Sex dimorphisms in the rate of age-related decline in spatial memory: Relevance to alterations in the estrous cycle

Journal of Neuroscience

Volumn 19, Issue 18, 1999, Pages 8122-8133

  Markowska, Alicja L ^a  

^a JOHNS HOPKINS UNIVERSITY   (United States)

Author keywords

Aging; Estrogen; Estrous cycle; Fischer 344 rats; Sex dimorphism; Spatial memory

Indexed keywords

AGING; ANIMAL EXPERIMENT; ARTICLE; ESTRUS CYCLE; FEMALE; MALE; NONHUMAN; PRIORITY JOURNAL; RAT; SENSORIMOTOR FUNCTION; SEX DIFFERENCE; SPATIAL MEMORY; WORKING MEMORY;

EID: 0033568869     PISSN: 02706474     EISSN: None     Source Type: Journal    
DOI: 10.1523/jneurosci.19-18-08122.1999     Document Type: Article

References (78)

1. Archer J (1979) Inbreeding and sex differences in rats and mice: a rejoinder to Gray. Br J Psychol 70:37.
2. Beatty WW (1979) Gonadal hormones and sex differences in nonreproductive behaviors in rodents: organizational and activational influences. Horm Behav 12:112-163.
3. Berger-Sweeney J, Arnold A, Gabeau D, Mills J (1995) Sex differences in learning and memory in mice: effects of sequence of testing and cholinergic blockade. Behav Neurosci 109:859-873.
4. Bucci DJ, Chiba AA, Gallagher M (1995) Spatial learning in male and female Long-Evans rats. Behav Neurosci 109:180-183.
5. Coleman PD, Finch CE, Joseph JA (1990) The need for multiple time points in aging studies. Neurobiol Aging 11:1-2.
6. Collins DW, Kimura D (1997) A large sex difference on a two-dimensional mental rotation task. Behav Neurosci 111:845-849.
7. Crook T, Bartus RT, Ferris SH, Whitehouse P, Cohen GD, Gershon S (1986) Age-associated memory impairment: proposed diagnostic criteria and measures of clinical change - report of a National Institute of Mental Health work group. Dev Neuropsychol 2:261-276.
8. Davis S, Markowska AL, Wenk GL, Barnes CA (1993) Acetyl-L-carnitine: behavioral, electrophysiological, and neurochemical effects. Neurobiol Aging 14:107-115.
9. Delgado AR, Prieto G (1996) Sex differences in visuospatial ability: do performance factors play such an important role? Mem Cognit 24:504-510.
10. Dudley SD (1982) Responsiveness to estradiol in central nervous system of aging female rats. Neurosci Biobehav Rev 6:39-45.
11. a concentration. PEPI investigators. Post-menopausal estrogen/progestin interventions. Circulation 97:979-986.
12. Finch CE, Felicio LS, Mobbs CV, Nelson JF (1984) Ovarian and steroidal influences on neuroendocrine aging processes in female rodents. Endocr Rev 5:467-497.
13. Fischer W, Chen KS, Gage FH, Bjorklund A (1991) Progressive decline in spatial learning and integrity of forebrain cholinergic neurons in rats during aging. Neurobiol Aging 13:9-23.
14. Frick KM, Baxter MG, Markowska AL, Olton DS, Price DL (1995) Age-related spatial reference and working memory deficits assessed in the water maze. Neurobiol Aging 16:149-160.
15. Gage FH, Dunnett SB, Bjorklund A (1989) Age-related impairments in spatial memory are independent of those in sensorimotor skills. Neurobiol Aging 10:347-352.
16. Gallagher M, Burwell RD (1989) Relationship of age-related decline across several behavioral domains. Neurobiol Aging 10:691-708.
17. Gallagher M, Pelleymounter M-A (1988) An age-related spatial learning deficit: choline uptake distinguishes "impaired" and "unimpaired" rats. Neurobiol Aging 9:363-369.
18. Garcia-Segura LM, Chowen JA, Parducz A, Naftolin F (1994) Gonadal hormones as promoters of structural synaptic plasticity: cellular mechanisms. Prog Neurobiol 44:279-307.
19. Gaulin SJ, FitzGerald RW, Wartell MS (1990) Sex differences in spatial ability and activity in two vole species (Microtus ochrogaster and M. pennsylvanicus). J Comp Psychol 104:88-93.
20. Gazzaley AH, Weiland NG, McEwen BS, Morrison JH (1996) Differential regulation of NMDAR1 and mRNA and protein by estradiol in the rat hippocampus. J Neurosci 16:6830-6838.
21. Geinisman Y, de Toledo-Morrell L, Morrell F (1986) Aged rats need a preserved complement of perforated axospinous synapses per hippocampal neuron to maintain good spatial memory. Brain Res 398:266-275.
22. Gibbs RB (1996) Expression of estrogen receptor-like immunoreactivity by different subgroups of basal forebrain cholinergic neurons in gonadectomized male and female rats. Brain Res 720:61-68.
23. Gibbs RB, Pfaff DW (1992) Effects of estrogen and fimbria/fornix transection on p75NGFR and ChAT expression in the medial septum and diagonal band of Broca. Exp Neurol 116:23-39.
24. Gibbs RB, Wu D, Hersh LB, Pfaff DW (1994) Effects of estrogen replacement on the relative levels of choline acetyltransferase, trkA, and nerve growth factor messenger RNAs in the basal forebrain and hippocampal formation of adult rats. Exp Neurol 129:70-80.
25. Gould E, Woolley CS, Frankfurt M, McEwen BS (1990) Gonadal steroids regulate dendritic spine density in hippocampal pyramidal cells in adulthood. J Neurosci 10:1286-1291.
26. Grinnell D, Markowska AL (1998) Ovarian steroid deficiency results in delayed memory impairment. Soc Neurosci Abstr 24:1848.
27. Halpern DF (1986) Sex differences in cognitive abilities. Hillsdale, NJ: Erlbaum.
28. Ingram DK (1988) Motor performance variability during aging in rodents. Ann NY Acad Sci 515:70-96.
29. Jarvik LF (1975) Human intelligence: sex differences. Acta Genet Med Gemellol (Rome) 24:189-211.
30. Juraska JM, Henderson C, Muller J (1984) Differential rearing experience, gender, and radial maze performance. Dev Psychol 17:209-215.
31. Kadar T, Silbermann M, Brandeis R, Levy A (1990) Age-related structural changes in the rat hippocampus: correlation with working memory deficiency. Brain Res 512:113-120.
32. Kampen DL, Sherwin BB (1996) Estradiol is related to visual memory in healthy young men. Behav Neurosci 110:613-617.
33. Kimura D, Hampson E (1994) Cognitive pattern in men and women is influenced by fluctuations in sex hormones. Curr Dir Psychol Sci 3:57-61.
34. Krasnoff A, Weston LM (1976) Puberal status and sex differences: activity and maze behavior in rats. Dev Psychobiol 9:261-269.
35. LeFevre J, McClintock MK (1988) Reproductive senescence in female rats: a longitudinal study of individual differences in estrous cycles and behavior. Biol Reprod 38:780-789.
36. LeFevre J, McClintock MK (1991) Isolation accelerates reproductive senescence and alters its predictors in female rats. Horm Behav 25:258-272.
37. Lindner MD (1997) Reliability, distribution, and validity of age-related cognitive deficits in the Morris water maze. Neurobiol Learn Mem 68:203-220.
38. Linn MC, Petersen AC (1985) Emergence and characterization of sex differences in spatial ability: a meta-analysis. Child Dev 56:1479-1498.
39. Luine VN (1997) Steriod hormone modulation of hippocampal dependent spatial memory. Stress 2:21-36.
40. Luine V, Rodriguez M (1994) Effects of estradiol on radial arm maze performance of young and aged rats. Behav Neural Biol 62:230-236.
41. Maren S, De Oca B, Fanselow MS (1994) Sex differences in hippocampal long-term potentiation (LTP) and Pavlovian fear conditioning in rats: positive correlation between LTP and contextual learning. Brain Res 661:25-34.
42. Markowska AL (1999) Life-long diet restriction failed to retard cognitive aging in Fischer-344 rats. Neurobiol Aging, in press.
43. Markowska AL, Breckler S (1999) Behavioral biomarkers of aging: an illustration of the multivariate approach for detecting age-related behavioral changes. J Gerontol, in press.
44. Markowska AL, Stone WS, Ingram DK, Reynolds J, Gold PE, Conti LH, Pontecorvo MJ, Wenk GL, Olton DS (1989) Individual differences in aging: behavioral and neurobiological correlates. Neurobiol Aging 10:31-43.
45. Markowska AL, Long JM, Johnson CT, Olton DS (1993) Variable-interval probe test as a tool for repeated measurements of spatial memory in the water maze. Behav Neurosci 107:627-632.
46. Markowska AL, Koliatsos VE, Breckler SJ, Price DL, Olton DS (1994) Human nerve growth factor improves spatial memory in aged but not in young rats. J Neurosci 14:4815-4824.
47. Markowska AL, Price D, Koliatsos VE (1996) Selective effects of nerve growth factor on spatial recent memory as assessed by a delayed nonmatching-to-position task in the water maze. J Neurosci 16:3541-3548.
48. Markus EJ, Zecevic M (1997) Sex differences and estrous cycle changes in hippocampus-dependent fear conditioning. Psychobiology 25:246-252.
49. McEwen BS, Alves SE, Bulloch K, Weiland NG (1997) Ovarian steroids and the brain: implications for cognition and aging. Neurology 48:S8-S15.
50. Means LW, Kennard KJP (1991) Working memory and the aged rat; deficient two-choice win-stay water-escape acquisition and retention. Physiol Behav 49:301-307.
51. Means LW, Alexander SR, O'Neal MF (1992) Those cheating rats: male and female rats use odor trails in a water-escape "working memory" task. Behav Neural Biol 58:144-151.
52. Mishima N, Higashitani F, Teraoka K, Yoshioka R (1986) Sex differences in appetitive learning of mice. Physiol Behav 37:263-268.
53. Olton DS, Papas BC (1979) Spatial memory and hippocampal function. Neuropsychologia 17:669-682.
54. Olton DS, Shapiro ML (1992) Mnemonic dissociation: the power of parameters. J Cogn Neurosci 4:200-227.
55. Olton DS, Markowska AL, Breckler SJ, Wenk GL, Pang K, Koliatsos VE, Price DL (1991) Individual differences in aging: behavioral and neural analyses. Biomed Environ Sci 4:166-172.
56. Perry EK (1986) The cholinergic hypothesis - ten years on. Br Med Bull 42:63-69.
57. Price DL, Sisodia SS (1994) Cellular and molecular biology of Alzheimer's disease and animal models. Annu Med Rev 45:435-446.
58. Rapp PR, Kansky MT, Roberts JA (1997) Impaired spatial information processing in aged monkeys with preserved recognition memory. NeuroReport 8:1923-1928.
59. Roberts JA, Guard KVK, Lasley B, Rapp PR (1997) Reproductive senescence predicts cognitive decline in aged female monkeys. NeuroReport 8:2047-2051.
60. Roof RL (1993) Neonatal exogenous testosterone modifies sex difference in radial arm and Morris water maze performance in prepubescent and adult rats. Behav Brain Res 53:1-10.
61. Sherwin BB (1994) Estrogenic effects on memory in women. Ann NY Acad Sci 743:213-230.
62. Sherwin BB (1997) Estrogen effects on cognition in menopausal women. Neurology 48:S21-S26.
63. Sherwin BB (1998a) Cognitive assessment for postmenopausal women and general assessment of their mental health. Psychopharmacol Bull 34:323-326.
64. Sherwin BB (1998b) Estrogen and cognitive functioning in women. Proc Soc Exp Biol Med 217:17-22.
65. Sherwin BB, Tulandi T (1996) "Add-back" estrogen reverses cognitive deficits induced by a gonadotropin-releasing hormone agonist in women with leiomyomata uteri [see comments]. J Clin Endocrinol Metab 81:2545-2549.
66. Simpkins JW, Singh M, Bishop J (1994) The potential role of estrogen replacement therapy in the treatment of the cognitive decline and neurodegeneration associated with Alzheimer's disease. Neurobiol Aging 15:S195-S197.
67. Singh M, Meyer EM, Millard WJ, Simpkins JW (1994) Ovarian steroid deprivation results in a reversible learning impairment and compromised cholinergic function in female Sprague Dawley rats. Brain Res 644:305-312.
68. Terry RD, Katzman R (1983) Senile dementia of the Alzheimer type. Ann Neurol 14:497-506.
69. Toran-Allerand CD (1996) Mechanisms of estrogen action during neural development: mediation by interactions with the neurotrophins and their receptors? J Steroid Biochem Mol Biol 56:169-178.
70. van der Staay FJ, de Jonge M (1993) Effects of age on water escape behavior and on repeated acquisition in rats. Behav Neural Biol 60:33-41.
71. van Haaren F, Wouters M, van de Poll NE (1987) Absence of behavioral differences between male and female rats in different radial maze procedures. Physiol Behav 39:409-412.
72. Wade SE, Maier SF (1986) Effects of individual housing and stressor exposure upon the acquisition of water maze escape. Learn Motiv 17:287-310.
73. Warren SG, Juraska JM (1997) Spatial and nonspatial learning across the rat estrous cycle. Behav Neurosci 111:259-266.
74. Williams CL, Meek WH (1991) The organizational effects of gonadal steroids on sexually dimorphic spatial ability. Psychoneuroendocrinology 16:155-176.
75. Williams CL, Barnett AM, Meek WH (1990) Organizational effects of early gonadal secretions on sexual differentiation in spatial memory. Behav Neurosci 104:84-97.
76. Woolley CS, McEwen BS (1993) Roles of estradiol and progesterone in regulation of hippocampal dendritic spine density during the estrous cycle in the rat. J Comp Neurol 336:293-306.
77. Woolley CS, Gould E, Frankfurt M, McEwen BS (1990) Naturally occurring fluctuation in dendritic spine density on adult hippocampal pyramidal neurons. J Neurosci 10:4035-4039.
78. Zola-Morgan S, Squire LR, Amaral DG (1986) Human amnesia and the medial temporal region: enduring memory impairment after a bilateral lesion limited to field CA1 of the hippocampus. J Neurosci 6:2950-2967.