Exercise and hippocampal neurogenesis: a dogma re-examined and lessons learned.
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ABSTRACT:
SUBMITTER: Liu PZ
PROVIDER: S-EPMC6108220 | biostudies-literature | 2018 Aug
REPOSITORIES: biostudies-literature
Publications
Exercise and hippocampal neurogenesis: a dogma re-examined and lessons learned.
Liu Patrick Z PZ Nusslock Robin R
Neural regeneration research 20180801 8
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Project description:The rate of neurogenesis is determined by 1) the number of neural stem/progenitor cells (NSCs), 2) proliferation of NSCs, 3) neuron lineage specification, and 4) survival rate of the newborn neurons. Aging lowers the rate of hippocampal neurogenesis, while exercise (Ex) increases this rate. However, it remains unclear which of the determinants are affected by aging and Ex. We characterized the four determinants in different age groups (3, 6, 9, 12, 21 months) of mice that either received one month of Ex training or remained sedentary. Bromodeoxyuridine (BrdU) was injected two hours before sacrificing the mice to label the proliferating cells. The results showed that the number of newborn neurons massively decreased (>95%) by the time the mice reached nine months of age. The number of NSC was mildly reduced during aging, while Ex delayed such decline. The proliferation rates were greatly decreased by the time the mice were 9-month-old and Ex could not improve the rates. The rates of neuron specification were decreased during aging, while Ex increased the rates. The survival rate was not affected by age or Ex. Aging greatly reduced newborn neuron maturation, while Ex potently enhanced it. In conclusion, age-associated decline of hippocampal neurogenesis is mainly caused by reduction of NSC proliferation. Although Ex increases the NSC number and neuron specification rates, it doesn't restore the massive decline of NSC proliferation rate. Hence, the effect of Ex on the rate of hippocampal neurogenesis during aging is limited, but Ex does enhance the maturation of newborn neurons.
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Project description:Hippocampal neurogenesis persists throughout adult life and plays an important role in learning and memory. Although the influence of physical exercise on neurogenesis has been intensively studied, there is controversy in regard to how the impact of exercise may vary with its regime. Less is known about how distinct exercise paradigms may differentially affect the learning behavior. Here we found that, chronic moderate treadmill running led to an increase of cell proliferation, survival, neuronal differentiation, and migration. In contrast, intense running only promoted neuronal differentiation and migration, which was accompanied with lower expressions of vascular endothelial growth factor, brain-derived neurotrophic factor, insulin-like growth factor 1, and erythropoietin. In addition, the intensely but not mildly exercised animals exhibited a lower mitochondrial activity in the dentate gyrus. Correspondingly, neurogenesis induced by moderate but not intense exercise was sufficient to improve the animal's ability in spatial pattern separation. Our data indicate that the effect of exercise on spatial learning is intensity-dependent and may involve mechanisms other than a simple increase in the number of new neurons.
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Project description:IntroductionThe United States Veterans Health Administration (VHA) Office of Rural Health funds Enterprise-Wide Initiatives (system-wide initiatives) to spread promising practices to rural Veterans. The Office requires that evaluations of Enterprise-Wide Initiatives use the Reach, Effectiveness, Adoption, Implementation, and Maintenance (RE-AIM) framework. This presents a unique opportunity to understand the experience of using RE-AIM across a series of evaluations. The authors conducted a study to document the benefits and pitfalls of using RE-AIM, capture the variety of ways that the team captured the elements of RE-AIM, and develop recommendations for the future use of RE-AIM in evaluation.Materials and methodsThe authors first conducted a document review to capture pre-existing information about how RE-AIM was used. They subsequently facilitated two focus groups to gather more detailed information from team members who had used RE-AIM. Finally, they used member-checking throughout the writing process to ensure accurate data representation and interpretation and to gather additional feedback.ResultsFour themes emerged from the document review, focus groups, and member checking. RE-AIM: provides parameters and controls the evaluation scope, "buckets" are logical, plays well with other frameworks, and can foster collaboration or silo within a team. Challenges and attributes for each RE-AIM dimension were also described.DiscussionOverall, participants reported both strengths and challenges to using RE-AIM as an evaluation framework. The overarching theme around the challenges with RE-AIM dimensions was the importance of context. Many of these benefits and challenges of using RE-AIM may not be unique to RE-AIM and would likely occur when using any prescribed framework. The participants reported on the RE-AIM domains in a variety of ways in their evaluation reports and were not always able capture data as originally planned. Recommendations included: start with an evaluation framework (or frameworks) and revisit it throughout the evaluation, consider applying RE-AIM PRISM (Practical Robust Implementation Framework) to gain a broader perspective, and intentionally integrate quantitative and qualitative team members, regardless of the framework used.
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Project description:Adult hippocampal neurogenesis (AHN), the lifelong process of formation of new neurons in the mammalian brain, plays an important role in learning and memory. Exercise is an effective enhancer of AHN; however, the molecular mediators of exercise-induced AHN are unknown. Recently, lactate was considered as an important mediator of exercise-induced AHN. Therefore, we hypothesized that exercise with lactate intake could augment exercise-induced AHN. This study was conducted for 5 weeks with 7-week-old ICR male mice that performed mild-intensity exercise (just below lactate threshold, 55-60%VO2max) with or without oral administration of lactate 5 days/week. Cell proliferation, neuronal differentiation, neurogenesis-relevant factors, reference and retention memory, and spatial working memory were evaluated at the end of the experiment. The results showed that AHN was enhanced by lactate intake, but exercise-induced AHN was not augmented by exercise with lactate intake. Nevertheless, exercise-induced improvement in reference and retention memory was augmented by exercise with lactate intake. And spatial working memory was promoted by the co-treatment, also protein expression of hippocampal FNDC5, BDNF, PGC1α, and MCT2 were elevated by the co-treatment. Therefore, our findings suggest that lactate has a potential to be developed as a novel supplement that improves the positive effects of exercise on the hippocampus and its cognitive function.
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Project description:Exposure to exercise or to environmental enrichment increases the generation of new neurons in the adult hippocampus and promotes certain kinds of learning and memory. While the precise role of neurogenesis in cognition has been debated intensely, comparatively few studies have addressed the mechanisms linking environmental exposures to cellular and behavioral outcomes. Here we show that bone morphogenetic protein (BMP) signaling mediates the effects of exercise on neurogenesis and cognition in the adult hippocampus. Elective exercise reduces levels of hippocampal BMP signaling before and during its promotion of neurogenesis and learning. Transgenic mice with decreased BMP signaling or wild type mice infused with a BMP inhibitor both exhibit remarkable gains in hippocampal cognitive performance and neurogenesis, mirroring the effects of exercise. Conversely, transgenic mice with increased BMP signaling have diminished hippocampal neurogenesis and impaired cognition. Exercise exposure does not rescue these deficits, suggesting that reduced BMP signaling is required for environmental effects on neurogenesis and learning. Together, these observations show that BMP signaling is a fundamental mechanism linking environmental exposure with changes in cognitive function and cellular properties in the hippocampus.
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Project description:The genetic background of mice has various influences on the efficacy of physical exercise, as well as adult neurogenesis in the hippocampus. In this study, we investigated the basal level of hippocampal neurogenesis, as well as the effects of treadmill exercise on adult hippocampal neurogenesis in 9 mouse strains: 8 very commonly used laboratory inbred mouse strains (C57BL/6, BALB/c, A/J, C3H/HeJ, DBA/1, DBA/2, 129/SvJ, and FVB) and 1 outbred mouse strain (ICR). All 9 strains showed diverse basal levels of cell proliferation, neuroblast differentiation, and integration into granule cells in the sedentary group. C57BL/6 mice showed the highest levels of cell proliferation, neuroblast differentiation, and integration into granule cells at basal levels, and the DBA/2 mice showed the lowest levels. The efficacy of integration into granule cells was maximal in ICR mice. Treadmill exercise increased adult hippocampal neurogenesis in all 9 mouse strains. These results suggest that the genetic background of mice affects hippocampal neurogenesis and C57BL/6 mice are the most useful strain to assess basal levels of cell proliferation and neuroblast differentiation, but not maturation into granule cells. In addition, the DBA/2 strain is not suitable for studying hippocampal neurogenesis.
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Project description:Mild exercise (ME) with an intensity below the lactate threshold (LT) is sufficient to enhance hippocampal function, while intense exercise (IE) above the LT negates such benefits. However, the question as to why ME more effectively enhances hippocampal function than does IE remains to be clarified. Here, we investigated adult hippocampal neurogenesis (AHN) as a mechanism of ME-induced cognitive improvement, and comprehensively delineated the transcriptomic profile of the hippocampus, using a rat whole-genome microarray approach through comparison with IE. Immunohistochemical results showed that less intense exercise (ME) is better suited to improve AHN, especially in regards to the survival and maturation of newborn neurons. DNA microarray analysis revealed that ME regulated more genes than did IE (ME: 604 genes, IE: 415 genes), and only 44 genes were modified with both exercise intensities. The identified molecular components did not comprise well-known factors related to exercise-induced AHN, such as brain-derived neurotrophic factor (BDNF) and insulin-like growth factor 1 (IGF1), probably due to the timing of hippocampal tissue collection after the last training session and the technical feature of microarray. Rather, network analysis of the microarray data using Ingenuity Pathway Analysis algorithms revealed that the ME-influenced genes were principally related to lipid metabolism, protein synthesis and inflammatory response, which are recognized as associated with hippocampal neuroadaptations including AHN. In contrast, IE-influenced genes linked to immune response, a negative regulatory system of AHN and hippocampal function, were identified. Collectively, these results support our hypothesis that AHN could explain why ME enhances hippocampal function, and provide the ME-specific gene list that contain some potential regulators of this positive regulation. The list will become a foundation to elucidate the molecular pathway involving the ME-induced cognitive gain.
2014-04-05 | GSE45813 | GEO