Female hippocampal estrogens have a significant correlation with cyclic fluctuation of hippocampal spines

Kato, Asami; Hojo, Yasushi; Higo, Shimpei; Komatsuzaki, Yoshimasa; Murakami, Gen; Yoshino, Hinako; Uebayashi, Masanao; Kawato, Suguru

doi:10.3389/fncir.2013.00149

Cited by 133 publications

(163 citation statements)

References 53 publications

(78 reference statements)

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“…Thus, it would appear that gonadally derived E 2 makes a fairly minimal contribution to hippocampal E 2 levels in males. Interestingly, E 2 levels in the hippocampus of male rats were found to be substantially higher than those of gonadally intact female rats, even during proestrus (Kato et al 2013). During proestrus, hippocampal E 2 levels were 4.3 + 1.0 nM, compared with values of 1.0 nM and lower during other phases of the cycle (Kato et al 2013).…”

Section: Hippocampally Synthesized E 2 and Memorymentioning

confidence: 99%

“…Interestingly, E 2 levels in the hippocampus of male rats were found to be substantially higher than those of gonadally intact female rats, even during proestrus (Kato et al 2013). During proestrus, hippocampal E 2 levels were 4.3 + 1.0 nM, compared with values of 1.0 nM and lower during other phases of the cycle (Kato et al 2013). Relative to the nonproestrus phases of the cycle, ovariectomy did not significantly decrease hippocampal E 2 levels (Kato et al 2013), suggesting that the hippocampus continues to synthesize E 2 even in the absence of ovaries.…”

Section: Hippocampally Synthesized E 2 and Memorymentioning

confidence: 99%

“…During proestrus, hippocampal E 2 levels were 4.3 + 1.0 nM, compared with values of 1.0 nM and lower during other phases of the cycle (Kato et al 2013). Relative to the nonproestrus phases of the cycle, ovariectomy did not significantly decrease hippocampal E 2 levels (Kato et al 2013), suggesting that the hippocampus continues to synthesize E 2 even in the absence of ovaries. Moreover, as in males, hippocampal levels of E 2 were substantially higher than in plasma among intact and ovariectomized females (Kato et al 2013), supporting the notion that the hippocampus is a significant source of E 2 in females as well.…”

Section: Hippocampally Synthesized E 2 and Memorymentioning

confidence: 99%

“…However, the enzymes for synthesizing progestins, androgens, and estrogens are present within the adult male and female rodent hippocampus (Hojo et al 2004), and aromatase activity in the hippocampus regulates hippocampal E 2 synthesis (Kretz et al 2004). Surprisingly, E 2 levels are substantially higher in the hippocampus than in plasma in adult male and female rats (Hojo et al 2009;Kato et al 2013). In gonadally intact males, for instance, E 2 levels have been reported at 8.4 + 1.5 nM in the hippocampus and only 0.014 + 0.003 nM in plasma (Hojo et al 2009).…”

Section: Hippocampally Synthesized E 2 and Memorymentioning

confidence: 99%

“…1). Spine density plunges 30% within 24 h to reach its nadir during the estrus phase of the cycle (Woolley and McEwen 1992;Kato et al 2013), which is characterized by low levels of estrogens and progesterone (Fig. 1).…”

Section: Spine Densitymentioning

confidence: 99%

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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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Section: Hippocampally Synthesized E 2 and Memorymentioning

confidence: 99%

Section: Hippocampally Synthesized E 2 and Memorymentioning

confidence: 99%

Section: Hippocampally Synthesized E 2 and Memorymentioning

confidence: 99%

Section: Hippocampally Synthesized E 2 and Memorymentioning

confidence: 99%

Section: Spine Densitymentioning

confidence: 99%

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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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The stability of the transcriptome during the estrous cycle in four regions of the mouse brain

DiCarlo

Vied

Nowakowski

2017

J of Comparative Neurology

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We analyzed the transcriptome of the C57BL/6J mouse hypothalamus, hippocampus, neocortex, and cerebellum to determine estrous cycle-specific changes in these four brain regions. We found almost 16,000 genes are present in one or more of the brain areas but only 210 genes, ∼1.3%, are significantly changed as a result of the estrous cycle. The hippocampus has the largest number of differentially expressed genes (DEGs) (82), followed by the neocortex (76), hypothalamus (63), and cerebellum (26). Most of these DEGs (186/210) are differentially expressed in only one of the four brain regions. A key finding is the unique expression pattern of growth hormone (Gh) and prolactin (Prl). Gh and Prl are the only DEGs to be expressed during only one stage of the estrous cycle (metestrus). To gain insight into the function of the DEGs, we examined gene ontology and phenotype enrichment and found significant enrichment for genes associated with myelination, hormone stimulus, and abnormal hormone levels. Additionally, 61 of the 210 DEGs are known to change in response to estrogen in the brain. 50 of the 210 genes differentially expressed as a result of the estrous cycle are related to myelin and oligodendrocytes and 12 of the 63 DEGs in the hypothalamus are oligodendrocyte- and myelin-specific genes. This transcriptomic analysis reveals that gene expression in the female mouse brain is remarkably stable during the estrous cycle and demonstrates that the genes that do fluctuate are functionally related.

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Sex Hormones and Cognition: Neuroendocrine Influences on Memory and Learning

Hamson

Roes

Galea

2016

Comprehensive Physiology

165

110

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Sex differences in neurological disease exist in incidence, severity, progression, and symptoms and may ultimately influence treatment. Cognitive disturbances are frequent in neuropsychiatric disease with men showing greater cognitive impairment in schizophrenia, but women showing more severe dementia and cognitive decline with Alzheimer's disease. Although there are no overall differences in intelligence between the sexes, men, and women demonstrate slight but consistent differences in a number of cognitive domains. These include a male advantage, on average, in some types of spatial abilities and a female advantage on some measures of verbal fluency and memory. Sex differences in traits or behaviors generally indicate the involvement of sex hormones, such as androgens and estrogens. We review the literature on whether adult levels of testosterone and estradiol influence spatial ability in both males and females from rodent models to humans. We also include information on estrogens and their ability to modulate verbal memory in men and women. Estrone and progestins are common components of hormone therapies, and we also review the existing literature concerning their effects on cognition. We also review the sex differences in the hippocampus and prefrontal cortex as they relate to cognitive performance in both rodents and humans. There has been greater recognition in the scientific literature that it is important to study both sexes and also to analyze study findings with sex as a variable. Only by examining these sex differences can we progress to finding treatments that will improve the cognitive health of both men and women. © 2016 American Physiological Society. Compr Physiol 6:1295-1337, 2016.

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Female hippocampal estrogens have a significant correlation with cyclic fluctuation of hippocampal spines

Cited by 133 publications

References 53 publications

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

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

The stability of the transcriptome during the estrous cycle in four regions of the mouse brain

Sex Hormones and Cognition: Neuroendocrine Influences on Memory and Learning

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