Effects of Maternal Voluntary Wheel Running During Pregnancy on Adult Hippocampal Neurogenesis, Temporal Order Memory, and Depression-Like Behavior in Adult Female and Male Offspring

Yau, Suk-Yu; Lee, Thomas H.; Formolo, Douglas Affonso; Lee, Wing-Lun; Li, Leo Chun-Kit; Siu, Parco M.; Chan, Che Hin Chetwyn

doi:10.3389/fnins.2019.00470

Cited by 18 publications

(6 citation statements)

References 35 publications

(64 reference statements)

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“…Immunostaining was performed by the free-floating method, as previously performed [ 85 ]. For BrdU staining, the antigens were retrieved in the citric acid buffer (pH 6.0) at 95 °C for 15 min, then denatured in 2 N HCl for 30 min and neutralized by 0.1 M borate buffer (pH 8.5) for 15 min at room temperature.…”

Section: Methodsmentioning

confidence: 99%

AdipoRon Treatment Induces a Dose-Dependent Response in Adult Hippocampal Neurogenesis

Lee

Christie

Praag

et al. 2021

IJMS

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AdipoRon, an adiponectin receptor agonist, elicits similar antidiabetic, anti–atherogenic, and anti–inflammatory effects on mouse models as adiponectin does. Since AdipoRon can cross the blood–brain barrier, its chronic effects on regulating hippocampal function are yet to be examined. This study investigated whether AdipoRon treatment promotes hippocampal neurogenesis and spatial recognition memory in a dose–dependent manner. Adolescent male C57BL/6J mice received continuous treatment of either 20 mg/kg (low dose) or 50 mg/kg (high dose) AdipoRon or vehicle intraperitoneally for 14 days, followed by the open field test to examine anxiety and locomotor activity, and the Y maze test to examine hippocampal–dependent spatial recognition memory. Immunopositive cell markers of neural progenitor cells, immature neurons, and newborn cells in the hippocampal dentate gyrus were quantified. Immunosorbent assays were used to measure the serum levels of factors that can regulate hippocampal neurogenesis, including adiponectin, brain–derived neurotrophic factor (BDNF), and corticosterone. Our results showed that 20 mg/kg AdipoRon treatment significantly promoted hippocampal cell proliferation and increased serum levels of adiponectin and BDNF, though there were no effects on spatial recognition memory and locomotor activity. On the contrary, 50 mg/kg AdipoRon treatment impaired spatial recognition memory, suppressed cell proliferation, neuronal differentiation, and cell survival associated with reduced serum levels of BDNF and adiponectin. The results suggest that a low-dose AdipoRon treatment promotes hippocampal cell proliferation, while a high–dose AdipoRon treatment is detrimental to the hippocampus function.

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Section: Methodsmentioning

confidence: 99%

AdipoRon Treatment Induces a Dose-Dependent Response in Adult Hippocampal Neurogenesis

Lee

Christie

Praag

et al. 2021

IJMS

Self Cite

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“…However, many other studies reported no sex differences in these behaviors (e.g., [57]) and some have reported decreased anxiety-and depressive-like behaviors in male rats [58]. In mice, sex differences in anxiety-and depressive-like behaviors are inconsistently reported [59,60], and also similar to rats, the appearance of sex differences varies by genetic background as reflected by strain differences [59,61,62]. Sprague Dawley rats, for example, exhibit stable sex differences in immobility measures in a modified and extended version of the forced swim test, whereas a lack of sex differences was present in Long Evans rats across tests [63].…”

Section: Sex Differences In Anxiety/depressive-like Behaviors In Humamentioning

confidence: 99%

Roles for androgens in mediating the sex differences of neuroendocrine and behavioral stress responses

et al. 2020

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Estradiol and testosterone are powerful steroid hormones that impact brain function in numerous ways. During development, these hormones can act to program the adult brain in a male or female direction. During adulthood, gonadal steroid hormones can activate or inhibit brain regions to modulate adult functions. Sex differences in behavioral and neuroendocrine (i.e., hypothalamic pituitary adrenal (HPA) axis) responses to stress arise as a result of these organizational and activational actions. The sex differences that are present in the HPA and behavioral responses to stress are particularly important considering their role in maintaining homeostasis. Furthermore, dysregulation of these systems can underlie the sex biases in risk for complex, stress-related diseases that are found in humans. Although many studies have explored the role of estrogen and estrogen receptors in mediating sex differences in stress-related behaviors and HPA function, much less consideration has been given to the role of androgens. While circulating androgens can act by binding and activating androgen receptors, they can also act by metabolism to estrogenic molecules to impact estrogen signaling in the brain and periphery. This review focuses on androgens as an important hormone for modulating the HPA axis and behaviors throughout life and for setting up sex differences in key stress regulatory systems that could impact risk for disease in adulthood. In particular, impacts of androgens on neuropeptide systems known to play key roles in HPA and behavioral responses to stress (corticotropin-releasing factor, vasopressin, and oxytocin) are discussed. A greater knowledge of androgen action in the brain is key to understanding the neurobiology of stress in both sexes.

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“…An animal study on rats investigated the effects of maternal physical activity on gene expression of the neurotrophic factors, and upregulation was found in placenta of the very active mothers (Fragoso et al, 2020). Additionally, other studies found voluntary exercise during pregnancy significantly increased the level of neurotrophic factors protein in hippocampus of rat pups; and female offspring born to pregnant mice with voluntary running wheels showed enhanced cell proliferation in the dorsal hippocampus (Akhavan et al, 2013;Yau et al, 2019). These animal studies suggest that maternal physical activity during pregnancy may promote fetal brain development in a biological point of view.…”

Section: Discussionmentioning

confidence: 99%

Mother’s physical activity during pregnancy and newborn’s brain cortical development

Raja²,

Phelan³

et al. 2022

Front. Hum. Neurosci.

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BackgroundPhysical activity is known to improve mental health, and is regarded as safe and desirable for uncomplicated pregnancy. In this novel study, we aim to evaluate whether there are associations between maternal physical activity during pregnancy and neonatal brain cortical development.MethodsForty-four mother/newborn dyads were included in this longitudinal study. Healthy pregnant women were recruited and their physical activity throughout pregnancy were documented using accelerometers worn for 3–7 days for each of the 6 time points at 4–10, ∼12, ∼18, ∼24, ∼30, and ∼36 weeks of pregnancy. Average daily total steps and daily total activity count as well as daily minutes spent in sedentary/light/moderate/vigorous activity modes were extracted from the accelerometers for each time point. At ∼2 weeks of postnatal age, their newborns underwent an MRI examination of the brain without sedation, and 3D T1-weighted brain structural images were post-processed by the iBEAT2.0 software utilizing advanced deep learning approaches. Cortical surface maps were reconstructed from the segmented brain images and parcellated to 34 regions in each brain hemisphere, and mean cortical thickness for each region was computed for partial correlation analyses with physical activity measures, with appropriate multiple comparison corrections and potential confounders controlled.ResultsAt 4–10 weeks of pregnancy, mother’s daily total activity count positively correlated (FDR corrected P ≤ 0.05) with newborn’s cortical thickness in the left caudal middle frontal gyrus (rho = 0.48, P = 0.04), right medial orbital frontal gyrus (rho = 0.48, P = 0.04), and right transverse temporal gyrus (rho = 0.48, P = 0.04); mother’s daily time in moderate activity mode positively correlated with newborn’s cortical thickness in the right transverse temporal gyrus (rho = 0.53, P = 0.03). At ∼24 weeks of pregnancy, mother’s daily total activity count positively correlated (FDR corrected P ≤ 0.05) with newborn’s cortical thickness in the left (rho = 0.56, P = 0.02) and right isthmus cingulate gyrus (rho = 0.50, P = 0.05).ConclusionWe identified significant relationships between physical activity in healthy pregnant women during the 1st and 2nd trimester and brain cortical development in newborns. Higher maternal physical activity level is associated with greater neonatal brain cortical thickness, presumably indicating better cortical development.

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Effects of Maternal Voluntary Wheel Running During Pregnancy on Adult Hippocampal Neurogenesis, Temporal Order Memory, and Depression-Like Behavior in Adult Female and Male Offspring

Cited by 18 publications

References 35 publications

AdipoRon Treatment Induces a Dose-Dependent Response in Adult Hippocampal Neurogenesis

AdipoRon Treatment Induces a Dose-Dependent Response in Adult Hippocampal Neurogenesis

Roles for androgens in mediating the sex differences of neuroendocrine and behavioral stress responses

Mother’s physical activity during pregnancy and newborn’s brain cortical development

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