Sex Differences in Neurophysiological Changes Following Voluntary Exercise in Adolescent Rats

Ferguson, Lindsay; Giza, Christopher C.; Serpa, Rebecka; Greco, Tiffany; Robert, Hannah; Folkerts, Michael; Prins, Mayumi L.

doi:10.3389/fneur.2021.685822

Cited by 7 publications

(3 citation statements)

References 76 publications

(111 reference statements)

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“…In exercise addiction, an individual develops an obsession with exercise causing features such as withdrawal symptoms and mood modification (Peluso & Guerra de Andrade, 2005;Weinstein et al, 2015). Although previous studies in rats have used different methods of reporting distance run or number of wheel revolutions over different time periods (Fan et al, 2022;Ferguson et al, 2020;Ferguson et al, 2021;Ishikawa et al, 2014;, the amount of exercise experienced by the rats in our study generally appears high by comparison. This may be a possible explanation for the increase in anxiety-and depressionlike behaviors seen in our exercise rats.…”

Section: Duration and Severity Of Exercisementioning

confidence: 68%

Chronic running‐wheel exercise from adolescence leads to increased anxiety and depression‐like phenotypes in adulthood in rats: Effects on stress markers and interaction with BDNF Val66Met genotype

Jaehne

Kent

Lam

et al. 2022

Developmental Psychobiology

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Exercise has been shown to be beneficial in reducing symptoms of affective disorders and to increase the expression of brain-derived neurotrophic factor (BDNF). The BDNF Val66Met polymorphism is associated with reduced activity-dependent BDNF release and increased risk for anxiety and depression. Male and female Val66Met rats were given access to running wheels from 3 weeks of age and compared to sedentary controls. Anxiety-and depression-like behaviors were measured in adulthood using the elevated plus maze (EPM), open field (OF), and forced swim test (FST). Expression of BDNF and a number of stress-related genes, the glucocorticoid receptor (Nr3c1), serum/glucocorticoid-regulated kinase 1 (Sgk1), and FK506 binding protein 51 (Fkbp5) in the hippocampus were also measured. Rats given access to running wheels developed high levels of voluntary exercise, decreased open-arm time on the EPM and center-field time in the OF, reduced overall exploratory activity in the open field, and increased immobility time in the FST with no differences between genotypes. Chronic exercise induced a significant increase in Bdnf mRNA and BDNF protein levels in the hippocampus with some of these effects being genotype specific. Exercise decreased the expression of Nr3c1 and Sgk1, but increased the expression of Fkbp5. These results suggest that chronic running-wheel exercise from adolescence increased anxiety and depression-like phenotypes in adulthood, independent of BDNF Val66Met genotype.Further studies are required to confirm that increased indices of anxiety-like behavior are independent from reduced overall locomotor activity.

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Section: Duration and Severity Of Exercisementioning

confidence: 68%

Chronic running‐wheel exercise from adolescence leads to increased anxiety and depression‐like phenotypes in adulthood in rats: Effects on stress markers and interaction with BDNF Val66Met genotype

Jaehne

Kent

Lam

et al. 2022

Developmental Psychobiology

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“…The expression and activity of some myokines appear to be different among sexes. As an example, the brain-derived neurotrophic factor (BDNF), a muscle-generated myokine that controls metabolic reprograming upon fasting in a similar manner as physical exercise, displays sexual dimorphism [67,68]. In addition, the effects of interleukin 6 (IL-6) and myostatin, whose expressions are influenced by fasting, are fiber type-dependent and sex-dependent [69]; IL-6 plays different roles in muscle metabolism in female and male mice [70], and the effects of myostatin on muscle tissue are dose-, sex-, and muscle typedependent [71].…”

Section: Sex Differences In Muscle Homeostasis and Metabolismmentioning

confidence: 99%

Sex Differences in Inflammation and Muscle Wasting in Aging and Disease

Peruta

Lozanoska-Ochser

Renzini

et al. 2023

IJMS

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Only in recent years, thanks to a precision medicine-based approach, have treatments tailored to the sex of each patient emerged in clinical trials. In this regard, both striated muscle tissues present significant differences between the two sexes, which may have important consequences for diagnosis and therapy in aging and chronic illness. In fact, preservation of muscle mass in disease conditions correlates with survival; however, sex should be considered when protocols for the maintenance of muscle mass are designed. One obvious difference is that men have more muscle than women. Moreover, the two sexes differ in inflammation parameters, particularly in response to infection and disease. Therefore, unsurprisingly, men and women respond differently to therapies. In this review, we present an up-to-date overview on what is known about sex differences in skeletal muscle physiology and disfunction, such as disuse atrophy, age-related sarcopenia, and cachexia. In addition, we summarize sex differences in inflammation which may underly the aforementioned conditions because pro-inflammatory cytokines deeply affect muscle homeostasis. The comparison of these three conditions and their sex-related bases is interesting because different forms of muscle atrophy share common mechanisms; for instance, those responsible for protein dismantling are similar although differing in terms of kinetics, severity, and regulatory mechanisms. In pre-clinical research, exploring sexual dimorphism in disease conditions could highlight new efficacious treatments or recommend implementation of an existing one. Any protective factors discovered in one sex could be exploited to achieve lower morbidity, reduce the severity of the disease, or avoid mortality in the opposite sex. Thus, the understanding of sex-dependent responses to different forms of muscle atrophy and inflammation is of pivotal importance to design innovative, tailored, and efficient interventions.

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“…The female mice used in the present rotarod learning study were excluded if they were in the proestrous/estrous (P/E) stage of the ovarian cycle. This would result in estrous stages (diestrus, metestrus) that are associated with similar levels of locomotor activity (assessed by the running wheel) compared to males (Ferguson et al, 2021 ).…”

Section: Discussionmentioning

confidence: 99%

Sex differences in motor learning flexibility are accompanied by sex differences in mushroom spine pruning of the mouse primary motor cortex during adolescence

Tekin,

Shen,

Smith

2024

Front. Neurosci.

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BackgroundAlthough males excel at motor tasks requiring strength, females exhibit greater motor learning flexibility. Cognitive flexibility is associated with low baseline mushroom spine densities achieved by pruning which can be triggered by α4βδ GABAA receptors (GABARs); defective synaptic pruning impairs this process.MethodsWe investigated sex differences in adolescent pruning of mushroom spine pruning of layer 5 pyramidal cells of primary motor cortex (L5M1), a site essential for motor learning, using microscopic evaluation of Golgi stained sections. We assessed α4GABAR expression using immunohistochemical and electrophysiological techniques (whole cell patch clamp responses to 100 nM gaboxadol, selective for α4βδ GABARs). We then compared performance of groups with different post-pubertal mushroom spine densities on motor learning (constant speed) and learning flexibility (accelerating speed following constant speed) rotarod tasks.ResultsMushroom spines in proximal L5M1 of female mice decreased >60% from PND35 (puberty onset) to PND56 (Pubertal: 2.23 ± 0.21 spines/10 μm; post-pubertal: 0.81 ± 0.14 spines/10 μm, P < 0.001); male mushroom spine density was unchanged. This was due to greater α4βδ GABAR expression in the female (P < 0.0001) because α4 -/- mice did not exhibit mushroom spine pruning. Although motor learning was similar for all groups, only female wild-type mice (low mushroom spine density) learned the accelerating rotarod task after the constant speed task (P = 0.006), a measure of motor learning flexibility.ConclusionsThese results suggest that optimal motor learning flexibility of female mice is associated with low baseline levels of post-pubertal mushroom spine density in L5M1 compared to male and female α4 -/- mice.

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Sex Differences in Neurophysiological Changes Following Voluntary Exercise in Adolescent Rats

Cited by 7 publications

References 76 publications

Chronic running‐wheel exercise from adolescence leads to increased anxiety and depression‐like phenotypes in adulthood in rats: Effects on stress markers and interaction with BDNF Val66Met genotype

Chronic running‐wheel exercise from adolescence leads to increased anxiety and depression‐like phenotypes in adulthood in rats: Effects on stress markers and interaction with BDNF Val66Met genotype

Sex Differences in Inflammation and Muscle Wasting in Aging and Disease

Sex differences in motor learning flexibility are accompanied by sex differences in mushroom spine pruning of the mouse primary motor cortex during adolescence

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