Temporal and bidirectional influences of estradiol on voluntary wheel running in adult female and male rats

Krentzel, Amanda A.; Proaño, Stephanie B.; Patisaul, Heather B.; Meitzen, John

doi:10.1016/j.yhbeh.2020.104694

Cited by 22 publications

(14 citation statements)

References 67 publications

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“…Surprisingly, male serum levels were unexpectedly high, similar to proestrus females ( Figure 2D ). Purification may increase estradiol-IR by removing interfering substances (Chao et al, 2011 ; Tuscher et al, 2016 ; Boyaci et al, 2020 ; Krentzel et al, 2020 ; Proaño et al, 2020 ). Indeed, extracting serum prior to ELISA enhanced estradiol-IR and distinguished male and female values ( Figure 2F ) but were higher than expected of mouse serum (Nilsson et al, 2015 ; but see Marbouti et al, 2020 , analyzed by ELISA).…”

Section: Discussionmentioning

confidence: 99%

“…100 μl thawed serum was extracted twice (5:1 ratio diethyl ether: serum). After 30 min, samples were frozen in a methanol/dry ice bath and the organic (unfrozen) phase was transferred to a new glass tube, dried, then stored until analysis (Krentzel et al, 2020 ; Proaño et al, 2020 ). Hippocampi (20 mg) were processed using liquid-liquid and solid-phase extraction (Chao et al, 2011 ; Tuscher et al, 2016 ).…”

Section: Methodsmentioning

confidence: 99%

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Sex-dependent effects of multiple acute concurrent stresses on memory: a role for hippocampal estrogens

Hokenson

Alam²,

Short³

et al. 2022

Front. Behav. Neurosci.

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Memory disruption commonly follows chronic stress, whereas acute stressors are generally benign. However, acute traumas such as mass shootings or natural disasters—lasting minutes to hours and consisting of simultaneous physical, social, and emotional stresses—are increasingly recognized as significant risk factors for memory problems and PTSD. Our prior work has revealed that these complex stresses (concurrent multiple acute stresses: MAS) disrupt hippocampus-dependent memory in male rodents. In females, the impacts of MAS are estrous cycle-dependent: MAS impairs memory during early proestrus (high estrogens phase), whereas the memory of female mice stressed during estrus (low estrogens phase) is protected. Female memory impairments limited to high estrogens phases suggest that higher levels of estrogens are necessary for MAS to disrupt memory, supported by evidence that males have higher hippocampal estradiol than estrous females. To test the role of estrogens in stress-induced memory deficits, we blocked estrogen production using aromatase inhibitors. A week of blockade protected male and female mice from MAS-induced memory disturbances, suggesting that high levels of estrogens are required for stress-provoked memory impairments in both males and females. To directly quantify 17β-estradiol in murine hippocampus we employed both ELISA and mass spectrometry and identified significant confounders in both procedures. Taken together, the cross-cycle and aromatase studies in males and females support the role for high hippocampal estrogens in mediating the effect of complex acute stress on memory. Future studies focus on the receptors involved, the longevity of these effects, and their relation to PTSD-like behaviors in experimental models.

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Section: Discussionmentioning

confidence: 99%

Section: Methodsmentioning

confidence: 99%

Sex-dependent effects of multiple acute concurrent stresses on memory: a role for hippocampal estrogens

Hokenson

Alam²,

Short³

et al. 2022

Front. Behav. Neurosci.

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“…109 There may also be differences in MSN electrophysiology in response to repeated doses of estradiol because several nucleus accumbens core related behaviors are sensitive to estrogen priming. [116][117][118] It is unknown whether inhibitory synaptic inputs and synaptic plasticity change across the estrous cycle.…”

Section: Excitatory Synaptic Inputmentioning

confidence: 99%

“…We favor the first interpretation: changing electrophysiological properties across the estrous cycle directly facilitate changes in nucleus accumbens core function, mostly regarding its role in motivated reproductive behaviors. 121 These behaviors could potentially include the changes in sexual receptivity detected during the estrous cycle, 18,89 paced mating behavior, 122 sexual reward, 123 sensorimotor locomotor, and exploratory/anxiety-related behaviors, 36,117,118,124 and, at least in some species, mate choice and pair bonding. 125,126 We do note that correlation is not causation, and an important future direction will be to establish causal roles of estrous cycle action and ovarian hormone effects in the nucleus accumbens core to specific behavioral phenotypes.…”

Section: Excitatory Synaptic Inputmentioning

confidence: 99%

“…A temporal difference in the impact of estradiol on electrophysiological properties, especially between the seconds to minutes to hours timescale, has been demonstrated in other systems 109 . There may also be differences in MSN electrophysiology in response to repeated doses of estradiol because several nucleus accumbens core related behaviors are sensitive to estrogen priming 116–118 . It is unknown whether inhibitory synaptic inputs and synaptic plasticity change across the estrous cycle.…”

Section: The Estrous Cycle Influences Nucleus Accumbens Core Msn Elec...mentioning

confidence: 99%

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The estrous cycle and 17β‐estradiol modulate the electrophysiological properties of rat nucleus accumbens core medium spiny neurons

Krentzel

Proaño

Dorris

et al. 2022

J Neuroendocrinology

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The nucleus accumbens core is a key nexus within the mammalian brain for integrating the premotor and limbic systems and regulating important cognitive functions such as motivated behaviors. Nucleus accumbens core functions show sex differences and are sensitive to the presence of hormones such as 17β-estradiol (estradiol) in normal and pathological contexts. The primary neuron type of the nucleus accumbens core, the medium spiny neuron (MSN), exhibits sex differences in both intrinsic excitability and glutamatergic excitatory synapse electrophysiological properties. Here, we provide a review of recent literature showing how estradiol modulates rat nucleus accumbens core MSN electrophysiology within the context of the estrous cycle. We review the changes in MSN electrophysiological properties across the estrous cycle and how these changes can be mimicked in response to exogenous estradiol exposure. We discuss in detail recent findings regarding how acute estradiol exposure rapidly modulates excitatory synapse properties in nucleus accumbens core but not caudate-putamen MSNs, which mirror the natural changes seen across estrous cycle phases. These recent insights demonstrate the strong impact of sex-specific estradiol action upon nucleus accumbens core neuron electrophysiology.

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Estrous cycle impacts on dendritic spine plasticity in rat nucleus accumbens core and shell and caudate–putamen

Beeson

Meitzen

2023

J of Comparative Neurology

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An important factor that can modulate neuron properties is sex-specific hormone fluctuations, including the human menstrual cycle and rat estrous cycle in adult females. Considering the striatal brain regions, the nucleus accumbens (NAc) core, NAc shell, and caudate-putamen (CPu), the estrous cycle has previously been shown to impact relevant behaviors and disorders, neuromodulator action, and medium spiny neuron (MSN) electrophysiology. Whether the estrous cycle impacts MSN dendritic spine attributes has not yet been examined, even though MSN spines and glutamatergic synapse properties are sensitive to exogenously applied estradiol. Thus, we hypothesized that MSN dendritic spine attributes would differ by estrous cycle phase. To test this hypothesis, brains from adult male rats and female rats in diestrus, proestrus AM, proestrus PM, and estrus were processed for Rapid Golgi-Cox staining. MSN dendritic spine density, size, and type were analyzed in the NAc core, NAc shell, and CPu. Overall spine size differed across estrous cycle phases in female NAc core and NAc shell, and spine length differed across estrous cycle phase in NAc shell and CPu. Consistent with previous work, dendritic spine density was increased in the NAc core compared to the NAc shell and CPu, independent of sex and estrous cycle.Spine attributes in all striatal regions did not differ by sex when estrous cycle was disregarded. These results indicate, for the first time, that estrous cycle phase impacts dendritic spine plasticity in striatal regions, providing a neuroanatomical avenue by which sex-specific hormone fluctuations can impact striatal function and disorders.

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Temporal and bidirectional influences of estradiol on voluntary wheel running in adult female and male rats

Cited by 22 publications

References 67 publications

Sex-dependent effects of multiple acute concurrent stresses on memory: a role for hippocampal estrogens

Sex-dependent effects of multiple acute concurrent stresses on memory: a role for hippocampal estrogens

The estrous cycle and 17β‐estradiol modulate the electrophysiological properties of rat nucleus accumbens core medium spiny neurons

Estrous cycle impacts on dendritic spine plasticity in rat nucleus accumbens core and shell and caudate–putamen

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