High serum androstenedione levels correlate with impaired memory in the surgically menopausal rat: A replication and new findings

European Journal of Neuroscience

Volumn 36, Issue 8, 2012, Pages 3086-3095

  Camp, Bryan W ^a,b   Gerson, Julia E ^a   Tsang, Candy Wing S ^a   Villa, Stephanie R ^a   Acosta, Jazmin I ^a,b   Blair Braden, B ^a,b   Hoffman, Ann N ^a   Conrad, Cheryl D ^a   Bimonte Nelson, Heather A ^a,b  

^a ARIZONA STATE UNIVERSITY   (United States)

^b ARIZONA ALZHEIMER S CONSORTIUM   (United States)

Author keywords

Aging; Animal model; GABA; Ovariectomy; Working memory

Indexed keywords

4 AMINOBUTYRIC ACID; ANDROSTENEDIONE; GLUTAMATE DECARBOXYLASE;

ANATOMICAL VARIATION; ANDROSTENEDIONE BLOOD LEVEL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN REGION; COGNITION; CORRELATION ANALYSIS; ELECTROENCEPHALOGRAM; ENTORHINAL CORTEX; ENZYME ACTIVITY; FEMALE; GABAERGIC SYSTEM; MAZE TEST; MEMORY CONSOLIDATION; MEMORY DISORDER; MENOPAUSE; NEUROTOXICITY; NONHUMAN; OVARIECTOMY; PRIORITY JOURNAL; RAT; REFERENCE MEMORY; SPATIAL MEMORY; TASK PERFORMANCE; WORKING MEMORY;

ANDROSTENEDIONE; ANIMALS; ENTORHINAL CORTEX; FEMALE; GLUTAMATE DECARBOXYLASE; MAZE LEARNING; MEMORY DISORDERS; MEMORY, SHORT-TERM; MENOPAUSE; OVARIECTOMY; RATS; RATS, INBRED F344; RETENTION (PSYCHOLOGY);

EID: 84867521890     PISSN: 0953816X     EISSN: 14609568     Source Type: Journal    
DOI: 10.1111/j.1460-9568.2012.08194.x     Document Type: Article

References (57)

1. Acosta, J.I., Mayer, L., Talboom, J.S., Tsang, C.W., Smith, C.J., Enders, C.K. & Bimonte-Nelson, H.A. (2009a) Transitional versus surgical menopause in a rodent model: etiology of ovarian hormone loss impacts memory and the acetylcholine system. Endocrinology, 151, 3795-3804.
2. Acosta, J.I., Mayer, L., Talboom, J.S., Zay, C., Scheldrup, M., Castillo, J., Demers, L.M., Enders, C.K. & Bimonte-Nelson, H.A. (2009b) Premarin improves memory, prevents scopolamine-induced amnesia and increases number of basal forebrain choline acetyltransferase positive cells in middle-aged surgically menopausal rats. Horm. Behav., 55, 454-464.
3. Acosta, J.I., Mayer, L.P., Braden, B.B., Nonnenmacher, S., Mennenga, S.E. & Bimonte-Nelson, H.A. (2010) The cognitive effects of conjugated equine estrogens depend on whether menopause etiology is transitional or surgical. Endocrinology, 151, 3795-3804.
4. Barha, C.K., Dalton, G.L. & Galea, L.A. (2010) Low doses of 17alpha-estradiol and 17beta-estradiol facilitate, whereas higher doses of estrone and 17alpha- and 17beta-estradiol impair, contextual fear conditioning in adult female rats. Neuropsychopharmacology, 35, 547-559.
5. Bauer, C.A., Brozoski, T.J., Holder, T.M. & Caspary, D.M. (2000) Effects of chronic salicylate on GABAergic activity in rat inferior colliculus. Hear. Res., 147, 175-182.
6. Bellani, R., Luecken, L.J. & Conrad, C.D. (2006) Peripubertal anxiety profile can predict predisposition to spatial memory impairments following chronic stress. Behav. Brain Res., 166, 263-270.
7. Benice, T.S. & Raber, J. (2009) Testosterone and dihydrotestosterone differentially improve cognition in aged female mice. Learn. Mem., 16, 479-485.
8. Bimonte, H.A. & Denenberg, V.H. (1999) Estradiol facilitates performance as working memory load increases. Psychoneuroendocrinology, 24, 161-173.
9. Bimonte, H.A., Hyde, L.A., Hoplight, B.J. & Denenberg, V.H. (2000) In two species, females exhibit superior working memory and inferior reference memory on the water radial-arm maze. Physiol. Behav., 70, 311-317.
10. Bimonte-Nelson, H.A., Singleton, R.S., Hunter, C.L., Price, K.L., Moore, A.B. & Granholm, A.C. (2003a) Ovarian hormones and cognition in the aged female rat: I. Long-term, but not short-term, ovariectomy enhances spatial performance. Behav. Neurosci., 117, 1395-1406.
11. Bimonte-Nelson, H.A., Singleton, R.S., Nelson, M.E., Eckman, C.B., Barber, J., Scott, T.Y. & Granholm, A.C. (2003b) Testosterone, but not nonaromatizable dihydrotestosterone, improves working memory and alters nerve growth factor levels in aged male rats. Exp. Neurol., 181, 301-312.
12. Bimonte-Nelson, H.A., Francis, K.R., Umphlet, C.D. & Granholm, A.C. (2006) Progesterone reverses the spatial memory enhancements initiated by tonic and cyclic oestrogen therapy in middle-aged ovariectomized female rats. Eur. J. Neurosci., 24, 229-242.
13. Birzniece, V., Turkmen, S., Lindblad, C., Zhu, D., Johansson, I.M., Backstrom, T. & Wahlstrom, G. (2006) GABA(A) receptor changes in acute allopregnanolone tolerance. Eur. J. Pharmacol., 535, 125-134.
14. Braden, B.B., Talboom, J.S., Crain, I.D., Simard, A.R., Lukas, R.J., Prokai, L., Scheldrup, M.R., Bowman, B.L. & Bimonte-Nelson, H.A. (2010) Medroxyprogesterone acetate impairs memory and alters the GABAergic system in aged surgically menopausal rats. Neurobiol. Learn. Mem., 93, 444-453.
15. 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. (2011) Cognitive-impairing effects of medroxyprogesterone acetate in the rat: independent and interactive effects across time. Psychopharmacology, 218, 405-418.
16. Brioni, J.D., Nagahara, A.H. & McGaugh, J.L. (1989) Involvement of the amygdala GABAergic system in the modulation of memory storage. Brain Res., 487, 105-112.
17. Castellano, C. & McGaugh, J.L. (1990) Effects of post-training bicuculline and muscimol on retention: lack of state dependency. Behav. Neural. Biol., 54, 156-164.
18. Castellano, C., Introini-Collison, I.B. & McGaugh, J.L. (1993) Interaction of beta-endorphin and GABAergic drugs in the regulation of memory storage. Behav. Neural. Biol., 60, 123-128.
19. Davis, D.M., Jacobson, T.K., Aliakbari, S. & Mizumori, S.J. (2005) Differential effects of estrogen on hippocampal- and striatal-dependent learning. Neurobiol. Learn. Mem., 84, 132-137.
20. Edinger, K.L., Lee, B. & Frye, C.A. (2004) Mnemonic effects of testosterone and its 5alpha-reduced metabolites in the conditioned fear and inhibitory avoidance tasks. Pharmacol. Biochem. Behav., 78, 559-568.
21. Enders, C.K. & Tofighi, D. (2007) Centering predictor variables in cross-sectional multilevel models: a new look at an old issue. Psychol. Methods, 12, 121-138.
22. Engler-Chiurazzi, E., Talboom, J.S., Braden, B.B., Tsang, C.W.S., Mennenga, S., Andrews, M., Demers, L.M. & Bimonte-Nelson, H.A. (2012) Tonic 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, 1-9.
23. Erlander, M.G. & Tobin, A.J. (1991) The structural and functional heterogeneity of glutamic acid decarboxylase: a review. Neurochem. Res., 16, 215-226.
24. Farr, S.A., Banks, W.A., Uezu, K., Gaskin, F.S. & Morley, J.E. (2004) DHEAS improves learning and memory in aged SAMP8 mice but not in diabetic mice. Life Sci., 75, 2775-2785.
25. Farrag, A.K., Khedr, E.M., Abdel-Aleem, H. & Rageh, T.A. (2002) Effect of surgical menopause on cognitive functions. Dement. Geriatr. Cogn. Disord., 13, 193-198.
26. Flood, J.F. & Roberts, E. (1988) Dehydroepiandrosterone sulfate improves memory in aging mice. Brain Res., 448, 178-181.
27. Flood, J.F., Farr, S.A., Kaiser, F.E., La Regina, M. & Morley, J.E. (1995) Age-related decrease of plasma testosterone in SAMP8 mice: replacement improves age-related impairment of learning and memory. Physiol. Behav., 57, 669-673.
28. Frick, K.M., Baxter, M.G., Markowska, A.L., Olton, D.S. & Price, D.L. (1995) Age-related spatial reference and working memory deficits assessed in the water maze. Neurobiol. Aging, 16, 149-160.
29. Goldman, J.M., Murr, A.S. & Cooper, R.L. (2007) The rodent estrous cycle: characterization of vaginal cytology and its utility in toxicological studies. Birth Defects Res. B Dev. Reprod. Toxicol., 80, 84-97.
30. Grodin, J.M., Siiteri, P.K. & MacDonald, P.C. (1973) Source of estrogen production in postmenopausal women. J. Clin. Endocrinol. Metab., 36, 207-214.
31. Hallahan, M. & Rosenthal, R. (2000) Interpreting and reporting results. In Tinsley, H.E.A. & Brown, S.D. (Eds), Handbook of Multivariate Statistics and Mathematical Modeling. Academic Press, San Diego, CA, pp. 183-208.
32. Horie, K., Takakura, K., Imai, K., Liao, S. & Mori, T. (1992) Immunohistochemical localization of androgen receptor in the human endometrium, decidua, placenta and pathological conditions of the endometrium. Hum. Reprod., 7, 1461-1466.
33. Huynh, T.N., Krigbaum, A.M., Hanna, J.J. & Conrad, C.D. (2011) Sex differences and phase of light cycle modify chronic stress effects on anxiety and depressive-like behavior. Behav. Brain Res., 222, 212-222.
34. Hyde, L.A., Stavnezer, A.J., Bimonte, H.A., Sherman, G.F. & Denenberg, V.H. (2002) Spatial and nonspatial Morris maze learning: impaired behavioral flexibility in mice with ectopias located in the prefrontal cortex. Behav. Brain Res., 133, 247-259.
35. Izquierdo, I., Medina, J.H., Bianchin, M., Walz, R., Zanatta, M.S., Da Silva, R.C., Bueno e Silva, M., Ruschel, A.C. & Paczko, N. (1993) Memory processing by the limbic system: role of specific neurotransmitter systems. Behav. Brain Res., 58, 91-98.
36. Jasuja, R., Ramaraj, P., Mac, R.P., Singh, A.B., Storer, T.W., Artaza, J., Miller, A., Singh, R., Taylor, W.E., Lee, M.L., Davidson, T., Sinha-Hikim, I., Gonzalez-Cadavid, N. & Bhasin, S. (2005) Delta-4-androstene-3, 17-dione binds androgen receptor, promotes myogenesis in vitro, and increases serum testosterone levels, fat-free mass, and muscle strength in hypogonadal men. J. Clin. Endocrinol. Metab., 90, 855-863.
37. Knowles, W.D. (1992) Normal anatomy and neurophysiology of the hippocampal formation. J. Clin. Neurophysiol., 9, 252-263.
38. Korol, D.L. (2004) Role of estrogen in balancing contributions from multiple memory systems. Neurobiol. Learn. Mem., 82, 309-323.
39. Lea, C.K. & Flanagan, A.M. (1998) Physiological plasma levels of androgens reduce bone loss in the ovariectomized rat. Am. J. Physiol., 274, E328-E335.
40. Milbrandt, J.C., Holder, T.M., Wilson, M.C., Salvi, R.J. & Caspary, D.M. (2000) GAD levels and muscimol binding in rat inferior colliculus following acoustic trauma. Hear. Res., 147, 251-260.
41. Morris, R.G., Garrud, P., Rawlins, J.N. & O'Keefe, J. (1982) Place navigation impaired in rats with hippocampal lesions. Nature, 297, 681-683.
42. Nantermet, P.V., Masarachia, P., Gentile, M.A., Pennypacker, B., Xu, J., Holder, D., Gerhold, D., Towler, D., Schmidt, A., Kimmel, D.B., Freedman, L.P., Harada, S. & Ray, W.J. (2005) Androgenic induction of growth and differentiation in the rodent uterus involves the modulation of estrogen-regulated genetic pathways. Endocrinology, 146, 564-578.
43. Nappi, R.E., Sinforiani, E., Mauri, M., Bono, G., Polatti, F. & Nappi, G. (1999) Memory functioning at menopause: impact of age in ovariectomized women. Gynecol. Obstet. Invest., 47, 29-36.
44. Pandey, S.C., Zhang, D., Mittal, N. & Nayyar, D. (1999) Potential role of the gene transcription factor cyclic AMP-responsive element binding protein in ethanol withdrawal-related anxiety. J. Pharmacol. Exp. Ther., 288, 866-878.
45. Paxinos, G. & Watson, C. (1998) The Rat Brain in Stereotaxic Coordinates, 4th edn. Academic Press, New York.
46. Raber, J., Bongers, G., LeFevour, A., Buttini, M. & Mucke, L. (2002) Androgens protect against apolipoprotein E4-induced cognitive deficits. J. Neurosci., 22, 5204-5209.
47. Rasband, W.S. (1997-2012) ImageJ, U.S. National Institutes of Health, Bethesda, Maryland, USA. Available at: http://imagej.nih.gov/ij/.
48. Reddy, D.S. & Jian, K. (2010) The testosterone-derived neurosteroid androstanediol is a positive allosteric modulator of GABAA receptors. J. Pharmacol. Exp. Ther., 334, 1031-1041.
49. Ruizeveld de Winter, J.A., Trapman, J., Vermey, M., Mulder, E., Zegers, N.D. & van der Kwast, T.H. (1991) Androgen receptor expression in human tissues: an immunohistochemical study. J. Histochem. Cytochem., 39, 927-936.
50. Schmidt, W.N. & Katzenellenbogen, B.S. (1979) Androgen-uterine interactions: an assessment of androgen interaction with the testosterone- and estrogen-receptor systems and stimulation of uterine growth and progesterone-receptor synthesis. Mol. Cell. Endocrinol., 15, 91-108.
51. Sprando, R.L., Collins, T.F., Black, T.N., Olejnik, N., Grundel, E. & Ruggles, D.I. (2004) Effects of androstenedione on in utero development in rats. Food Chem. Toxicol., 42, 917-924.
52. Talboom, J.S., Williams, B.J., Baxley, E.R., West, S.G. & Bimonte-Nelson, H.A. (2008) Higher levels of estradiol replacement correlate with better spatial memory in surgically menopausal young and middle-aged rats. Neurobiol. Learn. Mem., 90, 155-163.
53. Talboom, J.S., Engler-Chiurazzi, E.B., Whiteaker, P., Simard, A.R., Lukas, R., Acosta, J.I., Prokai, L. & Bimonte-Nelson, H.A. (2010) A component of Premarin((R)) enhances multiple cognitive functions and influences nicotinic receptor expression. Horm. Behav., 58, 917-928.
54. Weber, M. & Mapstone, M. (2009) Memory complaints and memory performance in the menopausal transition. Menopause, 16, 694-700.
55. Yonkov, D.I. & Georgiev, V.P. (1985) Memory effects of GABA-ergic antagonists in rats trained with two-way active avoidance tasks. Acta Physiol. Pharmacol. Bulg., 11, 44-49.
56. Yonkov, D., Georgiev, V., Kambourova, T. & Opitz, M. (1987) Participation of angiotensin II in learning and memory. III. Interactions of angiotensin II with GABAergic drugs. Methods Find. Exp. Clin. Pharmacol., 9, 205-208.
57. Zarrindast, M.R., Shamsi, T., Azarmina, P., Rostami, P. & Shafaghi, B. (2004) GABAergic system and imipramine-induced impairment of memory retention in rats. Eur. Neuropsychopharmacol., 14, 59-64s.