Testosterone and cognitive function in ageing men: Data from the Florey Adelaide Male Ageing Study (FAMAS)

Maturitas

Volumn 57, Issue 2, 2007, Pages 182-194

  Martin, Donel M ^a   Wittert, Gary ^b   Burns, Nicholas R ^a   Haren, Matthew T ^c   Sugarman, Roy ^d  

^a UNIVERSITY OF ADELAIDE   (Australia)

^b UNIVERSITY OF ADELAIDE   (Australia)

^c SAINT LOUIS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^d Anxiety Management Services   (Australia)

Author keywords

Ageing; Cognition; Males; Memory; Sex hormones; Testosterone

Indexed keywords

ESTRADIOL; FOLLITROPIN; LUTEINIZING HORMONE; SEX HORMONE BINDING GLOBULIN; TESTOSTERONE;

ADULT; AGED; AGING; ALCOHOL CONSUMPTION; ANTHROPOMETRY; ARTICLE; BIOAVAILABILITY; COGNITION; DRUG USE; HEALTH STATUS; HORMONE DETERMINATION; HUMAN; MAJOR CLINICAL STUDY; MALE; MOOD; NEUROPSYCHOLOGICAL TEST; NEUROPSYCHOLOGY; SMOKING HABIT; VELOCITY; VERBAL MEMORY;

ADULT; AGED; AGED, 80 AND OVER; AGING; COGNITION DISORDERS; CROSS-SECTIONAL STUDIES; ESTRADIOL; FOLLICLE STIMULATING HORMONE; HUMANS; LUTEINIZING HORMONE; MALE; MIDDLE AGED; SEX HORMONE-BINDING GLOBULIN; SOUTH AUSTRALIA; TESTOSTERONE;

EID: 34249105649     PISSN: 03785122     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.maturitas.2006.12.007     Document Type: Article

References (85)

1. Access Economics. Dementia estimates and projections: Australian states and territories. Report for Alzheimers Australia 2005. Available from http://www.alzheimers.org.au.
2. Backman L., Wahlin A., Small B.J., Herlitz A., Winblad B., and Fratiglioni L. Cognitive functioning in aging and dementia: the Kungsholmen project. Aging Neuropsychol Cognit 11 (2004) 212-244
3. Greenwood P.M., Sunderland T., Putnam K., Levy J., and Parasuraman R. Scaling of visuospatial attention undergoes differential longitudinal change as a function of APOE genotype prior to old age: results from the NIMH BIOCARD study. Neuropsychology 19 (2005) 830-840
4. Flory J.D., Manuck S.B., Ferrell R.E., Ryan C.M., and Muldoon M.F. Memory performance and the apolipoprotein E polymorphism in a community sample of middle-aged adults. Am J Med Genet 96 (2000) 707-711
5. Chen P., Ratcliff G., Belle S.H., Cauley J.A., DeKosky S.T., and Ganguli M. Cognitive tests that best discriminate between presymptomatic AD and those who remain nondemented. Neurology 55 (2000) 1847-1853
6. Albert M.S., Moss M.B., Tanzi R., and Jones K. Preclinical prediction of AD using neuropsychological tests. J Int Neuropsychol Soc 7 (2001) 631-639
7. Rapp M.A., and Reischies F.M. Attention and executive control predict Alzheimer disease in late life: results from the Berlin Aging Study (BASE). Am J Geriatr Psychiatry 13 (2005) 134-141
8. Perry R.J., Watson P., and Hodges J.R. The nature and staging of attention dysfunction in early (minimal and mild) Alzheimer's disease: relationship to episodic and semantic memory impairment. Neuropsychologia 38 (2000) 252-271
9. Salthouse T.A. What and when of cognitive aging. Curr Dir Psychol Sci 13 (2004) 140-144
10. Schaie K.W. The course of adult intellectual development. Am Psychol 49 (1994) 304-313
11. Verhaeghen P., and Salthouse T.A. Meta-analyses of age-cognition relations in adulthood: estimates of linear and nonlinear age effects and structural models. Psychol Bull 122 (1997) 231-249
12. Tan R.S., and Pu S.J. The andropause and memory loss: is there a link between androgen decline and dementia in the aging male?. Asian J Androl 3 (2001) 169-174
13. Muller M., den Tonkelaar I., Thijssen J.H., Grobbee D.E., and van der Schouw Y.T. Endogenous sex hormones in men aged 40-80 years. Eur J Endocrinol 149 (2003) 583-589
14. Vermeulen A., and Kaufman J.M. Ageing of the hypothalamo-pituitary-testicular axis in men. Horm Res 43 (1995) 25-28
15. Orwoll E., Lambert L.C., Marshall L.M., et al. Testosterone and estradiol among older men. J Clin Endocrinol Metab 91 (2006) 1336-1344
16. Morley J.E., Kaiser F., Raum W.J., et al. Potentially predictive and manipulable blood serum correlates of aging in the healthy human male: progressive decreases in bioavailable testosterone, dehydroepiandrosterone sulfate, and the ratio of insulin-like growth factor 1 to growth hormone. Proc Natl Acad Sci USA 94 (1997) 7537-7542
17. Moffat S.D., Zonderman A.B., Metter E.J., Blackman M.R., Harman S.M., and Resnick S.M. Longitudinal assessment of serum free testosterone concentration predicts memory performance and cognitive status in elderly men. J Clin Endocrinol Metab 87 (2002) 5001-5007
18. Barrett-Connor E., Goodman-Gruen D., and Patay B. Endogenous sex hormones and cognitive function in older men. J Clin Endocrinol Metab 84 (1999) 3681-3685
19. Thilers P.P., Macdonald S.W., and Herlitz A. The association between endogenous free testosterone and cognitive performance: a population-based study in 35 to 90 year-old men and women. Psychoneuroendocrinology 31 (2006) 565-576
20. Hogervorst E., De Jager C., Budge M., and Smith A.D. Serum levels of oestradiol and testosterone and performance in different cognitive domains in healthy elderly men and women. Psychoneuroendocrinology 29 (2004) 405-421
21. Yaffe K., Lui L.Y., Zmuda J., and Cauley J. Sex hormones and cognitive function in older men. J Am Geriatr Soc 50 (2002) 707-712
22. Muller M., Aleman A., Grobbee D.E., de Haan E.H., and van der Schouw Y.T. Endogenous sex hormone levels and cognitive function in aging men: is there an optimal level?. Neurology 64 (2005) 866-871
23. Perry P.J., Lund B.C., Arndt S., et al. Bioavailable testosterone as a correlate of cognition, psychological status, quality of life, and sexual function in aging males: implications for testosterone replacement therapy. Ann Clin Psychiatry 13 (2001) 75-80
24. Ware J.E., and Sherbourne C.D. The MOS 36-item Short-Form Health Survey (SF-36). I. Conceptual framework and item selection. Med Care 30 (1992) 473-483
25. Hodge A., Patterson A.J., Brown W.J., Ireland P., and Giles G. The Anti Cancer Council of Victoria FFQ: relative validity of nutrient intakes compared with weighed food records in young to middle-aged women in a study of iron supplementation. Aust N Z J Public Health 24 (2000) 576-583
26. Beck A.T., Ward C.H., Mendelson M., Mock J., and Erbaugh J. Beck depression inventory. An inventory for measuring depression. Arch Gen Psychiatry 4 (1961) 561-571
27. Reitan R.M., and Wolfson D. The Halstead-Reitan Neuropsychological Test Battery (1993), Neuropsychology Press, Tucson, AZ
28. Fuld P.A. Guaranteed stimulus-processing in the evaluation of memory and learning. Cortex 16 (1980) 255-271
29. Arbuthnott K., and Frank J. Trail making test, part B as a measure of executive control: validation using a set-switching paradigm. J Clin Exp Neuropsychol 22 (2000) 518-528
30. O'Connor S., Baker H.W., Dulmanis A., and Hudson B. The measurement of sex steroid binding globulin by differential ammonium sulphate precipitation. J Steroid Biochem 4 (1973) 331-339
31. Ly L.P., and Handelsman D.J. Empirical estimation of free testosterone from testosterone and sex hormone-binding globulin immunoassays. Eur J Endocrinol 152 (2005) 471-478
32. Baron R.M., and Kenny D.A. The moderator-mediator variable distinction in social psychological research: conceptual, strategic and statistical considerations. J Pers Soc Psychol 51 (1986) 1173-1182
33. Sobel M.E. Asymptotic confidence intervals for indirect effects in structural equation models. In: Leinhardt S. (Ed). Sociological methodology (1982), American Sociological Association 290-312
34. Fonda S.J., Bertrand R., O'Donnell A., Longcope C., and McKinlay J.B. Age, hormones, and cognitive functioning among middle-aged and elderly men: cross-sectional evidence from the massachusetts male aging study. J Gerontol A Biol Sci Med Sci 60 (2005) 385-390
35. Wechsler D. Wechsler Adult Intelligence Scale-Revised (1981), Psychological Corporation, San Antonio
36. Kreiner DS, Ryan JJ. Memory and motor skill components of the WAIS-III Digit Symbol-Coding subtest; 2001.
37. Smith A.B., Taylor E., Brammer M., and Rubia K. Neural correlates of switching set as measured in fast, event-related functional magnetic resonance imaging. Hum Brain Mapp 21 (2004) 247-256
38. Nagahama Y., Okada T., Katsumi Y., et al. Dissociable mechanisms of attentional control within the human prefrontal cortex. Cereb Cortex 11 (2001) 85-92
39. D'Esposito M., Postle B.R., Ballard D., and Lease J. Maintenance versus manipulation of information held in working memory: an event-related fMRI study. Brain Cogn 41 (1999) 66-86
40. D'Esposito M., Postle B.R., and Rypma B. Prefrontal cortical contributions to working memory: evidence from event-related fMRI studies. Exp Brain Res 133 (2000) 3-11
41. Barde L.H., and Thompson-Schill S.L. Models of functional organization of the lateral prefrontal cortex in verbal working memory: evidence in favor of the process model. J Cogn Neurosci 14 (2002) 1054-1063
42. Rossi S., Cappa S.F., Babiloni C., et al. Prefrontal (correction of Prefontal) cortex in long-term memory: an "interference" approach using magnetic stimulation. Nat Neurosci 4 (2001) 948-952
43. Rossi S., Miniussi C., Pasqualetti P., Babiloni C., Rossini P.M., and Cappa S.F. Age-related functional changes of prefrontal cortex in long-term memory: a repetitive transcranial magnetic stimulation study. J Neurosci 24 (2004) 7939-7944
44. Simons J.S., and Spiers H.J. Prefrontal and medial temporal lobe interactions in long-term memory. Nat Rev Neurosci 4 (2003) 637-648
45. Fletcher P.C., Shallice T., and Dolan R.J. The functional roles of prefrontal cortex in episodic memory. I. Encoding Brain 121 Pt 7 (1998) 1239-1248
46. Blumenfeld R.S., and Ranganath C. Dorsolateral prefrontal cortex promotes long-term memory formation through its role in working memory organization. J Neurosci 26 (2006) 916-925
47. Dobbins I.G., Foley H., Schacter D.L., and Wagner A.D. Executive control during episodic retrieval: multiple prefrontal processes subserve source memory. Neuron 35 (2002) 989-996
48. Achim A.M., and Lepage M. Dorsolateral prefrontal cortex involvement in memory post-retrieval monitoring revealed in both item and associative recognition tests. Neuroimage 24 (2005) 1113-1121
49. Cooke R.R., McIntosh J.E., and McIntosh R.P. Circadian variation in serum free and non-SHBG-bound testosterone in normal men: measurements, and simulation using a mass action model. Clin Endocrinol (Oxf) 39 (1993) 163-171
50. Cooke R.R., McIntosh J.E., and Murray-McIntosh R.P. Effect of cortisol on percentage of non-sex-hormone-bound steroid: implications for distribution of steroids on binding proteins in serum. Clin Chem 42 (1996) 249-254
51. Maki PM, Brandt J, Dobs A, Mordecai-Strom K, Resnick SM. Effects of testosterone supplementation on brain function in eugonadal elderly men. 9th Annual Meeting of the Organization for Human Brain Mapping. Budapest, Hungary; June 13-17, 2004.
52. Wolf O.T., and Kirschbaum C. Endogenous oestradiol and testosterone levels are associated with cognitive performance in older women and men. Horm Behav 41 (2002) 259-266
53. Aleman A., de Vries W.R., Koppeschaar H.P., et al. Relationship between circulating levels of sex hormones and insulin-like growth factor-1 and fluid intelligence in older men. Exp Aging Res 27 (2001) 283-291
54. Carlson L.E., and Sherwin B.B. Steroid hormones, memory and mood in a healthy elderly population. Psychoneuroendocrinology 23 (1998) 583-603
55. Delis D.C., Kramer J.H., Kaplan E., and Ober B.A. California verbal learning test. Research ed. (1987), Psychological Corp., New York
56. Naghdi N., Nafisy N., and Majlessi N. The effects of intrahippocampal testosterone and flutamide on spatial localization in the Morris water maze. Brain Res 897 (2001) 44-51
57. Naghdi N., and Asadollahi A. Genomic and nongenomic effects of intrahippocampal microinjection of testosterone on long-term memory in male adult rats. Behav Brain Res 153 (2004) 1-6
58. Moradpour F., Naghdi N., and Fathollahi Y. Anastrozole improved testosterone-induced impairment acquisition of spatial learning and memory in the hippocampal CA1 region in adult male rats. Behav Brain Res 175 (2006) 223-232
59. Naghdi N., Majlessi N., and Bozorgmehr T. The effect of intrahippocampal injection of testosterone enanthate (an androgen receptor agonist) and anisomycin (protein synthesis inhibitor) on spatial learning and memory in adult, male rats. Behav Brain Res 156 (2005) 263-268
60. Cherrier M.M., Asthana S., Plymate S., et al. Testosterone supplementation improves spatial and verbal memory in healthy older men. Neurology 57 (2001) 80-88
61. Cherrier M.M., Craft S., and Matsumoto A.H. Cognitive changes associated with supplementation of testosterone or dihydrotestosterone in mildly hypogonadal men: a preliminary report. J Androl 24 (2003) 568-576
62. Cherrier M.M., Matsumoto A.M., Amory J.K., et al. The role of aromatization in testosterone supplementation: effects on cognition in older men. Neurology 64 (2005) 290-296
63. Wolf O.T., Preut R., Hellhammer D.H., Kudielka B.M., Schurmeyer T.H., and Kirschbaum C. Testosterone and cognition in elderly men: a single testosterone injection blocks the practice effect in verbal fluency, but has no effect on spatial or verbal memory. Biol Psychiatry 47 (2000) 650-654
64. Janowsky J.S., Oviatt S.K., and Orwoll E.S. Testosterone influences spatial cognition in older men. Behav Neurosci 108 (1994) 325-332
65. Lu P.H., Masterman D.A., Mulnard R., et al. Effects of testosterone on cognition and mood in male patients with mild Alzheimer disease and healthy elderly men. Arch Neurol (2005)
66. Sih R., Morley J.E., Kaiser F.E., Perry III H.M., Patrick P., and Ross C. Testosterone replacement in older hypogonadal men: a 12-month randomized controlled trial. J Clin Endocrinol Metab 82 (1997) 1661-1667
67. Beer T.M., Bland L.B., Bussiere J.R., et al. Testosterone loss and estradiol administration modify memory in men. J Urol 175 (2006) 130-135
68. Pike C.J. Testosterone attenuates beta-amyloid toxicity in cultured hippocampal neurons. Brain Res 919 (2001) 160-165
69. Papasozomenos S.C. The heat shock-induced hyperphosphorylation of tau is estrogen-independent and prevented by androgens: implications for Alzheimer disease. Proc Natl Acad Sci USA 94 (1997) 6612-6617
70. Gillett M.J., Martins R.N., Clarnette R.M., Chubb S.A., Bruce D.G., and Yeap B.B. Relationship between testosterone, sex hormone binding globulin and plasma amyloid beta peptide 40 in older men with subjective memory loss or dementia. J Alzheimers Dis 5 (2003) 267-269
71. Gandy S., Almeida O.P., Fonte J., et al. Chemical andropause and amyloid-beta peptide. Jama 285 (2001) 2195-2196
72. Moffat S.D., Zonderman A.B., Metter E.J., et al. Free testosterone and risk for Alzheimer disease in older men. Neurology 62 (2004) 188-193
73. Kapoor P., Luttrell B.M., and Williams D. The free androgen index is not valid for adult males. J Steroid Biochem Mol Biol 45 (1993) 325-326
74. Watanabe T., Koba S., Kawamura M., et al. Small dense low-density lipoprotein and carotid atherosclerosis in relation to vascular dementia. Metabolism 53 (2004) 476-482
75. Hogervorst E., Bandelow S., Combrinck M., and Smith A.D. Low free testosterone is an independent risk factor for Alzheimer's disease. Exp Gerontol 39 (2004) 1633-1639
76. Hogervorst E., Williams J., Budge M., Barnetson L., Combrinck M., and Smith A.D. Serum total testosterone is lower in men with Alzheimer's disease. Neuro Endocrinol Lett 22 (2001) 163-168
77. Geerlings M.I., Strozyk D., Masaki K., et al. Endogenous sex hormones, cognitive decline, and future dementia in old men. Ann Neurol 60 (2006) 346-355
78. Corder E.H., Lannfelt L., Bogdanovic N., Fratiglioni L., and Mori H. The role of APOE polymorphisms in late-onset dementias. Cell Mol Life Sci 54 (1998) 928-934
79. Burkhardt M.S., Foster J.K., Clarnette R.M., et al. Interaction between testosterone and APOE {epsilon}4 status on cognition in healthy older men. J Clin Endocrinol Metab (2005)
80. Bondi M.W., Salmon D.P., Monsch A.U., et al. Episodic memory changes are associated with the APOE-epsilon 4 allele in nondemented older adults. Neurology 45 (1995) 2203-2206
81. Bondi M.W., Salmon D.P., Galasko D., Thomas R.G., and Thal L.J. Neuropsychological function and apolipoprotein E genotype in the preclinical detection of Alzheimer's disease. Psychol Aging 14 (1999) 295-303
82. Wetter S.R., Delis D.C., Houston W.S., et al. Deficits in inhibition and flexibility are associated with the APOE-E4 allele in nondemented older adults. J Clin Exp Neuropsychol 27 (2005) 943-952
83. Rosen V.M., Bergeson J.L., Putnam K., Harwell A., and Sunderland T. Working memory and apolipoprotein E: what's the connection?. Neuropsychologia 40 (2002) 2226-2233
84. Greenwood P.M., Lambert C., Sunderland T., and Parasuraman R. Effects of apolipoprotein E genotype on spatial attention, working memory, and their interaction in healthy, middle-aged adults: results From the National Institute of Mental Health's BIOCARD study. Neuropsychology 19 (2005) 199-211
85. Hogervorst E., Lehmann D.J., Warden D.R., McBroom J., and Smith A.D. Apolipoprotein E epsilon4 and testosterone interact in the risk of Alzheimer's disease in men. Int J Geriatr Psychiatry 17 (2002) 938-940