Progesterone enhances learning and memory of aged wildtype and progestin receptor knockout mice

Neuroscience Letters

Volumn 472, Issue 1, 2010, Pages 38-42

  Frye, Cheryl A ^a   Walf, Alicia A ^a  

^a STATE UNIVERSITY OF NEW YORK   (United States)

Author keywords

Aging; Cognition; Estradiol; Estrogen; Learning; Memory

Indexed keywords

PROGESTERONE; PROGESTERONE RECEPTOR;

AGED; ANIMAL EXPERIMENT; ARTICLE; AVOIDANCE BEHAVIOR; COGNITION; CONDITIONING; CONTROLLED STUDY; DRUG MECHANISM; FEMALE; GENOTYPE; KNOCKOUT MOUSE; LEARNING; LIGHT DARK CYCLE; MALE; MEMORY; MOUSE; NONHUMAN; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; WILD TYPE;

AGING; ANIMALS; CHOICE BEHAVIOR; CONDITIONING (PSYCHOLOGY); CUES; EXPLORATORY BEHAVIOR; FEAR; FEMALE; LEARNING; MALE; MAZE LEARNING; MEMORY; MICE; MICE, KNOCKOUT; PROGESTERONE; RECEPTORS, PROGESTERONE;

EID: 76949086563     PISSN: 03043940     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.neulet.2010.01.051     Document Type: Article

References (42)

1. Beason-Held L.L., Golski S., Kraut M.A., Esposito G., and Resnick S.M. Brain activation during encoding and recognition of verbal and figural information in older adults. Neurobiol. Aging 26 (2005) 237-250
2. Bernardi F., Lanzone A., Cento R.M., Spada R.S., Pezzani I., Genazzani A.D., Luisi S., Luisi M., Petraglia F., and Genazzani A.R. Allopregnanolone and dehydroepiandrosterone response to corticotropin-releasing factor in patients suffering from Alzheimer's disease and vascular dementia. Eur. J. Endocrinol. 142 (2000) 466-471
3. Bimonte-Nelson H.A., Singleton R.S., Hunter C.L., Price K.L., Moore A.B., and Granholm A.C. Ovarian hormones and cognition in the aged female rat. I. Long-term, but not short-term, ovariectomy enhances spatial performance. Behav. Neurosci. 117 (2003) 1395-1406
4. Bimonte-Nelson H.A., Singleton R.S., Williams B.J., and Granholm A.C. Ovarian hormones and cognition in the aged female rat. II. Progesterone supplementation reverses the cognitive enhancing effects of ovariectomy. Behav. Neurosci. 118 (2004) 707-714
5. Ennaceur A., Neave N., and Aggleton J.P. Spontaneous object recognition and object location memory in rats: the effects of lesions in the cingulate cortices, the medial prefrontal cortex, the cingulum bundle and the fornix. Exp. Brain Res. 113 (1997) 509-519
6. Farr S.A., Flood J.F., Scherrer J.F., Kaiser F.E., Taylor G.T., and Morley J.E. Effect of ovarian steroids on footshock avoidance learning and retention in female mice. Physiol. Behav. 58 (1995) 715-723
7. Frye C.A. Neurosteroids-from basic research to clinical perspectives. In: Rubin R.T., and Pfaff D.W. (Eds). Hormones/Behavior Relations of Clinical Importance (2009), Academic Press, San Diego 395-416
8. Frye C.A., Duffy C.K., and Walf A.A. Estrogens and progestins enhance spatial learning of intact and ovariectomized rats in the object placement task. Neurobiol. Learn. Mem. 88 (2007) 208-216
9. Frye C.A., and Lacey E.H. Progestins influence performance on cognitive tasks independent of changes in affective behavior. Psychobiology 28 (2001) 550-563
10. Frye C.A., Rhodes M.E., and Dudek B. Estradiol to aged female or male mice improves learning in inhibitory avoidance and water maze tasks. Brain Res. 1036 (2005) 101-108
11. Frye C.A., and Sturgis J.D. Neurosteroids affect spatial/reference, working, and long-term memory of female rats. Neurobiol. Learn. Mem. 64 (1995) 83-96
12. Frye C.A., Sumida K., Dudek B.C., Harney J.P., Lydon J.P., O'Malley B.W., Pfaff D.W., and Rhodes M.E. Progesterone's effects to reduce anxiety behavior of aged mice do not require actions via intracellular progestin receptors. Psychopharmacology 186 (2006) 312-322
13. Frye C.A., Sumida K., Lydon J.P., O'Malley B.W., and Pfaff D.W. Mid-aged and aged wild-type and progestin receptor knockout (PRKO) mice demonstrate rapid progesterone and 3α,5α-THP-facilitated lordosis. Psychopharmacology 185 (2006) 423-432
14. Frye C.A., and Walf A.A. Progesterone enhances performance of aged mice in cortical or hippocampal tasks. Neurosci. Lett. 437 (2008) 116-120
15. Frye C.A., and Walf A.A. Progesterone to ovariectomized mice enhances cognitive performance in the spontaneous alternation, object recognition, but not placement, water maze, and contextual and cued conditioned fear tasks. Neurobiol. Learn. Mem. 90 (2008) 171-177
16. Frye C.A., and Walf A.A. Effects of progesterone administration and APPswe + PSEN1Deltae9 mutation for cognitive performance of mid-aged mice. Neurobiol. Learn. Mem. 89 (2008) 17-26
17. Gibbs R.B. Long-term treatment with estrogen and progesterone enhances acquisition of a spatial memory task by ovariectomized aged rats. Neurobiol. Aging 21 (2000) 107-116
18. Gibbs R.B. Effects of ageing and long-term hormone replacement on cholinergic neurones in the medial septum and nucleus basalis magnocellularis of ovariectomized rats. J. Neuroendocrinol. 15 (2003) 477-485
19. Harburger L.L., Bennett J.C., and Frick K.M. Effects of estrogen and progesterone on spatial memory consolidation in aged females. Neurobiol. Aging 28 (2007) 602-610
20. Hirst J.J., Palliser H.K., Yates D.M., Yawno T., and Walker D.W. Neurosteroids in the fetus and neonate: potential protective role in compromised pregnancies. Neurochem. Int. 52 (2008) 602-610
21. Iswari S., Colas A.E., and Karavolas H.J. Binding of 5α-dihydroprogesterone and other progestins to female rat anterior pituitary nuclear extracts. Steroids 47 (1986) 189-203
22. Izquierdo I., and Medina J.H. Memory formation: the sequence of biochemical events in the hippocampus and its connection to activity in other brain structures. Neurobiol. Learn. Mem. 68 (1997) 285-316
23. Kinsley C.H., and Lambert K.G. Reproduction-induced neuroplasticity: natural behavioural and neuronal alterations associated with the production and care of offspring. J. Neuroendocrinol. 20 (2008) 515-525
24. Klotz U. Effect of age on pharmacokinetics and pharmacodynamics in man. Int. J. Clin. Pharmacol. Ther. 36 (1998) 581-585
25. Lewis M.C., Orr P.T., and Frick K.M. Differential effects of acute progesterone administration on spatial and object memory in middle-aged and aged female C57BL/6 mice. Horm. Behav. 54 (2008) 455-462
26. Li X., Lonard D.M., and O'Malley B.W. A contemporary understanding of progesterone receptor function. Mech. Ageing Dev. 125 (2004) 669-678
27. Lydon J.P., DeMayo F.J., Conneely O.M., and O'Malley B.W. Reproductive phenotypes of the progesterone receptor null mutant mouse. J. Steroid Biochem. Mol. Biol. 56 (1996) 67-77
28. Macbeth A.H., Scharfman H.E., Maclusky N.J., Gautreaux C., and Luine V.N. Effects of multiparity on recognition memory, monoaminergic neurotransmitters, and brain-derived neurotrophic factor (BDNF). Horm. Behav. 54 (2008) 7-17
29. Mani S.K., Blaustein J.D., and O'Malley B.W. Progesterone receptor function from a behavioral perspective. Horm. Behav. 31 (1997) 244-255
30. Markham J.A., Pych J.C., and Juraska J.M. Ovarian hormone replacement to aged ovariectomized female rats benefits acquisition of the morris water maze. Horm. Behav. 42 (2002) 284-293
31. McBride W.J., Murphy J.M., and Ikemoto S. Localization of brain reinforcement mechanisms: intracranial self-administration and intracranial place-conditioning studies. Behav. Brain Res. 101 (1999) 129-152
32. McEchron M.D., Cheng A.Y., and Gilmartin M.R. Trace fear conditioning is reduced in the aging rat. Neurobiol. Learn. Mem. 82 (2004) 71-76
33. Morris R.G.M., Garrud P., Rawlins J.N.P., and O'Keefe J. Place navigation impaired in rats with hippocampal lesions. Nature 297 (1982) 681-683
34. Paris J.J., and Frye C.A. Estrous cycle, pregnancy, and parity enhance performance of rats in object recognition or object placement tasks. Reproduction 136 (2008) 105-115
35. Pawluski J.L., Walker S.K., and Galea L.A. Reproductive experience differentially affects spatial reference and working memory performance in the mother. Horm. Behav. 49 (2006) 143-149
36. Phillips R.G., and LeDoux J.F. Differential contribution of amygdala and hippocampus to cued and contextual fear conditioning. Behav. Neurosci. 106 (1992) 274-285
37. Sandstrom N.J., and Williams C.L. Memory retention is modulated by acute estradiol and progesterone replacement. Behav. Neurosci. 115 (2001) 384-393
38. Sato T., Tanaka K., Ohnishi Y., Teramoto T., Irifune M., and Nishikawa T. Effects of estradiol and progesterone on radial maze performance in middle-aged female rats fed a low-calcium diet. Behav. Brain Res. 150 (2004) 33-42
39. Smith C.D., Wekstein D.R., Markesbery W.R., and Frye C.A. 3α,5α-THP: a potential plasma neurosteroid biomarker in Alzheimer's disease and perhaps non-Alzheimer's dementia. Psychopharmacology 186 (2006) 481-485
40. Smith H.E., Smith R.G., Toft D.O., Neergaard J.R., Burrows E.P., and O'Malley B.W. Binding of steroids to progesterone receptor proteins in chick oviduct and human uterus. J. Biol. Chem. 249 (1974) 5924-5932
41. Wagner C.K. Progesterone receptors and neural development: a gap between bench and bedside?. Endocrinology 149 (2008) 2743-2749
42. Walf A.A., Rhodes M.E., and Frye C.A. Ovarian steroids enhance object recognition in naturally cycling and ovariectomized, hormone-primed rats. Neurobiol. Learn. Mem. 86 (2006) 35-46