Raloxifene exposure enhances brain activation during memory performance in healthy elderly males; Its possible relevance to behavior

NeuroImage

Volumn 25, Issue 1, 2005, Pages 63-75

  Goekoop, R ^a   Duschek, E J J ^a   Knol, D L ^a   Barkhof, F ^a   Netelenbos, C ^a   Scheltens, Ph ^a   Rombouts, S A R B ^a  

^a VU UNIVERSITY MEDICAL CENTER   (Netherlands)

Author keywords

Arousal; Estrogen; fMRI; Memory; Raloxifene; SERM

Indexed keywords

PLACEBO; RALOXIFENE;

ACCURACY; ADULT; AGED; ARTICLE; BEHAVIOR; BRAIN FUNCTION; CINGULATE GYRUS; CLINICAL TRIAL; CONTROLLED CLINICAL TRIAL; CONTROLLED STUDY; DOUBLE BLIND PROCEDURE; DRUG EFFECT; FUNCTIONAL MAGNETIC RESONANCE IMAGING; HUMAN; MALE; MEMORY; NORMAL HUMAN; OCCIPITAL LOBE; PARIETAL LOBE; PREFRONTAL CORTEX; PRIORITY JOURNAL; RANDOMIZED CONTROLLED TRIAL; STATISTICAL ANALYSIS; TASK PERFORMANCE; TEMPORAL LOBE;

EID: 14244264343     PISSN: 10538119     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.neuroimage.2004.11.012     Document Type: Article

References (79)

1. N. Azad, S. Pitale, W.E. Barnes, and N. Friedman Testosterone treatment enhances regional brain perfusion in hypogonadal men J. Clin. Endocrinol. Metab. 88 2003 3064 3068
2. D. Badre, and A.D. Wagner Selection, integration, and conflict monitoring; assessing the nature and generality of prefrontal cognitive control mechanisms Neuron 41 2004 473 487
3. E. Barrett-Connor, D. Goodman-Gruen, and B. Patay Endogenous sex hormones and cognitive function in older men J. Clin. Endocrinol. Metab. 84 1999 3681 3685
4. C.F. Beckmann, M. Jenkinson, and S.M. Smith General multilevel linear modeling for group analysis in FMRI NeuroImage 20 2003 1052 1063
5. P. Bentley, M. Husain, and R.J. Dolan Effects of cholinergic enhancement on visual stimulation, spatial attention, and spatial working memory Neuron 41 2004 969 982
6. F. Bernardi, N. Pluchino, M. Stomati, M. Pieri, and A.R. Genazzani CNS: sex steroids and SERMs Ann. N. Y. Acad. Sci. 997 2003 378 388
7. V. Bisagno, R.E. Bowman, and V.N. Luine Functional aspects of estrogen neuroprotection Endocrine 21 2003 33 41
8. A. Blum, L. Hathaway, R. Mincemoyer, W.H. Schenke, G. Csako, M.A. Waclawiw, J.A. Panza, and R.O. Cannon III Hormonal, lipoprotein, and vascular effects of the selective estrogen receptor modulator raloxifene in hypercholesterolemic men Am. J. Cardiol. 85 2000 1491 1494
9. T.S. Braver, and D.A. Barch A theory of cognitive control, aging cognition, and neuromodulation Neurosci. Biobehav. Rev. 26 2002 809 817
10. J.T. Coull Neural correlates of attention and arousal: insights from electrophysiology, functional neuroimaging and psychopharmacology Prog. Neurobiol. 55 1998 343 361
11. S.R. Cummings, S. Eckert, K.A. Krueger, D. Grady, T.J. Powles, J.A. Cauley, L. Norton, T. Nickelsen, N.H. Bjarnason, M. Morrow, M.E. Lippman, D. Black, J.E. Glusman, A. Costa, and V.C. Jordan The effect of raloxifene on risk of breast cancer in postmenopausal women: results from the MORE randomized trial. Multiple Outcomes of Raloxifene Evaluation JAMA 281 1999 2189 2197
12. M. D'Esposito, E. Zarahn, G.K. Aguirre, and B. Rypma The effect of normal aging on the coupling of neural activity to the bold hemodynamic response NeuroImage 10 1999 6 14
13. G.W. de Valk-de Roo, C.D. Stehouwer, P. Meijer, V. Mijatovic, C. Kluft, P. Kenemans, F. Cohen, S. Watts, and C. Netelenbos Both raloxifene and estrogen reduce major cardiovascular risk factors in healthy postmenopausal women: a 2-year, placebo-controlled study Arterioscler. Thromb. Vasc. Biol. 19 1999 2993 3000
14. P.D. Delmas, N.H. Bjarnason, B.H. Mitlak, A.C. Ravoux, A.S. Shah, W.J. Huster, M. Draper, and C. Christiansen Effects of raloxifene on bone mineral density, serum cholesterol concentrations, and uterine endometrium in postmenopausal women N. Engl. J. Med. 337 1997 1641 1647
15. P.D. Delmas, K.E. Ensrud, J.D. Adachi, K.D. Harper, S. Sarkar, C. Gennari, J.Y. Reginster, H.A. Pols, R.R. Recker, S.T. Harris, W. Wu, H.K. Genant, D.M. Black, and R. Eastell Efficacy of raloxifene on vertebral fracture risk reduction in postmenopausal women with osteoporosis: four-year results from a randomized clinical trial J. Clin. Endocrinol. Metab. 87 2002 3609 3617
16. T. Dietrich, T. Krings, J. Neulen, K. Willmes, S. Erberich, A. Thron, and W. Sturm Effects of blood estrogen level on cortical activation patterns during cognitive activation as measured by functional MRI NeuroImage 13 2001 425 432
17. P.M. Doran, B.L. Riggs, E.J. Atkinson, and S. Khosla Effects of raloxifene, a selective estrogen receptor modulator, on bone turnover markers and serum sex steroid and lipid levels in elderly men J. Bone Miner. Res. 16 2001 2118 2125
18. B. Ettinger, D.M. Black, B.H. Mitlak, R.K. Knickerbocker, T. Nickelsen, H.K. Genant, C. Christiansen, P.D. Delmas, J.R. Zanchetta, J. Stakkestad, C.C. Gluer, K. Krueger, F.J. Cohen, S. Eckert, K.E. Ensrud, L.V. Avioli, P. Lips, and S.R. Cummings Reduction of vertebral fracture risk in postmenopausal women with osteoporosis treated with raloxifene: results from a 3-year randomized clinical trial. Multiple Outcomes of Raloxifene Evaluation (MORE) Investigators JAMA 282 1999 637 645
19. G.R. Fink, J.C. Marshall, P.W. Halligan, C.D. Frith, J. Driver, R.S.J. Frackowiak, and R.J. Dolan The neural consequences of conflict between intention and the senses Brain 122 1999 497 512
20. S.D. Forman, J.D. Cohen, M. Fitzgerald, W.F. Eddy, M.A. Mintun, and D.C. Noll Improved assessment of significant activation in Functional Magnetic-Resonance-Imaging (Fmri)-use of a cluster-size threshold Magn. Reson. Med. 33 1995 636 647
21. U. Freo, G. Pizzolato, M. Dam, C. Ori, and L. Battistin A short review of cognitive and functional neuroimaging studies of cholinergic drugs: implications for therapeutic potentials J. Neural. Transm. 109 2002 857 870
22. K.J. Friston, K.J. Worsley, R.S.J. Frackowiak, J.C. Mazziotta, and A. Evans Assessing the significance of focal activations using their spatial extent Hum. Brain Mapp. 1 1994 210 220
23. M.L. Furey, P. Pietrini, and J.V. Haxby Cholinergic enhancement and increased selectivity of perceptual processing during working memory Science 290 2000 2315 2319
24. R. Goekoop, S.A.R.B. Rombouts, C. Jonker, A. Hibbel, D.L. Knol, L. Truyen, F. Barkhof, and Ph. Scheltens Challenging the cholinergic system in mild cognitive impairment; a pharmacological fMRI study NeuroImage 2004 (in press)
25. M.D. Greicius, B. Krasnow, J.M. Boyett-Anderson, S. Eliez, A.F. Schatzberg, A.L. Reiss, and V. Menon Regional analysis of hippocampal activation during memory encoding and retrieval: fMRI study Hippocampus 13 2003 164 174
26. M. Jenkinson, and S. Smith A global optimisation method for robust affine registration of brain images Med. Image Anal. 5 2001 143 156
27. M. Jenkinson, P. Bannister, M. Brady, and S. Smith Improved optimization for the robust and accurate linear registration and motion correction of brain images NeuroImage 17 2002 825 841
28. D.L. Kampen, and B.B. Sherwin Estradiol is related to visual memory in healthy young men Behav. Neurosci. 110 1996 613 617
29. P.A. Keenan, W.H. Ezzat, K. Ginsburg, and G.J. Moore Prefrontal cortex as the site of estrogen's effect on cognition Psychoneuroendocrinology 26 2001 577 590
30. W.M. Kelley, F.M. Miezin, K.B. Mcdermott, R.L. Buckner, M.E. Raichle, N.J. Cohen, J.M. Ollinger, E. Akbudak, T.E. Conturo, A.Z. Snyder, and S.E. Petersen Hemispheric specialization in human dorsal frontal cortex and medial temporal lobe for verbal and nonverbal memory encoding Neuron 20 1998 927 936
31. F.P. Kruijver, R. Balesar, A.M. Espila, U.A. Unmehopa, and D.F. Swaab Estrogen-receptor-beta distribution in the human hypothalamus: similarities and differences with ER alpha distribution J. Comp. Neurol. 466 2003 251 277
32. V. Kumari, J.A. Gray, D.H. Ffytche, M.T. Mitterschiffthaler, M. Das, E. Zachariah, G.N. Vythelingum, S.C.R. Williams, A. Simmons, and T. Sharma Cognitive effects of nicotine in humans: an fMRI study NeuroImage 19 2003 1002 1013
33. N.S. Lawrence, T.J. Ross, and E.A. Stein Cognitive mechanisms of nicotine on visual attention Neuron 36 2002 539 548
34. Z.H. Li, X.W. Sun, Z.X. Wang, X.C. Zhang, D.R. Zhang, S. He, and X.P. Hu Behavioral and functional MRI study of attention shift in human verbal working memory NeuroImage 21 2004 181 191
35. C. Longcope, T. Kato, and R. Horton Conversion of blood androgens to estrogens in normal adult men and women J. Clin. Invest. 48 1969 2191 2201
36. I. Loubinoux, C. Carel, F. Alary, K. Boulanouar, G. Viallard, C. Manelfe, O. Rascol, P. Celsis, and F. Chollet Within-session and between-session reproducibility of cerebral sensorimotor activation: a test-retest effect evidenced with functional magnetic resonance imaging J. Cereb. Blood Flow Metab. 21 2001 592 607
37. B. Luna, K.R. Thulborn, M.H. Strojwas, B.J. McCurtain, R.A. Berman, C.R. Genovese, and J.A. Sweeney Dorsal cortical regions subserving visually guided saccades in humans: an fMRI study Cereb. Cortex 8 1998 40 47
38. P.C. MacDonald, J.D. Madden, P.F. Brenner, J.D. Wilson, and P.K. Siiteri Origin of estrogen in normal men and in women with testicular feminization J. Clin. Endocrinol. Metab. 49 1979 905 916
39. M.M. Machulda, H.A. Ward, B. Borowski, J.L. Gunter, R.H. Cha, P.C. O'Brien, R.C. Petersen, B.F. Boeve, D. Knopman, D.F. Tang-Wai, R.J. Ivnik, G.E. Smith, E.G. Tangalos, and C.R. Jack Comparison of memory fMRI response among normal, MCI, and Alzheimer's patients Neurology 61 2003 500 506
40. P.M. Maki, and S.M. Resnick Longitudinal effects of estrogen replacement therapy on PET cerebral blood flow and cognition Neurobiol. Aging 21 2000 373 383
41. P.M. Maki, and S.M. Resnick Effects of estrogen on patterns of brain activity at rest and during cognitive activity: a review of neuroimaging studies NeuroImage 14 2001 789 801
42. B. McEwen Estrogen actions throughout the brain Recent Prog. Horm. Res. 57 2002 357 384
43. M.A. Morgan, J. Schulkin, and D.W. Pfaff Estrogens and non-reproductive behaviors related to activity and fear Neurosci. Biobehav. Rev. 28 2004 55 63
44. J.E. Morley, F. Kaiser, W.J. Raum, H.M. Perry III, J.F. Flood, J. Jensen, A.J. Silver, and E. Roberts 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. U. S. A. 94 1997 7537 7542
45. S.J. Murphy, L.D. McCullough, M.T. Littleton-Kearney, and P.D. Hurn Estrogen and selective estrogen receptor modulators-Neuroprotection in the Women's Health Initiative Era Endocrine 21 2003 17 26
46. S.J. Neele, S.A. Rombouts, M.A. Bierlaagh, F. Barkhof, P. Scheltens, and J.C. Netelenbos Raloxifene affects brain activation patterns in postmenopausal women during visual encoding J. Clin. Endocrinol. Metab. 86 2001 1422 1424
47. M.K. Osterlund, J.A. Gustafsson, E. Keller, and Y.L. Hurd Estrogen receptor beta (ERbeta) messenger ribonucleic acid (mRNA) expression within the human forebrain: distinct distribution pattern to ERalpha mRNA J. Clin. Endocrinol. Metab. 85 2000 3840 3846
48. A. Paganini-Hill, and V.W. Henderson Estrogen replacement therapy and risk of Alzheimer disease Arch. Intern. Med. 156 1996 2213 2217
49. R.C. Petersen, R. Doody, A. Kurz, R.C. Mohs, J.C. Morris, P.V. Rabins, K. Ritchie, M. Rossor, L. Thal, and B. Winblad Current concepts in mild cognitive impairment Arch. Neurol. 58 2001 1985 1992
50. P. Polo-Kantola, R. Portin, O. Polo, H. Helenius, K. Irjala, and R. Erkkola The effect of short-term estrogen replacement therapy on cognition: a randomized, double-blind, cross-over trial in postmenopausal women Obstet. Gynecol. 91 1998 459 466
51. S.R. Rapp, M.A. Espeland, S.A. Shumaker, V.W. Henderson, R.L. Brunner, J.E. Manson, M.L.S. Gass, M.L. Stefanick, D.S. Lane, J. Hays, K.C. Johnson, L.H. Coker, M. Dailey, and D. Bowen Effect of estrogen plus progestin on global cognitive function in postmenopausal women-The Women's Health Initiative Memory Study: a randomized controlled trial JAMA 289 2003 2663 2672
52. A.H. Rezvani, and E.D. Levin Cognitive effects of nicotine Biol. Psychiatry 49 2001 258 267
53. K. Rice, and C. Morse Measuring cognition in menopause research: a review of test use Climacteric 6 2003 2 22
54. B.L. Riggs, and L.C. Hartmann Selective estrogen-receptor modulators-mechanisms of action and application to clinical practice N. Engl. J. Med. 348 2003 618 629
55. J.B. Rowe, I. Toni, O. Josephs, R.S.J. Frackowiak, and R.E. Passingham The prefrontal cortex: response selection or maintenance within working memory? Science 288 2000 1656 1660
56. D.L. Schacter, and A.D. Wagner Medial temporal lobe activations in fMRI and PET studies of episodic encoding and retrieval Hippocampus 9 1999 7 24
57. V. Senanarong, S. Vannasaeng, N. Poungvarin, S. Ploybutr, S. Udompunthurak, P. Jamjumras, L. Fairbanks, and J.L. Cummings Endogenous estradiol in elderly individuals: cognitive and noncognitive associations Arch. Neurol. 59 2002 385 389
58. S.E. Shaywitz, 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 1999 1197 1202
59. B.B. Sherwin Estrogen and cognitive functioning in women Endocr. Rev. 24 2003 133 151
60. B.B. Sherwin Steroid hormones and cognitive functioning in aging men: a mini-review J. Mol. Neurosci. 20 2003 385 393
61. S.A. Shumaker, C. Legault, S.R. Rapp, L. Thal, R.B. Wallace, J.K. Ockene, S.L. Hendrix, B.N. Jones, A.R. Assaf, R.D. Jackson, J.M. Kotchen, S. Wassertheil-Smoller, and J. Wactawski-Wende Estrogen plus progestin and the incidence of dementia and mild cognitive impairment in postmenopausal women-The Women's Health Initiative Memory Study: a randomized controlled trial JAMA 289 2003 2651 2662
62. J.W. Simpkins, P.S. Green, K.E. Gridley, M. Singh, N.C. de Fiebre, and G. Rajakumar Role of estrogen replacement therapy in memory enhancement and the prevention of neuronal loss associated with Alzheimer's disease Am. J. Med. 103 1997 19S 25S
63. S.A. Small, G.M. Perera, R. DeLaPaz, R. Mayeux, and Y. Stern Differential regional dysfunction of the hippocampal formation among elderly with memory decline and Alzheimer's disease Ann. Neurol. 45 1999 466 472
64. S.M. Smith Fast robust automated brain extraction Hum. Brain Mapp. 17 2002 143 155
65. B.A. Strange, and R.J. Dolan beta-Adrenergic modulation of emotional memory-evoked human amygdala and hippocampal responses Proc. Acad. Natl. Sci. U. S. A. 101 2004 11454 11458
66. J. Talairach, and P. Tournoux Co-Planar Stereotaxic Atlas of the Human Brain 1988 Thieme Verlag Stuttgart, Germany
67. M.J. Tarr, and I. Gauthier FFA: a flexible fusiform area for subordinate-level visual processing automatized by expertise Nat. Neurosci. 3 2000 764 769
68. C.M. Thiel Cholinergic modulation of learning and memory in the human brain as detected with functional neuroimaging Neurobiol. Learn. Mem. 80 2003 234 244
69. B.W. Walsh, L.H. Kuller, R.A. Wild, S. Paul, M. Farmer, J.B. Lawrence, A.S. Shah, and P.W. Anderson Effects of raloxifene on serum lipids and coagulation factors in healthy postmenopausal women JAMA 279 1998 1445 1451
70. S. Wassertheil-Smoller, S.L. Hendrix, M. Limacher, G. Heiss, C. Kooperberg, A. Baird, T. Kotchen, J.D. Curb, H. Black, J.E. Rossouw, A. Aragaki, M. Safford, E. Stein, S. Laowattana, and W.J. Mysiw Effect of estrogen plus progestin on stroke in postmenopausal women-The Women's Health Initiative: a randomized trial JAMA 289 2003 2673 2684
71. D.H. Weissman, B. Giesbrecht, A.W. Song, G.R. Mangun, and M.G. Woldorff Conflict monitoring in the human anterior cingulate cortex during selective attention to global and local object features NeuroImage 19 2003 1361 1368
72. D. Wilkinson, and P. Halligan Opinion-The relevance of behavioural measures for functional-imaging studies of cognition Nature Rev. Neurosci. 5 2004 67 73
73. O.T. Wolf, B.M. Kudielka, D.H. Hellhammer, S. Torber, B.S. McEwen, and C. Kirschbaum Two weeks of transdermal estradiol treatment in postmenopausal elderly women and its effect on memory and mood: verbal memory changes are associated with the treatment induced estradiol levels Psychoneuroendocrinology 24 1999 727 741
74. O.T. Wolf, R. Preut, D.H. Hellhammer, B.M. Kudielka, T.H. Schurmeyer, and C. Kirschbaum 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
75. M.W. Woolrich, B.D. Ripley, M. Brady, and S.M. Smith Temporal autocorrelation in univariate linear modeling of FMRI data NeuroImage 14 2001 1370 1386
76. M.W. Woolrich, T.E.J. Behrens, C.F. Beckmann, M. Jenkinson, and S.M. Smith Multilevel linear modelling for FMRI group analysis using Bayesian inference NeuroImage 21 2004 1732 1747
77. K.J. Worsley, A.C. Evans, S. Marrett, and P. Neelin A 3-dimensional statistical-analysis for Cbf activation studies in human brain J. Cereb. Blood Flow Metab. 12 1992 900 918
78. J.E. Yonker, E. Eriksson, L.G. Nilsson, and A. Herlitz Sex differences in episodic memory: minimal influence of estradiol Brain Cogn. 52 2003 231 238
79. J.Q. Zhang, W.Q. Cai, D.S. Zhou, and B.Y. Su Distribution and differences of estrogen receptor beta immunoreactivity in the brain of adult male and female rats Brain Res. 935 2002 73 80