Sex differences in aerobic exercise efficacy to improve cognition: A systematic review and meta-analysis of studies in older rodents

Barha, Cindy K.; Falck, Ryan S.; Davis, Jennifer C.; Nagamatsu, Lindsay S.; Liu-Ambrose, Teresa

doi:10.1016/j.yfrne.2017.06.001

Cited by 63 publications

(61 citation statements)

References 103 publications

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“…It has been suggested that for rodents activity and cognition function decline in parallel (Shoji et al, 2016;Logan et al, 2018). Moreover, female rodents are more active than males (Stowie and Glass, 2015;Rosenfeld, 2017) and cognition may be differentially influenced by exercise (Barha et al, 2017). We confirmed heightened activity of females as increased wheel running during a 24 h period.…”

Section: Discussionsupporting

confidence: 73%

Longitudinal Characterization and Biomarkers of Age and Sex Differences in the Decline of Spatial Memory

Febo

Rani

Yegla

et al. 2020

Front. Aging Neurosci.

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The current longitudinal study examined factors (sex, physical function, response to novelty, ability to adapt to a shift in light/dark cycle, brain connectivity), which might predict the emergence of impaired memory during aging. Male and female Fisher 344 rats were tested at 6, 12, and 18 months of age. Impaired spatial memory developed in middle-age (12 months), particularly in males, and the propensity for impairment increased with advanced age. A reduced response to novelty was observed over the course of aging, which is inconsistent with cross-sectional studies. This divergence likely resulted from differences in the history of environmental enrichment/impoverishment for cross-sectional and longitudinal studies. Animals that exhibited lower level exploration of the inner region on the open field test exhibited better memory at 12 months. Furthermore, males that exhibited a longer latency to enter a novel environment at 6 months, exhibited better memory at 12 months. For females, memory at 12 months was correlated with the ability to behaviorally adapt to a shift in light/dark cycle. Functional magnetic resonance imaging of the brain, conducted at 12 months, indicated that the decline in memory was associated with altered functional connectivity within different memory systems, most notably between the hippocampus and multiple regions such as the retrosplenial cortex, thalamus, striatum, and amygdala. Overall, some factors, specifically response to novelty at an early age and the capacity to adapt to shifts in light cycle, predicted spatial memory in middle-age, and spatial memory is associated with corresponding changes in brain connectivity. We discuss similarities and differences related to previous longitudinal and cross-sectional studies, as well as the role of sex differences in providing a theoretical framework to guide future longitudinal research on the trajectory of cognitive decline. In addition to demonstrating the power of longitudinal studies, these data highlight the importance of middle-age for identifying potential predictive indicators of sexual dimorphism in the trajectory in brain and cognitive aging.

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Section: Discussionsupporting

confidence: 73%

Longitudinal Characterization and Biomarkers of Age and Sex Differences in the Decline of Spatial Memory

Febo

Rani

Yegla

et al. 2020

Front. Aging Neurosci.

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“…Biological sex is recognized as an important variable to consider in exercise efficacy on brain health. [31][32][33][34] We focus our review mainly on randomized controlled trials (RCTs), as self-reported leisure time physical activity levels are different in males vs females. Several studies have found that males report higher levels of total physical activity and higher moderate-and vigorous-intensity physical activity [35][36][37] ; though amount of walking was shown to be similar between males and females.…”

Section: Introductionmentioning

confidence: 99%

Sex differences in exercise efficacy: Is midlife a critical window for promoting healthy cognitive aging?

Barha

Liu‐Ambrose

2020

FASEB j.

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Dementia is one of the most pressing health care issues of this century. As no curative treatment for dementia exists, research efforts are growing to identify effective lifestyle interventions to prevent or delay onset. One such promising strategy that promotes cognitive and brain health is engaging in physical exercise. However, current exercise recommendations are imprecise. To advance the potential of exercise as a preventative and treatment strategy, important questions regarding moderators (ie, biological sex and age) are being addressed in the literature. Biological sex is recognized as an important variable to consider in exercise efficacy on brain health, with females showing greater cognitive gains. This may be related to sex differences in underlying mechanisms. Here, we argue to better understand the sex differences in exercise efficacy, the timing of exercise intervention should also be considered. Specifically, we present the hypothesis that midlife in females is a critical window for the implementation of exercise as an early intervention to promote brain health and prevent dementia. Further, we speculate that exercise interventions targeting midlife will be of critical importance for the female brain, as females exit this period of the lifespan at greater risk for cognitive impairment. Given the potential sex differences in dementia risk and prevalence, it is imperative to assess potential sex differences in exercise efficacy as an early intervention during midlife.

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“…Translation of biomarkers and behavioral measures to human subjects therefore needs to consider the influence of the light-dark cycle on these parameters, as even artificial lighting can affect performance and growth factors in humans 34 . Biological sex also influences the response to AE 35 , with male subjects exhibiting larger effects 35 .…”

Section: Introductionmentioning

confidence: 99%

Biological effects of dosing aerobic exercise and neuromuscular electrical stimulation in rats

Dalise

Cavalli

Ghuman

et al. 2017

Sci Rep

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Aerobic exercise (AE) and non-aerobic neuromuscular electric stimulation (NMES) are common interventions used in physical therapy. We explored the dose-dependency (low, medium, high) of these interventions on biochemical factors, such as brain derived neurotrophic growth factor (BDNF), vascular endothelial growth factor-A (VEGF-A), insulin-like growth factor-1 (IGF-1) and Klotho, in the blood and brain of normal rats, as well as a treadmill-based maximum capacity test (MCT). A medium dose of AE produced the most improvement in MCT with dose-dependent changes in Klotho in the blood. A dose-dependent increase of BDNF was evident following completion of an NMES protocol, but there was no improvement in MCT performance. Gene expression in the hippocampus was increased after both AE and NMES, with IGF-1 being a signaling molecule that correlated with MCT performance in the AE conditions, but also highly correlated with VEGF-A and Klotho. Blood Klotho levels can serve as a biomarker of therapeutic dosing of AE, whereas IGF-1 is a key molecule coupled to gene expression of other molecules in the hippocampus. This approach provides a translatable paradigm to investigate the mode and mechanism of action of interventions employed in physical therapy that can improve our understanding of how these factors change under pathological conditions.

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Sex differences in aerobic exercise efficacy to improve cognition: A systematic review and meta-analysis of studies in older rodents

Cited by 63 publications

References 103 publications

Longitudinal Characterization and Biomarkers of Age and Sex Differences in the Decline of Spatial Memory

Longitudinal Characterization and Biomarkers of Age and Sex Differences in the Decline of Spatial Memory

Sex differences in exercise efficacy: Is midlife a critical window for promoting healthy cognitive aging?

Biological effects of dosing aerobic exercise and neuromuscular electrical stimulation in rats

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