Circulating testosterone and dehydroepiandrosterone are associated with individual motor unit features in untrained and highly active older men

Yuxiao Guo,Yuxiao Guo,Agnieszka Swiecicka,Agnieszka Swiecicka,Mathew Piasecki,Jessica Piasecki,Daniel Stashuk,Martin K Rutter,Martin K Rutter,Martin K Rutter,Philip J Atherton,Philip J Atherton,Alex Ireland,Jamie S Mcphee,Bethan E Phillips

doi:10.1007/s11357-021-00482-3

Abstract

Long-term exercise training has been considered as an effective strategy to counteract age-related hormonal declines and minimise muscle atrophy. However, human data relating circulating hormone levels with motor nerve function are scant. The aims of the study were to explore associations between circulating sex hormone levels and motor unit (MU) characteristics in older men, including masters athletes competing in endurance and power events. Forty-three older men (mean ± SD age: 69.9 ± 4.6 years) were studied based on competitive status. The serum concentrations of dehydroepiandrosterone (DHEA), total testosterone (T) and estradiol were quantified using liquid chromatography mass spectrometry. Intramuscular electromyographic signals were recorded from vastus lateralis (VL) during 25% of maximum voluntary isometric contractions and processed to extract MU firing rate (FR), and motor unit potential (MUP) features. After adjusting for athletic status, MU FR was positively associated with DHEA levels (p = 0.019). Higher testosterone and estradiol were associated with lower MUP complexity; these relationships remained significant after adjusting for athletic status (p = 0.006 and p = 0.019, respectively). Circulating DHEA was positively associated with MU firing rate in these older men. Higher testosterone levels were associated with reduced MUP complexity, indicating reduced electrophysiological temporal dispersion, which is related to decreased differences in conduction times along axonal branches and/or MU fibres. Although evident in males only, this work highlights the potential of hormone administration as a therapeutic interventional strategy specifically targeting human motor units in older age.

Highlights

Ageing of the neuromuscular system is a complex process encompassing numerous pathophysiological conditions which is further compounded by sedentary behaviour [1]
Some aspects of muscle strength may be maintained in masters athletes when compared to age-matched controls [6], this finding is equivocal [7] and progressive muscle atrophy demonstrates that lifelong exercise does not completely offset the muscle mass and strength decline caused by ageing [8]
Previous studies of older females reported a greater improvement in muscle strength and power in those receiving estrogen hormone therapy [85, 86], and here we report a similar association in older men

Summary

Introduction

Ageing of the neuromuscular system is a complex process encompassing numerous pathophysiological conditions which is further compounded by sedentary behaviour [1]. The failure to maintain regular physical exercise while advancing in age induces weakness of the extremities [2] and increases the probability of developing chronic disease [3] and associated co-morbidities [4]. Masters athletes provide a useful model to examine the effects of inherent ageing disassociated from negative factors such as physical inactivity [5]. Some aspects of muscle strength may be maintained in masters athletes when compared to age-matched controls [6], this finding is equivocal [7] and progressive muscle atrophy demonstrates that lifelong exercise does not completely offset the muscle mass and strength decline caused by ageing [8]. A range of additional factors are involved, such as. Rutter Diabetes, Endocrinology and Metabolism Centre, Manchester University NHS Foundation Trust, Manchester Academic Health Science Centre, Manchester, UK

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