Cognitive changes across the menopause transition: A longitudinal evaluation of the impact of age and ovarian status on spatial memory

Hormones and Behavior

Volumn 87, Issue , 2017, Pages 96-114

  Koebele, Stephanie V ^a,b   Mennenga, Sarah E ^a,b   Hiroi, Ryoko ^a,b   Quihuis, Alicia M ^a,b   Hewitt, Lauren T ^a,b   Poisson, Mallori L ^a,b   George, Christina ^c   Mayer, Loretta P ^c   Dyer, Cheryl A ^c   Aiken, Leona S ^a   Demers, Laurence M ^d   Carson, Catherine ^a,b   Bimonte Nelson, Heather A ^a,b  

^a ARIZONA STATE UNIVERSITY   (United States)

^b ARIZONA ALZHEIMER S CONSORTIUM   (United States)

^c SenesTech Inc   (United States)

^d PENN STATE COLLEGE OF MEDICINE   (United States)

Author keywords

Aging; Cognition; Hormone; Learning; Memory; Menopause; Ovary; VCD

Indexed keywords

4 VINYLCYCLOHEXENE DIEPOXIDE; ANDROSTENEDIONE; CYCLOHEXENE DERIVATIVE; ESTRADIOL; ESTRONE; PROGESTERONE; UNCLASSIFIED DRUG; 4-VINYL-1-CYCLOHEXENE DIOXIDE; VINYL DERIVATIVE;

ADULT; AGE; AGING; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; COGNITION; CONTROLLED STUDY; FEMALE; HORMONE DETERMINATION; LEARNING; LONGITUDINAL STUDY; MEMORY CONSOLIDATION; MENOPAUSE; MIDDLE AGED; NONHUMAN; OVARY FOLLICLE; OVARY FUNCTION; PHASE TRANSITION; PRIORITY JOURNAL; RADIAL ARM MAZE TEST; RAT; REFERENCE MEMORY; SPATIAL MEMORY; WORKING MEMORY; ANIMAL; CYTOLOGY; DRUG EFFECTS; FISCHER 344 RAT; OVARIAN RESERVE; OVARY; PHYSIOLOGY; PSYCHOLOGY;

AGING; ANIMALS; COGNITION; CYCLOHEXENES; FEMALE; MENOPAUSE; OVARIAN FOLLICLE; OVARIAN RESERVE; OVARY; RATS; RATS, INBRED F344; SPATIAL MEMORY; VINYL COMPOUNDS;

EID: 84996721598     PISSN: 0018506X     EISSN: 10956867     Source Type: Journal    
DOI: 10.1016/j.yhbeh.2016.10.010     Document Type: Article

References (98)

1. Acosta, J.I., Mayer, L., Talboom, J.S., Tsang, C.W., Smith, C.J., Enders, C.K., Bimonte-Nelson, H.A., Transitional versus surgical menopause in a rodent model: etiology of ovarian hormone loss impacts memory and the acetylcholine system. Endocrinology 150:9 (2009), 4248–4259, 10.1210/en.2008-1802.
2. Acosta, J.I., Mayer, L.P., Braden, B.B., Nonnenmacher, S., Mennenga, S.E., Bimonte-Nelson, H.A., The cognitive effects of conjugated equine estrogens depend on whether menopause etiology is transitional or surgical. Endocrinology 151:8 (2010), 3795–3804, 10.1210/en.2010-0055.
3. Al-Safi, Z., Santoro, N., Menopausal hormone therapy and menopausal symptoms. Fertil. Steril. 101:4 (2014), 905–915, 10.1016/j.fertnstert.2014.02.032.
4. Anderson, R., Nelson, S., Wallace, W., Measuring anti-Müllerian hormone for the assessment of ovarian reserve: when and for whom is it indicated?. Maturitas 71 (2012), 28–33.
5. Bakeman, R., Recommended effect size statistics for repeated measures designs. Behav. Res. Methods 37:3 (2005), 379–384.
6. Barnes, C.A., Memory deficits associated with senescence: a neurophysiological and behavioral study in the rat. J. Comp. Physiol. Psychol. 93:1 (1979), 74–104.
7. Bimonte, H.A., Denenberg, V.H., Estradiol facilitates performance as working memory load increases. Psychoneuroendocrinology 24:2 (1999), 161–173 (Retrieved from) http://www.ncbi.nlm.nih.gov/pubmed/10101725.
8. Bimonte, H.A., Hyde, L.A., Hoplight, B.J., Denenberg, V.H., In two species, females exhibit superior working memory and inferior reference memory on the water radial-arm maze. Physiol. Behav. 70:3–4 (2000), 311–317.
9. Bimonte, H.A., Granholm, A.C., Seo, H., Isacson, O., Spatial memory testing decreases hippocampal amyloid precursor protein in young, but not in aged, female rats. Neurosci. Lett. 328:1 (2002), 50–54.
10. Bimonte, H.A., Nelson, M.E., Granholm, A.-C.E.C., Age-related deficits as working memory load increases: relationships with growth factors. Neurobiol. Aging 24:1 (2003), 37–48 (Retrieved from) http://www.ncbi.nlm.nih.gov/pubmed/12493549.
11. Bimonte-Nelson, H.A., Singleton, R.S., Hunter, C.L., Price, K.L., Moore, A.B., Granholm, A.-C.E.C., Ovarian hormones and cognition in the aged female rat: I. Long-term, but not short-term, ovariectomy enhances spatial performance. Behav. Neurosci. 117:6 (2003), 1395–1406, 10.1037/0735-7044.117.6.1395.
12. Bimonte-Nelson, H.A., Singleton, R.S., Williams, B.J., Granholm, A.-C.E.C., Ovarian hormones and cognition in the aged female rat: II. Progesterone supplementation reverses the cognitive enhancing effects of ovariectomy. Behav. Neurosci. 118:4 (2004), 707–714, 10.1037/0735-7044.118.4.707.
13. Bimonte-Nelson, H.A., Francis, K.R., Umphlet, C.D., Granholm, A.-C.C., Progesterone reverses the spatial memory enhancements initiated by tonic and cyclic oestrogen therapy in middle-aged ovariectomized female rats. Eur. J. Neurosci. 24:1 (2006), 229–242, 10.1111/j.1460-9568.2006.04867.x.
14. Bimonte-Nelson, H.A., Daniel, J.M., Koebele, S.V., The mazes. Bimonte-Nelson, H.A., (eds.) The Maze Book: Theories, Practice, and Protocols for Testing Rodent Cognition, 2015, Springer Publishing, Humana Press, NY, 37–72.
15. Bizon, J., LaSarge, C., Montgomery, K., McDermott, A., Setlow, B., Griffith, W., Spatial reference and working memory across the lifespan of male Fischer 344 rats. Neurobiol. Aging 30:4 (2009), 646–655, 10.1016/j.neurobiolaging.2007.08.004.
16. Borman, S.M., VanDePol, B.J., Kao, S., Thompson, K.E., Sipes, I.G., Hoyer, P.B., A Single Dose of the Ovotoxicant 4-Vinylcyclohexene Diepoxide Is Protective in Rat Primary Ovarian Follicles. 158, 1999, 244–252.
17. Braden, B.B., Talboom, J.S., Crain, I.D., Simard, A.R., Lukas, R.J., Prokai, L.,. Bimonte-Nelson, H.A., Medroxyprogesterone acetate impairs memory and alters the GABAergic system in aged surgically menopausal rats. Neurobiol. Learn. Mem. 93:3 (2010), 444–453, 10.1016/j.nlm.2010.01.002.
18. Braden, B.B., Garcia, A.N., Mennenga, S.E., Prokai, L., Villa, S.R., Acosta, J.I., Lefort, N., Simard, A.R., Bimonte-Nelson, H.A., Cognitive-impairing effects of medroxyprogesterone acetate in the rat: independent and interactive effects across time. Psychopharmacology (Berl) 218 (2011), 405–418.
19. Brody, S., Wiqvist, N., Ovarian hormones and uterine growth: effects of estradiol, progesterone and relaxin on cell growth and cell division in the rat uterus. Endocrinology 68 (1961), 971–977.
20. Broer, S., Eijkemans, M., Scheffer, G., Rooij, I., Vet, A., Themmen, A., Laven, J., Jong, F., Velde, E., Fauser, B., Broekmans, F., Anti-Mullerian hormone predicts menopause: a long-term follow-up study in normoovulatory women. J. Clin. Endocrinol. Metab., 96, 2011, 25322539.
21. Burger, H.G., Physiology and endocrinology of the menopause. Medicine (Baltimore) 34:1 (2006), 27–30.
22. Camp, B.W., Gerson, J.E., Tsang, C.W., Villa, S.R., Acosta, J.I., Blair Braden, B.,. Bimonte-Nelson, H.A., High serum androstenedione levels correlate with impaired memory in the surgically menopausal rat: a replication and new findings. Eur. J. Neurosci. 36:8 (2012), 3086–3095, 10.1111/j.1460-9568.2012.08194.x.
23. Centers for Disease Control and Prevention, Number of All-listed Procedures for Discharges From Short-stay Hospitals, by Procedure Category and Age: United States, 2010. CDC/NCHS National Hospital Discharge Survey, 2010. 2010.
24. Cohen, J., Statistical Power Analysis for the Behavioral Sciences. 2nd ed, 1988, Erlbaum, Hillsdale, NJ.
25. Cohen, J., A power primer. Psychol. Bull. 112:1 (1992), 155–158.
26. Cohen, J., Cohen, P., West, S.G., Aiken, L.S., Applied Multiple Regression/Correlation Analysis in the Behavioral Sciences. Third Edition, 2003, Erlbaum, Mahwah, NJ.
27. Downs, J., Wise, P., The role of the brain in female reproductive aging. Mol. Cell. Endocrinol. 299 (2009), 32–38.
28. Engler-Chiurazzi, E.B., Talboom, J.S., Braden, B.B., Tsang, C.W., Mennenga, S., Andrews, M., Demers, L.M., Bimonte-Nelson, H.A., Continuous estrone treatment impairs spatial memory and does not impact number of basal forebrain cholinergic neurons in the surgically menopausal middle-aged rat. Horm. Behav. 62:1 (2012), 1–9, 10.1016/j.yhbeh.2012.04.004.
29. Farrag, A.F., Khedr, E.M., Abdel-Aleem, H., Rageh, T.A., Effects of surgical menopause on cognitive functions. Dement. Geriatr. Cogn. Disord. 13 (2002), 193–198.
30. Finch, C., The menopause and aging, a comparative perspective. J. Steroid Biochem. Mol. Biol. 142 (2014), 132–141, 10.1016/j.jsbmb.2013.03.010.
31. Flaws, J.A., Doerr, J.K., Sipes, I.G., Hoyer, P.B., Destruction of preantral follicles in adult rats by 4-vinyl-1-cyclohexene diepoxide. Reprod. Toxicol. 8:6 (1994), 509–514.
32. Fleming, R., Kelsey, T., Anderson, R., Wallace, W., Nelson, S., Interpreting human follicular recruitment and antiMüllerian hormone concentrations throughout life. Fertil. Steril., 98, 2012, 10971102.
33. Frick, K., Baxter, M., Markowska, A., Olton, D., Price, D., Age-related spatial reference and working memory deficits assessed in the water maze. Neurobiol. Aging 16:2 (1995), 149–160, 10.1016/0197-4580(94)00155-3.
34. Frye, J.B., Lukefahr, A.L., Wright, L.E., Marion, S.L., Hoyer, P.B., Funk, J.L., Modeling perimenopause in Sprague Dawley rats by chemical manipulation of the transition to ovarian failure. Comp. Med. 62:3 (2012), 193–202, 10.1148/106.2.470a.
35. Fugate Woods, N., Sullivan Mitchell, E., Adams, C., Memory functioning among midlife women: observations from the Seattle midlife women's health study. Menopause 7:4 (2000), 257–265.
36. Gougeon, A., Chainy, G.B., Morphometric studies of small follicles in ovaries of women at different ages. J. Reprod. Fertil. 81:2 (1987), 433–442.
37. Haas, J., Christian, P., Hoyer, P., Effects of impending ovarian failure induced by 4-vinylcyclohexene diepoxide on fertility in C57BL/6 female mice. Comp. Med. 57:5 (2007), 443–449.
38. Hale, G., Robertson, D., Burger, H., The perimenopausal woman: endocrinology and management. J. Steroid Biochem. Mol. Biol. 142 (2014), 121–131, 10.1016/j.jsbmb.2013.08.015.
39. Hall, M.J., DeFrances, C.J., Williams, S.N., Golosinskiy, A., Schwartzman, A., National hospital discharge survey: 2007 summary. Natl. Health Stat. Rep., 29(1–20), 2010, 24.
40. Hirshfield, A., Development of follicles in the mammalian ovary. Int. Rev. Cytol. 124 (1991), 43–101.
41. Hoffman, B.L., Schorge, J.O., Schaffer, J.I., Halvorson, L.M., Bradshaw, K.D., Cunningham, F.G., Calver, L.E., Fried, A., Boyle, P.J., (eds.) Williams Gynecology, 2nd edition, 2012, McGraw-Hill, New York.
42. Hoyer, P., Devine, P., Hu, X., Thompson, K., Sipes, I., Ovarian toxicity of 4-vinylcyclohexene diepoxide: a mechanistic model. Toxicol. Pathol. 29:1 (2001), 91–99, 10.1080/019262301301418892.
43. Hu, X., Christian, P., Sipes, I., Hoyer, P., Expression and redistribution of cellular Bad, Bax, and Bcl-xL protein is associated with VCD-induced ovotoxicity in rats. Biol. Reprod. 65:5 (2001), 1489–1495, 10.1095/biolreprod65.5.1489.
44. Hu, X., Christian, P., Thompson, K., Sipes, I., Hoyer, P., Apoptosis induced in rats by 4-vinylcyclohexene diepoxide is associated with activation of the caspase cascades. Biol. Reprod. 65:1 (2001), 87–93, 10.1095/biolreprod65.1.87.
45. Huynh, H., Feldt, L.S., Estimation of the box correlation for degrees of freedom from sample data in randomized bloc and split-plot designs. J. Educ. Stat. 1:1 (1976), 69–82.
46. Hyde, L.A., Sherman, G.F., Denenberg, V.H., Non-spatial water radial-arm maze learning in mice. Brain Res. 863:1–2 (2000), 151–159, 10.1016/S0006-8993(00)02113-2.
47. Kang, Y., Anderson, W.A., DeSombre, E.R., Modulation of uterine morphology and growth by estradiol-17β and an estrogen antagonist. J. Cell Biol. 64 (1975), 682–691.
48. Kao, S., Sipes, I., Hoyer, P., Early effects of ovotoxicity induced by 4-vinylcyclohexene diepoxide in rats and mice. Reprod. Toxicol. 13:1 (1999), 67–75, 10.1016/S0890-6238(98)00061-6.
49. Koebele, S.V., Bimonte-Nelson, H., Trajectories and phenotypes with estrogen exposures across the lifespan: what does goldilocks have to do with it?. Horm. Behav., 2015, 10.1016/j.yhbeh.2015.06.009.
50. Koebele, S.V., Bimonte-Nelson, H.A., Modeling menopause: the utility of rodents in translational behavioral endocrinology research. Maturitas 87 (2016), 5–17, 10.1016/j.maturitas.2016.01.015 (PMID: 27013283).
51. Korol, D.L., Malin, E.L., Borden, K.A., Busby, R.A., Couper-Leo, J., Shifts in preferred learning strategy across the estrous cycle in female rats. Horm. Behav. 45 (2004), 330–338, 10.1016/j.yhbeh.2004.01.005.
52. Lacreuse, A., Kim, C.B., Rosene, D.L., Killiany, R.J., Moss, M.B., Moore, T.L., Chennareddi, L., Herndon, J.G., Sex, age, and training modulate spatial memory in the rhesus monkey (Macaca mulatta). Behav. Neurosci., 119, 2005, 118e126.
53. Lohff, J.C., Christian, P.J., Marion, S.L., Arrandale, A., Hoyer, P.B., Characterization of cyclicity and hormonal profile with impending ovarian failure in a novel chemical-induced mouse model of perimenopause. Comp. Med. 55:6 (2005), 523–527.
54. Markowska, A., Life-long diet restriction failed to retard cognitive aging in Fischer-344 rat. Neurobiol. Aging 20:2 (1999), 177–189, 10.1016/S0197-4580(99)00031-7.
55. Markowska, A., Sex dimorphisms in the rate of age-related decline in spatial memory: relevance to alterations in the estrous cycle. J. Neurosci. 19:18 (1999), 8122–8133.
56. Markowska, A., Breckler, S., Behavioral biomarkers of aging: illustration of a multivariate approach for detecting age-related behavioral changes. J. Gerontol. A Biol. Sci. Med. Sci. 54:12 (1999), B549–B566, 10.1093/gerona/54.12.B549.
57. Markowska, A.L., Savonenko, A.V., Protective effect of practice on cognition during aging: implications for predictive characteristics of performance and efficacy of practice. Neurobiol. Learn. Mem., 78, 2002, 294e320.
58. Markowska, A.L., Savovnenko, A.V., Effectiveness of estrogen replacement in restoration of cognitive function after long-term estrogen withdrawal in aging rats. J. Neurosci. 22:24 (2002), 10985–10995.
59. Mayer, L., Pearsall, N., Christian, P., Devine, P., Payne, C., McCuskey, M.,. Hoyer, P., Long-term effects of ovarian follicular depletion in rats by 4-vinylcyclohexene diepoxide. Reprod. Toxicol. 16:6 (2002), 775–781, 10.1016/S0890-6238(02)00048-5.
60. Mayer, L., Devine, P., Dyer, C., Hoyer, P., The follicle-deplete mouse ovary produces androgen. Biol. Reprod. 71:1 (2004), 130–138, 10.1095/biolreprod.103.016113.
61. Mayer, L., Dyer, C., Eastgard, R., Hoyer, P., Banka, C., Atherosclerotic lesion development in a novel ovary-intact mouse model of perimenopause. Arterioscler. Thromb. Vasc. Biol. 25:9 (2005), 1910–1916, 10.1161/01.ATV.0000175767.46520.6a.
62. Meites, J., Lu, J.K.H., Reproductive aging and neuroendocrine function. Charlton, H.M., (eds.) Oxford Review of Reproductive Biology, 1994, Oxford Press, New York, NY, USA.
63. Mennenga, S., Koebele, S., Mousa, A., Alderete, T., Tsang, C., Acosta, J.,. Bimonte-Nelson, H., Pharmacological blockade of the aromatase enzyme, but not the androgen receptor, reverses androstenedione-induced cognitive impairments in young surgically menopausal rats. Steroids 99 (2015), 16–25, 10.1016/j.steroids.2014.08.010.
64. Mennenga, S., Gerson, J., Koebele, S., Kingston, M., Tsang, C., Engler-Chiurazzi, E.,. Bimonte-Nelson, H., Understanding the cognitive impact of the contraceptive estrogen ethinyl estradiol: tonic and cyclic administration impairs memory, and performance correlates with basal forebrain cholinergic system integrity. Psychoneuroendocrinology 54 (2015), 1–13, 10.1016/j.psyneuen.2015.01.002.
65. Morris, R., Garrud, P., Rawlins, J., O'Keefe, J., Place navigation impaired in rats with hippocampal lesions. Nature 297:5868 (1982), 681–683, 10.1038/297681a0.
66. Murray, C., Barber, R., Foreman, K., Ozgoren, A., Abd-Allah, F.,. Vos, T., Global, regional, and national disability-adjusted life years (DALYs) for 306 diseases and injuries and healthy life expectancy (HALE) for 188 countries, 1990–2013: quantifying the epidemiological transition. Lancet, 2015, 10.1016/S0140-6736(15)61340-X.
67. Nappi, R.E., Sinforiani, E., Mauri, M., Bono, G., Polatti, F., Nappi, G., Memory functioning at menopause: impact of age in ovariectomized women. Gynecol. Obstet. Investig. 47 (1999), 29–36.
68. North American Menopause Society (NAMS), A Clinician's Guide. 5th edition, 2015.
69. O'Connor, K.A., Ferrell, R., Brindle, E., Trumble, B., Shofer, J., Holman, D.J., Weinstein, M., Progesterone and ovulation across stages of the transition to menopause. Menopause 16:6 (2009), 1178–1187, 10.1097/gme.0b013e3181aa192d.
70. Olejnik, S., Algina, J., Generalized eta and omega squared statistics: measures of effect size for some common research designs. Psychol. Methods 8:4 (2003), 434–447.
71. Pal, L., Santoro, N., Premature ovarian failure (POF): discordance between somatic and reproductive aging. Ageing Res. Rev. 1:3 (2002), 413–423.
72. Poe, G.R., Teed, R.G.W., Insel, N., White, R., McNaughton, B.L., Barnes, C.A., Partial hippocampal inactivation: effects on spatial memory performance in aged and young rats. Behav. Neurosci. 114:5 (2000), 940–949.
73. Rocca, W.A., Bower, J.H., Maraganore, D.M., Ahlskog, J.E., Grossardt, B.R., de Andrade, M., Melton, L.J. 3rd, Increased risk of cognitive impairment or dementia in women who underwent oophorectomy before menopause. Neurology 69:11 (2007), 1074–1083.
74. Rocca, W., Grossardt, B.R., Shuster, L.T., Oophorectomy, menopause, estrogen treatment, and cognitive aging: clinical evidence for a window of opportunity. Brain Res. 1379 (2011), 188–198.
75. Rocca, W., Grossardt, B.R., Shuster, L.T., Stewart, E.A., Hysterectomy, oophorectomy, estrogen, and the risk of dementia. Neurodegener. Dis. 10:1–4 (2012), 175–178, 10.1159/000334764.
76. Ryan, J., Scali, J., Carriere, I., Amieva, H., Rouaud, O., Berr, C., Ritchie, K., Ancelin, M.-L., Impact of a premature menopause on cognitive function in later life. BJOG 121:13 (2014), 1729–1739, 10.1111/1471-0528.12828.
77. Samson, R.D., Venkatesh, A., Lester, A.W., Weinstein, A.T., Lipa, P., Barnes, C.A., Age differences in strategy selection and risk preference during risk-based decision making. Behav. Neurosci. 129:2 (2015), 138–148, 10.1037/bne0000037.
78. Shuster, L.T., Rhodes, D.J., Gostout, B.S., Grossardt, B.R., Rocca, W.A., Premature menopause or early menopause: long-term health consequences. Maturitas 65:2 (2010), 161–166, 10.1016/j.maturitas.2009.08.003.
79. Simpson, J., Rajkovic, A., Ovarian differentiation and gonadal failure. Am. J. Med. Genet. 89:4 (1999), 186–200.
80. Singh, G.K., Kochanek, K.D., MacDorman, M.F., Advance Report of Final Mortality Statistics, 1994. Monthly Vital Statistics Report CDC/NCHS, 45(3S), 1996, 1–80.
81. Soules, M., Sherman, S., Parrott, E., Rebar, R., Santoro, N., Utian, W., Woods, N., Executive summary: stages of reproductive aging workshop (STRAW). Fertil. Steril. 76:5 (2001), 874–878, 10.1016/S0015-0282(01)02909-0.
82. Springer, L., Flaws, J., Sipes, I., Hoyer, P., Follicular mechanisms associated with 4-vinylcyclohexene diepoxide-induced ovotoxicity in rats. Reprod. Toxicol. 10:2 (1996), 137–143, 10.1016/0890-6238(95)02056-X.
83. Springer, L., McAsey, M.E., Flaws, J., Tilly, J.L., Sipes, I., Hoyer, P., Involvement of apoptosis in 4-vinylcyclohexene diepoxide-induced ovotoxicity in rats. Toxicol. Appl. Pharmacol. 139:2 (1996), 394–401, 10.1006/taap.1996.0180.
84. Springer, L., Tilly, J., Sipes, I., Hoyer, P., Enhanced expression of bax in small preantral follicles during 4-vinylcyclohexene diepoxide-induced ovotoxicity in the rat. Toxicol. Appl. Pharmacol. 139:2 (1996), 402–410, 10.1006/taap.1996.0181.
85. Sullivan Mitchell, E., Fugate Woods, N., Midlife women's attributions about perceived memory changes: observations from the Seattle midlife women's health study. J. Womens Health Gend. Based Med. 10:4 (2001), 351–362.
86. Talboom, J., West, S., Engler-Chiurazzi, E., Enders, C., Crain, I., Bimonte-Nelson, H., Learning to remember: cognitive training-induced attenuation of age-related memory decline depends on sex and cognitive demand, and can transfer to untrained cognitive domains. Neurobiol. Aging, 35(12), 2014, 27912802, 10.1016/j.neurobiolaging.2014.06.008.
87. The World Factbook 2014–15, Washington, DC: Central Intelligence Agency. https://www.cia.gov/library/publications/the-world-factbook/index.html, 2015.
88. Timiras, P., Quay, W., Vernadakis, A., Horm. Aging. 1995, CRC Press, Boca Raton. NY.
89. Tulving, E., Craik, F.I.M., (eds.) The Oxford Handbook of Memory, 2000, Oxford University Press, New York, NY.
90. Weber, M., Mapstone, M., Staskiewicz, J., Maki, P.M., Reconciling subjective memory complaints with objective memory performance in the menopausal transition. Menopause 19:7 (2012), 735–741, 10.1097/gme.0b013e318241fd22.
91. Weber, M.T., Rubin, L.H., Maki, P.M., Cognition in perimenopause: the effect of the transition stage. Menopause 20:5 (2013), 511–517, 10.1097/GME.0b013e31827655e5.
92. Weber, M.T., Maki, P.M., McDermott, M.P., Cognition and mood in perimenopause: a systematic review and meta-analysis. J. Steroid Biochem. Mol. Biol. 142 (2014), 90–98, 10.1016/j.jsbmb.2013.06.001.
93. Wise, P.M., Neuroendocrine modulation and repercussions of female reproductive aging. J. Phys. Colloq. 57 (2002), 235–256.
94. Wise, P.M., Weiland, N.G., Scarbrough, K., Sortino, M.A., Cohen, I.R., Larson, G.H., Changing hypothalamopituitary function: its role in aging of the female reproductive system. Horm. Res. 31 (1989), 39–44.
95. Wise, P.M., Krajnak, K.M., Kashon, M.L., Menopause: the aging of multiple pacemarkers. Science 273 (1996), 67–70.
96. Wise, P.M., Kashon, M.L., Krajnak, K.M., Rosewell, K.L., Cai, A., Scarbrough, K., Harney, J.P., McShane, T., Lloyd, J.M., Weiland, N.G., Aging of the female reproductive system: a window into brain aging. Recent Prog. Horm. Res. 52 (1997), 279–305.
97. Wise, P., Smith, M., Dubal, D., Wilson, M., Krajnak, K., Rosewell, K., Neuroendocrine influences and repercussions of the menopause. Endocr. Rev. 20 (1999), 243–248.
98. Xu, J.Q., Kochanek, K.D., Murphy, S.L., Arias, E., Mortality in the United States, 2012. NCHS Data Brief, No. 168, 2014, National Center for Health Statistics, Hyattsville, MD.