Shifts in preferred learning strategy across the estrous cycle in female rats

Korol, Donna L.; Malin, Emily L.; Borden, Kristine A; Busby, Rachel A; Couper-Leo, Julia

doi:10.1016/j.yhbeh.2004.01.005

Cited by 225 publications

(189 citation statements)

References 87 publications

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“…In contrast, rodents in proestrus perform no differently or worse in the water maze, radial arm maze, and active avoidance (Farr et al, 1995;Frye, 1995;Rubinow et al, 2004;Stackman et al, 1997;Warren and Juraska, 1997). Together, these findings suggest that effects on spatial ability of hormones over the cycle may differ with task demand, stress, and/or shifts in cognitive strategy (Galea et al, 2000;Korol et al, 2004;Korol & Kolo, 2002;Rubinow et al, 2004). As such, using a task, e.g.…”

Section: Discussionmentioning

confidence: 93%

Estrogens and progestins enhance spatial learning of intact and ovariectomized rats in the object placement task

Frye

Duffy

Walf

2007

Neurobiology of Learning and Memory

218

219

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Steroid modulation of cognitive function has focused on estrogen (E 2 ), but progestins naturally covary with E 2 and may also influence cognitive performance. Spatial performance in the object placement task over endogenous hormonal states in which E 2 and progestins vary, and when E 2 and/ or progestins were administered, was examined. Experiment 1: Rats in proestrus or estrus had significantly better performance in the object placement task than did diestrous rats. Experiment 2: Rats in the third trimester, post-partum, or lactation exhibited significantly better performance in the object placement task than did rats in the first trimester. Experiment 3: Ovariectomized (ovx) rats administered 17β-estradiol (0.9 mg/kg, subcutaneously (sc), progesterone (P; 4 mg/kg, sc), or E 2 and P, immediately after training in the object placement task, performed significantly better when tested 4 hours later, than did control rats administered vehicle (sesame oil 0.2 cc). Experiment 4: Ovx rats administered E 2 or P with a one and a half hour delay after training in the object placement task, did not perform differently than vehicle-administered controls. Experiment 5: Ovx rats administered post-training E 2 , which has a high affinity for both E 2 receptor (ER)α and β isoforms, or propyl pyrazole triol (PPT; 0.9 mg/kg, sc), which is more selective for ERα than ERβ, had significantly better performance in the object placement task than did rats administered vehicle or diarylpropionitrile (DPN; 0.9 mg/kg, sc), an ERβ selective ligand. Experiment 6: Ovx rats administered P, or its metabolite, 5α-pregnan-3α-ol-20-one (3α,5α-THP; 4 mg/kg, sc), immediately post-training performed significantly better in the object placement task than did vehicle control rats. Thus, performance in the object placement task is better when E 2 and/or P are naturally elevated or when E 2 , the ERα selective ER modulator PPT, P, or its metabolite, 3α,5α-THP, are administered post-training.

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Section: Discussionmentioning

confidence: 93%

Estrogens and progestins enhance spatial learning of intact and ovariectomized rats in the object placement task

Frye

Duffy

Walf

2007

Neurobiology of Learning and Memory

218

219

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“…Lastly, some researchers report stable spatial-memory performance across the estrous cycle (Stackman et al, 1997). Results are more convergent for spatial strategies used to solve navigation tasks: rats prefer allocentric (hippocampal-based) strategies when exposed to high estrogen levels and egocentric (striatal-based) strategies when exposed to low levels (Hussain et al, 2014;Korol et al, 2004;Qiu et al, 2013). The different degrees to which spatial memory tasks rely on these learning strategies make comparisons between studies difficult.…”

Section: Introductionmentioning

confidence: 99%

Hippocampal volume and functional connectivity changes during the female menstrual cycle

et al. 2015

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Hippocampal volume has been shown to be sensitive to variations in estrogen and progesterone levels across rodents' estrous cycle. However, little is known about the covariation of hormone levels and brain structure in the course of the human menstrual cycle. Here, we examine this covariation with a multi-method approach that includes several brain imaging methods and hormonal assessments. We acquired structural and functional scans from 21 naturally cycling women on four time points during their cycles (early follicular phase, late follicular phase, ovulation and luteal phase). Hormone blood concentrations and cognitive performance in different domains were assessed on each of the measurement occasions. Structural MRI images were processed by means of whole-brain voxel-based morphometry and FreeSurfer. With either method, bilateral increases in hippocampal volume were found in the late follicular phase relative to the early follicular phase. The gray matter probability in regions of hippocampal volume increase was associated with lower mean diffusivity in the same region. In addition, we observed higher functional connectivity between the hippocampi and the bilateral superior parietal lobe in the late follicular phase. We did not find any reliable cycle-related performance variations on the cognitive tasks. The present results show that hormonal fluctuations covary with hippocampal structure and function in the course of the human menstrual cycle.

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“…For example, female rats in proestrus, when endogenous plasma levels of estrogen are highest, show impaired performance on different hippocampus-dependent tasks compared with female rats in estrus, when endogenous plasma levels of estrogen are lowest (Frye, 1995;Warren and Juraska, 1997;Markus and Zecevic, 1997). Intriguingly however, rats during proestrus are more likely to use a spatial strategy when solving certain tasks (Korol et al, 2004). In addition, exogenous administration of estradiol to ovariectomized female rats shows a dose-dependent relationship between estradiol and memory.…”

Section: Introductionmentioning

confidence: 99%

Low Doses of 17α-Estradiol and 17β-Estradiol Facilitate, Whereas Higher Doses of Estrone and 17α- and 17β-Estradiol Impair, Contextual Fear Conditioning in Adult Female Rats

Barha

Dalton

Galea

2009

Neuropsychopharmacol

109

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Estrogens are known to exert significant structural and functional effects in the hippocampus of adult rodents. In particular, 17b-estradiol can improve, impair, or have no effect on hippocampus-dependent learning and memory depending on dose and time of administration. The effects of other forms of estrogen, such as estrone and 17a-estradiol, on hippocampus-dependent learning have not been as thoroughly investigated. Therefore, the purpose of this study was to investigate the effects of 17b-estradiol, estrone, and 17a-estradiol at three different doses on two different tasks: hippocampus-dependent contextual fear conditioning and hippocampusindependent cued fear conditioning. Adult ovariectomized female rats were injected with one of the estrogens at one of the three doses 30 mins before conditioning to assess the rapid effects of these estrogens on acquisition. Twenty-four hours later memory for the context was examined and 1 h later memory for the cue (tone) was assessed. Levels of synaptophysin were examined in the dorsal hippocampus of rats to identify a potential synaptic correlate of hormonal effects on contextual fear conditioning. Low 17b-estradiol and 17a-estradiol enhanced, whereas high 17b-estradiol and 17a-estradiol impaired, contextual fear conditioning. Only the middle dose of estrone severely impaired contextual fear conditioning. Estrogens did not alter performance in the hippocampus-independent cued task. Synaptophysin expression was increased by estrone (at a middle and high dose) and 17b-estradiol (at a middle dose) in the CA3 region of the hippocampus and was not correlated with cognition. The results of this study indicate that estradiol can positively or negatively influence hippocampus-dependent learning and memory, whereas estrone impairs hippocampus-dependent learning and memory in a dose-dependent manner. These results have important therapeutic implications, as estrone, a main component of a widely used hormone replacement therapy, was shown to have either a negative effect or no effect on learning and memory. It may be possible to use 17a-estradiol and lower doses of estrogens as potential alternatives in hormone replacement therapies.

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Shifts in preferred learning strategy across the estrous cycle in female rats

Cited by 225 publications

References 87 publications

Estrogens and progestins enhance spatial learning of intact and ovariectomized rats in the object placement task

Estrogens and progestins enhance spatial learning of intact and ovariectomized rats in the object placement task

Hippocampal volume and functional connectivity changes during the female menstrual cycle

Low Doses of 17α-Estradiol and 17β-Estradiol Facilitate, Whereas Higher Doses of Estrone and 17α- and 17β-Estradiol Impair, Contextual Fear Conditioning in Adult Female Rats

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