Cognitive function and its neural mechanisms in nonhuman primate models of aging, Alzheimer's disease, and menopause

Frontiers in Bioscience

Volumn 9, Issue , 2004, Pages 1899-1914

  Voytko, M L ^a   Tinkler, G P ^a  

^a WAKE FOREST SCHOOL OF MEDICINE   (United States)

Author keywords

Aging; Alzheimer's disease; Animal models; Attention; Cholinergic system; Functional imaging; Memory; Menopause; Monkeys; Review

Indexed keywords

ACETYLCHOLINESTERASE; ESTROGEN;

AGING; ALZHEIMER DISEASE; COGNITION; DEGENERATIVE DISEASE; ENZYME ACTIVITY; ESTROGEN DEFICIENCY; ESTROGEN THERAPY; LEARNING; MEMORY DISORDER; MENOPAUSAL SYNDROME; MENOPAUSE; MONKEY; NEUROBIOLOGY; NEUROPATHOLOGY; NONHUMAN; OVARIECTOMY; PHOTON EMISSION TOMOGRAPHY; PRIMATE; REVIEW; ANIMAL; ANIMAL MODEL; BIOLOGICAL MODEL; DISEASE MODEL; FEMALE; HUMAN; MACACA; PHYSIOLOGY;

ANIMALIA; PRIMATES;

AGING; ALZHEIMER DISEASE; ANIMALS; COGNITION; DISEASE MODELS, ANIMAL; FEMALE; HUMANS; MACACA MULATTA; MENOPAUSE; MODELS, ANIMAL; MODELS, NEUROLOGICAL;

EID: 2442676889     PISSN: 27686701     EISSN: 27686698     Source Type: Journal    
DOI: 10.2741/1370     Document Type: Review

References (141)

1. Walker, M.L: Menopause in female rhesus monkeys. Am J Primatol 35, 59-71 (1995)
2. Gilardi, K.V.K, S.E. Shideler, C.R. Valverde, J.A. Roberts and B.L. Lasley: Characterization of the onset of menopause in the rhesus macaque. Biol Reprod 57, 335-340 (1997)
3. Bellino, F. L and P.M. Wise: Nonhuman primate models of menopause workshop. Biol Reprod 68, 10-18 (2003)
4. Tigges, J., T.P. Gordon, H.M. McClure, E.C. Hall and A. Peters: Survival rate and life span of rhesus monkeys at the Yerkes Regional Primate Research Center. Amer J Primatol 15, 263-273 (1988)
5. Uno, H: Age-related pathology and biosenescent markers in captive rhesus macaques. Age 20, 1-13 (1997)
6. Cork, L.C. and L.C. Walker: Age-related lesions, Nervous System. In: Nonhuman Primates II. Eds: Jones T.C, Mohr U and Hunt R.D, Springer-Verlag, Berlin, 173-183 (1993)
7. Bachevalier, J., L.S. Landis, L.C. Walker, M. Brickson, M. Mishkin, D.L. Price and L.C. Cork: Aged monkeys exhibit behavioral deficits indicative of widespread cerebral dysfunction. Neurobiol Aging 12, 99-111 (1991)
8. Peters, A., D.L. Rosene, M.B. Moss, T.L. Kemper, C.R. Abraham, J. Tigges, and M.S. Albert: Neurobiological bases of age-related cognitive decline in the rhesus monkey. J Neuropathol Exp Neurol 55, 861-874 (1996)
9. Terasawa, E., T. E. Nass, R. R. Yeoman, M. D. Loose and N. J. Schultz: Hypothalamic control of puberty in the female rhesus macaque. In: Neuroendocrine Aspects of Reproduction. Ed: Norman RL, Academic Press, NY, 149-182 (1983)
10. rd International Conference. Eds: Delemarre-van de Waal HA, Plant TM, Van Rees GP and Schoemaker J, Elsevier, NY, 123-136 (1989)
11. Trotter, M., B.B. Hixon and S.S. Deaton: Sequential changes in weight of the skeleton and in length of long limb bones of Macaca mulatta. Am J Phys Anthropol 43, 79-93 (1975)
12. Welford, A.T: Motor skills and aging. In: The Aging Motor System, Advances in Neurogerontology, volume 3. Eds: Mortimer J.A, Pirozzolo FJ and Maletta GJ, Praeger Publishers, New York, 152-187 (1982)
13. Plude, D.J. and W.J. Hoyer: Attention and performance: identifying and localizing age deficits. In: Aging and Human Performance. Eds: Charness N, Wiley and Sons, New York, 47-99 (1985)
14. Poon, L.W: Differences in human memory with aging: nature, causes, and clinical implications. In: Handbook of the Psychology of Aging. Eds: Birren JE and Schaie KW, Van Nostrand Reinhold Co., New York, 427-462 (1985)
15. Albert, M.S: Cognitive Function. In: Geriatric Neuropsychology. Eds: Albert MS and Moss MB, Guilford Press, New York, 33-53 (1988)
16. Craik, F.I.M. and J.M. Jennings: Human memory. In: Handbook of Aging and Cognition. Eds: Craik FIM and Salthouse TA, Lawrence Erlbaum Assoc., New Jersey, 51-110 (1992)
17. Hartley, A.A: Attention. In: Handbook of Aging and Cognition. Eds: Craik FIM and Salthouse TA, Erlbaum Assoc., New Jersey, 3-49 (1992)
18. Voytko, M.L: Impairments in acquisition and reversal of two-choice discriminations by aged rhesus monkeys. Neurobiol Aging 20, 617-627 (1999)
19. Bartus, R.T., R.L. Dean and D.L. Fleming: Aging in the rhesus monkey: effects on visual discrimination learning and reversal learning. J Gerontol 34, 209-219 (1979)
20. Arnsten, A.F. and P.S. Goldman-Rakic: Catecholamines and cognitive decline in aged nonhuman primates. Ann NY Acad Sci 444, 218-234 (1985)
21. Moss, M.B., D.L. Rosene and A. Peters: Effects of aging on visual recognition memory in the rhesus monkey. Neurobiol Aging 9, 495-502 (1988)
22. Rapp, P.R: Visual discrimination and reversal learning in the aged monkey (Macaca mulatta). Behav Neurosci 104, 876-884 (1990)
23. Lai, Z.C., M.B. Moss, R.J. Killiany, D.L. Rosene and J.G. Herndon: Executive system dysfunction in the aged monkey: spatial and object reversal learning. Neurobiol Aging 16, 947-954 (1995)
24. Botwinick, J: Aging and Behavior. Springer Publishing Co., New York (1978)
25. Davis, R.T: Old monkey behavior. Exp Gerontol 13, 237-250 (1978)
26. Moore, T. L., R.J. Killiany, J.G. Herndon, D.L. Rosene and M.B. Moss: Impairment in abstraction and set shifting in aged rhesus monkeys. Neurobiol Aging 24, 125-134 (2003)
27. Fristoe, N.M., T.A. Salthouse and J. L. Woodward: Examination of age-related deficits on the Wisconsin Card Sorting task. Neuropsychology 11, 428-436 (1997)
28. Medin, D.L: Form perception and pattern reproduction in monkeys. J Comp Physiol Psychol 68, 412-419 (1969)
29. Bartus, R.T., D. Fleming and H. R. Johnson: Aging in the rhesus monkey: debilitating effects on short-term memory. J Gerontol 33, 858-871 (1978)
30. Marriott, J.G. and J.S. Abelson: Age differences in short-term memory of test-sophisticated rhesus monkeys. Age 3, 7-9 (1980)
31. Rapp, P.R. and D.G. Amaral: Evidence for task-dependent memory dysfunction in the aged monkey. J Neurosci 9, 3568-3576 (1989)
32. Flicker, C. R.T., Bartus, T.H. Crook and S.H. Ferris: Effects of aging and dementia upon recent visuospatial memory. Neurobiol Aging 5, 275-283 (1984)
33. Voytko, M.L: Cognitive changes during normal aging in monkeys assessed with an automated test apparatus. Neurobiol Aging 14, 634-644 (1993)
34. Davis, R.T., C. A. Bennett and W.P. Weisenburger: Repeated measurements of forgetting by rhesus monkeys (macaca mulatta). Percept Mot Skills 55, 703-709 (1982)
35. Craik, F. I. M., M. Byrd and J. M. Swanson: Patterns of memory loss in three elderly samples. Psychol Aging 2, 79-86 (1987)
36. West, R.L., T.H. Crook and K.L. Barron: Everyday memory performance across the life span: effects of age and noncognitive individual differences. Psychol Aging 7, 72-82 (1992)
37. Zelinski, E.M., M.J. Gilewski and K.W. Schaie: Individual differences in cross-sectional and 3-year longitudinal memory performance across the adult life span. Psychol Aging 8, 176-186 (1993)
38. Morse, C.K: Does variability increase with age? An archival study of cognitive measures. Psychol Aging 8, 156-164 (1993)
39. Schneider, N.G., E.R. Gritz, and M.E. Jarvik: Age differences in simple paced tasks of attention and perception. Gerontology 23, 142-147 (1977)
40. Ponds, R.W.H.M., W.H. Vrouwer and P.C. van Wolffelaar: Age differences in divided attention in a simulated driving task. J Gerontol Psychol Sci 43, 151-156 (1988)
41. McDowd, J.M and J.E. Birren: Aging and attentional processes. In: Handbook of the Psychology of Aging, third edition. Eds: Birren JE and Schaie, KW, Academic Press, New York, 222-233 (1990)
42. Hartley, A.A., J.M. Kieley and E.H. Slabach: Age differences and similarities in the effects of cues and prompts. J Exp Psychol Human Perception Performance 16, 523-537 (1990)
43. Greenwood, P.M., R. Parasuraman and J.V. Haxby: Changes in visuospatial attention over the adult lifespan. Neuropsychologia 31, 471-485 (1993)
44. Davis, R.T: Monkeys as perceivers. In: Primate Behavior: Developments in the Field and Laboratory Research, volume 3. Eds: Rosenblum LA, Academic Press, New York (1974)
45. Posner, M.I: Orienting of attention. Quart J Exp Psychol 32, 3-25 (1980)
46. Posner, M.I. and Y. Cohen: Components of visual orienting. In: Attention and Performance X: Control of Language Processes. Eds: Bouma H and Bowhuis DG. New Jersey, Lawrence Erlbaum Assoc, New Jersey, 531-556 (1984)
47. Robinson, D.L. and C. Kertzman: Visuospatial attention: effects of age, gender, and spatial reference. Neuropsychologia 28, 291-301 (1990)
48. Folk, C.L. and W.J. Hoyer: Aging and shifts of visual spatial attention. Psychol Aging 7, 453-463 (1992)
49. Madden, D.J: Adult age differences in the time course of visual attention. J Gerontol Psychol Sci 45, 9-16 (1994)
50. Baxter, M.G. and M.L. Voytko: Spatial orienting of attention in adult and aged rhesus monkeys. Behav Neurosci 110, 898-904 (1996)
51. Davis, R.T. and F.T. Ruggiero: Memory in monkeys as a function of preparatory interval and pattern complexity of matrix displays. Amer J Phys Anthropol 38, 573-577 (1973)
52. Gottsdanker, R: Age and simple reaction time. J Gerontol 37, 342-348 (1982)
53. Stuss, D.T., L.L. Stethem, T.W. Picton, E.E. Leech and G. Pelchat: Traumatic brain injury, aging and reaction time. Can J Neurol Sci 16, 161-167 (1989)
54. Light, K.E: Information processing for motor performance in aging adults. Phys Ther 70, 820-826 (1990)
55. Voytko, M.L: Functional and neurobiological similarities of aging in monkeys and humans. Age 20, 29-44 (1997)
56. Voytko, M.L: Nonhuman primates as models for aging and alzheimer's disease. Lab Anim Sci 48, 611-617 (1998)
57. Voytko, M.L, D.S. Olton, R.T. Richardson, L.K. Gorman, J.R. Tobin and D.L. Price: Basal forebrain lesions in monkeys disrupt attention but not learning and memory. J Neurosci 14, 167-186 (1994)
58. Everitt, B.J and T.W. Robbins: Central cholinergic systems and cognition. Ann Rev Psychol 48, 649-684 (1997)
59. Sarter, M. and J.P. Bruno: Cognitive functions of cortical acetylcholine: toward a unifying hypothesis. Brain Res Rev 23, 28-46 (1997)
60. Baxter, M.G. and A.A. Chiba: Cognitive functions of the basal forebrain. Curr Opin Neurobiol 9, 178-83 (1999)
61. Mesulam, M.-M, E.J. Mufson, A.I. Levey and B.H. Wainer: Cholinergic innervation of cortex by the basal forebrain: cytochemistry and cortical connections of the septal area, diagonal band nuclei, nucleus basalis (substantia innominata), and hypothalamus in the rhesus monkey. J Comp Neurol 214, 170-197 (1983)
62. Saper, C.B: Organization of cerebral cortical afferent systems in the rat. I. Magnocellular basal nucleus. J Comp Neurol 222, 313-342 (1984)
63. Voytko, M.L., R.R. Sukhov, L.C. Walker, S.L. Breckler, D.L. Price and V.E. Koliatsos: Neuronal number and size are preserved in the nucleus basalis of aged rhesus monkeys. Dementia 6, 131-141 (1995)
64. Presty, S.K., J. Bachevalier, L.C. Walker, R.G. Struble, D.L. Price, M. Mishkin and L.C. Cork: Age differences in recognition memory of the rhesus monkeys (macaca mulatta). Neurobiol Aging 8, 435-440 (1987)
65. Parsons, S.M., C. Prior and I.G. Marshall: Acetylcholine transport, storage and release. Int Rev Neurobiol 35, 279-390 (1993)
66. Parsons, S.M. and G. Rogers: In vivo diagnostics for Alzheimer's disease based on the acetylcholine transporter. Ann Reports Med Chem 28, 247-255 (1993)
67. Efange, S.M.N, R.H. Mach, A. Khare, R.H. Michelson, P.A. Nowak and P.H. Evora: p-[18F] Fluorobenzyltrozamicol ([18F] FBT): molecular decomposition-reconstitution approach to vesamicol receptor radioligands for positron emission tomography. App Radiat Isot 45, 465-472 (1994)
68. Efange, S.M.N., R.H. Mach, C.R. Smith, A.B. Khare, C. Foulon, S.K. Akella, S.R. Childers and S.M. Parsons: Vesamicol analogues as sigma ligands. Molecular determinants of selectivity at the vesamicol receptor. Biochem Pharmacol 49, 791-797 (1995)
69. Efange, S.M., E.M. Garland, J.K. Staley, A.B. Khare and D.C. Mash: Vesicular acetylcholine transporter density and Alzheimer's disease. Neurobiol Aging 18, 407-13 (1997)
70. Mach, R.H., M.L. Voytko, R.L.E. Ehrenkaufer, M.A. Nader, J.R. Tobin, S.M.N. Efange, S.M. Parsons, H.D. Gage, C.R. Smith and E.T. Morton: Imaging of cholinergic terminals using the radiotracer [18F] 4-fluorobenzyltrozamicol. In vitro binding studies and positron emission tomography studies in nonhuman primates. Synapse 25, 68-380 (1997)
71. Quirion, R: Characterization and autoradiographic distribution of hemicholinium-3 high-affinity choline uptake sites in mammalian brain. Synapse 1, 293-303 (1987)
72. Ingvar, M., S. Stone-Elander, G.A. Rogers, B. Johansson, L. Eriksson, S.M. Parsons and L. Widen: Striatal D2/acetylcholine interactions: PET studies of the vesamicol receptor. Neuroreport 4, 1311-1314 (1993)
73. Mulholland, G.K., Y.-W. Jung, D.M. Wieland, M.R. Kilbourn and D.E. Kuhl: Synthesis of [18F] fluoroethoxybenzovesamicol, a radiotracer for cholinergic neurons. J Labelled Comp Radiopharm 33, 583-591 (1993)
74. Jung, Y.-W., D.L. Gildersleeve, M.E. Van Dort, D.E. Kuhl and D.M. Wieland: Synthesis and in vivo evaluation of radioiodinated (+)-7- iodobenzvesamicol: a high affinity ligand for the sigma binding site. J Labelled Comp Radiopharm 35, 202-204 (1994)
75. Kuhl, D. E., R.A. Koeppe, J.A. Fessier, S. Minoshima, R.J. Ackermann, J.E. Carey, D.L. Gildersleeve, K.A. Frey and D.M. Wieland: In vivo mapping of cholinergic neurons in the human brain using SPECT and IBVM. J Nucl Med 35, 405-410 (1994)
76. Voytko, M.L., R.H. Mach, R.L.E. Ehrenkaufer, H.D. Gage, S.M.N. Efange and J.R. Tobin: Cholinergic activity of aged rhesus monkeys revealed by PET. Synapse 39, 95-100 (2001)
77. Bartus, R.T., R.L. Dean RL, B. Beer and A.S. Lippa: The cholinergic hypothesis of geriatric memory dysfunction. Science 217, 408-14 (1982)
78. Bartus, R.T: On neurodegenerative diseases, models, and treatment strategies: lessons learned and lessons forgotten a generation following the cholinergic hypothesis. Exp Neurol 163, 495-529 (2000)
79. Voytko, M.L: Cognitive functions of the basal forebrain cholinergic system in monkeys: memory or attention? Behav Brain Res 75, 13-25 (1996)
80. Freed, D.M., S. Corkin, J.H. Growdon and M.J. Nissen: Selective attention in Alzheimer's disease: characterizing cognitive subgroups of patients. Neuropsychologia 27, 325-339 (1989)
81. Parasuraman, R., P.M. Greenwood, J.V. Haxby and C.L. Grady: Visuospatial attention in dementia of the Alzheimer type. Brain 115, 711-733 (1992)
82. Oken, B.S., S.S. Kishiyama, J.A. Kaye and D.B. Howieson: Attention deficit in Alzheimer's disease is not simulated by an anticholinergic/ antihistaminergic drug and is distinct from deficits in healthy aging. Neurology 44, 657-662 (1994)
83. Sunderland, T., P.N. Tariot, E.A. Mueller, D.L. Murphy, H. Weingartner and R.M. Cohen: Cognitive and behavioral sensitivity to scopolamine in Alzheimer patients and controls. Psychopharmacology Bull 21, 676-679 (1985)
84. Sunderland, T., P.N. Tariot, D.L. Murphy, H. Weingartner, E.A. Mueller and R.M. Cohen: Scopolamine challenges in Alzheimer's disease. Psychopharmacology 87, 247-249 (1985)
85. Sunderland, T., P.N. Tariot, R.M. Cohen, H. Weingartner, E.A. Mueller and D.L. Murphy: Anticholinergic sensitivity in patients with dementia of the Alzheimer type and age-matched controls. A dose-response study. Arch Gen Psychiatry 44, 418-26 (1987)
86. Aigner, T.G., S.J. Mitchell, J.P. Aggleton, M.R. DeLong, R.G. Struble, D.L. Price, G.L. Wenk, K.D. Pettigrew and M. Mishkin: Transient impairment of recognition memory following ibotenic-acid lesions of the basal forebrain in macaques. Exp Brain Res 86, 18-26 (1991)
87. Ridley, R. M., H. F. Baker and T. K Murray: Basal nucleus lesions in monkeys: recognition memory impairment or visual agnosia? Psychopharmacology 95, 289-290 (1988)
88. Ridley, R. M, T. K. Murray, J. A. Johnson and H.F. Baker: Learning impairment following lesion of the basal nucleus of Meynert in the marmoset: modification by cholinergic drugs. Brain Res 376, 108-116 (1986)
89. Ridley, R.M., H.F. Baker, B. Drewett and J.A. Johnson: Effects of ibotenic acid lesions of the basal forebrain on serial reversal learning in marmosets. Psychopharmacology 86, 438-443 (1985)
90. Roberts, A.C., T.W. Robbins, B.J. Everitt, G.H. Jones, T.E. Sirkia, J. Wilkinson and K. Page: The effects of excitoxic lesions of the basal forebrain on the acquisition, retention and serial reversal of visual discriminations in marmosets. Neuroscience 34, 311-329 (1990)
91. Haskell, S.G., E. D. Richardson and R.I. Horwitz: The effect of estrogen replacement therapy on cognitive function in women: A critical review of the literature. J Clin Epidemiol 50, 1249-1264 (1997)
92. Rice, M.M., A. B. Graves, S.M. McCurry and E.B. Larson: Estrogen replacement therapy and cognitive function in postmenopausal women without dementia. Am J Med 103, 26S-35S (1997)
93. Yaffe, K., G. Sawaya, I. Lieberburg and D.Grady: Estrogen therapy in postmenopausal women. JAMA 279, 688-695 (1998)
94. Hogervorst, E., J. Williams, M. Budge, W. Riedel and J.Jolles: The nature of the effect of female gonadal hormone replacement therapy on cognitive function in post-menopausal women: a meta-analysis. Neuroscience 101, 485-512 (2000)
95. LeBlanc, E.S., J. Janowsky, B.K.S. Chan and H.D. Nelson: Hormone replacement therapy and cognition: A systematic review and meta-analysis. JAMA 285, 1489-1499 (2001)
96. Jewitt, D.A. and W.R. Dukelow, W.R: Cyclicity and gestation length of Macaca fascicularis. Primates 13, 327-330 (1972)
97. Goodman, A.L., C.D. Descalzi, D.K. Johnson and G.D. Hodgen: Composite pattern of circulating LH, FSH, estradiol, and progesterone during the menstrual cycle in cynomolgus monkeys. Proc Soc Exp Biol and Med 155, 479-481 (1977)
98. Johnson, R.L. and E. Kapsalis: Ageing, infecundity, and reproductive senescence in free-ranging female rhesus monkeys. Journal of Repro Fertil 105, 271-278 (1995)
99. Adams, M.R., J.R. Kaplan, S.B. Manuck, D.R. Koritnik, J.S. Parks, M.S.Wolfe and T.B.Clarkson: Inhibition of coronary artery atherosclerosis by 17-beta estradiol in ovariectomized monkeys: Lack of an effect of added progesterone. Arteriosclerosis 10, 1051-1057 (1990)
100. Jerome, C.P., C.S. Carlson, T.C. Register, F.T. Bain, M.J. Jayo, D.S.Weaver and M.R. Adams: Bone functional changes in intact, ovariectomized, hormone-supplemented adult cynomolgus monkeys (Macaca fascicularis) evaluated by serum markers and dynamic histomorphometry. Journal of Bone Miner Res 9, 527-540 (1994)
101. Jayo, M.J., T.C. Register and C.S. Carlson: Effects on bone of oral hormone replacement therapy initiated 2 years after ovariectomy in young adult monkeys. Bone 23, 361-355 (1998)
102. Steger, R.W. and J. J. Peluso: Sex hormones in the aging female. Endocrinlogy Metabol Clinics 16, 1027-1043 (1987)
103. Voytko, M.L: The effects of long-term ovariectomy and estrogen replacement therapy on learning and memory in monkeys. Behav Neurosci 114, 1078-1087 (2000)
104. Voytko, M.L: Estrogen and the cholinergic system modulate visuospatial attention in monkeys. Behav Neurosci 116, 187-197 (2002)
105. Lacreuse, A. and J.G. Herndon: Estradiol selectively affects processing of conspecifics' faces in female rhesus monkeys. Psychoneuroendocrinology 28, 885-905 (2003)
106. Vanhulle, G. and R Demol: A double-blind study into the influence of estriol on a number of pscyhological tests in post-menopausal women. In: Concensus on Menopause Research. Eds: van Keep PA, Greenblatt RB, Albeaux-Funet M, MTP Press, London, UK, 94-99 (1976)
107. Fedor-Freybergh, P: The influence of oestrogens on the wellbeing and mental performance in climacteric and postmenopausal women. In: Acta Obstetricia et Gynecologica Scandinavica Eds: Ingelman-Sundberg A and Joelsson I, The Scandinavian Association of Obstetricians and Gynaecologists, Stockholm, Sweden, Suppl 64, 1-91 (1977)
108. Sherwin, B.B: Estrogen and/or androgen replacement therapy and cognitive functioning in surgically menopausal women. Psychoneuroendocrinology 13, 345-357 (1988)
109. Schmidt, R., F. Fazekas, B. Reinhart, P. Kapeller, G. Fazekas, H. Offenbacher, B. Eber, M. Schumacher and W. Freidl: Estrogen replacement therapy in older women: a neuropsychological and brain MRI study. J Am Geriatr Soc 44, 1307-1313 (1996)
110. Matthews, K., J. Cauley, K. Yaffe and J.M. Zmuda: Estrogen replacement therapy and cognitive decline in older community women. J Am Geriatr Soc 47, 518-523 (1999)
111. Smith, Y.R., B. Giordani, R. Lajiness-O'Neil and J.-K, Zubieta: Long-term estrogen replacement is associated with improved nonverbal memory and attentional measures in postmenopausal women. Fertil Steril 76, 1101-1107 (2001)
112. Keenan, P.A., W.H. Ezzat, K. Ginsburg and G.J. Moore: Prefrontal cortex as the site of estrogen's effect on cognition. Psychoneuroendocrinology 26, 577-590 (2001)
113. Packard, M.G. and L.A. Teather: Posttraining estradiol injections enhance memory in ovariectomized rats: cholinergic blockade and synergism. Neurobiol Learn Mem 68, 172-188 (1997)
114. Luine, V.N., S.T. Richards, V.Y. Wu and K.D. Beck: Estradiol enhances learning and memory in a spatial memory task and effects levels of monoaminergic neurotransmitters. Horm Behav 34, 149-162 (1998)
115. Fader, A.J., P.E.M. Johnson and G.P. Dohanich: Estrogen improves working but not reference memory and prevents amnestic effects of scopolamine on a radial-arm maze. Pharmacol Biochem Behav 62, 711-717 (1999)
116. Bimonte, H.A. and V.H. Denenberg: Estradiol facilitates performance as working memory load increases. Psychoneuroendocrinology 24, 161-173 (1999)
117. Watanabe, T. and H. Niki: Hippocampal unit activity and delayed response in the monkey. Brain Res 325, 241-254 (1985)
118. Cahusac, P.B.B., Y. Miyashita and E.T. Rolls: Responses of hippocampal formation neurons in the monkey related to delayed spatial response and object-place memory tasks. Behav Brain Res 33, 229-240 (1989)
119. Nishijo, H.T., Ono, S. Eifuku and R. Tamura: The relationship between monkey hippocampus place-related neural activity and action in space. Neurosci Lett 226, 57-60 (1997)
120. Matsumura, N., H. Nishijo, R. Tamura, S. Eifuku, S. Endo and T. Ono: Spatial- and task-dependent neuronal response during real and virtual translocation in the monkey hippocampal formation. J Neurosci 19, 2381-2393 (1999)
121. Gibbs, R.B: Estrogen replacement enhances acquisition of a spatial memory task and reduces deficits associated with hippocampal muscarinic receptor inhibition. Horm Behav 36, 222-233 (1999)
122. Roberts, J.A., K.V.K. Gilardi, B. Lasley and P.R. Rapp: Reproductive senescence predicts cognitive decline in aged female monkeys. NeuroReport 8, 2047-2051 (1997)
123. Rapp, P.R., J.H. Morrison and J.A. Roberts: Cyclic estrogen replacement improves cognitive function in aged ovariectomized rhesus monkeys. J Neurosci 23, 5708-5714 (2003)
124. Tinkler, G.P. and M.L.Voytko: Multiple cognitive domains are affected by estrogen state in middle-aged surgically-menopausal monkeys. Soc Neurosci Abstr 26, 1745 (2000)
125. Lacreuse, A., J.G. Herndon and M.B. Moss: Cognitive function in aged ovariectomized female rhesus monkeys. Behav Neurosci 114, 506-513 (2000)
126. Lacreuse, A., M.E. Wilson and J.G. Herndon: Estradiol, but not raloxifene, improves aspects of spatial working memory in aged ovariectomized rhesus monkeys. Neurobiol Aging 23, 589-600 (2002)
127. Dohanich, G.P., A.J. Fader and D.J. Javorsky: Estrogen and estrogen-progesterone treatments counteract the effect of scopolamine on reinforced t-maze alternation in female rats. Behav Neurosci 108, 988-992 (1994)
128. Fader, A.J., A. W. Hendricson and G.P. Dohanich: Estrogen improves performance of reinforced t-maze alternation and prevents the amnestic effects of scopolamine administered systemically or intrahippocampally. Neurobiol Learn Mem 69, 225-240 (1998)
129. Gibbs, R.B., A. M. Burke and D.A. Johnson: Estrogen replacement attenuates effects of scopolamine and lorazepam on memory acquisition and retention. Horm Behav 34, 112-125 (1998)
130. Kritzer, M.F. and S.G. Kohama: Ovarian hormones differentially influence immunoreactivity for dopamine beta-hydroxylase, choline actetyltransferase, and serotonin in the dorsolateral prefrontal cortex of adult rhesus monkeys. J Comp Neurol 409, 438-451 (1999)
131. Tinkler, G.P., J.R. Tobin and M.L. Voytko: Effects of two years estrogen loss or replacement on nucleus basalis cholinergic neurons and cholinergic fibers to dorsolateral prefrontal and inferior parietal cortex of monkeys. J Comp Neurol (in press)
132. Gibbs, R.B: Effects of gonadal hormone replacement on measures of basal forebrain cholinergic function. Neuroscience 101, 931-8 (2000)
133. Gibbs, R.B., D. Nelson, M.S. Anthony and T.B. Clarkson: Effects of long-term hormone replacement and of tibolone on choline acetyltransferase and acetylcholinesterase activities in the brains of ovariectomized, cynomolgus monkeys. Neuroscience 113, 907-14 (2002)
134. Resnick, S.M., P.M. Maki, S. Golski, M.A. Kraut and A.B. Zonderman: Effects of estrogen replacement therapy on PET cerebral blood flow and neuropsychological performance. Horm Behav 34, 171-182 (1998)
135. Shaywitz, S.E., B.A. Shaywitz, K.R. Pugh, R.K. Fulbright, P. Skudlarski, W.E. Mencl, R.T. Constable, F. Naftolin, S.F. Palter, K.E. Marchione, L. Katz, D.P. Shankweiler, J.M. Fletcher, C. Lacadie, M. Keltz and J.C. Gore: Effect of estrogen on brain activation patterns in postmenopausal women during working memory tasks. JAMA 281, 1197-1202 (1999)
136. Maki, P.M. and S.M. Resnick: Longitudinal effects of estrogen replacement therapy on PET cerebral blood flow and cognition. Neurobiol Aging 21, 373-83 (2000)
137. Smith, Y.R., S. Minoshima, D.E. Kuhl and J-K Zubieta: Effects of long-term hormone therapy on cholinergic synaptic concentrations in healthy postmenopausal women. J Clin Endocrinol Metab 86, 679-684 (2001)
138. Davidson, M. C., E. B. Cutrell and R.T. Marrocco: Scopolamine slows the orienting of attention in primates to cued visual targets. Psychopharmacology 142, 1-8 (1999)
139. Witt, E. A., M. C. Davidson and R.T. Marrocco: Effects of altering brain cholinergic activity on covert orienting of attention: Comparison of monkey and human performance. Psychopharmacology 132, 324-334 (1997)
140. Gabor, R., R. Nagle, D.A. Johnson, and R.B. Gibbs: Estrogen enhances potassium-stimulated acetylcholine release in the rat hippocampus. Brain Res 962, 244-7 (2003)
141. Voytko, M.L: Bridging the gap between animal and human cognitive testing. In: Alzheimer's Disease and Related Disorders: Research Advances. Eds: K Iqbal and B Winblad, (in press)