Estradiol alters Fos-immunoreactivity in the hippocampus and dorsal striatum during place and response learning in middle-aged but not young adult female rats

Endocrinology

Volumn 152, Issue 3, 2011, Pages 946-956

  Pleil, Kristen E ^a   Glenn, Melissa J ^b   Williams, Christina L ^a  

^a DUKE UNIVERSITY   (United States)

^b University of Connecticut   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ESTRADIOL; PROTEIN FOS;

ANIMAL EXPERIMENT; ARTICLE; CELL COUNT; CONTROLLED STUDY; CORPUS STRIATUM; DENTATE GYRUS; FEMALE; HIPPOCAMPUS; IMMUNOREACTIVITY; LEARNING; NONHUMAN; OVARIECTOMY; PRIORITY JOURNAL; RAT;

AGING; ANIMALS; ESTRADIOL; FEMALE; HIPPOCAMPUS; LEARNING; OVARIECTOMY; PROTO-ONCOGENE PROTEINS C-FOS; RATS; RATS, SPRAGUE-DAWLEY;

EID: 79951929236     PISSN: 00137227     EISSN: 00137227     Source Type: Journal    
DOI: 10.1210/en.2010-0715     Document Type: Article

References (63)

1. Olton DS, Papas BC 1979 Spatial memory and hippocampal function. Neuropsychologia 17:669-682 (Pubitemid 10167907)
2. Chang Q, Gold PE 2003 Intra-hippocampal lidocaine injections impair acquisition of a place task and facilitate acquisition of a response task in rats. Behav Brain Res 144:19-24 (Pubitemid 37011162)
3. Mitchell JA, Hall G 1988 Caudate-putamen lesions in the rat may impair or potentiate maze learning depending upon availability of stimulus cues and relevance of response cues. Q J Exp Psychol B 40:243-258
4. Devan BD, McDonald RJ, White NM 1999 Effects of medial and lateral caudate-putamen lesions on place- and cue-guided behaviors in the water maze: relation to thigmotaxis. Behav Brain Res 100: 5-14 (Pubitemid 29130236)
5. White NM, McDonald RJ 2002 Multiple parallel memory systems in the brain of the rat. Neurobiol Learn Mem 77:125-184 (Pubitemid 34971650)
6. Korol DL, Kolo LL 2002 Estrogen-induced changes in place and response learning in young adult female rats. Behav Neurosci 116: 411-420 (Pubitemid 34533577)
7. Zurkovsky L, Brown SL, Boyd SE, Fell JA, Korol DL 2007 Estrogen modulates learning in female rats by acting directly at distinct memory systems. Neuroscience 144:26-37 (Pubitemid 44839046)
8. Zurkovsky L, Brown SL, Korol DL 2006 Estrogen modulates place learning through estrogen receptors in the hippocampus. Neurobiol Learn Mem 86:336-343 (Pubitemid 44436982)
9. Joppa MA, Meisel RL, Garber MA 1995 -Fos expression in female hamster brain following sexual and aggressive behaviors. Neuroscience 68:783-792
10. Pfaus JG, Heeb MM 1997 Implications of immediate-early gene induction in the brain following sexual stimulation of female and male rodents. Brain Res Bull 44:397-407 (Pubitemid 27467285)
11. Dudley CA, Rajendren G, Moss RL 1992 Induction of FOS immunoreactivity in central accessory olfactory structures of the female rat following exposure to conspecific males. Mol Cell Neurosci 3:360-369
12. Bennett AL, Greco B, Blasberg ME, Blaustein JD 2002 Response to male odours in progestin receptor- and oestrogen receptor-containing cells in female rat brain. J Neuroendocrinol 14:442-449 (Pubitemid 34537732)
13. Sheehan T, Numan M 2002 Estrogen, progesterone, and pregnancy termination alter neural activity in brain regions that control maternal behavior in rats. Neuroendocrinology 75:12-23 (Pubitemid 34124213)
14. Gill KM, Bernstein IL, Mizumori SJ 2007 Immediate early gene activation in hippocampus and dorsal striatum: effects of explicit place and response training. Neurobiol Learn Mem 87:583-596 (Pubitemid 46483132)
15. Teather LA, Packard MG, Smith DE, Ellis-Behnke RG, Bazan NG 2005 Differential induction of c-Jun and Fos-like proteins in rat hippocampus and dorsal striatum after training in two water maze tasks. Neurobiol Learn Mem 84:75-84 (Pubitemid 41140407)
16. Colombo PJ, Brightwell JJ, Countryman RA 2003 Cognitive strategy-specific increases in phosphorylated cAMP response element-binding protein and c-Fos in the hippocampus and dorsal striatum. J Neurosci 23:3547-3554 (Pubitemid 36531998)
17. Hogervorst E, Williams J, Budge M, Riedel W, Jolles J 2000 The nature of the effect of female gonadal hormone replacement therapy on cognitive function in post-menopausal women: a meta-analysis. Neuroscience 101:485-512
18. Markowska AL 1999 Sex dimorphisms in the rate of age-related decline in spatial memory: relevance to alterations in the estrous cycle. J Neurosci 19:8122-8133 (Pubitemid 30225808)
19. Markham JA, Pych JC, Juraska JM 2002 Ovarian hormone replacement to aged ovariectomized female rats benefits acquisition of the morris water maze. Horm Behav 42:284-293 (Pubitemid 35435622)
20. Talboom JS, Williams BJ, Baxley ER, West SG, Bimonte-Nelson HA 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
21. Bimonte-Nelson HA, Francis KR, Umphlet CD, Granholm AC 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 (Pubitemid 44050682)
22. Daniel JM, Hulst JL, Berbling JL 2006 Estradiol replacement enhances working memory in middle-aged rats when initiated immediately after ovariectomy but not after a long-term period of ovarian hormone deprivation. Endocrinology 147:607-614 (Pubitemid 43004315)
23. Rodgers SP, Bohacek J, Daniel JM 2010 Transient estradiol exposure during middle age in ovariectomized rats exerts lasting effects on cognitive function and the hippocampus. Endocrinology 151: 1194-1203.
24. Morgan JI, Cohen DR, Hempstead JL, Curran T 1987 Mapping patterns of c-fos expression in the central nervous system after seizure. Science 237:192-197
25. Feng Z, Cheng Y, Zhang JT 2004 Long-term effects of melatonin or 17 beta-estradiol on improving spatial memory performance in cognitively impaired, ovariectomized adult rats. J Pineal Res 37:198-206 (Pubitemid 39274118)
26. Ziegler DR, Gallagher M 2005 Spatial memory in middle-aged female rats: assessment of estrogen replacement after ovariectomy. Brain Res 1052:163-173 (Pubitemid 41116774)
27. Roy EJ, Sheinkop S, Wilson MA 1982 Age alters dopaminergic responses to estradiol. Eur J Pharmacol 82:73-75 (Pubitemid 12039145)
28. Markowska AL, Savonenko AV 2002 Effectiveness of estrogen replacement in restoration of cognitive function after long-term estrogen withdrawal in aging rats. J Neurosci 22:10985-10995 (Pubitemid 36005175)
29. Frick KM, Burlingame LA, Arters JA, Berger-Sweeney J 2000 Reference memory, anxiety and estrous cyclicity in C57BL/6NIA mice are affected by age and sex. Neuroscience 95:293-307
30. Bimonte-Nelson HA, Singleton RS, Hunter CL, Price KL, Moore AB, Granholm AC 2003 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
31. Gould E, Woolley CS, Frankfurt M, McEwen BS 1990 Gonadal steroids regulate dendritic spine density in hippocampal pyramidal cells in adulthood. J Neurosci 10:1286-1291
32. Woolley CS, McEwen BS 1993 Roles of estradiol and progesterone in regulation of hippocampal dendritic spine density during the estrous cycle in the rat. J Comp Neurol 336:293-306 (Pubitemid 23289665)
33. Hoffman GE, Lyo D 2002 Anatomical markers of activity in neuroendocrine systems: are we all 'fos-ed out?' J Neuroendocrinol 14:259-268
34. Hoffman GE, Smith MS, Verbalis JG 1993 c-Fos and related immediate early gene products as markers of activity in neuroendocrine systems. Front Neuroendocrinol 14:173-213 (Pubitemid 23195792)
35. Sagar SM, Sharp FR, Curran T 1988 Expression of c-fos protein in brain: metabolic mapping at the cellular level. Science 240:1328-1331
36. Matthews Jr MK, Kenyon R 1984 Four- versus five-day estrous cycles in rats: vaginal cycling and pregnancy. Physiol Behav 33: 65-67 (Pubitemid 15211984)
37. Paxinos G, Watson C 1998 The rat brain in stereotaxic coordinates. New York: Academic Press
38. Packard MG, McGaugh JL 1996 Inactivation of hippocampus or caudate nucleus with lidocaine differentially affects expression of place and response learning. Neurobiol Learn Mem 65:65-72 (Pubitemid 26112655)
39. Dominguez-Salazar E, Shetty S, Rissman EF 2006 Rapid neural Fos responses to oestradiol in oestrogen receptor alphabeta double knockout mice. J Neuroendocrinol 18:195-202
40. Rudick CN, Woolley CS 2000 Estradiol induces a phasic Fos response in the hippocampal CA1 and CA3 regions of adult female rats. Hippocampus 10:274-283 (Pubitemid 30438663)
41. Pfaff D, Montgomery M, Lewis C 1977 Somatosensory determinants of lordosis in female rats: behavioral definition of the estrogen effect. J Comp Physiol Psychol 91:134-145 (Pubitemid 8101303)
42. Gresack JE, Kerr KM, Frick KM 2007 Life-long environmental enrichment differentially affects the mnemonic response to estrogen in young, middle-aged, and aged female mice. Neurobiol Learn Mem 88:393-408 (Pubitemid 47513554)
43. Packard MG, Teather LA 1997 Intra-hippocampal estradiol infusion enhances memory in ovariectomized rats. Neuroreport 8:3009-3013 (Pubitemid 27421724)
44. Packard MG, Teather LA 1997 Posttraining estradiol injections enhancememoryin ovariectomized rats: cholinergic blockade and synergism. Neurobiol Learn Mem 68:172-188 (Pubitemid 27413708)
45. Gresack JE, Frick KM 2006 Post-training estrogen enhances spatial and object memory consolidation in female mice. Pharmacol Biochem Behav 84:112-119 (Pubitemid 43975555)
46. Yin HH, Knowlton BJ 2006 The role of the basal ganglia in habit formation. Nat Rev Neurosci 7:464-476 (Pubitemid 44012286)
47. Yin HH, Knowlton BJ, Balleine BW 2004 Lesions of dorsolateral striatum preserve outcome expectancy but disrupt habit formation in instrumental learning. Eur J Neurosci 19:181-189 (Pubitemid 38122084)
48. Finch DM 1996 Neurophysiology of converging synaptic inputs from the rat prefrontal cortex, amygdala, midline thalamus, and hippocampal formation onto single neurons of the caudate/putamen and nucleus accumbens. Hippocampus 6:495-512 (Pubitemid 26413936)
49. Finch DM, Gigg J, Tan AM, Kosoyan OP 1995 Neurophysiology and neuropharmacology of projections from entorhinal cortex to striatum in the rat. Brain Res 670:233-247
50. Dolorfo CL, Amaral DG 1998 Entorhinal cortex of the rat: topographic organization of the cells of origin of the perforant path projection to the dentate gyrus. J Comp Neurol 398:25-48 (Pubitemid 28373875)
51. Hammond R, Nelson D, Gibbs RB 7 August 2010 GPR30 co-localizes with cholinergic neurons in the basal forebrain and enhances potassium-stimulated acetylcholine release in the hippocampus. Psychoneuroendocrinology 10.1016/j.psyneuen.2010.07.007
52. Pych JC, Chang Q, Colon-Rivera C, Haag R, Gold PE 2005 Acetylcholine release in the hippocampus and striatum during place and response training. Learn Mem 12:564-572 (Pubitemid 41770079)
53. Chang Q, Gold PE 2003 Switchingmemorysystems during learning: changes in patterns of brain acetylcholine release in the hippocampus and striatum in rats. J Neurosci 23:3001-3005 (Pubitemid 36418636)
54. Gazzaley AH, Weiland NG, McEwen BS, Morrison JH 1996 Differential regulation of NMDAR1 mRNA and protein by estradiol in the rat hippocampus. J Neurosci 16:6830-6838 (Pubitemid 26359365)
55. Romeo RD, McCarthy JB, Wang A, Milner TA, McEwen BS 2005 Sex differences in hippocampal estradiol-induced N-methyl-D-aspartic acid binding and ultrastructural localization of estrogen receptor-alpha. Neuroendocrinology 81:391-399 (Pubitemid 41779653)
56. Weiland NG 1992 Estradiol selectively regulates agonist binding sites on the N-methyl-D-aspartate receptor complex in the CA1 region of the hippocampus. Endocrinology 131:662-668
57. Woolley CS, Weiland NG, McEwen BS, Schwartzkroin PA 1997 Estradiol increases the sensitivity of hippocampal CA1 pyramidal cells to NMDA receptor-mediated synaptic input: correlation with dendritic spine density. J Neurosci 17:1848-1859 (Pubitemid 27089829)
58. Murphy DD, Segal M 1996 Regulation of dendritic spine density in cultured rat hippocampal neurons by steroid hormones. J Neurosci 16:4059-4068 (Pubitemid 26192402)
59. Daniel JM, Dohanich GP 2001 Acetylcholine mediates the estrogen-induced increase in NMDA receptor binding in CA1 of the hippocampus and the associated improvement in working memory. J Neurosci 21:6949-6956 (Pubitemid 32781137)
60. Leuner B, Falduto J, Shors TJ 2003 Associative memory formation increases the observation of dendritic spines in the hippocampus. J Neurosci 23:659-665 (Pubitemid 36139564)
61. Cyr M, Ghribi O, Di Paolo T 2000 Regional and selective effects of oestradiol and progesterone on NMDA and AMPA receptors in the rat brain. J Neuroendocrinol 12:445-452 (Pubitemid 30223992)
62. Lovinger DM 2010 Neurotransmitter roles in synaptic modulation, plasticity and learning in the dorsal striatum. Neuropharmacology 58:951-961.
63. Yin HH, Mulcare SP, Hilario MR, Clouse E, Holloway T, Davis MI, Hansson AC, Lovinger DM, Costa RM 2009 Dynamic reorganization of striatal circuits during the acquisition and consolidation of a skill. Nat Neurosci 12:333-341