Paternal treadmill exercise enhances spatial learning and memory related to hippocampus among male offspring

Yin, Mei; Wang, W.; Sun, Jie; Liu, S.; Liu, X.L.; Niu, Yanmei; Yuan, Hairui; Yang, Fengying; Li, Fu

doi:10.1016/j.bbr.2013.07.040

Cited by 52 publications

(43 citation statements)

References 62 publications

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“…In this study, pups born from mothers that ran during their pregnancy time exhibited a reduction in β-amyloid (Aβ) plaque burden and amyloid precursor protein (APP), decreased expression of proinflammatory mediators, and an increased expression of genes involved in synaptic plasticity and memory formation. In addition to the positive effects of maternal exercise on the progeny, pups from physically active fathers are also privileged in terms of cognitive function (Yin et al, 2013). As demonstrated by Yin et al (2013), 6 wk of paternal exercise enhanced the spatial learning and memory of F1 mice offspring, with a concomitant increase in hippocampal BDNF and reelin expression.…”

Section: Can the Beneficial Effects Of Physical Exercise Be Transmmentioning

confidence: 99%

Physical exercise as an epigenetic modulator of brain plasticity and cognition

Fernandes

Arida

Gómez‐Pinilla

2017

Neuroscience & Biobehavioral Reviews

221

172

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A large amount of evidence has demonstrated the power of exercise to support cognitive function, the effects of which can last for considerable time. An emerging line of scientific evidence indicates that the effects of exercise are longer lasting than previously thought up to the point to affect future generations. The action of exercise on epigenetic regulation of gene expression seem central to building an “epigenetic memory” to influence long-term brain function and behavior. In this review article, we discuss new developments in the epigenetic field connecting exercise with changes in cognitive function, including DNA methylation, histone modifications and microRNAs (miRNAs). The understanding of how exercise promotes long-term cognitive effects is crucial for directing the power of exercise to reduce the burden of neurological and psychiatric disorders.

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Section: Can the Beneficial Effects Of Physical Exercise Be Transmmentioning

confidence: 99%

Physical exercise as an epigenetic modulator of brain plasticity and cognition

Fernandes

Arida

Gómez‐Pinilla

2017

Neuroscience & Biobehavioral Reviews

221

172

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“…Exercise improved metabolic status and sperm function in obese men (Palmer et al, 2012). Paternal treadmill exercise enhanced hippocampus-dependent spatial learning and memory in the male pups (Yin et al, 2013). …”

Section: Discussionmentioning

confidence: 99%

Paternal physical exercise improves spatial learning ability by enhancing hippocampal neuroplasticity in male pups born from obese maternal rats

Park

Kim

2017

J Exerc Rehabil

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Maternal obesity exerts negative effects on cognitive function and behavior of the offspring. In the present study, we assessed the effects of paternal physical exercise on spatial learning ability in relation with hippocampal neuroplasticity in the rat pups born from the obese maternal rats. There were four experimental groups: paternal nonexercised male pups from normal maternal rats, paternal exercised male pups from normal maternal rats, paternal nonexercised male pups from obese maternal rats, and paternal exercised male pups from obese maternal rats. Normal diet was supplied for normal maternal rats and high-fat diet was supplied for obese maternal rats for a 12-week period until mating, and the same diet for each group continued throughout pregnancy and lactation period. Male rats in the exercising groups exercised for a 12-week period. Spatial learning ability was reduced in the male rat pups born from the obese maternal rats. Expressions of brain-derived neurotrophic factor (BDNF) and tyrosine kinase B receptor (TrkB) in the hippocampus were suppressed and cell proliferation and differentiation in the hippocampus were reduced in the male rat pups born from the obese maternal rats. Paternal treadmill exercise improved spatial learning ability, increased BDNF and TrkB expressions, and enhanced cell proliferation and differentiation in the male rat pups born from the obese maternal rats. It can be suggested that paternal exercise enhances hippocampal neuroplasticity and consequently improved spatial learning ability in the rat pups born from the obese maternal rats.

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“…Even though these studies reported significantly greater Bdnf expression in offspring of exercise mothers compared to offspring of sedentary mothers one month after birth, our youngest time point was two months of age which may explain why even in our youngest group of offspring, we observed no differences in neurotrophin ( Bdnf ) or growth factor ( Igf1 and Vegf ) mRNA expression. Yin et al [15] reported enhanced Bdnf expression (mRNA and protein) and spatial memory performance in ~one-month old male offspring of treadmill exercised male C57BL/6J mice. Again, this is much younger than our youngest group, suggesting the influence of parental exercise is relatively short-lived.…”

Section: Discussionmentioning

confidence: 99%

“…Numerous studies in rodents show that in utero exercise exposure increases hippocampal expression of brain derived neurotrophic factor (Bdnf) [4; 5; 7; 12]; cell proliferation and neuron differentiation [5; 6]; increased mitochondrial content and expression of genes associated with mitochondrial biogenesis [13]; and improved performance on spatial [4; 8] and non-spatial memory tasks [5; 7; 14]. In addition to the influence of maternal exercise, long-term paternal forced exercise enhances male offspring neurotrophin expression and spatial learning and memory performance [15], suggesting transgenerational inheritance of exercise effects beyond direct in utero exposure. There is remarkable consistency between the effects of in utero and adult exercise exposure on the hippocampus.…”

Section: Introductionmentioning

confidence: 99%

Lifelong parental voluntary wheel running increases offspring hippocampal Pgc-1α mRNA expression but not mitochondrial content or Bdnf expression

Venezia

Guth²,

Spangenburg³

et al. 2015

NeuroReport

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When exercise is initiated during pregnancy, offspring of physically active mothers have higher hippocampal expression of brain derived neurotrophic factor (Bdnf) and other plasticity and mitochondrial-associated genes, resulting in hippocampal structural and functional adaptations. In the present study, we examined the effects of lifelong parental voluntary wheel running (before, during, and after pregnancy) on offspring hippocampal mRNA expression of genes implicated in the exercise-induced improvement of cognitive function. C57BL/6 mice were individually housed at 8 weeks of age with (EX; n=20) or without (SED; n=20) access to a computer-monitored voluntary running wheel (VRW) for 12 weeks prior to breeding. EX breeders maintained access to the VRW throughout breeding, pregnancy, and lactation. Male offspring were housed in sedentary cages, regardless of parental group, and were sacrificed at 8 (n=18) or 28 weeks (n=19). PCR was used to assess mRNA expression of several genes and mitochondrial content (ratio of mitochondrial to nuclear DNA) in hippocampal homogenates. We found significantly higher peroxisome proliferator-activated receptor γ coactivator 1 alpha (Pgc-1α) mRNA expression in EX offspring compared to SED offspring at 8 wks (p=0.04), though the effect was no longer present at 28 wks. There was no difference in mitochondrial content or expression of Bdnf or any other mRNA targets between offspring at 8 or 28 wks. In contrast to exercise initiated during pregnancy, parental voluntary physical activity initiated early in life and maintained throughout pregnancy has little effect on offspring mRNA expression of genes implicated in exercise-induced hippocampal plasticity.

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Paternal treadmill exercise enhances spatial learning and memory related to hippocampus among male offspring

Cited by 52 publications

References 62 publications

Physical exercise as an epigenetic modulator of brain plasticity and cognition

Physical exercise as an epigenetic modulator of brain plasticity and cognition

Paternal physical exercise improves spatial learning ability by enhancing hippocampal neuroplasticity in male pups born from obese maternal rats

Lifelong parental voluntary wheel running increases offspring hippocampal Pgc-1α mRNA expression but not mitochondrial content or Bdnf expression

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