Early and late effects of maternal experience on hippocampal neurogenesis, microglia, and the circulating cytokine milieu

Eid, Rand S.; Chaiton, Jessica A; Lieblich, Stephanie E.; Bodnar, Tamara S.; Weinberg, Joanne; Galea, Liisa A.M.

doi:10.1016/j.neurobiolaging.2019.01.021

Cited by 74 publications

(54 citation statements)

References 101 publications

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“…The increased exposure to estradiol across pregnancy may underlie the persistent changes in endogenous estradiol documented in parous rats and women (17,22,23). For example, primiparous rats have lower levels of circulating estradiol compared to nulliparous rats during proestrus [ (17,22); but see (61) for opposite findings in middle age], and human mothers have lower estradiol levels than nonmothers across the menstrual cycle (23). Reproductive experience has also been shown to alter the expression of oestrogen receptors in primiparous rats in brain regions such as the medial amygdala (62).…”

Section: Discussionmentioning

confidence: 99%

Maternal Experience Does Not Predict Fear Extinction and Anxiety-Like Behaviour in Primiparous Rats Post-weaning

Pestana

McCutcheon

Harmon-Jones

et al. 2021

Front. Glob. Womens Health

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Reproductive experience leads to long-lasting changes in anxiety-like behaviour and fear extinction, the laboratory model of exposure therapy for anxiety disorders. For example, fear extinction is influenced by estrous cycle in nulliparous (no reproductive experience) female rats, but this effect is abolished in primiparous (one reproductive experience) females. It is unclear whether such changes are driven by pregnancy, maternal experience of caring for offspring during the postpartum period, or a combination of both experiences. The present study sought to determine the influence of maternal experience (i.e., exposure to pups and mother-pup interactions) on fear extinction in primiparous rats. In Experiment 1, we tested whether pup exposure is necessary to mitigate estrous effects on fear extinction in primiparous rats. Age-matched nulliparous rats, primiparous rats, and primiparous rats who experienced pregnancy but not pup exposure, underwent fear conditioning on day 1 (2 months post-parturition), extinction training during proestrus (high sex hormones) or metestrus (low sex hormones) on day 2, and extinction recall on day 3. Replicating past research, nulliparous rats showed impaired extinction recall when they were extinguished during metestrus compared to proestrus. In contrast, primiparous rats with and without pup exposure showed comparable extinction recall irrespective of estrous phase. In Experiment 2, we assessed whether naturally-occurring variation in mother-pup interactions predict future fear extinction performance and anxiety-like behaviour. During the first week of lactation, primiparous rats were measured for maternal behaviours toward pups. Primiparous rats were then tested on the light-dark box and elevated plus maze to measure anxiety-like behaviour and underwent a fear extinction protocol 1 month post-weaning. We found no significant correlations between maternal behaviour and fear extinction outcomes or anxiety-like behaviour. Our findings suggest that pregnancy, not maternal experience, mitigates the impact of estrous cycle on fear extinction. In addition, natural variation in maternal experience does not appear to contribute to variability in future fear extinction outcomes or anxiety-like behaviour in primiparous rats.

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Section: Discussionmentioning

confidence: 99%

Maternal Experience Does Not Predict Fear Extinction and Anxiety-Like Behaviour in Primiparous Rats Post-weaning

Pestana

McCutcheon

Harmon-Jones

et al. 2021

Front. Glob. Womens Health

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“…Continued pain and discomfort throughout the pregnancy can induce both a sensitization of the maternal nervous system, with a lower pain threshold (Gintzler, 1980;Cogan and Spinnato, 1986;Eid et al, 2019), and a dysregulation in the inflammatory response, mediated by the CAP via the vagus nerve (Garzoni et al, 2013).…”

Section: Maternal Painmentioning

confidence: 99%

A Review on the Vagus Nerve and Autonomic Nervous System During Fetal Development: Searching for Critical Windows

Cerritelli¹,

Frasch²,

Antonelli³

et al. 2021

Front. Neurosci.

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The autonomic nervous system (ANS) is one of the main biological systems that regulates the body's physiology. Autonomic nervous system regulatory capacity begins before birth as the sympathetic and parasympathetic activity contributes significantly to the fetus' development. In particular, several studies have shown how vagus nerve is involved in many vital processes during fetal, perinatal, and postnatal life: from the regulation of inflammation through the anti-inflammatory cholinergic pathway, which may affect the functioning of each organ, to the production of hormones involved in bioenergetic metabolism. In addition, the vagus nerve has been recognized as the primary afferent pathway capable of transmitting information to the brain from every organ of the body. Therefore, this hypothesis paper aims to review the development of ANS during fetal and perinatal life, focusing particularly on the vagus nerve, to identify possible “critical windows” that could impact its maturation. These “critical windows” could help clinicians know when to monitor fetuses to effectively assess the developmental status of both ANS and specifically the vagus nerve. In addition, this paper will focus on which factors—i.e., fetal characteristics and behaviors, maternal lifestyle and pathologies, placental health and dysfunction, labor, incubator conditions, and drug exposure—may have an impact on the development of the vagus during the above-mentioned “critical window” and how. This analysis could help clinicians and stakeholders define precise guidelines for improving the management of fetuses and newborns, particularly to reduce the potential adverse environmental impacts on ANS development that may lead to persistent long-term consequences. Since the development of ANS and the vagus influence have been shown to be reflected in cardiac variability, this paper will rely in particular on studies using fetal heart rate variability (fHRV) to monitor the continued growth and health of both animal and human fetuses. In fact, fHRV is a non-invasive marker whose changes have been associated with ANS development, vagal modulation, systemic and neurological inflammatory reactions, and even fetal distress during labor.

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“…The following lower limits of detection (LLODs) were observed: IL-1β: 0.74-0.88 pg/ml; IL-2: 2.1-2.6 pg/ml; IL-4: 0.35-0.45 pg/ml; IL-6: 5.6-6.2 pg/ml; IL-10: 1.1-1.8 pg/ml; IFN-γ: 0.07-0.11 pg/ml; TNF-α: 0.88-1.32 pg/ml; CXCL1: 0.17-0.36 pg/ml; GM-CSF: 0.09-0.13 pg/ml; and VEGF: 0.31-0.38 pg/ml. Values below the LLOD were assigned 0pg/mL, as published previously (Bodnar et al, 2017;Eid et al, 2019a).…”

Section: Cytokine Quantificationmentioning

confidence: 99%

“…This approach was used to derive information about the amount of variance in the data that can be accounted for by potential cytokine networks. Because PCA does not take into account group membership, ANOVAs were subsequently applied to individual PC scores as we have published previously (Eid et al, 2019a), in order to explore the effects of treatments and CUS exposure on cytokine networks. DEX was used as a covariate in all cytokine analyses as DEX was administered to half the animals on tissue collection day, and because glucocorticoids have anti-inflammatory effects (Bereshchenko et al, 2018).…”

Section: Statistical Analysesmentioning

confidence: 99%

Selective activation of estrogen receptors α and β: Implications for depressive-like phenotypes in female mice exposed to chronic unpredictable stress

Eid

Lieblich

Duarte‐Guterman

et al. 2019

Preprint

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The estrogen receptor (ER) mechanisms by which 17β-estradiol influences depressive-like behaviour have primarily been investigated acutely and not within an animal model of depression. Therefore, the current study aimed to dissect the contribution of ERα and ERβ to the effects of 17β-estradiol under non-stress and chronic stress conditions. Ovariectomized (OVX) or sham-operated mice were treated chronically (47 days) with 17β-estradiol (E2), the ERβ agonist diarylpropionitrile (DPN), the ERα agonist propylpyrazole-triol (PPT), or vehicle. On day 15 of treatment, mice from each group were assigned to Chronic Unpredictable Stress (CUS; 28 days) or non-CUS conditions. Mice were assessed for anxiety-and depressive-like behaviour and hypothalamic-pituitary-adrenal (HPA) axis function.Immune mediators and markers of plasticity (postsynaptic density protein 95 and neurogenesis) were measured in the hippocampus and frontal cortex. Overall, the effects of CUS were more robust that those of estrogenic treatments, as seen by increased immobility in the tail suspension test (TST), reduced PSD-95 expression, reduced neurogenesis in the ventral hippocampus, and HPA axis negative feedback dysregulation. However, we also observe CUS-dependent and -independent effects of ovarian status and estrogenic treatments. The effects of CUS on PSD-95 expression, the cytokine milieu, and in TST were largely driven by PPT and DPN, indicating that these treatments were not protective.Independent of CUS, estradiol increased neurogenesis in the ventral hippocampus, blunted the corticosterone response to an acute stressor, but increased anxiety-like behaviour. These findings provide insights into the complexities of estrogen signaling in modulating depressive-like phenotypes under non-stress and chronic stress conditions.

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Early and late effects of maternal experience on hippocampal neurogenesis, microglia, and the circulating cytokine milieu

Cited by 74 publications

References 101 publications

Maternal Experience Does Not Predict Fear Extinction and Anxiety-Like Behaviour in Primiparous Rats Post-weaning

Maternal Experience Does Not Predict Fear Extinction and Anxiety-Like Behaviour in Primiparous Rats Post-weaning

A Review on the Vagus Nerve and Autonomic Nervous System During Fetal Development: Searching for Critical Windows

Selective activation of estrogen receptors α and β: Implications for depressive-like phenotypes in female mice exposed to chronic unpredictable stress

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