Medial preoptic estrogen receptor-beta blunts the estrogen receptor-alpha mediated increases in wheel-running behavior of female rats

Grigsby, Kolter B.; Kovarik, Cathleen M.; Mao, Xuansong; Booth, Frank W.

doi:10.1016/j.bbr.2019.112341

Cited by 5 publications

(8 citation statements)

References 57 publications

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“…The results for NAC are consistent with past studies in birds and mammals (Cunningham and Kelley, 1992;Maksimoski et al, 2021). Although we found no reports on the impact of MOR in POM on motor activity, prior studies have revealed a role for the POM in voluntary wheel running in mice (King, 1979;Grigsby et al, 2020;Ladyman et al, 2021).…”

Section: Mu Opioid Receptor Stimulation In Nac or Pom Stimulates Moto...supporting

confidence: 92%

Mu opioid receptor stimulation in the medial preoptic area or nucleus accumbens facilitates song and reward in flocking European starlings

et al. 2022

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It has been proposed that social cohesion in gregarious animals is reinforced both by a positive affective state induced by social interactions and by the prevention of a negative state that would be caused by social separation. Opioids that bind to mu opioid receptors (MORs) act in numerous brain regions to induce positive and to reduce negative affective states. Here we explored a potential role for MORs in affective states that may impact flocking behavior in mixed-sex flocks of nonbreeding European starlings, Sturnus vulgaris. Singing behavior, which is considered central to flock cohesion, and other social behaviors were quantified after infusions of the MOR agonist D-Ala2, N-Me-Phe4, glycinol5-ENK (DAMGO) into either the medial preoptic area (POM) or the nucleus accumbens (NAC), regions previously implicated in affective state and flock cohesion. We focused on beak wiping, a potential sign of stress or redirected aggression in this species, to provide insight into a presumed negative state. We also used conditioned place preference (CPP) tests to provide insight into the extent to which infusions of DAMGO into POM or NAC that stimulated song might be rewarding. We found that MOR stimulation in either POM or NAC dose-dependently promoted singing behavior, reduced beak wiping, and induced a CPP. Subtle differences in responses to MOR stimulation between NAC and POM also suggest potential functional differences in the roles of these two regions. Finally, because the location of NAC has only recently been identified in songbirds, we additionally performed a tract tracing study that confirmed the presence of dopaminergic projections from the ventral tegmental area to NAC, suggesting homology with mammalian NAC. These findings support the possibility that MORs in POM and NAC play a dual role in reinforcing social cohesion in flocks by facilitating positive and reducing negative affective states.

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Section: Mu Opioid Receptor Stimulation In Nac or Pom Stimulates Moto...supporting

confidence: 92%

Mu opioid receptor stimulation in the medial preoptic area or nucleus accumbens facilitates song and reward in flocking European starlings

et al. 2022

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“…Our previous work has identified the medial POA as a key site mediating prolactin action on behavioral adaptations associated with pregnancy ( Brown et al, 2017 ). This region has also been linked to the hormonal regulation of RWA during the estrous cycle ( Grigsby et al, 2020 ; King, 1979 ). The MPOA contains the largest concentration of Prlr-expressing neurons in the hypothalamus ( Brown et al, 2010 ), and over 50% of these neurons are GABAergic ( Brown et al, 2017 ).…”

Section: Resultsmentioning

confidence: 99%

“…Despite losing only approximately 50% of Prlr in the MPOA, these animals clearly showed attenuated pregnancy-induced and early lactation-induced suppression of RWA, suggesting that either the neurons influencing RWA are only a subset of those required for the expression of maternal behavior or that there is no major overlap in these neuronal pathways. The MPOA has previously been linked to RWA, with the increased running in response to estradiol treatment apparently mediated through estrogen receptor alpha (ERα) in the MPOA ( Grigsby et al, 2020 ; King, 1979 ; Wei et al, 2018 ). The neuronal cell types mediating the RWA response to estradiol have not been elucidated, but an estrogen-responsive MPOA circuit projecting to the VTA has been shown to be critical for maternal behavior ( Wei et al, 2018 ; Fang et al, 2018 ), and at least some of these ERα-expressing neurons in the MPOA are GABAergic ( Herbison, 1997 ).…”

Section: Discussionmentioning

confidence: 99%

A reduction in voluntary physical activity in early pregnancy in mice is mediated by prolactin

Ladyman

Carter

Gillett

et al. 2021

eLife

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As part of the maternal adaptations to pregnancy, mice show a rapid, profound reduction in voluntary running wheel activity (RWA) as soon as pregnancy is achieved. Here, we evaluate the hypothesis that prolactin, one of the first hormones to change secretion pattern following mating, is involved in driving this suppression of physical activity levels during pregnancy. We show that prolactin can acutely suppress RWA in non-pregnant female mice, and that conditional deletion of prolactin receptors (Prlr) from either most forebrain neurons or from GABA neurons prevented the early pregnancy-induced suppression of RWA. Deletion of Prlr specifically from the medial preoptic area, a brain region associated with multiple homeostatic and behavioural roles including parental behaviour, completely abolished the early pregnancy-induced suppression of RWA. As pregnancy progresses, prolactin action continues to contribute to the further suppression of RWA, although it is not the only factor involved. Our data demonstrate a key role for prolactin in suppressing voluntary physical activity during early pregnancy, highlighting a novel biological basis for reduced physical activity in pregnancy.

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“…Due to much overlap in functions mediated through ERα and ERβ (e.g., regulation of DA metabolism, which appears more attributed to Esr2 vs. Esr1 [12,31]), it is possible that compensatory signaling through ERβ may have prevented more robust genotype differences from being observed. ERb, while not influencing PA [32], is the major E2 receptor expressed in the brain [33] and has recently been shown (using various ERb-selective ligands administered systemically) to improve metabolism, in part by inducing the browning of WAT [29,34]. No studies have yet directly tested the effect of neuronal ERb on adiposity or metabolism, but one recent study found that deletion of a tumor suppressor unexpectedly promoted leanness in female (but not male) mice, an effect that coincided with increased neuronal ERb, while not influencing PA [32], is the major E2 receptor expressed in the brain [33] and has recently been shown (using various ERb-selective ligands administered systemically) to improve metabolism, in part by inducing the browning of WAT [29,34].…”

Section: Discussionmentioning

confidence: 80%

Knockdown of Esr1 from DRD1-Rich Brain Regions Affects Adipose Tissue Metabolism: Potential Crosstalk between Nucleus Accumbens and Adipose Tissue

Shay,

Welly,

Mao

et al. 2024

IJMS

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Declining estrogen (E2) leads to physical inactivity and adipose tissue (AT) dysfunction. Mechanisms are not fully understood, but E2’s effects on dopamine (DA) activity in the nucleus accumbens (NAc) brain region may mediate changes in mood and voluntary physical activity (PA). Our prior work revealed that loss of E2 robustly affected NAc DA-related gene expression, and the pattern correlated with sedentary behavior and visceral fat. The current study used a new transgenic mouse model (D1ERKO) to determine whether the abolishment of E2 receptor alpha (ERα) signaling within DA-rich brain regions affects PA and AT metabolism. Adult male and female wild-type (WT) and D1ERKO (KD) mice were assessed for body composition, energy intake (EE), spontaneous PA (SPA), and energy expenditure (EE); underwent glucose tolerance testing; and were assessed for blood biochemistry. Perigonadal white AT (PGAT), brown AT (BAT), and NAc brain regions were assessed for genes and proteins associated with DA, E2 signaling, and metabolism; AT sections were also assessed for uncoupling protein (UCP1). KD mice had greater lean mass and EE (genotype effects) and a visible change in BAT phenotype characterized by increased UCP1 staining and lipid depletion, an effect seen only among females. Female KD had higher NAc Oprm1 transcript levels and greater PGAT UCP1. This group tended to have improved glucose tolerance (p = 0.07). NAc suppression of Esr1 does not appear to affect PA, yet it may directly affect metabolism. This work may lead to novel targets to improve metabolic dysfunction following E2 loss, possibly by targeting the NAc.

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Medial preoptic estrogen receptor-beta blunts the estrogen receptor-alpha mediated increases in wheel-running behavior of female rats

Cited by 5 publications

References 57 publications

Mu opioid receptor stimulation in the medial preoptic area or nucleus accumbens facilitates song and reward in flocking European starlings

Mu opioid receptor stimulation in the medial preoptic area or nucleus accumbens facilitates song and reward in flocking European starlings

A reduction in voluntary physical activity in early pregnancy in mice is mediated by prolactin

Knockdown of Esr1 from DRD1-Rich Brain Regions Affects Adipose Tissue Metabolism: Potential Crosstalk between Nucleus Accumbens and Adipose Tissue

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