Subscribe to RSS
DOI: 10.1055/a-1265-7073
Age Related Changes in Motor Function (II). Decline in Motor Performance Outcomes
![](https://www.thieme-connect.de/media/sportsmed/202103/lookinside/thumbnails/8250_10-1055-a-1265-7073-1.jpg)
Abstract
Age-related impairments in motor performance are caused by a deterioration in mechanical and neuromuscular functions, which have been investigated from the macro-level of muscle-tendon unit to the micro-level of the single muscle fiber. When compared to the healthy young skeletal muscle, aged skeletal muscle is: (1) weaker, slower and less powerful during the performance of voluntary contractions; (2) less steady during the performance of isometric contractions, particularly at low levels of force; and (3) less susceptible to fatigue during the performance of sustained isometric contractions, but more susceptible to fatigue during the performance of high-velocity dynamic contractions. These impairments have been discussed to be mainly the result of: a) loss of muscle mass and selective atrophy of type II muscle fibers; b) altered tendon mechanical properties (decreased tendon stiffness); c) reduced number and altered function of motor units; d) slower muscle fiber shortening velocity; e) increased oscillation in common synaptic input to motor neurons; and f) altered properties and activity of sarcoplasmic reticulum. In this second part of a two-part review we have detailed the age-related impairments in motor performance with a reference to the most important mechanical and neuromuscular contributing factors.
Publication History
Received: 21 April 2020
Accepted: 08 September 2020
Article published online:
02 November 2020
© 2020. Thieme. All rights reserved.
Georg Thieme Verlag KG
Rüdigerstraße 14, 70469 Stuttgart, Germany
-
References
- 1 Wu R, De Vito G, Delahunt E. et al. Age-related changes in motor function (I). Mechanical and neuromuscular factors. Int J Sports Med 2020; 41: 709-719 DOI: 10.1055/a-1144-3408.
- 2 Larsson L, Grimby G, Karlsson J. Muscle strength and speed of movement in relation to age and muscle morphology. J Appl Physiol Respir Environ Exerc Physiol 1979; 46: 451-456
- 3 Narici MV, Bordini M, Cerretelli P. Effect of aging on human adductor pollicis muscle function. J Appl Physiol (1985) 1991; 71: 1277-1281
- 4 Vandervoort AA, McComas AJ. Contractile changes in opposing muscles of the human ankle joint with aging. J Appl Physiol (1985) 1986; 61: 361-367
- 5 Lindle RS, Metter EJ, Lynch NA. et al. Age and gender comparisons of muscle strength in 654 women and men aged 20-93 yr. J Appl Physiol (1985) 1997; 83: 1581-1587
- 6 Macaluso A, De Vito G. Muscle strength, power and adaptations to resistance training in older people. Eur J Appl Physiol 2004; 91: 450-472
- 7 Ditroilo M, Forte R, Benelli P. et al. Effects of age and limb dominance on upper and lower limb muscle function in healthy males and females aged 40-80 years. J Sports Sci 2010; 28: 667-677
- 8 Frontera WR, Hughes VA, Lutz KJ. et al. A cross-sectional study of muscle strength and mass in 45- to 78-yr-old men and women. J Appl Physiol (1985) 1991; 71: 644-650
- 9 Frontera WR, Hughes VA, Fielding RA. et al. Aging of skeletal muscle: A 12-yr longitudinal study. J Appl Physiol (1985) 2000; 88: 1321-1326
- 10 Hunter SK, Thompson MW, Adams RD. Relationships among age-associated strength changes and physical activity level, limb dominance, and muscle group in women. J Gerontol A Biol Sci Med Sci 2000; 55: B264-B273
- 11 Vandervoort AA, Kramer JF, Wharram ER. Eccentric knee strength of elderly females. J Gerontol 1990; 45: B125-B128
- 12 Hortobagyi T, Zheng D, Weidner M. et al. The influence of aging on muscle strength and muscle fiber characteristics with special reference to eccentric strength. J Gerontol A Biol Sci Med Sci 1995; 50: B399-B406
- 13 Porter MM, Myint A, Kramer JF. et al. Concentric and eccentric knee extension strength in older and younger men and women. Can J Appl Physiol 1995; 20: 429-439
- 14 Dalton BH, Power GA, Vandervoort AA. et al. The age-related slowing of voluntary shortening velocity exacerbates power loss during repeated fast knee extensions. Exp Gerontol 2012; 47: 85-92
- 15 Lanza IR, Towse TF, Caldwell GE. et al. Effects of age on human muscle torque, velocity, and power in two muscle groups. J Appl Physiol (1985) 2003; 95: 2361-2369
- 16 McPhee JS, Cameron J, Maden-Wilkinson T. et al. The contributions of fiber atrophy, fiber loss, in situ specific force, and voluntary activation to weakness in sarcopenia. J Gerontol A Biol Sci Med Sci 2018; 73: 1287-1294
- 17 Hepple RT, Rice CL. Innervation and neuromuscular control in ageing skeletal muscle. J Physiol 2016; 594: 1965-1978
- 18 Lexell J. Human aging, muscle mass, and fiber type composition. J Gerontol A Biol Sci Med Sci 1995; 50 Spec no 11-6
- 19 Raj IS, Bird SR, Shield AJ. Aging and the force-velocity relationship of muscles. Exp Gerontol 2010; 45: 81-90
- 20 D'Antona G, Pellegrino MA, Adami R. et al. The effect of ageing and immobilization on structure and function of human skeletal muscle fibres. J Physiol 2003; 552: 499-511
- 21 Connelly DM, Rice CL, Roos MR. et al. Motor unit firing rates and contractile properties in tibialis anterior of young and old men. J Appl Physiol (1985) 1999; 87: 843-852
- 22 Hughes VA, Frontera WR, Wood M. et al. Longitudinal muscle strength changes in older adults: influence of muscle mass, physical activity, and health. J Gerontol A Biol Sci Med Sci 2001; 56: B209-B217
- 23 Aniansson A, Hedberg M, Henning GB. et al. Muscle morphology, enzymatic activity, and muscle strength in elderly men: A follow-up study. Muscle Nerve 1986; 9: 585-591
- 24 Delmonico MJ, Harris TB, Visser M. et al. Longitudinal study of muscle strength, quality, and adipose tissue infiltration. Am J Clin Nutr 2009; 90: 1579-1585
- 25 Vandervoort AA. Aging of the human neuromuscular system. Muscle Nerve 2002; 25: 17-25
- 26 Frontera WR, Suh D, Krivickas LS. et al. Skeletal muscle fiber quality in older men and women. Am J Physiol Cell Physiol 2000; 279: C611-C618
- 27 Stackhouse SK, Stevens JE, Lee SC. et al. Maximum voluntary activation in nonfatigued and fatigued muscle of young and elderly individuals. Phys Ther 2001; 81: 1102-1109
- 28 Yue GH, Ranganathan VK, Siemionow V. et al. Older adults exhibit a reduced ability to fully activate their biceps brachii muscle. J Gerontol A Biol Sci Med Sci 1999; 54: M249-M253
- 29 Klein CS, Rice CL, Marsh GD. Normalized force, activation, and coactivation in the arm muscles of young and old men. J Appl Physiol (1985) 2001; 91: 1341-1349
- 30 Morse CI, Thom JM, Davis MG. et al. Reduced plantarflexor specific torque in the elderly is associated with a lower activation capacity. Eur J Appl Physiol 2004; 92: 219-226
- 31 McNeil CJ, Vandervoort AA, Rice CL. Peripheral impairments cause a progressive age-related loss of strength and velocity-dependent power in the dorsiflexors. J Appl Physiol (1985) 2007; 102: 1962-1968
- 32 Wu R, Delahunt E, Ditroilo M. et al. Effects of age and sex on neuromuscular-mechanical determinants of muscle strength. Age (Dordr) 2016; 38: 57
- 33 Strasser EM, Draskovits T, Praschak M. et al. Association between ultrasound measurements of muscle thickness, pennation angle, echogenicity and skeletal muscle strength in the elderly. Age (Dordr) 2013; 35: 2377-2388
- 34 Powell PL, Roy RR, Kanim P. et al. Predictability of skeletal muscle tension from architectural determinations in guinea pig hindlimbs. J Appl Physiol Respir Environ Exerc Physiol 1984; 57: 1715-1721
- 35 Narici M. Human skeletal muscle architecture studied in vivo by non-invasive imaging techniques: functional significance and applications. J Electromyogr Kinesiol 1999; 9: 97-103
- 36 Hooper AC. Length, diameter and number of ageing skeletal muscle fibres. Gerontology 1981; 27: 121-126
- 37 Lieber RL, Friden J. Functional and clinical significance of skeletal muscle architecture. Muscle Nerve 2000; 23: 1647-1666
- 38 Thom JM, Morse CI, Birch KM. et al. Influence of muscle architecture on the torque and power-velocity characteristics of young and elderly men. Eur J Appl Physiol 2007; 100: 613-619
- 39 Macaluso A, De Vito G. Comparison between young and older women in explosive power output and its determinants during a single leg-press action after optimisation of load. Eur J Appl Physiol 2003; 90: 458-463
- 40 Allison SJ, Brooke-Wavell K, Folland JP. Multiple joint muscle function with ageing: the force-velocity and power-velocity relationships in young and older men. Aging Clin Exp Res 2013; 25: 159-166
- 41 Suzuki T, Bean JF, Fielding RA. Muscle power of the ankle flexors predicts functional performance in community-dwelling older women. J Am Geriatr Soc 2001; 49: 1161-1167
- 42 Bean JF, Kiely DK, Herman S. et al. The relationship between leg power and physical performance in mobility-limited older people. J Am Geriatr Soc 2002; 50: 461-467
- 43 Bean JF, Leveille SG, Kiely DK. et al. A comparison of leg power and leg strength within the InCHIANTI study: Which influences mobility more?. J Gerontol A Biol Sci Med Sci 2003; 58: 728-733
- 44 Reid KF, Fielding RA. Skeletal muscle power: A critical determinant of physical functioning in older adults. Exerc Sport Sci Rev 2012; 40: 4-12
- 45 Izquierdo M, Ibanez J, Gorostiaga E. et al. Maximal strength and power characteristics in isometric and dynamic actions of the upper and lower extremities in middle-aged and older men. Acta Physiol Scand 1999; 167: 57-68
- 46 Thomas M, Fiatarone MA, Fielding RA. Leg power in young women: Relationship to body composition, strength, and function. Med Sci Sports Exerc 1996; 28: 1321-1326
- 47 Wakeling JM, Blake OM, Wong I. et al. Movement mechanics as a determinate of muscle structure, recruitment and coordination. Philos Trans R Soc Lond B Biol Sci 2011; 366: 1554-1564
- 48 Randhawa A, Wakeling JM. Associations between muscle structure and contractile performance in seniors. Clin Biomech (Bristol, Avon) 2013; 28: 705-711
- 49 Dalton BH, Power GA, Vandervoort AA. et al. Power loss is greater in old men than young men during fast plantar flexion contractions. J Appl Physiol (1985) 2010; 109: 1441-1447
- 50 Callahan DM, Kent-Braun JA. Effect of old age on human skeletal muscle force-velocity and fatigue properties. J Appl Physiol (1985) 2011; 111: 1345-1352
- 51 Hunter SK, Thompson MW, Ruell PA. et al. Human skeletal sarcoplasmic reticulum Ca2+ uptake and muscle function with aging and strength training. J Appl Physiol (1985) 1999; 86: 1858-1865
- 52 Moreno RJ, Messi ML, Zheng Z. et al. Role of sustained overexpression of central nervous system IGF-I in the age-dependent decline of mouse excitation-contraction coupling. J Membr Biol 2006; 212: 147-161
- 53 Tieland M, Trouwborst I, Clark BC. Skeletal muscle performance and ageing. J Cachexia Sarcopenia Muscle 2018; 9: 3-19
- 54 Heilmann C, Pette D. Molecular transformations in sarcoplasmic reticulum of fast-twitch muscle by electro-stimulation. Eur J Biochem 1979; 93: 437-446
- 55 Aagaard P, Simonsen EB, Andersen JL. et al. Increased rate of force development and neural drive of human skeletal muscle following resistance training. J Appl Physiol (1985) 2002; 93: 1318-1326
- 56 de Ruiter CJ, Kooistra RD, Paalman MI. et al. Initial phase of maximal voluntary and electrically stimulated knee extension torque development at different knee angles. J Appl Physiol (1985) 2004; 97: 1693-1701
- 57 Thompson BJ, Ryan ED, Sobolewski EJ. et al. Age related differences in maximal and rapid torque characteristics of the leg extensors and flexors in young, middle-aged and old men. Exp Gerontol 2013; 48: 277-282
- 58 Klass M, Baudry S, Duchateau J. Age-related decline in rate of torque development is accompanied by lower maximal motor unit discharge frequency during fast contractions. J Appl Physiol (1985) 2008; 104: 739-746
- 59 Thompson BJ, Ryan ED, Herda TJ. et al. Age-related changes in the rate of muscle activation and rapid force characteristics. Age (Dordr) 2014; 36: 839-849
- 60 Quinlan JI, Maganaris CN, Franchi MV. et al. Muscle and tendon contributions to reduced rate of torque development in healthy older males. J Gerontol A Biol Sci Med Sci 2018; 73: 539-545
- 61 Reeves ND, Maganaris CN, Narici MV. Effect of strength training on human patella tendon mechanical properties of older individuals.. J Physiol 2003; 548: 971-981
- 62 Maganaris CN, Narici MV, Reeves ND. In vivo human tendon mechanical properties: effect of resistance training in old age. J Musculoskelet Neuronal Interact 2004; 4: 204-208
- 63 Reeves ND, Narici MV, Maganaris CN. Strength training alters the viscoelastic properties of tendons in elderly humans. Muscle Nerve 2003; 28: 74-81
- 64 De Serres SJ, Enoka RM. Older adults can maximally activate the biceps brachii muscle by voluntary command. J Appl Physiol (1985) 1998; 84: 284-291
- 65 Stevens JE, Stackhouse SK, Binder-Macleod SA. et al. Are voluntary muscle activation deficits in older adults meaningful?. Muscle Nerve 2003; 27: 99-101
- 66 Kent-Braun JA, Ng AV. Specific strength and voluntary muscle activation in young and elderly women and men. J Appl Physiol (1985) 1999; 87: 22-29
- 67 Scaglioni G, Narici MV, Martin A. Neural activation during submaximal contractions seems more reflective of neuromuscular ageing than maximal voluntary activation. Front Aging Neurosci 2016; 8: 19
- 68 Gilmore KJ, Kirk EA, Doherty TJ. et al. Effect of very old age on anconeus motor unit loss and compensatory remodelling. Muscle Nerve 2018; 57: 659-663
- 69 Jakobi JM, Rice CL. Voluntary muscle activation varies with age and muscle group J Appl Physiol (1985) 2002; 93: 457-462
- 70 Hunter SK, Todd G, Butler JE. et al. Recovery from supraspinal fatigue is slowed in old adults after fatiguing maximal isometric contractions. J Appl Physiol (1985) 2008; 105: 1199-1209
- 71 Macaluso A, Nimmo MA, Foster JE. et al. Contractile muscle volume and agonist-antagonist coactivation account for differences in torque between young and older women. Muscle Nerve 2002; 25: 858-863
- 72 Häkkinen K, Kraemer WJ, Newton RU. et al. Changes in electromyographic activity, muscle fibre and force production characteristics during heavy resistance/power strength training in middle-aged and older men and women. Acta Physiol Scand 2001; 171: 51-62
- 73 Pearson SJ, Young A, Macaluso A. et al. Muscle function in elite master weightlifters. Med Sci Sports Exerc 2002; 34: 1199-206
- 74 Clark DJ, Patten C, Reid KF. et al. Impaired voluntary neuromuscular activation limits muscle power in mobility-limited older adults. J Gerontol A Biol Sci Med Sci 2010; 65: 495-502
- 75 Esposito F, Malgrati D, Veicsteinas A. et al. Time and frequency domain analysis of electromyogram and sound myogram in the elderly. Eur J Appl Physiol Occup Physiol 1996; 73: 503-510
- 76 Merletti R, Farina D, Gazzoni M. et al. Effect of age on muscle functions investigated with surface electromyography. Muscle Nerve 2002; 25: 65-76
- 77 Del Vecchio A, Negro F, Felici F. et al. Associations between motor unit action potential parameters and surface EMG features. J Appl Physiol (1985) 2017; 123: 835-843
- 78 Martinez-Valdes E, Negro F, Falla D. et al. Surface electromyographic amplitude does not identify differences in neural drive to synergistic muscles. J Appl Physiol (1985) 2018; 124: 1071-1079
- 79 Solomonow M, Baratta R, Bernardi M. et al. Surface and wire EMG crosstalk in neighbouring muscles. J Electromyogr Kinesiol 1994; 4: 131-142
- 80 Farina D, Merletti R, Enoka RM. The extraction of neural strategies from the surface EMG: an update. J Appl Physiol (1985) 2014; 117: 1215-1230
- 81 Watanabe K, Holobar A, Kouzaki M. et al. Age-related changes in motor unit firing pattern of vastus lateralis muscle during low-moderate contraction. Age (Dordr) 2016; 38: 48
- 82 Kamen G, Sison SV, Du CC. et al. Motor unit discharge behavior in older adults during maximal-effort contractions. J Appl Physiol (1985) 1995; 79: 1908-1913
- 83 Del Vecchio A, Negro F, Holobar A. et al. You are as fast as your motor neurons: Speed of recruitment and maximal discharge of motor neurons determine the maximal rate of force development in humans. J Physiol 2019; 597: 2445-2456 DOI: 10.1113/jp277396.
- 84 Farina D, Holobar A. Characterization of human motor units from surface EMG decomposition. Proceedings of the IEEE 2016; 104: 353-373
- 85 Holobar A, Zazula D. Multichannel blind source separation using convolution kernel compensation. IEEE Transactions on Signal Processing 2007; 55: 4487-4496
- 86 Clark DJ, Fielding RA. Neuromuscular contributions to age-related weakness. J Gerontol A Biol Sci Med Sci 2012; 67: 41-47
- 87 Farina D, Negro F. Common synaptic input to motor neurons, motor unit synchronization, and force control. Exerc Sport Sci Rev 2015; 43: 23-33
- 88 Piasecki M, Ireland A, Stashuk D. et al. Age-related neuromuscular changes affecting human vastus lateralis. J Physiol 2016; 594: 4525-4536
- 89 Afsharipour B, Soedirdjo S, Merletti R. Two-dimensional surface EMG: The effects of electrode size, interelectrode distance and image truncation. Biomedical Signal Processing and Control 2019; 49: 298-307
- 90 Hortobagyi T, Devita P. Mechanisms responsible for the age-associated increase in coactivation of antagonist muscles. Exerc Sport Sci Rev 2006; 34: 29-35
- 91 Carolan B, Cafarelli E. Adaptations in coactivation after isometric resistance training. J Appl Physiol (1985) 1992; 73: 911-917
- 92 Wu R, Delahunt E, Ditroilo M. et al. Effect of knee joint angle and contraction intensity on hamstrings coactivation. Med Sci Sports Exerc 2017; 49: 1668-1676
- 93 Kido A, Tanaka N, Stein RB. Spinal excitation and inhibition decrease as humans age. Can J Physiol Pharmacol 2004; 82: 238-248
- 94 Scaglioni G, Ferri A, Minetti AE. et al. Plantar flexor activation capacity and H reflex in older adults: adaptations to strength training. J Appl Physiol (1985) 2002; 92: 2292-2302
- 95 Dewhurst S, Riches PE, Nimmo MA. et al. Temperature dependence of soleus H-reflex and M wave in young and older women. Eur J Appl Physiol 2005; 94: 491-499
- 96 Baudry S, Penzer F, Duchateau J. Input-output characteristics of soleus homonymous Ia afferents and corticospinal pathways during upright standing differ between young and elderly adults. Acta Physiol (Oxf) 2014; 210: 667-677
- 97 Enoka RM, Christou EA, Hunter SK. et al. Mechanisms that contribute to differences in motor performance between young and old adults. J Electromyogr Kinesiol 2003; 13: 1-12
- 98 Hunter SK, Lepers R, MacGillis CJ. et al. Activation among the elbow flexor muscles differs when maintaining arm position during a fatiguing contraction. J Appl Physiol (1985) 2003; 94: 2439-2447
- 99 Tracy BL, Enoka RM. Older adults are less steady during submaximal isometric contractions with the knee extensor muscles. J Appl Physiol (1985) 2002; 92: 1004-1012
- 100 Oomen NM, van Dieen JH. Effects of age on force steadiness: A literature review and meta-analysis. Ageing Res Rev 2017; 35: 312-321 doi: 10.1016/j.arr.2016.11.004
- 101 Harris CM, Wolpert DM. Signal-dependent noise determines motor planning. Nature 1998; 394: 780-784
- 102 Stein RB, Gossen ER, Jones KE. Neuronal variability: Noise or part of the signal?. Nat Rev Neurosci 2005; 6: 389-97
- 103 Bazzucchi I, Felici F, Macaluso A. et al. Differences between young and older women in maximal force, force fluctuations, and surface EMG during isometric knee extension and elbow flexion. Muscle Nerve 2004; 30: 626-635
- 104 Tracy BL, Dinenno DV, Jorgensen B. et al. Aging, visuomotor correction, and force fluctuations in large muscles. Med Sci Sports Exerc 2007; 39: 469-479
- 105 Pereira HM, Schlinder-DeLap B, Keenan KG. et al. Oscillations in neural drive and age-related reductions in force steadiness with a cognitive challenge. J Appl Physiol (1985) 2019; 126: 1056-1065
- 106 Wu R, Delahunt E, Ditroilo M. et al. Changes in knee joint angle affect torque steadiness differently in young and older individuals. J Electromyogr Kinesiol 2019; 47: 49-56
- 107 Dewhurst S, Graven-Nielsen T, De Vito G. et al. Muscle temperature has a different effect on force fluctuations in young and older women. Clin Neurophysiol 2007; 118: 762-769
- 108 Tracy BL. Force control is impaired in the ankle plantarflexors of elderly adults. Eur J Appl Physiol 2007; 101: 629-636
- 109 Krishnan C, Allen EJ, Williams GN. Effect of knee position on quadriceps muscle force steadiness and activation strategies. Muscle Nerve 2011; 43: 563-573
- 110 Bigland-Ritchie BR, Furbush FH, Gandevia SC. et al. Voluntary discharge frequencies of human motoneurons at different muscle lengths. Muscle Nerve 1992; 15: 130-137
- 111 Becker R, Awiszus F. Physiological alterations of maximal voluntary quadriceps activation by changes of knee joint angle. Muscle Nerve 2001; 24: 667-672
- 112 Seynnes O, Hue OA, Garrandes F. et al. Force steadiness in the lower extremities as an independent predictor of functional performance in older women. J Aging Phys Act 2005; 13: 395-408
- 113 Carville SF, Perry MC, Rutherford OM. et al. Steadiness of quadriceps contractions in young and older adults with and without a history of falling. Eur J Appl Physiol 2007; 100: 527-533
- 114 Kobayashi H, Koyama Y, Enoka RM. et al. A unique form of light-load training improves steadiness and performance on some functional tasks in older adults. Scand J Med Sci Sports 2014; 24: 98-110
- 115 Erim Z, Beg MF, Burke DT. et al. Effects of aging on motor-unit control properties. J Neurophysiol 1999; 82: 2081-2091
- 116 Galganski ME, Fuglevand AJ, Enoka RM. Reduced control of motor output in a human hand muscle of elderly subjects during submaximal contractions. J Neurophysiol 1993; 69: 2108-2115
- 117 Laidlaw DH, Bilodeau M, Enoka RM. Steadiness is reduced and motor unit discharge is more variable in old adults. Muscle Nerve 2000; 23: 600-612
- 118 de Luca CJ, Foley PJ, Erim Z. Motor unit control properties in constant-force isometric contractions. J Neurophysiol 1996; 76: 1503-1516
- 119 Taylor AM, Steege JW, Enoka RM. Motor-unit synchronization alters spike-triggered average force in simulated contractions. J Neurophysiol 2002; 88: 265-276
- 120 Tracy BL, Maluf KS, Stephenson JL. et al. Variability of motor unit discharge and force fluctuations across a range of muscle forces in older adults. Muscle Nerve 2005; 32: 533-540
- 121 Castronovo AM, Mrachacz-Kersting N, Stevenson AJT. et al. The Decrease in Force Steadiness with Aging is associated with Increased Power of the Common but not Independent Input to Motor Neurons. J Neurophysiol 2018; 120: 1616-1624 DOI: 10.1152/jn.00093.2018.
- 122 Feeney DF, Mani D, Enoka RM. Variability in common synaptic input to motor neurons modulates both force steadiness and pegboard time in young and older adults. J Physiol 2018; 596: 3793-3806
- 123 Lodha N, Christou EA. Low-frequency oscillations and control of the motor output. Front Physiol 2017; 8: 78
- 124 Gandevia SC. Spinal and supraspinal factors in human muscle fatigue. Physiol Rev 2001; 81: 1725-1789
- 125 Enoka RM, Duchateau J. Muscle fatigue: what, why and how it influences muscle function. J Physiol 2008; 586: 11-23
- 126 Kent-Braun JA, Callahan DM, Fay JL. et al. Muscle weakness, fatigue, and torque variability: effects of age and mobility status. Muscle Nerve 2014; 49: 209-217
- 127 Senefeld J, Yoon T, Hunter SK. Age differences in dynamic fatigability and variability of arm and leg muscles: Associations with physical function. Exp Gerontol 2017; 87: 74-83
- 128 Kent-Braun JA.. Skeletal muscle fatigue in old age: whose advantage?. Exerc Sport Sci Rev 2009; 37: 3-9
- 129 Yoon T, Schlinder-Delap B, Hunter SK. Fatigability and recovery of arm muscles with advanced age for dynamic and isometric contractions. Exp Gerontol 2013; 48: 259-268
- 130 Yoon T, Doyel R, Widule C. et al. Sex differences with aging in the fatigability of dynamic contractions. Exp Gerontol 2015; 70: 1-10
- 131 Lanza IR, Russ DW, Kent-Braun JA. Age-related enhancement of fatigue resistance is evident in men during both isometric and dynamic tasks. J Appl Physiol (1985) 2004; 97: 967-975
- 132 Callahan DM, Foulis SA, Kent-Braun JA. Age-related fatigue resistance in the knee extensor muscles is specific to contraction mode. Muscle Nerve 2009; 39: 692-702
- 133 Hunter SK, Critchlow A, Enoka RM. Muscle endurance is greater for old men compared with strength-matched young men. J Appl Physiol (1985) 2005; 99: 890-897
- 134 Baudry S, Klass M, Pasquet B. et al. Age-related fatigability of the ankle dorsiflexor muscles during concentric and eccentric contractions. Eur J Appl Physiol 2007; 100: 515-525
- 135 Wu R, Delahunt E, Ditroilo M. et al. Torque steadiness and neuromuscular responses following fatiguing concentric exercise of the knee extensor and flexor muscles in young and older individuals. Exp Gerontol 2019; 124: 110636
- 136 Kruger RL, Aboodarda SJ, Samozino P. et al. Isometric versus dynamic measurements of fatigue: Does age matter? A meta-analysis. Med Sci Sports Exerc 2018; 50: 2132-2144
- 137 Piasecki M, Ireland A, Jones DA. et al. Age-dependent motor unit remodelling in human limb muscles. Biogerontology 2016; 17: 485-496
- 138 Lanza IR, Befroy DE, Kent-Braun JA. Age-related changes in ATP-producing pathways in human skeletal muscle in vivo. J Appl Physiol (1985) 2005; 99: 1736-1744
- 139 Lanza IR, Larsen RG, Kent-Braun JA. Effects of old age on human skeletal muscle energetics during fatiguing contractions with and without blood flow. J Physiol 2007; 583: 1093-1105
- 140 Layec G, Trinity JD, Hart CR. et al. Evidence of a metabolic reserve in the skeletal muscle of elderly people. Aging (Albany NY) 2016; 9: 52-67
- 141 Dalton BH, Power GA, Paturel JR. et al. Older men are more fatigable than young when matched for maximal power and knee extension angular velocity is unconstrained. Age (Dordr) 2015; 37: 9790
- 142 Miller MS, Bedrin NG, Callahan DM. et al. Age-related slowing of myosin actin cross-bridge kinetics is sex specific and predicts decrements in whole skeletal muscle performance in humans. J Appl Physiol (1985) 2013; 115: 1004-1014
- 143 Solianik R, Kreivenaite L, Streckis V. et al. Effects of age and sex on fatigability and recovery from a sustained maximal isometric voluntary contraction. J Electromyogr Kinesiol 2017; 32: 61-69
- 144 Hunter SK, Critchlow A, Enoka RM. Influence of aging on sex differences in muscle fatigability. J Appl Physiol (1985) 2004; 97: 1723-1732
- 145 Yoon T, De-Lap BS, Griffith EE. et al. Age-related muscle fatigue after a low-force fatiguing contraction is explained by central fatigue. Muscle Nerve 2008; 37: 457-466
- 146 Lavender AP, Nosaka K. Fluctuations of isometric force after eccentric exercise of the elbow flexors of young, middle-aged, and old men. Eur J Appl Physiol 2007; 100: 161-167
- 147 Harriss DJ, MacSween A, Atkinson G. Ethical standards in sport and exercise science research: 2020 update. Int J Sports Med 2019; 40: 813-817
- 148 Kubo K, Ishida Y, Komuro T. et al. Age-related differences in the force generation capabilities and tendon extensibilities of knee extensors and plantar flexors in men. J Gerontol A Biol Sci Med Sci 2007; 62: 1252-1258
- 149 Ditroilo M, Cully L, Boreham CA. et al. Assessment of musculo-articular and muscle stiffness in young and older men. Muscle Nerve 2012; 46: 559-565
- 150 Lynch NA, Metter EJ, Lindle RS. et al. Muscle quality. I. Age-associated differences between arm and leg muscle groups. J Appl Physiol (1985) 1999; 86: 188-194
- 151 Overend TJ, Cunningham DA, Kramer JF. et al. Knee extensor and knee flexor strength: cross-sectional area ratios in young and elderly men. J Gerontol 1992; 47: M204-M210
- 152 Young A, Stokes M, Crowe M. The size and strength of the quadriceps muscles of old and young men. Clin Physiol 1985; 5: 145-154
- 153 Couppe C, Hansen P, Kongsgaard M. et al. Mechanical properties and collagen cross-linking of the patellar tendon in old and young men. J Appl Physiol (1985) 2009; 107: 880-886
- 154 Piasecki M, Ireland A, Piasecki J. et al. Failure to expand the motor unit size to compensate for declining motor unit numbers distinguishes sarcopenic from non-sarcopenic older men. J Physiol 2018; 596: 1627-1637 DOI: 10.1113/JP275520.
- 155 Morse CI, Thom JM, Reeves ND. et al. In vivo physiological cross-sectional area and specific force are reduced in the gastrocnemius of elderly men. J Appl Physiol (1985) 2005; 99: 1050-1055
- 156 Stenroth L, Peltonen J, Cronin NJ. et al. Age-related differences in Achilles tendon properties and triceps surae muscle architecture in vivo. J Appl Physiol (1985) 2012; 113: 1537-1544
- 157 Akagi R, Takai Y, Ohta M. et al. Muscle volume compared to cross-sectional area is more appropriate for evaluating muscle strength in young and elderly individuals. Age Ageing 2009; 38: 564-569