinergic neuronal loss. Neuroscience. 43:1991;457-472.
210. Pallage V., Toniolo G., Will B., Hefti F. Long-term effects of nerve growth factor and neural transplants on behavior of rats with medial septal lesions. Brain Research. 386:1986;197-208.
211. Pang K., Williams M. J., Egeth H., Olton D. S. Nucleus basalis magnocellularis and attention: Effects of muscimol infusions. Behavioral Neuroscience. 107:1993;1031-1038.
212. Peele D. B., Baron S. P. Effects of scopolamine on repeated acquisition of radial-arm maze performance by rats. Journal of the Experimental Analysis of Behavior. 49:1988;275-290.
213. Peinado-Manzano M. A. The role of the amygdala and the hippocampus in working memory for spatial and non-spatial information. Behavioural Brain Research. 38:1990;117-134.
214. Penetar D. M., McDonough J. H. Effects of cholinergic drugs on delayed match-to-sample performance of rhesus monkeys. Pharmacology, Biochemistry and Behaviour. 19:1983;963-967.
215. Penick S., Solomon P. R. Hippocampus, context, and conditioning. Behavioral Neuroscience. 105:1991;611-617.
216. Pepeu G., Casamenti F., Pedata F., Cosi C., Pepeu I. M. Are the neurochemical and behavioral changes induced by lesions of the nucleus basalis in the rat a model of Alzheimer's disease? Progress in Neuropsychopharmacology and Biological Psychiatry. 10:1986;541-551.
217. Perry E. K. The cholinergic system in old age and Alzheimer's disease. Age and Ageing. 9:1980;1-8.
218. Perry E. K., Perry R. H., Tomlinson B. E. Dietary lecithin supplements in dementia of Alzheimer type [letter]. Lancet. 2:1977;242-243.
219. Perry E. K., Tomlinson B. E., Blessed G., Bergmann K., Gibson P. H., Perry R. H. Correlation of cholinergic abnormalities with senile plaques and mental test scores in senile dementia. British Medical Journal. 2:1978;1457-1459.
220. Perry T. L., Yong V. W., Bergeron C., Hansen S., Jones K. Amino acids, glutathione, and glutathione transferase activity in the brains of patients with Alzheimer's disease. Annals of Neurology. 21:1987;331-336.
221. Peterson L. R., Peterson M. J. Short-term retention of individual verbal items. Journal of Experimental Psychology. 58:1959;193-198.
222. Pollmann S., Haupt M., Romero B., Kurz A. Is impaired recall in dementia of the Alzheimer type a consequence of a contextual retrieval deficit? Dementia. 4:1993;102-108.
223. Pontecorvo M. J., Clissold D. B., White M. F., Ferkany J. W. N-methyl-D-aspartate antagonists and working memory performance: Comparison with effects of scopolamine, propanolol, diazepam and phenylisopropyladenosine. Behavioural Neuroscience. 105:1991;521-535.
224. Popper, K. R., The Logic of Scientific Discovery. Basic Books, New York, 1959.
225. Prohovnik I., Mayeux R., Sackeim H. A., Smith G., Stern Y., Alderson P. O. Cerebral perfusion as a diagnostic marker of early Alzheimer's disease. Neurology. 38:1988;931-937.
226. Quon D., Wang Y., Catalano R., Scardina J. M., Murakami K., Cordell B. Formation of β-amyloid protein deposits in brains of transgenic mice. Nature. 352:1991;239-241.
227. Raffaele K. C., Olton D. S. Hippocampal and amygdaloid involvement in working memory for nonspatial stimuli. Behavioral Neuroscience. 102:1988;349-355.
228. Rawlins J. N. P., Lyford G. L., Seferiades A., Deacon R. M. J., Cassaday H. J. Critical determinants of nonspatial working memory deficits in rats with conventional lesions of the hippocampus or fornix. Behavioral Neuroscience. 107:1993;420-433.
229. Rawlins J. N., Olton D. S. The septo-hippocampal system and cognitive mapping. Behavioural Brain Research. 5:1982;331-358.
230. Reisberg B., Ferris S. H., de Leon M. J., Crook T. The Global Deterioration Scale (GDS): An instrument for the assessment of primary degenerative dementia (PDD). American Journal of Psychiatry. 139:1982;1136-1139.
231. Ridley R. M., Baker H. F. A critical evaluation of monkey models of amnesia and dementia. Brain Research Reviews. 16:1991;15-37.
232. Ridley R. M., Baker H. F., Drewett B., Johnson J. A. Effects of ibotenic acid lesions of the basal forebrain on serial reversal learning in marmosets. Psychopharmacology (Berlin). 86:1985;438-443.
233. Ridley R. M., Baker H. F., Murray T. K. Basal nucleus lesions in monkeys: Recognition memory impairment or visual agnosia? Psychopharmacology (Berlin). 95:1988;289-290.
234. Ridley R. M., Bowes P. M., Baker H. F., Crow T. J. an involvement of acetylcholine in object discrimination learning and memory in the marmoset. Neuropsychologia. 22:1984;253-263.
235. Ridley R. M., Murray T. K., Johnson J. A., Baker H. F. Learning impairment following lesion of the basal nucleus of Meynert in the marmoset: Modification by cholinergic drugs. Brain Research. 376:1986;108-116.
236. Riekkinen M., Riekkinen P., Riekkinen P. Comparison of quisqualic and ibotenic acid nucleus basalis magnocellularis lesions on water-maze and passive avoidance performance. Brain Research Bulletin. 27:1991;119-123.
237. Riekkinen P., Riekkinen M., Lahtinen H., Sirviö J., Valjakka A., Riekkinen P. Tetrahydroaminoacridine improves passive avoidance retention defects induced by aging and medial septal lesion but not by fimbria-fornix lesion. Brain Research Bulletin. 27:1991;587-594.
238. Riekkinen P., Riekkinen M., Sirviö J., Miettinen R., Riekkinen P. Comparison of the effects of acute and chronic ibotenic and quisqualic acid nucleus basalis lesioning. Brain Research Bulletin. 27:1991;199-206.
239. Riekkinen P., Sirviö J., Riekkinen M. Serotonin depletion decreases the therapeutic effect of nicotine, but not THA, in medial septal-lesioned rats. Brain Research. 662:1994;95-102.
240. Riekkinen P., Sirviö J., Riekkinen P. The effects of THA on medial septal lesion-induced memory defects. Pharmacology, Biochemistry and Behavior. 36:1990;237-241.
241. Robbins T. W., Everitt B. J., Marston H. M., Wilkinson J., Jones G. H., Page K. J. Comparative effects of ibotenic acid- and quisqualic acid-induced lesions of the substantia innominata on attentional function in the rat: Further implications for the role of the cholinergic neurons of the nucleus basalis in cognitive processes. Behavioural Brain Research. 35:1989;221-240.
242. Robbins T. W., Everitt B. J., Ryan C. N., Marston H. M., Jones G. H., Page K. J. Comparative effects of quisqualic and ibotenic acid-induced lesions of the substantia innominata and globus pallidus on the acquisition of a conditional visual discrimination: Differential effects on cholinergic mechanisms. Neuroscience. 28:1989;337-352.
243. Robinson J. K., Crawley J. N. Intraseptal galanin potentiates scopolamine impairment of delayed nonmatching to sample. Journal of Neuroscience. 13:1993;5119-5125.
244. Robustelli F., Glick S. D., Goldfarb T. L., Geller A., Jarvik M. E. A further analysis of scopolamine impairment of delayed matching with monkeys. Communications in Behavioral Biology. 3A:1969;101-109.
245. Roeske L. C., Auchus A. P. Neuropeptide changes in cortical and deep gray structures in Alzheimer's disease. Reviews of Neuroscience. 6:1995;317-328.
246. Rothblat L. A., Kromer L. F. Object recognition memory in the rat: The role of the hippocampus. Behavioural Brain Research. 42:1991;25-32.
247. Rupniak N. M., Samson N. A., Steventon M. J., Iversen S. D. Induction of cognitive impairment by scopolamine and noncholinergic agents in rhesus monkeys. Life Sciences. 48:1991;893-899.
248. Sahakian B. J., Morris R. G., Evenden J. L., Heald A., Levy R., Philpot M., Robbins T. W. A comparative study of visuospatial memory and learning in Alzheimer-type dementia and Parkinson's disease. Brain. 11:1988;695-718.
249. Sahakian B. J., Owen A. M., Morant N. J., Eagger S. A., Boddington S., Crayton L., Crockford H. A., Crooks M., Hill K., Levy R. Further analysis of the cognitive effects of tetrahydroaminoacridine (THA) in Alzheimer's disease: Assessment of attentional and mnemonic function using CANTAB. Psychopharmacology (Berlin). 110:1993;395-401.
250. Sahgal A., Keith A. B. Combined serotonergic-cholinergic lesions do not disrupt memory in rats. Pharmacology, Biochemistry and Behavior. 45:1993;995-1001.
251. Sahgal A., Galloway P. H., McKeith I. G., Lloyd K. S., Cook J. H., Ferrier I. N., Edwardson J. A. Matching-to-sample deficits in patients with senile dementias of the Alzheimer and Lewy body types. Archives of Neurology. 49:1992;1043-1046.
252. Sahgal A., Keith A. B., Lloyd S., Kerwin J. M., Perry E. K., Edwardson J. A. Memory following cholinergic (NBM) and noradrenergic (DNAB) lesions made singly or in combination: Potentiation of disruption by scopolamine. Pharmacology, Biochemistry and Behavior. 37:1990;597-605.
253. Sakurai Y., Wenk G. L. The interaction of acetylcholinergic and serotonergic neural systems on performance in a continuous non-matching to sample task. Brain Research. 519:1990;118-121.
254. Salamone J. D. Behavioural functions of nucleus basalis magnocellularis and its relationship to dementia. Trends in Neuroscience. 9:1986;256-258.
255. Salvatierra A. T., Berry S. D. Scopolamine disruption of septo-hippocampal activity and classical conditioning. Behavioral Neuroscience. 103:1989;715-721.
256. Sandhu F. A., Salim M., Zain S. B. Expression of the human β-amyloid protein of Alzheimer's disease specifically in the brains of transgenic mice. Journal of Biological Chemistry. 266:1991;21331-21334.
257. Savage L. M., Stanchfield M. A., Overmier J. B. The effects of scopolamine, diazepam, and lorazepam on working memory in pigeons: An analysis of reinforcement procedures and sample problem type. Pharmacology, Biochemistry and Behavior. 48:1994;183-191.
258. Scavio M. J., Clift P. S., Wills J. C. Posttraining effects of amphetamine, chlorpromazine, ketamine, and scopolamine on the acquisition and extinction of the rabbit's conditioned nictitating membrane response. Behavioral Neuroscience. 106:1992;900-908.
259. Schonfield D., Robertson B. A. Memory storage and aging. Canadian Journal of Psychology. 20:1966;228-236.
260. Schulze G. E., Gillam M. P., Paule M. G. Effects of atropine on operant test battery performance in Rhesus monkeys. Life Sciences. 51:1992;487-497.
261. Schwarcz R., Foster A. C., French E. D., Whetsell W. O., Köhler C. Excitotoxic models for neurodegenerative disorders. Life Sciences. 35:1984;19-32.
262. Segal M. Physiological and pharmacological evidence for a serotonergic projection to the hippocampus. Brain Research. 94:1975;115-131.
263. Shannon H. E., Bemis K. G., Hendrix J. C., Ward J. S. Interactions between scopolamine and muscarinic cholinergic agonists or cholinesterase inhibitors on spatial alternation performance in rats. Journal of Pharmacology and Experimental Therapeutics. 255:1990;1071-1077.
264. Shaw C., Aggleton J. P. The effects of fornix and medial prefrontal lesions on delayed non-matching-to-sample by rats. Behavioural Brain Research. 54:1993;91-102.
265. Smith C. M., Swash M. Possible biochemical basis of memory disorder in Alzheimer disease. Annals of Neurology. 3:1978;471-473.
266. Smith G. Animal models of Alzheimer's disease: Experimental cholinergic denervation. Brain Research Reviews. 13:1988;103-118.
267. Snow A. D., Sekiguchi R., Nochlin D., Fraser P., Kimata K., Mizutani A., Arai M., Schreier W. A., Morgan D. G. An important role of heparan sulfate proteoglycan (Perlecan) in a model system for the deposition and persistence of fibrillar Aβ-amyloid in rat brain. Neuron. 12:1994;219-234.
268. Solomon P. R., Beal M. F., Pendlebury W. W. Age-related disruption of classical conditioning: A model systems approach to memory disorders. Neurobiology of Aging. 9:1988;535-546.
269. Solomon P. R., Brett M., Groccia-Ellison M. E., Oyler C., Tomasi M., Pendlebury W. W. Classical conditioning inpatients with Alzheimer's disease: A multiday study. Psychology of Aging. 10:1995;248-254.
270. Solomon P. R., Groccia-Ellison M. E., Flynn D., Mirak J., Edwards K. R., Dunehew A., Stanton M. E. Disruption of human eyeblink conditioning after central cholinergic blockade with scopolamine. Behavioral Neuroscience. 107:1993;271-279.
271. Solomon P. R., Groccia-Ellison M., Levine E., Blanchard S., Pendlebury W. W. Do temporal relationships in conditioning change across the life span? Perspectives from eyeblink conditioning in humans and rabbits. Annals of the New York Academy of Sciences. 608:1990;212-238.
272. Solomon P. R., Levine E., Bein T., Pendlebury W. W. Disruption of classical conditioning in patients with Alzheimer's disease. Neurobiology of Aging. 12:1991;283-287.
273. Solomon P. R., Solomon S. D., Schaaf E. V., Perry H. E. Altered activity in the hippocampus is more detrimental to classical conditioning than removing the structure. Science. 220:1983;329-331.
274. Solomon P. R., Vander Schaaf E. R., Thompson R. F., Weisz D. J. Hippocampus and trace conditioning of the rabbit's classically conditioned nictitating membrane response. Behavioral Neuroscience. 100:1986;729-744.
275. 192IgG -saporin and short-term recognition memory: Role of the septohippocampal projection Neuroscience. 66:1995;101-114.
276. Sutherland R. J., McDonald R. J., Hill C. R., Rudy J. W. Damage to the hippocampal formation in rats selectively impairs the ability to learn cue relationships. Behavioural Neural Biology. 52:1989;331-356.
277. Swanson L. W., Hartman B. K. The central adrenergic system: An immunoflourescence study of the location of cell bodies and their efferent connections in the rat. Journal of Comparative Neurology. 163:1975;487-506.
278. Sweeney W., Luedtke J., McDonald M. P., Overmier J. B. Intrahippocampal β-amyloid impairs win-shift radial maze performance in rats. Neurobiology of Learning and Memory. 68:1977;97-101.
279. Thomas G. J., Brito G. N. Recovery of delayed alternation in rats after lesions in medial frontal cortex and septum. Journal of Comparative Physiology and Psychology. 94:1980;808-818.
280. Thomas G. J., Gash D. M. Differential effects of posterior septal lesions on dispositional and representational memory. Behavioral Neuroscience. 100:1986;712-719.
281. Thomas G. J., Gash D. M. Differential effects of hippocampal ablations on dispositional and representational memory in the rat. Behavioral Neuroscience. 102:1988;635-642.
282. Thomas G. J., Spafford P. S. Deficits for representational memory induced by septal and cortical lesions (singly and combined) in rats. Behavioral Neuroscience. 98:1984;394-404.
283. Tomlinson B. E., Kitchener D. Granulovacuolar degeneration of hippocampal pyramidal cells. Journal of Pathology. 10:1972;165-185.
284. Torres E. M., Perry T. A., Blokland A., Wilkinson L. S., Wiley R. G., Lappi D. A., Dunnett S. B. Behavioural, histochemical and biochemical consequences of selective immunolesions in discrete regions of the basal forebrain cholinergic system. Neuroscience. 63:1994;95-122.
285. Ueda K., Fukui Y., Kageyama H. Amyloid β protein-induced neuronal cell death - neurotoxic properties of aggregated amyloid β protein. Brain Research. 639:1994;240-244.
286. Underwood, B. J., Psychological Research. Appleton-Century-Crofts, New York, 1957.
287. Van Hoesen G. W., Hyman B. T. Hippocampal formation: Anatomy and the patterns of pathology in Alzheimer's disease. Progress in Brain Research. 83:1990;445-457.
288. Vincent S. R., McGeer E. G. A substance P projection to the hippocampus. Brain Research. 215:1981;349-351.
289. Voytko M. L., Olton D. S., Richardson R. T., Gorman L. K., Tobin J. R., Price D. L. Basal forebrain lesions in monkeys disrupt attention but not learning and memory. Journal of Neuroscience. 14:1994;167-186.
290. 192immunoglobulin G-saporin produces graded behavioral and biochemical changes accompanying the loss of cholinergic neurons of the basal forebrain and cerebellar Purkinje cells Neuroscience. 65:1995;463-476.
291. 192IgG -saporin Neuroscience Letters. 169:1994;154-158.
292. Waite J. J., Chen A. D., Wardlow M. L., Thal L. J. Behavioral and biochemical consequences of combined lesions of the medial septum/diagonal band and nucleus basalis in the rat when ibotenic acid, quisqualic acid, and AMPA are used. Experimental Neurology. 130:1994;214-229.
293. Walsh T. J., Tilson H. A., DeHaven D. L., Mailman R. B., Fisher A., Hanin I. AF64A, a cholinergic neurotoxin, selectively depletes acetylcholine in hippocampus and cortex, and produces long-term passive avoidance and radial-arm maze deficits in the rat. Brain Research. 321:1984;91-102.
294. Watkins M. J. Mediationism and the obfuscation of memory. American Psychologist. 45:1990;328-335.
295. Wechsler, D., WAIS-R Manual: Wechsler Adult Intelligence Scale: 1972, norms edn. Houghton Mifflin, Boston, 1981.
296. Wenk G. L., Harrington C. A., Tucker D. A., Rance N. E., Walker L. C. Basal forebrain neurons and memory: A biochemical, histological, and behavioral study of differential vulnerability to ibotenate and quisqualate. Behavioral Neuroscience. 106:1992;909-923.
297. Whishaw I. Q., Cassel J. C., Jarrard L. E. Rats with fimbria-fornix lesions display a place response in a swimming pool: A dissociation between getting there and knowing where. Journal of Neuroscience. 15:1995;5779-5788.
298. Whishaw I., O'Connor W., Dunnett S. B. Disruption of central cholinergic systems in the rat brain by basal forebrain lesions or atropine: Effects on feeding, sensorimotor behavior, locomotor activity, and spatial navigation. Behavioural Brain Research. 17:1985;103-115.
299. Wible C. G., Shiber J. R., Olton D. S. Hippocampus, fimbria-fornix, amygdala, and memory: Objects discriminations in rats. Behavioral Neuroscience. 106:1992;751-761.
300. Wiley R. G., Oeltmann T. N., Lappi D. A. Immunolesioning: Selective destruction of neurons using immunotoxin to rat NGF receptor. Brain Research. 562:1991;149-153.
301. Wilson R. S., Bacon L. D., Fox J. H., Kasniak A. W. Primary memory and secondary memory in dementia of the Alzheimer type. Journal of Clinical Neuropsychology. 5:1983;337-344.
302. Winn P., Stone T. W., Latimer M., Hastings M. H., Clark A. J. M. A comparison of excitotoxic lesions of the basal forebrain by kainate, quinolinate, ibotenate, N-methyl-D-aspartate or quisqualate, and the effects on toxicity of 2-amino-5-phosphonovaleric acid and kynurenic acid in the rat. British Journal of Pharmacology. 102:1991;904-908.
303. Winocur G. A comparison of normal old rats and young adult rats with lesions to the hippocampus or prefrontal cortex on a test of matching-to-sample. Neuropsychologia. 30:1992;769-781.
304. Winocur G. A neuropsychological analysis of memory loss with age. Neurobiology of Aging. 9:1988;487-494.
305. Winocur G. Functional dissociation of the hippocampus and prefrontal cortex in learning and memory. Psychobiology. 19:1991;11-20.
306. Wirsching B., Beninger R., Jhamandas K., Boegman R., El-Defrawy S. Differential effects of scopolamine on working and reference memory of rats in the radial maze. Pharmacology, Biochemistry and Behavior. 20:1984;659-662.
307. Woodhams P. L., Roberts G. W., Polak J. M., Crow T. J. Distribution of neuropeptides in the limbic system of the rat: The bed nucleus of the stria terminalis, septum and preoptic area. Neuroscience. 8:1983;677-693.
308. Woodruff-Pak D. S., Finkbiner R. G., Sasse D. K. Eyeblink conditioning discriminates Alzheimer's patients from non-demented aged. Neuroreport. 1:1990;45-48.
309. Wortwein G., Stackman R. W., Walsh T. J. Vitamin E prevents the place learning deficit and the cholinergic hypofunction induced by AF64A. Experimental Neurology. 125:1994;15-21.
310. Wright A. A., Santiago H. C., Sands S. F., Kendrick D. F., Cook R. G. Memory processing of serial lists by pigeons, monkeys, and people. Science. 229:1985;287-289.
311. Yamaguchi F., Richards S., Beyreuther K., Salbaum M., Carlson G., Dunnett S. B. Transgenic mice for the amyloid precursor protein 695 isoform have impaired spatial memory. Neuroreport. 2:1991;781-784.
312. Yamamoto M., Ooyama M., Ozawa Y., Okada M., Tada S., Yamaguchi T., Endo H. Effects of indeloxazine hydrochloride, a cerebral activator, on passive avoidance learning impaired by disruption of cholinergic transmission in rats. Neuropharmacology. 32:1993;695-701.
313. Yamamoto M., Takahashi K., Ohyama M., Sasamata M., Yatsugi S., Okada M., Endoh H. Possible involvement of central cholinergic system in ameliorating effects of indeloxazine, a cerebral activator, on disturbance of learning behavior in rats. Progress in Neuropsychopharmacology and Biological Psychiatry. 18:1994;603-613.
314. Yankner B. A., Duffy L. K., Kirschner D. A. Neurotrophic and neurotoxic effects of amyloid β protein: Reversal by tachykinin neuropeptides. Science. 250:1990;279-282.
315. Yehuda S., Carraso R. L., Mostofsky D. I. Essential fatty acid preparation (SR-3) rehabilitates learning deficits induced by AF64A and 5:7-DHT. Neuroreport. 6:1995;511-515.