{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,6,10]],"date-time":"2026-06-10T05:57:10Z","timestamp":1781071030962,"version":"3.54.1"},"reference-count":88,"publisher":"Elsevier BV","issue":"1","license":[{"start":{"date-parts":[[2007,1,1]],"date-time":"2007-01-01T00:00:00Z","timestamp":1167609600000},"content-version":"tdm","delay-in-days":0,"URL":"https:\/\/www.elsevier.com\/tdm\/userlicense\/1.0\/"}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Neuroscience"],"published-print":{"date-parts":[[2007,1]]},"DOI":"10.1016\/j.neuroscience.2006.09.002","type":"journal-article","created":{"date-parts":[[2006,10,18]],"date-time":"2006-10-18T20:21:50Z","timestamp":1161202910000},"page":"26-37","source":"Crossref","is-referenced-by-count":126,"title":["Estrogen modulates learning in female rats by acting directly at distinct memory systems"],"prefix":"10.1016","volume":"144","author":[{"given":"L.","family":"Zurkovsky","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"S.L.","family":"Brown","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"S.E.","family":"Boyd","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"J.A.","family":"Fell","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"D.L.","family":"Korol","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"78","reference":[{"key":"10.1016\/j.neuroscience.2006.09.002_bib1","series-title":"The rat nervous system","first-page":"443","article-title":"Hippocampal formation","author":"Amaral","year":"1995"},{"key":"10.1016\/j.neuroscience.2006.09.002_bib2","doi-asserted-by":"crossref","first-page":"186","DOI":"10.1016\/S0006-8993(01)02161-8","article-title":"Estrogen increases G protein coupled receptor kinase 2 in the cortex of female rats","volume":"898","author":"Ansonoff","year":"2001","journal-title":"Brain Res"},{"key":"10.1016\/j.neuroscience.2006.09.002_bib3","doi-asserted-by":"crossref","first-page":"163","DOI":"10.1016\/0006-8993(94)91229-7","article-title":"Sex differences in the rapid and acute effects of estrogen on striatal D2 dopamine receptor binding","volume":"637","author":"Bazzett","year":"1994","journal-title":"Brain Res"},{"key":"10.1016\/j.neuroscience.2006.09.002_bib4","doi-asserted-by":"crossref","first-page":"157","DOI":"10.1002\/syn.890050211","article-title":"Direct effect of 17 beta-estradiol on striatum: sex differences in dopamine release","volume":"5","author":"Becker","year":"1990","journal-title":"Synapse"},{"key":"10.1016\/j.neuroscience.2006.09.002_bib5","doi-asserted-by":"crossref","first-page":"803","DOI":"10.1016\/S0091-3057(99)00168-9","article-title":"Gender differences in dopaminergic function in striatum and nucleus accumbens","volume":"64","author":"Becker","year":"1999","journal-title":"Pharmacol Biochem Behav"},{"key":"10.1016\/j.neuroscience.2006.09.002_bib6","doi-asserted-by":"crossref","first-page":"27","DOI":"10.1016\/0166-4328(86)90044-6","article-title":"The influence of estrogen on nigrostriatal dopamine activity: behavioral and neurochemical evidence for both pre- and postsynaptic components","volume":"19","author":"Becker","year":"1986","journal-title":"Behav Brain Res"},{"key":"10.1016\/j.neuroscience.2006.09.002_bib7","doi-asserted-by":"crossref","first-page":"307","DOI":"10.1016\/0006-8993(80)90922-1","article-title":"Neuroanatomical bases of spatial memory","volume":"200","author":"Becker","year":"1980","journal-title":"Brain Res"},{"key":"10.1016\/j.neuroscience.2006.09.002_bib8","doi-asserted-by":"crossref","first-page":"161","DOI":"10.1016\/S0306-4530(98)00068-7","article-title":"Estradiol facilitates performance as working memory load increases","volume":"24","author":"Bimonte","year":"1999","journal-title":"Psychoneuroendocrinology"},{"key":"10.1016\/j.neuroscience.2006.09.002_bib9","doi-asserted-by":"crossref","first-page":"174","DOI":"10.1046\/j.1460-9568.2003.02410.x","article-title":"Behavioural learning-induced increase in spontaneous GABAa-dependent synaptic activity in rat striatal cholinergic interneurons","volume":"17","author":"Bonsi","year":"2003","journal-title":"Eur J Neurosci"},{"key":"10.1016\/j.neuroscience.2006.09.002_bib10","doi-asserted-by":"crossref","first-page":"19","DOI":"10.1016\/S0166-4328(03)00063-9","article-title":"Intrahippocampal lidocaine injections impair acquisition of a place task and facilitate acquisition of a response task in rats","volume":"144","author":"Chang","year":"2003","journal-title":"Behav Brain Res"},{"key":"10.1016\/j.neuroscience.2006.09.002_bib11","doi-asserted-by":"crossref","first-page":"383","DOI":"10.1037\/0735-7044.118.2.383","article-title":"Inactivation of dorsolateral striatum impairs acquisition of response learning in cue-deficient, but not cue-available conditions","volume":"118","author":"Chang","year":"2004","journal-title":"Behav Neurosci"},{"key":"10.1016\/j.neuroscience.2006.09.002_bib12","doi-asserted-by":"crossref","first-page":"13","DOI":"10.1007\/BF01262954","article-title":"In vivo effects of estrogen and 2-hydroxyestradiol on D-2 dopamine receptor agonist affinity states in rat striatum","volume":"66","author":"Clopton","year":"1986","journal-title":"J Neural Transm"},{"key":"10.1016\/j.neuroscience.2006.09.002_bib13","doi-asserted-by":"crossref","first-page":"332","DOI":"10.1016\/S0163-1047(88)90338-X","article-title":"Caudate nucleus and memory for egocentric localizatin","volume":"49","author":"Cook","year":"1988","journal-title":"Behav Neural Biol"},{"key":"10.1016\/j.neuroscience.2006.09.002_bib14","doi-asserted-by":"crossref","first-page":"430","DOI":"10.1016\/S0006-8993(97)01206-7","article-title":"Estrogen facilitates induction of long term potentiation in the hippocampus of awake rats","volume":"778","author":"Cordoba Montoya","year":"1997","journal-title":"Brain Res"},{"key":"10.1016\/j.neuroscience.2006.09.002_bib15","doi-asserted-by":"crossref","first-page":"445","DOI":"10.1046\/j.1365-2826.2000.00471.x","article-title":"Regional and selective effects of oestradiol and progesterone on NMDA and AMPA receptors in the rat brain","volume":"12","author":"Cyr","year":"2000","journal-title":"J Neuroendocrinol"},{"key":"10.1016\/j.neuroscience.2006.09.002_bib16","doi-asserted-by":"crossref","first-page":"236","DOI":"10.1016\/S1074-7427(03)00008-X","article-title":"Evidence for the substantia nigra pars compacta as an essential component of a memory system independent of the hippocampal memory system","volume":"79","author":"Da Cunha","year":"2003","journal-title":"Neurobiol Learn Mem"},{"key":"10.1016\/j.neuroscience.2006.09.002_bib17","doi-asserted-by":"crossref","first-page":"6946","DOI":"10.1523\/JNEUROSCI.21-17-06949.2001","article-title":"Acetylcholine mediates the estrogen-induced increase in NMDA receptor binding in CA1 of the hippocampus and the associated improvements in working memory","volume":"21","author":"Daniel","year":"2001","journal-title":"J Neurosci"},{"key":"10.1016\/j.neuroscience.2006.09.002_bib18","doi-asserted-by":"crossref","first-page":"217","DOI":"10.1006\/hbeh.1997.1433","article-title":"Estrogen enhances performance of female rats during acquisition of a radial arm maze","volume":"32","author":"Daniel","year":"1997","journal-title":"Horm Behav"},{"key":"10.1016\/j.neuroscience.2006.09.002_bib19","doi-asserted-by":"crossref","first-page":"142","DOI":"10.1016\/j.nlm.2004.06.001","article-title":"Estrogen replacement in ovariectomized rats affects strategy selection in the Morris water maze","volume":"82","author":"Daniel","year":"2004","journal-title":"Neurobiol Learn Mem"},{"key":"10.1016\/j.neuroscience.2006.09.002_bib20","doi-asserted-by":"crossref","first-page":"38","DOI":"10.1016\/j.yhbeh.2005.05.001","article-title":"Estrogen increases the sensitivity of ovariectomized rats to the disruptive effects produced by the antagonism of D2 but not D1 dopamine receptors during performance of a response learning task","volume":"49","author":"Daniel","year":"2006","journal-title":"Horm Behav"},{"key":"10.1016\/j.neuroscience.2006.09.002_bib21","doi-asserted-by":"crossref","first-page":"907","DOI":"10.1139\/y02-113","article-title":"Effect of ovariectomy and estrogen supplementation on brain acetylcholinesterase activity and passive-avoidance learning in rats","volume":"80","author":"Das","year":"2002","journal-title":"Can J Physiol Pharmacol"},{"key":"10.1016\/j.neuroscience.2006.09.002_bib22","doi-asserted-by":"crossref","first-page":"13","DOI":"10.1016\/j.nlm.2004.06.009","article-title":"Ovariectomy-induced disruption of long-term synaptic depression in the hippocampal CA1 region in vivo is attenuated with chronic estrogen replacement","volume":"83","author":"Day","year":"2005","journal-title":"Neurobiol Learn Mem"},{"key":"10.1016\/j.neuroscience.2006.09.002_bib23","doi-asserted-by":"crossref","first-page":"2789","DOI":"10.1523\/JNEUROSCI.19-07-02789.1999","article-title":"Parallel information processing in the dorsal striatum: relation to hippocampal function","volume":"19","author":"Devan","year":"1999","journal-title":"J Neurosci"},{"key":"10.1016\/j.neuroscience.2006.09.002_bib24","first-page":"265","article-title":"Gonadal steroids, learning and memory","volume":"Vol. 2","author":"Dohanich","year":"2002"},{"key":"10.1016\/j.neuroscience.2006.09.002_bib25","doi-asserted-by":"crossref","first-page":"136","DOI":"10.1016\/S0006-8993(99)01619-4","article-title":"Steroid hormones affect limbic afterdischarge thresholds and kindling rates in adult female rats","volume":"838","author":"Edwards","year":"1999","journal-title":"Brain Res"},{"key":"10.1016\/j.neuroscience.2006.09.002_bib26","doi-asserted-by":"crossref","first-page":"215","DOI":"10.1016\/0006-8993(79)90392-5","article-title":"Effect of estrogen on changes in the activity of striatal cholinergic neurons induced by DA drugs","volume":"169","author":"Euvrard","year":"1979","journal-title":"Brain Res"},{"key":"10.1016\/j.neuroscience.2006.09.002_bib27","doi-asserted-by":"crossref","first-page":"225","DOI":"10.1006\/nlme.1998.3820","article-title":"Estrogen improves performance of reinforced T-maze alternation and prevents the amnestic effects of scopolamine administered systemically or intrahippocampally","volume":"69","author":"Fader","year":"1998","journal-title":"Neurobiol Learn Mem"},{"key":"10.1016\/j.neuroscience.2006.09.002_bib28","doi-asserted-by":"crossref","first-page":"711","DOI":"10.1016\/S0091-3057(98)00219-6","article-title":"Estrogen improves working but not reference memory and prevents amnestic effects of scopolamine of a radial-arm maze","volume":"62","author":"Fader","year":"1999","journal-title":"Pharmacol Biochem Behav"},{"key":"10.1016\/j.neuroscience.2006.09.002_bib29","doi-asserted-by":"crossref","first-page":"43","DOI":"10.1016\/0304-3940(87)90048-6","article-title":"Regional effect of estradiol on rat caudate-putamen dopamine receptors: lateral-medial differences","volume":"74","author":"Falardeau","year":"1987","journal-title":"Neurosci Lett"},{"key":"10.1016\/j.neuroscience.2006.09.002_bib30","doi-asserted-by":"crossref","first-page":"925","DOI":"10.1152\/jn.1999.81.2.925","article-title":"17beta-Estradiol enhances NMDA receptor-mediated EPSPs and long-term potentiation","volume":"81","author":"Foy","year":"1999","journal-title":"J Neurophysiol"},{"key":"10.1016\/j.neuroscience.2006.09.002_bib31","doi-asserted-by":"crossref","first-page":"115","DOI":"10.1016\/S0166-4328(01)00255-8","article-title":"High levels of estradiol disrupt conditioned place preference learning, stimulus response learning and reference memory but have limited effects on working memory","volume":"126","author":"Galea","year":"2001","journal-title":"Behav Brain Res"},{"key":"10.1016\/j.neuroscience.2006.09.002_bib32","doi-asserted-by":"crossref","first-page":"1049","DOI":"10.1523\/JNEUROSCI.16-03-01049.1996","article-title":"Fluctuations in relative levels of choline acetyltransferase mRNA in different regions of the rat basal forebrain across the estrous cycle: effects of estrogen and progesterone","volume":"16","author":"Gibbs","year":"1996","journal-title":"J Neurosci"},{"key":"10.1016\/j.neuroscience.2006.09.002_bib33","doi-asserted-by":"crossref","first-page":"222","DOI":"10.1006\/hbeh.1999.1541","article-title":"Estrogen replacement enhances acquisition of a spatial memory task and reduces deficits associated with hippocampal muscarinic receptor inhibition","volume":"36","author":"Gibbs","year":"1999","journal-title":"Horm Behav"},{"key":"10.1016\/j.neuroscience.2006.09.002_bib34","doi-asserted-by":"crossref","first-page":"107","DOI":"10.1016\/S0197-4580(00)00103-2","article-title":"Long-term treatment with estrogen and progesterone enhances acquisition of a spatial memory task by ovariectomized aged rats","volume":"21","author":"Gibbs","year":"2000","journal-title":"Neurobiol Aging"},{"key":"10.1016\/j.neuroscience.2006.09.002_bib35","doi-asserted-by":"crossref","first-page":"741","DOI":"10.1016\/S0306-4530(03)00118-5","article-title":"Effects of raloxifene and estradiol on hippocampal acetylcholine release and spatial learning in the rat","volume":"29","author":"Gibbs","year":"2004","journal-title":"Psychoneuroendocrinology"},{"key":"10.1016\/j.neuroscience.2006.09.002_bib36","doi-asserted-by":"crossref","first-page":"143","DOI":"10.1016\/S0006-8993(96)01375-3","article-title":"Effects of estrogen on potassium-stimulated acetylcholine release in the hippocampus and overlying cortex of adult rats","volume":"749","author":"Gibbs","year":"1997","journal-title":"Brain Res"},{"key":"10.1016\/j.neuroscience.2006.09.002_bib37","doi-asserted-by":"crossref","first-page":"1286","DOI":"10.1523\/JNEUROSCI.10-04-01286.1990","article-title":"Gonadal steroids regulate dendritic spine density in hippocampal pyramidal cells in adulthood","volume":"10","author":"Gould","year":"1990","journal-title":"J Neurosci"},{"key":"10.1016\/j.neuroscience.2006.09.002_bib38","doi-asserted-by":"crossref","first-page":"13","DOI":"10.1016\/S0303-7207(03)00255-7","article-title":"Activities of estrogen receptor \u03b1- and \u03b2-selective ligands at diverse estrogen responsive gene sites mediating transactivation or transrepression","volume":"206","author":"Harrington","year":"2003","journal-title":"Mol Cell Endocrinol"},{"key":"10.1016\/j.neuroscience.2006.09.002_bib39","doi-asserted-by":"crossref","first-page":"286","DOI":"10.1016\/S0006-8993(00)02372-6","article-title":"The effect of steroid sulfatase inhibition on learning and spatial memory","volume":"865","author":"Johnson","year":"2000","journal-title":"Brain Res"},{"key":"10.1016\/j.neuroscience.2006.09.002_bib40","doi-asserted-by":"crossref","first-page":"462","DOI":"10.1007\/BF00229361","article-title":"Memory for spatial locations, motor responses, and objects: triple dissociation among the hippocampus, caudate nucleus, and extrastriate visual cortex","volume":"93","author":"Kesner","year":"1993","journal-title":"Exp Brain Res"},{"key":"10.1016\/j.neuroscience.2006.09.002_bib41","first-page":"113","article-title":"Functional dissociation of striatal and hippocampal cholinergic systems in egocentric and allocentric localization: effect of overtraining","volume":"20","author":"Kobayashi","year":"2000","journal-title":"Nihon Shinkei Seishin Yakurigaku Zasshi"},{"key":"10.1016\/j.neuroscience.2006.09.002_bib42","doi-asserted-by":"crossref","first-page":"365","DOI":"10.1016\/0166-4328(82)90018-3","article-title":"Dissociation of the contributions of the prefrontal cortex and dorsomedial thalamic nucleus to spatially guided behavior in the rat","volume":"6","author":"Kolb","year":"1982","journal-title":"Behav Brain Res"},{"key":"10.1016\/j.neuroscience.2006.09.002_bib43","doi-asserted-by":"crossref","first-page":"309","DOI":"10.1016\/j.nlm.2004.07.006","article-title":"Role of estrogen in balancing contributions from multiple memory systems","volume":"82","author":"Korol","year":"2004","journal-title":"Neurobiol Learn Mem"},{"key":"10.1016\/j.neuroscience.2006.09.002_bib44","doi-asserted-by":"crossref","first-page":"411","DOI":"10.1037\/0735-7044.116.3.411","article-title":"Estrogen-induced changes in place and response learning in young adult female rats","volume":"116","author":"Korol","year":"2002","journal-title":"Behav Neurosci"},{"key":"10.1016\/j.neuroscience.2006.09.002_bib45","doi-asserted-by":"crossref","first-page":"330","DOI":"10.1016\/j.yhbeh.2004.01.005","article-title":"Shifts in preferred learning strategy across the estrous cycle in female rats","volume":"45","author":"Korol","year":"2004","journal-title":"Horm Behav"},{"key":"10.1016\/j.neuroscience.2006.09.002_bib46","first-page":"1","article-title":"The oestrous cycle in the rat and its associated phenomena","volume":"6","author":"Long","year":"1922","journal-title":"Mem Univ Calif"},{"key":"10.1016\/j.neuroscience.2006.09.002_bib47","doi-asserted-by":"crossref","first-page":"484","DOI":"10.1016\/0014-4886(85)90108-6","article-title":"Estradiol increases choline acetyltransferase activity in specific basal forebrain nuclei and projection areas of female rats","volume":"89","author":"Luine","year":"1985","journal-title":"Exp Neurol"},{"key":"10.1016\/j.neuroscience.2006.09.002_bib48","doi-asserted-by":"crossref","first-page":"149","DOI":"10.1006\/hbeh.1998.1473","article-title":"Estradiol enhances learning and memory in a spatial memory task and effects levels of monoaminergic neurotransmitters","volume":"34","author":"Luine","year":"1998","journal-title":"Horm Behav"},{"key":"10.1016\/j.neuroscience.2006.09.002_bib49","doi-asserted-by":"crossref","first-page":"315","DOI":"10.1016\/j.nlm.2003.08.003","article-title":"Short-term estrogen treatment in ovariectomized rats augments hippocampal acetylcholine release during place learning","volume":"80","author":"Marriott","year":"2003","journal-title":"Neurobiol Learn Mem"},{"key":"10.1016\/j.neuroscience.2006.09.002_bib50","doi-asserted-by":"crossref","first-page":"113","DOI":"10.3758\/BF03214415","article-title":"Fimbria\/fornix lesions facilitate the learning of a non-spatial response task","volume":"2","author":"Matthews","year":"1995","journal-title":"Psychon Bull Rev"},{"key":"10.1016\/j.neuroscience.2006.09.002_bib51","doi-asserted-by":"crossref","first-page":"3","DOI":"10.1037\/0735-7044.107.1.3","article-title":"A triple dissociation of memory systems: hippocampus, amygdala, and dorsal striatum","volume":"107","author":"McDonald","year":"1993","journal-title":"Behav Neurosci"},{"key":"10.1016\/j.neuroscience.2006.09.002_bib52","doi-asserted-by":"crossref","first-page":"260","DOI":"10.1016\/S0163-1047(05)80009-3","article-title":"Parallel information processing in the water maze: evidence for independent memory systems involving dorsal striatum and hippocampus","volume":"61","author":"McDonald","year":"1994","journal-title":"Behav Neural Biol"},{"key":"10.1016\/j.neuroscience.2006.09.002_bib53","doi-asserted-by":"crossref","first-page":"320","DOI":"10.1037\/0735-7044.117.2.320","article-title":"Cooperation between memory systems: acetylcholine release in the amygdala correlates positively with performance on a hippocampus-dependent task","volume":"117","author":"McIntyre","year":"2003","journal-title":"Behav Neurosci"},{"key":"10.1016\/j.neuroscience.2006.09.002_bib54","doi-asserted-by":"crossref","first-page":"41","DOI":"10.1016\/S0361-9230(02)00754-2","article-title":"Impaired learning in a spatial working memory version and in a cued version of the water maze in rats with MPTP-induced mesencephalic dopaminergic lesions","volume":"58","author":"Miyoshi","year":"2002","journal-title":"Brain Res Bull"},{"key":"10.1016\/j.neuroscience.2006.09.002_bib55","doi-asserted-by":"crossref","first-page":"278","DOI":"10.1016\/j.nlm.2004.07.007","article-title":"Parallel processing across neural systems: implications for a multiple memory system hypothesis","volume":"82","author":"Mizumori","year":"2004","journal-title":"Neurobiol Learn Mem"},{"key":"10.1016\/j.neuroscience.2006.09.002_bib56","doi-asserted-by":"crossref","first-page":"3916","DOI":"10.1523\/JNEUROSCI.13-09-03916.1993","article-title":"Spatial learning impairment parallels the magnitude of dorsal hippocampal lesions, but is hardly present following ventral lesions","volume":"13","author":"Moser","year":"1993","journal-title":"J Neurosci"},{"key":"10.1016\/j.neuroscience.2006.09.002_bib57","doi-asserted-by":"crossref","first-page":"229","DOI":"10.3758\/CABN.1.3.229","article-title":"Effects of dorsal-striatum lesions and fimbria-fornix on the problem-solving strategies of rats in a shallow water maze","volume":"1","author":"Okaichi","year":"2001","journal-title":"Cogn Affect Behav Neurosci"},{"key":"10.1016\/j.neuroscience.2006.09.002_bib58","doi-asserted-by":"crossref","first-page":"1465","DOI":"10.1523\/JNEUROSCI.09-05-01465.1989","article-title":"Differential effects of fornix and caudate nucleus lesions on two radial maze tasks: evidence for multiple memory systems","volume":"9","author":"Packard","year":"1989","journal-title":"J Neurosci"},{"key":"10.1016\/j.neuroscience.2006.09.002_bib59","doi-asserted-by":"crossref","first-page":"626","DOI":"10.1037\/0735-7044.110.3.626","article-title":"Posttraining intrahippocampal estradiol injections enhance spatial memory in male rats: interaction with cholinergic systems","volume":"110","author":"Packard","year":"1996","journal-title":"Behav Neurosci"},{"key":"10.1016\/j.neuroscience.2006.09.002_bib60","doi-asserted-by":"crossref","first-page":"439","DOI":"10.1037\/0735-7044.106.3.439","article-title":"Double dissociation of fornix and caudate nucleus lesions on acquisition of two water maze tasks: further evidence for multiple memory systems","volume":"106","author":"Packard","year":"1992","journal-title":"Behav Neurosci"},{"key":"10.1016\/j.neuroscience.2006.09.002_bib61","doi-asserted-by":"crossref","first-page":"65","DOI":"10.1006\/nlme.1996.0007","article-title":"Inactivation of hippocampus or caudate nucleus with lidocaine differentially affects expression of place and response learning","volume":"65","author":"Packard","year":"1996","journal-title":"Neurobiol Learn Mem"},{"key":"10.1016\/j.neuroscience.2006.09.002_bib62","doi-asserted-by":"crossref","first-page":"172","DOI":"10.1006\/nlme.1997.3785","article-title":"Posttraining estradiol injections enhance memory in ovariectomized rats: cholinergic blockade and synergism","volume":"68","author":"Packard","year":"1997","journal-title":"Neurobiol Learn Mem"},{"key":"10.1016\/j.neuroscience.2006.09.002_bib63","doi-asserted-by":"crossref","first-page":"543","DOI":"10.1037\/0735-7044.111.3.543","article-title":"Double dissociation of hippocampal and dorsal-striatal memory systems by posttraining intracerebral injections of 2-amino-5-phosphonopentanoic acid","volume":"111","author":"Packard","year":"1997","journal-title":"Behav Neurosci"},{"key":"10.1016\/j.neuroscience.2006.09.002_bib64","doi-asserted-by":"crossref","first-page":"3009","DOI":"10.1097\/00001756-199709290-00004","article-title":"Intra-hippocampal estradiol infusion enhances memory in ovariectomized rats","volume":"8","author":"Packard","year":"1997","journal-title":"Neuroreport"},{"key":"10.1016\/j.neuroscience.2006.09.002_bib65","doi-asserted-by":"crossref","first-page":"163","DOI":"10.1006\/nlme.1997.3815","article-title":"Amygdala modulation of multiple memory systems: hippocampus and caudate-putamen","volume":"69","author":"Packard","year":"1998","journal-title":"Neurobiol Learn Mem"},{"key":"10.1016\/j.neuroscience.2006.09.002_bib66","doi-asserted-by":"crossref","first-page":"295","DOI":"10.1037\/0735-7044.105.2.295","article-title":"Dissociation of hippocampus and caudate nucleus memory systems by posttraining intracerebral injection of dopamine agonists","volume":"105","author":"Packard","year":"1991","journal-title":"Behav Neurosci"},{"key":"10.1016\/j.neuroscience.2006.09.002_bib67","series-title":"The rat brain in stereotaxic coordinates","author":"Paxinos","year":"1986"},{"key":"10.1016\/j.neuroscience.2006.09.002_bib68","doi-asserted-by":"crossref","first-page":"564","DOI":"10.1101\/lm.33105","article-title":"Acetylcholine release in the hippocampus and striatum during place and response training","volume":"12","author":"Pych","year":"2005","journal-title":"Learn Mem"},{"key":"10.1016\/j.neuroscience.2006.09.002_bib69","doi-asserted-by":"crossref","first-page":"221","DOI":"10.1016\/0361-9230(90)90064-7","article-title":"Estradiol in the striatum: effects on behavior and dopamine receptors but no evidence for membrane steroid receptors","volume":"25","author":"Roy","year":"1990","journal-title":"Brain Res Bull"},{"key":"10.1016\/j.neuroscience.2006.09.002_bib70","doi-asserted-by":"crossref","first-page":"4479","DOI":"10.1523\/JNEUROSCI.23-11-04479.2003","article-title":"A role for the basal forebrain cholinergic system in estrogen-induced disinhibition of hippocampal pyramidal cells","volume":"23","author":"Rudick","year":"2003","journal-title":"J Neurosci"},{"key":"10.1016\/j.neuroscience.2006.09.002_bib71","doi-asserted-by":"crossref","first-page":"105","DOI":"10.1016\/S0006-8993(00)02757-8","article-title":"Autonomic and cardiovascular reflex responses to central estrogen injection in ovariectomized female rats","volume":"879","author":"Saleh","year":"2000","journal-title":"Brain Res"},{"key":"10.1016\/j.neuroscience.2006.09.002_bib72","doi-asserted-by":"crossref","first-page":"384","DOI":"10.1037\/0735-7044.115.2.384","article-title":"Memory retention is modulated by acute estradiol and progesterone replacement","volume":"115","author":"Sandstrom","year":"2001","journal-title":"Behav Neurosci"},{"key":"10.1016\/j.neuroscience.2006.09.002_bib73","doi-asserted-by":"crossref","first-page":"280","DOI":"10.1002\/hipo.10024","article-title":"Post-training reversible inactivation of hippocampus reveals interference between memory systems","volume":"12","author":"Schroeder","year":"2002","journal-title":"Hippocampus"},{"key":"10.1016\/j.neuroscience.2006.09.002_bib74","doi-asserted-by":"crossref","first-page":"507","DOI":"10.1002\/(SICI)1096-9861(19971201)388:4<507::AID-CNE1>3.0.CO;2-6","article-title":"Comparative distribution of estrogen receptor-alpha and -beta mRNA in the rat central nervous system","volume":"388","author":"Shughrue","year":"1997","journal-title":"J Comp Neurol"},{"key":"10.1016\/j.neuroscience.2006.09.002_bib75","doi-asserted-by":"crossref","first-page":"19S","DOI":"10.1016\/S0002-9343(97)00260-X","article-title":"Role of estrogen replacement therapy in memory enhancement and the prevention of neuronal loss associated with Alzheimer\u2019s Disease","volume":"103","author":"Simpkins","year":"1997","journal-title":"Am J Med"},{"key":"10.1016\/j.neuroscience.2006.09.002_bib76","doi-asserted-by":"crossref","first-page":"305","DOI":"10.1016\/0006-8993(94)91694-2","article-title":"Ovarian steroid deprivation results in a reversible learning impairment and compromised cholinergic function in female Sprague-Dawley rats","volume":"644","author":"Singh","year":"1994","journal-title":"Brain Res"},{"key":"10.1016\/j.neuroscience.2006.09.002_bib77","doi-asserted-by":"crossref","first-page":"403","DOI":"10.1046\/j.1471-4159.2004.02336.x","article-title":"Steroid sulfatase (STS) expression in the human temporal lobe: enzyme activity, mRNA expression and immunohistochemistry study","volume":"89","author":"Steckelbroeck","year":"2004","journal-title":"J Neurochem"},{"key":"10.1016\/j.neuroscience.2006.09.002_bib78","first-page":"534.2","article-title":"Chronic estradiol replacement in ovariectomized female rats shifts learning strategy in a time-dependent manner","volume":"27","author":"Thomas","year":"2002","journal-title":"Abstr Soc Neurosci"},{"key":"10.1016\/j.neuroscience.2006.09.002_bib79","doi-asserted-by":"crossref","first-page":"143","DOI":"10.1016\/S0166-4328(00)00345-4","article-title":"Sex differences in the dynamics of cue utilization and exploratory behavior","volume":"119","author":"Tropp","year":"2001","journal-title":"Behav Brain Res"},{"key":"10.1016\/j.neuroscience.2006.09.002_bib80","doi-asserted-by":"crossref","first-page":"87","DOI":"10.1016\/S0197-4580(01)00250-0","article-title":"Estrogen effects on object memory and cholinergic receptors in young and old female mice","volume":"23","author":"Vaucher","year":"2002","journal-title":"Neurobiol Aging"},{"key":"10.1016\/j.neuroscience.2006.09.002_bib81","doi-asserted-by":"crossref","first-page":"832","DOI":"10.1210\/en.2002-220899","article-title":"Estrogen activation of cyclic adenosine 5\u2032-monophosphate response element-mediated transcription requires the extracellular regulated kinase\/mitogen-activated protein kinase pathway","volume":"144","author":"Wade","year":"2003","journal-title":"Endocrinology"},{"key":"10.1016\/j.neuroscience.2006.09.002_bib82","doi-asserted-by":"crossref","first-page":"216","DOI":"10.1016\/j.nlm.2004.05.004","article-title":"The role of stimulus ambiguity and movement in spatial navigation: a multiple memory system analysis of location discrimination","volume":"82","author":"White","year":"2004","journal-title":"Neurobiol Learn Mem"},{"key":"10.1016\/j.neuroscience.2006.09.002_bib83","doi-asserted-by":"crossref","first-page":"125","DOI":"10.1006\/nlme.2001.4008","article-title":"Multiple parallel memory systems in the brain of the rat","volume":"77","author":"White","year":"2002","journal-title":"Neurobiol Learn Mem"},{"key":"10.1016\/j.neuroscience.2006.09.002_bib84","doi-asserted-by":"crossref","first-page":"93","DOI":"10.1016\/S0014-2999(99)00583-X","article-title":"Estrogen and NMDA receptor antagonism: effects upon reference and working memory","volume":"381","author":"Wilson","year":"1999","journal-title":"Eur J Pharmacol"},{"key":"10.1016\/j.neuroscience.2006.09.002_bib85","doi-asserted-by":"crossref","first-page":"83","DOI":"10.1016\/S0304-3940(02)00871-6","article-title":"17\u03b2 Estradiol reduces excitatory postsynaptic potential (EPSP) amplitude in rat basolateral amygdala neurons","volume":"331","author":"Womble","year":"2002","journal-title":"Neurosci Lett"},{"key":"10.1016\/j.neuroscience.2006.09.002_bib86","doi-asserted-by":"crossref","first-page":"40666","DOI":"10.1073\/pnas.95.7.4066","article-title":"Stress facilitates classical conditioning in males, but impairs classical conditioning in females through activational effects of ovarian hormones","volume":"95","author":"Wood","year":"1998","journal-title":"Proc Natl Acad Sci U S A"},{"key":"10.1016\/j.neuroscience.2006.09.002_bib87","doi-asserted-by":"crossref","first-page":"293","DOI":"10.1002\/cne.903360210","article-title":"Roles of estradiol and progesterone in regulation of hippocampal dendritic spine density during the estrous cycle in the rat","volume":"336","author":"Woolley","year":"1993","journal-title":"J Comp Neurol"},{"key":"10.1016\/j.neuroscience.2006.09.002_bib88","doi-asserted-by":"crossref","first-page":"590","DOI":"10.1002\/neu.10150","article-title":"Cholinergic interneuron characteristics and nicotinic properties in the striatum","volume":"53","author":"Zhou","year":"2002","journal-title":"J Neurobiol"}],"container-title":["Neuroscience"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/api.elsevier.com\/content\/article\/PII:S0306452206011912?httpAccept=text\/xml","content-type":"text\/xml","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/api.elsevier.com\/content\/article\/PII:S0306452206011912?httpAccept=text\/plain","content-type":"text\/plain","content-version":"vor","intended-application":"text-mining"}],"deposited":{"date-parts":[[2019,4,21]],"date-time":"2019-04-21T22:26:26Z","timestamp":1555885586000},"score":1,"resource":{"primary":{"URL":"https:\/\/linkinghub.elsevier.com\/retrieve\/pii\/S0306452206011912"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2007,1]]},"references-count":88,"journal-issue":{"issue":"1","published-print":{"date-parts":[[2007,1]]}},"alternative-id":["S0306452206011912"],"URL":"https:\/\/doi.org\/10.1016\/j.neuroscience.2006.09.002","relation":{},"ISSN":["0306-4522"],"issn-type":[{"value":"0306-4522","type":"print"}],"subject":[],"published":{"date-parts":[[2007,1]]}}}