Estradiol enhances object recognition memory in Swiss female mice by activating hippocampal estrogen receptor α

Pereira, Luciana Melo; Bastos, Cristiane Perácio; Souza, Jéssica M. de; Ribeiro, Fabíola M.; Pereira, Grace Schenatto

doi:10.1016/j.nlm.2014.04.001

Cited by 54 publications

(52 citation statements)

References 58 publications

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“…These tasks were chosen because they are sensitive to E 2 , and the single training trial used for each is ideal for linking rapid biochemical alterations to memory formation. In ovariectomized mice, immediate post-training bilateral infusion of 5 g E 2 into the dorsal hippocampus enhances OR tested 48 h after infusion (Fernandez et al, 2008;Boulware et al, 2013;Fortress et al, 2013Fortress et al, , 2014Pereira et al, 2014) and OP tested 24 h after infusion (Boulware et al, 2013;Fortress et al, 2014). Each task used unique sets of objects to maintain novelty and prevent interference from one task to the other.…”

Section: Methodsmentioning

confidence: 99%

“…As such, chance levels of performance represent no memory of the training objects. Because vehicle-infused female mice do not remember the familiar object 48 h after training (Gresack et al, 2007;Boulware et al, 2013;Fortress et al, 2014;Pereira et al, 2014), a 48 h delay was used to test the memory-enhancing effects of E 2 and G-1. However, vehicleinfused female mice do remember the familiar object 24 h after training (Gresack et al, 2007;Boulware et al, 2013), so the shorter 24 h delay was used to test the potential memory impairing effects of G-15 and cell-signaling inhibitors.…”

Section: Methodsmentioning

confidence: 99%

“…For OR and OP data, one-sample t tests were conducted using SPSS (IBM) to determine whether each group spent more time than chance (15 s) exploring the novel or moved object (Gresack and Frick, 2003;Gervais et al, 2013;Pereira et al, 2014). This analysis is essential to determine whether learning occurred within each group.…”

Section: Methodsmentioning

confidence: 99%

“…E 2 can enhance hippocampal-dependent object recognition and spatial memory in female rodents by rapidly activating numerous cell-signaling cascades, including the extracellular signalregulated kinase (ERK) pathway (Fernandez et al, 2008;Boulware et al, 2013;Fortress et al, 2013;Pereira et al, 2014). Yet the estrogen receptors (ERs) that mediate these rapid effects remain unclear.…”

Section: Introductionmentioning

confidence: 99%

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17β-Estradiol and Agonism of G-protein-Coupled Estrogen Receptor Enhance Hippocampal Memory via Different Cell-Signaling Mechanisms

et al. 2016

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The ability of 17␤-estradiol (E 2 ) to enhance hippocampal object recognition and spatial memory depends on rapid activation of extracellular signal-regulated kinase (ERK) in the dorsal hippocampus (DH). Although this activation can be mediated by the intracellular estrogen receptors ER␣ and ER␤, little is known about the role that the membrane estrogen receptor GPER plays in regulating ERK or E 2 -mediated memory formation. In this study, post-training DH infusion of the GPER agonist G-1 enhanced object recognition and spatial memory in ovariectomized female mice, whereas the GPER antagonist G-15 impaired memory, suggesting that GPER activation, like E 2 , promotes hippocampal memory formation. However, unlike E 2 , G-1 did not increase ERK phosphorylation, but instead significantly increased phosphorylation of c-Jun N-terminal kinase (JNK) in the DH. Moreover, DH infusion of the JNK inhibitor SP600125 prevented G-1 from enhancing object recognition and spatial memory, but the ERK inhibitor U0126 did not. These data suggest that GPER enhances memory via different cell-signaling mechanisms than E 2 . This conclusion was supported by data showing that the ability of E 2 to facilitate memory and activate ERK signaling was not blocked by G-15 or SP600125, which demonstrates that the memory-enhancing effects of E 2 are not dependent on JNK or GPER activation in the DH. Together, these data indicate that GPER regulates memory independently from ER␣ and ER␤ by activating JNK signaling, rather than ERK signaling. Thus, the findings suggest that GPER in the DH may not function as an estrogen receptor to regulate object recognition and spatial memory.

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Section: Methodsmentioning

confidence: 99%

Section: Methodsmentioning

confidence: 99%

Section: Methodsmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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17β-Estradiol and Agonism of G-protein-Coupled Estrogen Receptor Enhance Hippocampal Memory via Different Cell-Signaling Mechanisms

et al. 2016

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“…4A), spatial memory consolidation in an object location task, and object recognition memory consolidation ( Fig. 4B; Packard and Teather 1997a,b;Fernandez et al 2008;Lewis et al 2008;Zhao et al 2010Zhao et al , 2012Boulware et al 2013;Fortress et al 2013;Pereira et al 2014). Post-training systemic injection of noncyclodextrin-encapsulated E 2 or estradiol benzoate also enhanced spatial and object recognition memory in object-based tasks in both rats and mice (Luine et al 2003;Walf et al 2006Walf et al , 2008Frye et al 2007;Inagaki et al 2010).…”

Section: Effects Of Exogenous E 2 On Memory In Femalesmentioning

confidence: 99%

Sex steroid hormones matter for learning and memory: estrogenic regulation of hippocampal function in male and female rodents

et al. 2015

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Ample evidence has demonstrated that sex steroid hormones, such as the potent estrogen 17b-estradiol (E 2 ), affect hippocampal morphology, plasticity, and memory in male and female rodents. Yet relatively few investigators who work with male subjects consider the effects of these hormones on learning and memory. This review describes the effects of E 2 on hippocampal spinogenesis, neurogenesis, physiology, and memory, with particular attention paid to the effects of E 2 in male rodents. The estrogen receptors, cell-signaling pathways, and epigenetic processes necessary for E 2 to enhance memory in female rodents are also discussed in detail. Finally, practical considerations for working with female rodents are described for those investigators thinking of adding females to their experimental designs.Hormones have long been known to play key roles in regulating learning and memory. Many hormones, including epinephrine, glucocorticoids, and insulin influence learning and memory via inverted U-shaped dose-response relationships in which memory is enhanced by moderate, but not low or high, hormone levels (Roozendaal 2000;Korol and Gold 2007;McNay and Recknagel 2011). Research from the past two decades has demonstrated that sex steroid hormones, particularly the potent estrogen 17b-estradiol (E 2 ), also regulate learning and memory in male and female rodents via an inverted U-shaped dose-response function that is influenced by estrogen receptor expression (Packard and Teather 1997a;Packard 1998;Foster 2012). Yet E 2 has not gained widespread acceptance as a hormonal modulator of memory in both females and males, perhaps because the majority of this research has been conducted in female rodents. Moreover, the common view of E 2 as a "female" hormone may contribute to the misperception that E 2 is not relevant for cognitive function in males. However, considerable evidence supports a vital role for E 2 in mediating neural function and behavior in male rodents. Therefore, it is important for investigators working with males to understand the ways in which E 2 and other sex steroid hormones (e.g., androgens, progestins, and other estrogens) may influence their brain regions and behaviors of interest.Another reason for investigators to be cognizant of sex steroid hormone-induced regulation of learning and memory is that males and females may respond differently to various treatments and environmental factors. A classic example is that of acute stress, which enhances classical conditioning and increases apical CA1 dendritic spine density in male rats, but impairs classical conditioning and decreases CA1 spine density in female rats (Wood and Shors 1998;Shors et al. 2001). Therefore, investigators hoping to comply with National Institutes of Health policies that encourage the inclusion of females in biomedical research must be aware that adding females to a study is not as simple as adding another group. In some ways, females are fundamentally different from males, the most obvious of which is the presence of reproductive...

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Paternal morphine self-administration produces object recognition memory deficits in female, but not male offspring

et al. 2020

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Rationale: Parental drug use around or before conception can have adverse consequences for offspring. Historically, this research has focused on the effects of maternal substance use on future generations but less is known about the influence of the paternal lineage. This study focused on the impact of chronic paternal morphine exposure prior to conception on behavioral outcomes in male and female progeny. Objectives: This study sought to investigate the impact of paternal morphine self-administration on anxiety-like behavior, the stress response, and memory in male and female offspring. Methods: Adult, drug-naïve male and female progeny of morphine-treated sires and controls were evaluated for anxiety-like behavior using defensive probe burying and novelty-induced hypophagia paradigms. Hypothalamic-pituitary-adrenal (HPA) axis function was assessed by measuring plasma corticosterone levels following a restraint stressor in male and female progeny. Memory was probed using a battery of tests including object location memory, novel object recognition and contextual fear conditioning. Results: Paternal morphine exposure did not alter anxiety-like behavior or stress-induced HPA axis activation in male or female offspring. Morphine-sired male and female offspring showed intact hippocampus-dependent memory: they performed normally on the long-term fear conditioning and object location memory tests. In contrast, paternal morphine exposure selectively disrupted novel object recognition in female, but not male progeny. Conclusions: Our findings demonstrate that paternal morphine taking produces sex-specific and selective impairments in object recognition memory while leaving hippocampal function largely intact.

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Estradiol enhances object recognition memory in Swiss female mice by activating hippocampal estrogen receptor α

Cited by 54 publications

References 58 publications

17β-Estradiol and Agonism of G-protein-Coupled Estrogen Receptor Enhance Hippocampal Memory via Different Cell-Signaling Mechanisms

17β-Estradiol and Agonism of G-protein-Coupled Estrogen Receptor Enhance Hippocampal Memory via Different Cell-Signaling Mechanisms

Sex steroid hormones matter for learning and memory: estrogenic regulation of hippocampal function in male and female rodents

Paternal morphine self-administration produces object recognition memory deficits in female, but not male offspring

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