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      Motor unit number estimates and neuromuscular transmission in the tibialis anterior of master athletes: evidence that athletic older people are not spared from age‐related motor unit remodeling

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          Abstract

          Muscle motor unit numbers decrease markedly in old age, while remaining motor units are enlarged and can have reduced neuromuscular junction transmission stability. However, it is possible that regular intense physical activity throughout life can attenuate this remodeling. The aim of this study was to compare the number, size, and neuromuscular junction transmission stability of tibialis anterior ( TA) motor units in healthy young and older men with those of exceptionally active master runners. The distribution of motor unit potential ( MUP) size was determined from intramuscular electromyographic signals recorded in healthy male Young (mean ±  SD, 26 ± 5 years), Old (71 ± 4 years) and Master Athletes (69 ± 3 years). Relative differences between groups in numbers of motor units was assessed using two methods, one comparing MUP size and muscle cross‐sectional area ( CSA) determined with MRI, the other comparing surface recorded MUPs with maximal compound muscle action potentials and commonly known as a “motor unit number estimate ( MUNE)”. Near fiber ( NF) jiggle was measured to assess neuromuscular junction transmission stability. TA CSA did not differ between groups. MUNE values for the Old and Master Athletes were 45% and 40%, respectively, of the Young. Intramuscular MUPs of Old and Master Athletes were 43% and 56% larger than Young. NF jiggle was slightly higher in the Master Athletes, with no difference between Young and Old. These results show substantial and similar motor unit loss and remodeling in Master Athletes and Old individuals compared with Young, which suggests that lifelong training does not attenuate the age‐related loss of motor units.

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          Most cited references27

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          Excitability and inhibitability of motoneurons of different sizes.

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            Age-related decline in rate of torque development is accompanied by lower maximal motor unit discharge frequency during fast contractions.

            The aim of this study was to investigate the association between the rate of torque development and maximal motor unit discharge frequency in young and elderly adults as they performed rapid submaximal contractions with the ankle dorsiflexors. Recordings were obtained of the torque exerted by the dorsiflexors during the isometric contractions and the surface and intramuscular electromyograms (EMGs) from the tibialis anterior. The maximal rate of torque development and integrated EMG (percentage of total EMG burst) at peak rate of torque development during fast contractions were lower in elderly than young adults by 48% (P < 0.05) and 16.5% (P < 0.05), respectively. The young adults, but not the elderly adults, exhibited a positive association (r2 = 0.33; P < 0.01) between the integrated EMG computed up to the peak rate of torque development and the maximal rate of torque development achieved during the fast contractions. These age-related changes during fast voluntary contractions were accompanied by a decline (P < 0.001) in motor unit discharge frequency (19, 28, and 34% for first 3 interspike intervals, respectively) and in the percentage of units (45%; P < 0.05) that exhibited double discharges (doublets) at brief intervals (<5 ms). Because aging decreased the maximal rate of torque development of fast voluntary contractions to a greater extent ( approximately 10%) than that of an electrically evoked twitch, collectively the results indicate that the age-related decline in maximal motor unit discharge frequency likely limit, in addition to the slowing of muscle contractile properties, the performance of fast voluntary contractions.
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              Motor unit number estimates in the tibialis anterior muscle of young, old, and very old men.

              The rate of motor unit (MU) loss and its influence on the progression of sarcopenia is not well understood. Therefore, the main purpose of this study was to estimate and compare numbers of MUs in the tibialis anterior (TA) of young men ( approximately 25 years) and two groups of older men ( approximately 65 years and >/=80 years). Decomposition-enhanced spike-triggered averaging was used to collect surface and intramuscular electromyographic signals during isometric dorsiflexions at 25% of maximum voluntary contraction. The mean surface-MU potential size was divided into the maximum M wave to calculate the motor unit number estimate (MUNE). The MUNE was significantly reduced in the old (91) compared to young (150) men, and further reduced in the very old men (59). Despite the smaller MUNE at age 65, strength was not reduced until beyond 80 years. This suggests that age-related MU loss in the TA does not limit function until a critical threshold is reached.
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                Author and article information

                Contributors
                j.s.mcphee@mmu.ac.uk
                Journal
                Physiol Rep
                Physiol Rep
                10.1002/(ISSN)2051-817X
                PHY2
                physreports
                Physiological Reports
                John Wiley and Sons Inc. (Hoboken )
                2051-817X
                30 September 2016
                October 2016
                : 4
                : 19 ( doiID: 10.1111/phy2.2016.4.issue-19 )
                : e12987
                Affiliations
                [ 1 ] School of Healthcare ScienceManchester Metropolitan University ManchesterUK
                [ 2 ] Department of Systems Design EngineeringUniversity of Waterloo Waterloo OntarioCanada
                [ 3 ] Mathematics and Computer ScienceMount Allison University Sackville New BrunswickCanada
                [ 4 ] Andrology Research Unit Cardiovascular, Metabolic and Nutritional Sciences Domain Faculty of Biology, Medicine and HealthUniversity of Manchester ManchesterUK
                [ 5 ] Manchester Diabetes Centre Central Manchester University Hospitals NHS Foundation TrustManchester Academic Health Science Centre ManchesterUK
                Author notes
                [*] [* ] Correspondence

                Jamie S. McPhee, School of Healthcare Science, Manchester Metropolitan University, Manchester M15GD, UK.

                Tel: +44 161 2475675

                Fax: +44 161 2472000

                E‐mail: j.s.mcphee@ 123456mmu.ac.uk

                Article
                PHY212987
                10.14814/phy2.12987
                5064139
                27694526
                2d2b9a84-f60d-4048-b8a8-1b8ffb330648
                © 2016 The Authors. Physiological Reports published by Wiley Periodicals, Inc. on behalf of the American Physiological Society and The Physiological Society.

                This is an open access article under the terms of the Creative Commons Attribution License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited.

                History
                : 17 July 2016
                : 01 September 2016
                : 06 September 2016
                Page count
                Figures: 5, Tables: 2, Pages: 11, Words: 6811
                Funding
                Funded by: UK Medical Research Council
                Award ID: MR/K025252/1
                Categories
                Ageing and Degeneration
                Motor Control
                Neuromuscular Junction
                Skeletal Muscle
                Endurance and Performance
                Original Research
                Original Research
                Custom metadata
                2.0
                phy212987
                October 2016
                Converter:WILEY_ML3GV2_TO_NLMPMC version:4.9.4 mode:remove_FC converted:14.10.2016

                aging,electromyography,master athletes,motor unit,skeletal muscle

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