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Maternal physical activity during pregnancy has been shown to confer benefits on the brain functions of offspring. This study investigated the positive effects of maternal exercise during pregnancy on enhancing hippocampal synaptic plasticity and resilience to stress-induced depressive behavior in adult murine offspring. Using a mouse model with mother mice engaged in voluntary wheel running during pregnancy, we assessed changes in long-term potentiation (LTP) in the hippocampal dentate gyrus, synaptic protein expression, and behavioral responses to chronic stress in adult male and female offspring from exercised dams compared with those from sedentary dams. We found that maternal exercise enhanced LTP in offspring of both sexes. Western blot analysis of hippocampal synaptoneurosome extractions revealed significant main effects of maternal exercise on increasing the expression of brain-derived neurotrophic factor (BDNF), PSD-95, synaptophysin, and phosphorylation of N-methyl-D-aspartate receptor subunit GluN2A and α-amino-3-hydroxy-5-methyl-4-isoxazolepropionic acid receptor subunit GluA1. Maternal exercise significantly increased synaptophysin levels in both male and female offspring, with sex-specific effects on increasing PSD-95 levels in male offspring and increased p-GluN2A levels in female offspring from exercised dams. Golgi staining revealed a significant increase in hippocampal dendritic spine density in female offspring only. Maternal exercise-induced improvements in hippocampal synaptic plasticity were associated with reduced depression-like behaviors in both male and female offspring exposed to chronic unpredictable stress. Additionally, male offspring displayed reduced anxiety-like behavior, while female offspring showed no significant anxiolytic changes. These findings elucidate the sex-specific effects of maternal exercise on enhancing hippocampal synaptic plasticity, which may contribute to increased resilience against stress-induced depressive behaviors in adult offspring. Show less

Maternal separation (MS) is a widely used model of early-life stress that induces long-lasting behavioral and neurobiological alterations in offspring. Maternal exercise during pregnancy has been proposed as a non-pharmacological strategy to counteract these adverse effects. Pregnant Wistar rats were assigned to either a sedentary or exercise group, with the exercise group having free access to a running wheel throughout pregnancy. Offspring were divided into four experimental groups: offspring of sedentary mothers without MS (SedMS-), offspring of sedentary mothers with MS (SedMS+), offspring of exercised mothers without MS (ExMS-), and offspring of exercised mothers with MS (ExMS+). Behavioral assessments, conducted in adulthood starting at postnatal day 90 (P90), included the open field, elevated plus maze, forced swim test, and contextual fear conditioning. Morphological analysis of the hippocampus was performed using isotropic fractionation to quantify total neuronal and non-neuronal cells. Epigenetic changes were evaluated through chromatin immunoprecipitation (ChIP) using anti-acetylated histone H3 and H4, followed by amplification of bdnf exons IV and VI. Maternal separation increased depressive-like behavior and impaired hippocampus-dependent memory, effects that were attenuated by maternal exercise. MS also elevated non-neuronal cell numbers and reduced neuronal cells in the hippocampus, whereas prenatal exercise reversed these alterations. No significant group differences were found in histone acetylation at the Bdnf loci examined. Maternal exercise during pregnancy mitigates behavioral and morphological deficits induced by early-life stress, supporting its neuroprotective role in preserving hippocampal integrity and function. Although no significant epigenetic changes were detected, these findings suggest that maternal physical activity may be a promising intervention to mitigate the long-term neurobiological consequences of early-life adversity. Show less