Running-induced memory enhancement correlates with the preservation of thin spines in the hippocampal area CA1 of old C57BL/6 mice

Xu, Benke; Sun, Anbang; He, Yun; Qian, Feng; Chen, Yuncai; Luo, Hongyu

doi:10.1016/j.neurobiolaging.2017.01.002

Cited by 20 publications

(38 citation statements)

References 80 publications

Supporting

Mentioning

Contrasting

Order By: Relevance

“…These effects contribute to restore hippocampal-dependent plasticity and correlate with adaptive behavior. Thus, aged animals that perform poorly in spatial learning and pattern separation tasks, improve their performance after exercise (van Praag et al, 2005; Marlatt et al, 2012; Wu et al, 2015; Duzel et al, 2016; Xu et al, 2017).…”

Section: Introductionmentioning

confidence: 99%

Rejuvenating the Brain With Chronic Exercise Through Adult Neurogenesis

2019

View full text Add to dashboard Cite

The aging brain presents a general decline in plasticity that also affects hippocampal neurogenesis. Besides the well-known reduction in the rate of neuronal generation, development of new neurons is largely delayed in the aging brain. We have recently shown that this slow development is accelerated when middle-aged mice perform voluntary exercise in a running wheel. It is unclear whether the effects of exercise on neurogenic plasticity are persistent in time in a manner that might influence neuronal cohorts generated over an extended time span. To clarify these issues, we examined the effects of exercise length in 3-week-old neurons and found that their development is accelerated only when running occurs for long (3-4 weeks) but not short periods (1 week). Furthermore, chronic running acted with similar efficiency on neurons that were born at the onset, within, or at the end of the exercise period, lasting until 3 months. Interestingly, no effects were observed on neurons born 1 month after exercise had ended. Our results indicate that multiple neuronal cohorts born throughout the exercise span integrate very rapidly in the aging brain, such that the effects of running will accumulate and expand network assembly promoted by neurogenesis. These networks are likely to be more complex than those assembled in a sedentary mouse due to the faster and more efficient integration of new neurons.

show abstract

Section: Introductionmentioning

confidence: 99%

Rejuvenating the Brain With Chronic Exercise Through Adult Neurogenesis

2019

View full text Add to dashboard Cite

show abstract

“…Physical activity has emerged as a promising, low-cost strategy to improving neurocognitive function (Kramer and Erickson, 2007 ; Gomez-Pinilla and Hillman, 2013 ), fighting hippocampal impairment, and protecting against memory decline (de Bruijn et al, 2013 ). As reported above, voluntary wheel exercise increases neurogenesis and cell proliferation in the hippocampus of old rats (van Praag et al, 2005 ) and enhances synaptic density in young (Dietrich et al, 2008 ) and old (Xu et al, 2017 ) mice. Our findings suggest that moderate physical activity in late aging is able to revert SMCA1 synaptic density to the values of the middle-aged group and hippocampal plasticity is retained in aging.…”

Section: Discussionmentioning

confidence: 65%

Modulatory Effect of Aerobic Physical Activity on Synaptic Ultrastructure in the Old Mouse Hippocampus

Fattoretti

Malatesta

Cisterna

et al. 2018

Front. Aging Neurosci.

View full text Add to dashboard Cite

Aerobic physical exercise (APE) leads to improved brain functions. To better understand the beneficial effect of APE on the aging brain, a morphometric study was carried out of changes in hippocampal synapses of old (>27 months) Balb/c mice undergoing treadmill training (OTT) for 4 weeks in comparison with old sedentary (OS), middle-aged sedentary (MAS) and middle-aged treadmill training (MATT) mice. The inner molecular layer of the hippocampal dentate gyrus (IMLDG) and the molecular stratum of Ammon’s horn1 neurons (SMCA1) were investigated. The number of synapses per cubic micron of tissue (numeric density, Nv), overall synaptic area per cubic micron of tissue (surface density, Sv), average area of synaptic contact zones (S), and frequency (%) of perforated synapses (PS) were measured in electron micrographs of ethanol-phosphotungstic acid (E-PTA) stained tissue. Data were analyzed with analysis of variance (ANOVA). In IMLDG, an effect of age was found for Nv and Sv, but not S and %PS. Similar results were found for exercise and the interaction of age and exercise. In post hoc analysis Nv was higher (60.6% to 75.1%; p < 0.001) in MATT vs. MAS, OS and OTT. Sv was higher (32.3% to 54.6%; p < 0.001) in MATT vs. MAS, OS and OTT. In SMCA1, age affected Nv, Sv and %PS, but not S. The effect of exercise was significant for Sv only. The interaction of age and exercise was significant for Nv, Sv and %PS. In post hoc analysis Nv was lower in OS vs. MAS, MATT and OTT (−26.1% to −32.1%; p < 0.038). MAS and OTT were similar. Sv was lower in OS vs. MAS, MATT and OTT (−23.4 to −30.3%, p < 0.004). MAS and OTT were similar. PS frequency was higher in OS vs. MAS, MATT and OTT (48.3% to +96.6%, p < 0.023). APE positively modulated synaptic structural dynamics in the aging hippocampus, possibly in a region-specific way. The APE-associated reduction in PS frequency in SMCA1 of old mice suggests that an increasing complement of PS is a compensatory phenomenon to maintain synaptic efficacy. In conclusion, the modulation of synaptic plasticity by APE gives quantitative support to the concept that APE protects from neurodegeneration and improves learning and memory in aging.

show abstract

“…The morphological and biochemical markers of brain plasticity, such as hippocampal neurogenesis, synaptic protein expressions, and synaptic morphology, are involved in the positive impact of EE on cognition. For instance, the beneficial effect of prolonged running wheels (a component of EE) on spatial learning and memory in older mice is coupled with the increased thin spines carrying small synapses expressing PSD-95 in the Schaffer pathway [63]. Postpubertal EE rescues the disrupted spatial discrimination ability induced by LPS injection during midgestation in offspring rats.…”

Section: Neural Plasticitymentioning

confidence: 99%

Effects of Gestational Inflammation with Postpartum Enriched Environment on Age-Related Changes in Cognition and Hippocampal Synaptic Plasticity-Related Proteins

Sun

et al. 2020

Neural Plasticity

View full text Add to dashboard Cite

Increasing evidence indicates that exposure to inflammation during pregnancy intensifies the offspring’s cognitive impairment during aging, which might be correlated with changes in some synaptic plasticity-related proteins. In addition, an enriched environment (EE) can significantly exert a beneficial impact on cognition and synaptic plasticity. However, it is unclear whether gestational inflammation combined with postnatal EE affects the changes in cognition and synaptic plasticity-related proteins during aging. In this study, pregnant mice were intraperitoneally injected with lipopolysaccharides (LPS, 50 μg/kg) or normal saline at days 15–17 of pregnancy. At 21 days after delivery, some LPS-treated mice were randomly selected for EE treatment. At the age of 6 and 18 months, Morris water maze (MWM) and western blotting were, respectively, used to evaluate or measure the ability of spatial learning and memory and the levels of postsynaptic plasticity-related proteins in the hippocampus, including postsynaptic density protein 95 (PSD-95), α-amino-3-hydroxy-5-methyl-4-isoxazolepropionic acid receptor (AMPAR) GluA1 subunit, and Homer-1b/c. The results showed that 18-month-old control mice had worse spatial learning and memory and lower levels of these synaptic plasticity-related proteins (PSD-95, GluA1, and Homer-1b/c) than the 6-month-old controls. Gestational LPS exposure exacerbated these age-related changes of cognition and synaptic proteins, but EE could alleviate the treatment effect of LPS. In addition, the performance during learning and memory periods in the MWM correlated with the hippocampal levels of PSD-95, GluA1, and Homer-1b/c. Our results suggested that gestational inflammation accelerated age-related cognitive impairment and the decline of PSD-95, GluA1, and Homer-1b/c protein expression, and postpartum EE could alleviate these changes.

show abstract

Running-induced memory enhancement correlates with the preservation of thin spines in the hippocampal area CA1 of old C57BL/6 mice

Cited by 20 publications

References 80 publications

Rejuvenating the Brain With Chronic Exercise Through Adult Neurogenesis

Rejuvenating the Brain With Chronic Exercise Through Adult Neurogenesis

Modulatory Effect of Aerobic Physical Activity on Synaptic Ultrastructure in the Old Mouse Hippocampus

Effects of Gestational Inflammation with Postpartum Enriched Environment on Age-Related Changes in Cognition and Hippocampal Synaptic Plasticity-Related Proteins

Contact Info

Product

Resources

About