Intra-striatal estradiol in female rats impairs response learning within two hours of treatment

Hormones and Behavior

Volumn 60, Issue 5, 2011, Pages 470-477

  Zurkovsky, L ^a   Serio, S J ^a   Korol, D L ^a  

^a UNIVERSITY OF ILLINOIS AT URBANA CHAMPAIGN   (United States)

Author keywords

Caudate nucleus; Egocentric; Estrogens; Habit; Learning strategy; Memory; Navigation; Steroid hormones

Indexed keywords

ESTRADIOL; ESTROGEN RECEPTOR;

ANIMAL EXPERIMENT; ARTICLE; CONTROLLED STUDY; CORPUS STRIATUM; DRUG DOSE COMPARISON; DRUG INFUSION; FEMALE; HORMONE ACTION; LEARNING; NONHUMAN; OVARIECTOMY; PRIORITY JOURNAL; RAT; TASK PERFORMANCE; TRAINING;

ANIMALS; CORPUS STRIATUM; ESTRADIOL; FEMALE; HIPPOCAMPUS; MAZE LEARNING; OVARIECTOMY; RATS; RATS, SPRAGUE-DAWLEY;

EID: 80555150718     PISSN: 0018506X     EISSN: 10956867     Source Type: Journal    
DOI: 10.1016/j.yhbeh.2011.07.014     Document Type: Article

References (62)

1. Andersson C., Hamer R.H., Lawler C.P., Mailman R.B., Lieberman J.A. Striatal volume changes in the rat following long-term administration of typical and atypical antipsychotic drugs. Neuropsychopharmacology 2002, 27:143-151.
2. Becker J.B. Estrogen rapidly potentiates amphetamine-induced striatal dopamine release and rotational behavior during microdialysis. Neurosci. Lett. 1990, 118:169-171.
3. Becker J.B. Direct effect of 17 beta-estradiol on striatum: sex differences in dopamine release. Synapse 1990, 5:157-164.
4. Becker J.B. Gender differences in dopaminergic function in striatum and nucleus accumbens. Pharmacol. Biochem. Behav. 1999, 64:803-812.
5. Becker J.B., Snyder P.J., Miller M.M., Westgate S.A., Jenuwine M.J. The influence of estrous cycle and intrastriatal estradiol on sensorimotor performance in the female rat. Pharmacol. Biochem. Behav. 1987, 27:53-59.
6. Boulware M.I., Kordasiewicz H., Mermelstein P.G. Caveolin proteins are essential for distinct effects of membrane estrogen receptors in neurons. J. Neurosci. 2007, 27:9941-9950.
7. Brailoiu E., Dun S.L., Brailoiu G.C., Mizuo K., Sklar L.A., Oprea T.I., Prossnitz E.R., Dun N.J. Distribution and characterization of estrogen receptor G protein-coupled receptor 30 in the rat central nervous system. J. Endocrinol. 2007, 193:311-321.
8. Chang Q., Gold P.E. Intra-hippocampal lidocaine injections impair acquisition of a place task and facilitate acquisition of a response task in rats. Behav. Brain Res. 2003, 144:19-24.
9. Chang Q., Gold P.E. Inactivation of dorsolateral striatum impairs acquisition of response learning in cue-deficient, but not cue-available, conditions. Behav. Neurosci. 2004, 118:383-388.
10. Colombo P.J., Brightwell J.J., Countryman R.A. Cognitive strategy-specific increases in phosphorylated cAMP response element-binding protein and c-Fos in the hippocampus and dorsal striatum. J. Neurosci. 2003, 23:3547-3554.
11. Daniel J.M., Lee C.D. Estrogen replacement in ovariectomized rats affects strategy selection in the Morris water maze. Neurobiol. Learn. Mem. 2004, 82:142-149.
12. Daniel J.M., Sulzer J.K., Hulst J.L. Estrogen increases the sensitivity of ovariectomized rats to the disruptive effects produced by antagonism of D2 but not D1 dopamine receptors during performance of a response learning task. Horm. Behav. 2006, 49:38-44.
13. Davis D.M., Jacobson T.K., Aliabari S., Mizumori S.J. Differential effects of estrogen on hippocampal- and striatal-dependent learning. Neurobiol. Learn. Mem. 2005, 84:132-137.
14. Diaz-Veliz G., Urresta F., Dussaubat N., Mora S. Effects of estradiol replacement in ovariectomized rats on conditioned avoidance responses and other behaviors I. Physiol. Behav. 1991, 50:61-65.
15. Dohanich G.P., Korol D.L., Shors T. Steroids and Cognition. Hormones, Brain and Behavior 2009, 539-576. Academic Press, New York. 2nd Edition. D. Pfaff, A. Arnold, R. Rubin, S. Fahrbach, A. Etgen (Eds.).
16. Edeline J.M., Hars B., Hennevin E., Cotillon N. Muscimol diffusion after intracerebral microinjections: a reevaluation based on electrophysiological and autoradiographic quantifications. Neurobiol. Learn. Mem. 2002, 78:100-124.
17. Galea L.A., Wide J.K., Paine T.A., Holmes M.M., Ormerod B.K., Floresco S.B. High levels of estradiol disrupt conditioned place preference learning, stimulus response learning and reference memory but have limited effects on working memory. Behav. Brain Res. 2001, 126:115-126.
18. Gold P.E., Korol D.L. Hormones and Memory. Encyclopedia of Behavioral Neuroscience 2010, Volume 2:57-64. Academic Press, Oxford.
19. Gordon J.H. Modulation of apomorphine-induced stereotypy by estrogen: time course and dose response. Brain Res. Bull. 1980, 5:679-682.
20. Gordon J.H., Gorski R.A., Borison R.L., Diamond B.I. Postsynaptic efficacy of dopamine: possible suppression by estrogen. Pharmacol. Biochem. Behav. 1980, 12:515-518.
21. Grove-Strawser D., Boulware M.I., Mermelstien P.G. Membrane estrogen receptors activate the metabotropic glutamate receptors mGluR5 and mGluR3 to bidirectionally regulate CREB phosphorylation in female rat striatal neurons. Neuroscience 2010, 170:1045-1055.
22. Hu M., Watson C.J., Kennedy R.T., Becker J.B. Estradiol attenuates the K+-induced increase in extracellular GABA in rat striatum. Synapse 2006, 59:122-124.
23. Joyce J.N., Smith R.L., van Hartesveldt C. Estradiol suppresses then enhances intracaudate dopamine-induced contralateral deviation. Eur. J. Pharmacol. 1982, 81:117-122.
24. Joyce J.N., Montero E., Van Hartesveldt C. Dopamine-mediated behaviors: characteristics of modulation by estrogen. Pharmacol. Biochem. Behav. 1984, 21:791-800.
25. Kelly M.J., Levin E.R. Rapid actions of plasma membrane estrogen receptors. Trends Endocrinol. Metab. 2001, 12:152-156.
26. Kent M.H., Zurkovsky L., Fornelli D.C., Fell J.A., Korol D.L. Intra-striatal antiestrogen ICI 182,780 attenuates the impairing effects of peripheral estradiol treatment on response learning in young adult ovariectomized rats. Program No. 883.3 2005, Neuroscience Meeting Planner 2005, Society for Neuroscience, Washington, D.C., Online.
27. Korol D.L. Role of estrogen in balancing contributions from multiple memory systems. Neurobiol. Learn. Mem. 2004, 82:309-323.
28. Korol D.L., Kolo L.L. Estrogen-induced changes in place and response learning in young adult female rats. Behav. Neurosci. 2002, 116:411-420.
29. 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. 2004, 45:330-338.
30. Kow L.M., Pfaff D.W. The membrane actions of estrogens can potentiate their lordosis behavior-facilitating genomic actions. Proc. Natl. Acad. Sci. U.S.A. 2004, 101:12354-12357.
31. Le Saux M., Di Paolo T. Influence of oestrogenic compounds on monoamine transporters in rat striatum. J. Neuroendocrinol. 2006, 18:25-32.
32. Le Saux M., Morissette M., Di Paolo T. ERbeta mediates the estradiol increase of D2 receptors in rat striatum and nucleus accumbens. Neuropharmacology 2006, 50:451-457.
33. Lindberg M.K., Weihua Z., Andersson N., Moverare S., Gao H., Vidal O., Erlandsson M., Windahl S., Andersson G., Lubahn D.B., Carlsten H., Dahlman-Wright K., Gustafsson J.A., Ohlsson C. Estrogen receptor specificity for the effects of estrogen in ovariectomized mice. J. Endocrinol. 2002, 174:167-178.
34. Long J.A., Evans H.M. The oestrous cycle in the rat and its associated phenomena. Mem. Univ. Calif. 1922, 6:1-148.
35. Luine V., Jacome L.F., Maclusky N.J. Rapid enhancement of visual and place memory by estrogen in rats. Endocrinology 2003, 144:2836-2844.
36. Maricq A.V., Church R.M. The differential effects of haloperidol and methamphetamine on time estimation in the rat. Psychopharmacology (Berl) 1983, 79:10-15.
37. McDonald R.J., White N.M. A triple dissociation of memory systems: hippocampus, amygdala, and dorsal striatum. Behav. Neurosci. 1993, 107:3-22.
38. McElroy M.W., Korol D.K. Intrahippocampal muscimol shifts learning strategy in gonadally intact young adult female rats. Learn. Mem. 2005, 12:150-158.
39. Mermelstein P.G., Becker J.B., Surmeier D.J. Estradiol reduces calcium currents in rat neostriatal neurons via a membrane receptor. J. Neurosci. 1996, 16:595-604.
40. Micevych P.E., Mermelstein P.G. Membrane estrogen receptors acting through metabotropic glutamate receptors: an emerging mechanism of estrogen action in brain. Mol. Neurobiol. 2009, 36:66-77.
41. Montes G.S., Luque E.H. Effects of ovarian steroids on vaginal smears in the rat. Acta Anat. (Basel) 1988, 133:192-199.
42. Morissette M., Garcia-Segura L.M., Belanger A., Di Paolo T. Changes of rat striatal neuronal membrane morphology and steroid content during the estrous cycle. Neuroscience 1992, 49:893-902.
43. Neese S.L., Wang V.C., Doerge D.R., Helferich W.G., Korol D.L., Schantz S.L. Impact of dietary genistein and aging on executive function in rats. Neurotoxicol. Teratol. 2010, 32:200-211.
44. Nilsson S., Makela S., Treuter E., Tujague M., Thomsen J., Andersson G., Enmark E., Pettersson K., Gustafsson J.A. Mechanisms of estrogen action. Physiol. Rev. 2001, 81:1535-1565.
45. Packard M.G., Teather L.A. Intra-hippocampal estradiol infusion enhances memory in ovariectomized rats. Neuroreport 1997, 8:3009-3013.
46. Packard M.G., Kohlmaier J.R., Alexander G.M. Posttraining intrahippocampal estradiol injections enhance spatial memory in male rats: interaction with cholinergic systems. Behav. Neurosci. 1996, 110:626-632.
47. Paxinos G., Watson C. The Rat Brain in Stereotaxic Coordinates 1986, Academic Press, North Ryde, NSW, Australia.
48. Pfaff D., Keiner M. Atlas of estradiol-concentrating cells in the central nervous system of the female rat. J. Comp. Neurol. 1973, 151:121-158.
49. Rhodes M.E., Frye C.A. Estrogen has mnemonic-enhancing effects in the inhibitory avoidance task. Pharmacol. Biochem. Behav. 2004, 78:551-558.
50. Sandstrom N.J. Estradiol modulation of the speed of an internal clock. Behav. Neurosci. 2007, 121:422-432.
51. Shughrue P.J., Merchenthaler I. Distribution of estrogen receptor beta immunoreactivity in the rat central nervous system. J. Comp. Neurol. 2001, 436:64-81.
52. Shughrue P.J., Lane M.V., Merchenthaler I. Comparative distribution of estrogen receptor-alpha and -beta mRNA in the rat central nervous system. J. Comp. Neurol. 1997, 388:507-525.
53. Sinopoli K.J., Floresco S.B., Galea L.A. Systemic and local administration of estradiol into the prefrontal cortex or hippocampus differentially alters working memory. Neurobiol. Learn. Mem. 2006, 86:293-304.
54. Smith R.L., Van Hartesveldt C. Effects of ovariectomy and estrogen replacement on intrastriatal dopamine-elicited postural deviation. Pharmacol. Biochem. Behav. 1985, 22:689-693.
55. Wang V.C., Sable H.J., Ju Y.H., Allred C.D., Helferich W.G., Korol D.L., Schantz S.L. Behav. Neurosci. 2008, 122:794-804.
56. Wang V.C., Neese S.L., Korol D.L., Schantz S.L. Chronic estradiol replacement impairs performance on an operant delayed spatial alternation task in young, middle-aged, and old rats. Horm. Behav. 2009, 56:382-390.
57. Wang, V.C., Neese, S.L., Korol, D.L., Schantz, S.L., 2011. Estradiol impairs response inhibition in young and middle-aged, but not old rats. Neurotoxicol. Teratol. 33, 405-414.
58. White N.M., McDonald R.J. Multiple parallel memory systems in the brain of the rat. Neurobiol. Learn. Mem. 2002, 77:125-184.
59. Winocur G., Eskes G. Prefrontal cortex and caudate nucleus in conditional associative learning: dissociated effects of selective brain lesions in rats. Behav. Neurosci. 1998, 112:89-101.
60. 2+ influx via L-type calcium channels activates the Src/ERK/cyclic-AMP response element binding protein signal pathway and BCL-2 expression in rat hippocampal neurons: a potential initiation mechanism for estrogen-induced neuroprotection. Neuroscience 2005, 135:59-72.
61. Xiao L., Becker J.B. Hormonal activation of the striatum and the nucleus accumbens modulates paced mating behavior in the female rat. Horm. Behav. 1997, 32:114-124.
62. Zurkovsky L., Brown S.L., Boyd S.E., Fell J.A., Korol D.L. Estrogen modulates learning in female rats by acting directly at distinct memory systems. Neuroscience 2007, 144:26-37.