Role of the nervous system in sarcopenia and muscle atrophy with aging: Strength training as a countermeasure

Scandinavian Journal of Medicine and Science in Sports

Volumn 20, Issue 1, 2010, Pages 49-64

  Aagaard, P ^a   Suetta, C ^b   Caserotti, P ^a,d   Magnusson, S P ^b,c   Kjaer M ^b  

^a UNIVERSITY OF SOUTHERN DENMARK   (Denmark)

^b BISPEBJERG HOSPITAL   (Denmark)

^c UNIVERSITY OF COPENHAGEN   (Denmark)

^d NATIONAL INSTITUTES OF HEALTH   (United States)

Author keywords

CNS; Motor neurons; Muscle power; RFD; Strength training

Indexed keywords

SOMATOMEDIN C;

AGING; ANIMAL; APOPTOSIS; CYTOLOGY; ELECTROMYOGRAPHY; HUMAN; MOTONEURON; MUSCLE ATROPHY; NERVE FIBER; PATHOPHYSIOLOGY; PHYSIOLOGY; RESISTANCE TRAINING; REVIEW; SKELETAL MUSCLE;

AGING; ANIMALS; APOPTOSIS; AXONS; ELECTROMYOGRAPHY; HUMANS; INSULIN-LIKE GROWTH FACTOR I; MOTOR NEURONS; MUSCLE, SKELETAL; MUSCULAR ATROPHY; RESISTANCE TRAINING; SARCOPENIA;

EID: 75649152800     PISSN: 09057188     EISSN: 16000838     Source Type: Journal    
DOI: 10.1111/j.1600-0838.2009.01084.x     Document Type: Review

References (137)

1. Aagaard P, Andersen JL, Leffers AM, Wagner Å, Magnusson SP, Halkjær-Kristensen J, Dyhre-Poulsen P, Simonsen EB. A mechanism for increased contractile strength of human pennate muscle in response to strength training - changes in muscle architecture. J Physiol 2001 : 534 (2) : 613 623.
2. Aagaard P, Magnusson SP, Larsson B, Kjær M, Krustrup P. Mechanical muscle function, morphology and fibertype in life-long trained elderly. Med Sci Sports Exerc 2007 : 39 : 1989 1996.
3. Aagaard P, Simonsen EB, Andersen JL, Magnusson P, Dyhre-Poulsen P. Increased rate of force development and neural drive of human skeletal muscle following resistance training. J Appl Physiol 2002 : 93 : 1318 1326.
4. Adinolfi AM, Yamuy J, Morales FR, Chase MH. Segmental demyelination in peripheral nerves of old cats. Neurobiol Aging 1991 : 12 : 175 179.
5. Andersen JL. Muscle fibre type adaptation in the elderly human muscle. Scan J Med Sci Sports 2003 : 13 : 40 47.
6. Atherton PJ, Babraj J, Smith K, Singh J, Rennie MJ, Wackerhage H. Selective activation of AMPK PGC-1alpha or PKB-TSC2-mTOR signaling can explain specific adaptive responses to endurance or resistance training-like electrical muscle stimulation. FASEB J 2005 : 19 : 786 788.
7. Balagopal P, Rooyackers OE, Adey DB, Ades PA, Sreekumaran Nair K. Effects of aging on in vivo synthesis of skeletal muscle myosin heavy-chain and sarcoplasmic protein in humans. Am J Physiol 1997 : 273 : E790 E800.
8. Baldissera F, Campadelli P, Piccinelli L. The dynamic response of cat gastrocnemius motor units investigated by ramp-current injection into their motoneurones. J Physiol 1987 : 387 : 317 330.
9. Barry BK, Pascoe MA, Jesunathadas M, Enoka RM. Rate coding is compressed but variability is unaltered for motor units in a hand muscle of old adults. J Neurophysiol 2007 : 97 : 3206 3218.
10. Barry BK, Warman GE, Carson RG. Age-related differences in rapid muscle activation after rate of force development training of the elbow flexors. Exp Brain Res 2005 : 162 : 122 132.
11. Bassey EJ, Fiatarone MA, O'Neill EF, Kelly M, Evans WJ, Lipsitz LA. Leg extensor power and functional performance in very old men and women. Clin Sci (Lond) 1992 : 82 : 321 327.
12. Beyer N, Simonsen L, Bülow J, Lorenzen T, Jensen DV, Larsen L, Rasmussen U, Rennie M, Kjaer M. Old women with a recent fall history show improved muscle strength and function sustained for six months after finishing training. Aging Clin Exp Res 2007 : 19 : 300 309.
13. Brown WF. A method for estimating the number of motor units in thenar muscles and the changes in motor unit count with ageing. J Neurol Neurosurg Psychiatry 1972 : 35 : 845 852.
14. Brown WF, Strong MJ, Snow R. Methods for estimating numbers of motor units in biceps-brachialis muscles and losses of motor units with aging. Muscle Nerve 1988 : 11 : 423 432.
15. Buchman AS, Wilson RS, Boyle PA, Tang Y, Fleischman DA, Bennett DA. Physical activity and leg strength predict decline in mobility performance in older persons. J Am Geriatr Soc 2007 : 55 : 1618 1623.
16. Campbell MJ, McComas AJ, Petito F. Physiological changes in ageing muscles. J Neurol Neurosurg Psychiatry 1973 : 36 : 174 182.
17. Carlson M, Suetta C, Conboy M, Aagaard P, Mackey A, Kjaer K, Conboy I. Molecular aging and rejuvenation of human muscle stem cells. EMBO Mol Med 2009 : 1 : 1 11.
18. Caserotti P, Aagaard P, Larsen JB, Puggaard P. Explosive heavy-resistance training in old and very old adults: changes in rapid muscle force, strength and power. Scand J Med Sci Sports 2008b : 18 : 773 782.
19. Caserotti P, Aagaard P, Puggaard L. Changes in power and force generation during coupled eccentric concentric versus concentric muscle contraction with training and aging. Eur J Appl Physiol 2008a : 103 : 151 161.
20. Chandler JM, Duncan PW, Kochersberger G, Studenski S. Is lower extremity strength gain associated with improvement in physical performance and disability in frail, community-dwelling elders? Arch Phys Med Rehabil 1998 : 79 : 24 30.
21. Christie A, Kamen G. Doublet discharges in motoneurons of young and older adults. J Neurophysiol 2006 : 95 : 2787 2795.
22. Clavel S, Coldefy AS, Kurkdjian E, Salles J, Margaritis I, Derijard B. Atrophy-related ubiquitin ligases, atrogin-1 and MuRF1 are upregulated in aged rat tibialis anterior muscle. Mech Ageing Dev 2006 : 127 : 794 801.
23. Connelly DM, Rice CL, Roos MR, Vandervoort AA. Motor unit firing rate and contractile properties in tibialis anterior of young and old men. J Appl Physiol 1999 : 87 : 843 852.
24. Dalton BH, McNeil CJ, Doherty TJ, Rice CL. Age-related reductions in the estimated numbers of motor units are minimal in the human soleus. Muscle Nerve 2008 : 38 : 1108 1115.
25. de Boer MD, Morse CI, Thom JM, de Haan A, Narici MV. Changes in antagonist muscles' coactivation in response to strength training in older women. J Gerontol Med Sci 2007 : 2062A : 1022 1027.
26. de Koning P, Wienceke GH, Van der Most van Spijk D, Van Huffelen AC, Gispen WH, Jennekens FGI. Estimation of the number of motor units based on macro-EMG. J Neurol Neurosurg Psychiatry 1988 : 51 : 403 411.
27. de Vos NJ, Singh NA, Ross DA, Stavrinos TM, Orr R, Fiatarone Singh MA. Optimal load for increasing muscle power during explosive resistance training in older adults. J Gerontol Med Sci 2005 : 60A : 638 647.
28. Del Balso C, Cafarelli E. Adaptations in the activation of human skeletal muscle induced by short-term isometric resistance training. J Appl Physiol 2007 : 103 : 402 411.
29. Doherty TJ, Brown WF. The estimated numbers and relative sizes of thenar motor units as selected by multiple point stimulation in young and older adults. Muscle Nerve 1993 : 16 : 355 366.
30. Doherty TJ, Stashuk DW, Brown WF. Determinants of mean motor unit size: impact on estimates of motor unit number. Muscle Nerve 1993 : 16 : 1326 1331.
31. Earles DR, Koceja DM, Shively CW. Enviromental changes in soleus H-reflex excitability in young and elderly subjects. Int J Neurosci 2000 : 105 : 1 13.
32. Edström E, Altun M, Bergman E, Johnson H, Kullberg S, Ramírez-León V, Ulfhake B. Factors contributing to neuromuscular impairment and sarcopenia during aging. Physiol Behav 2007 : 92 : 129 135.
33. Edström E, Altun M, Hägglund M, Ulfhake B. Atrogin-1 and MuRF1 are downregulated in aging related loss of skeletal muscle. J Gerontol A Biol Sci Med Sci 2006 : 61 : 663 674.
34. Edström L, Larsson L. Effects of age on contractile and enzyme-histochemical properties of fast- and slow-twitch single motor units in the rat. J Physiol 1987 : 392 : 129 145.
35. Einsiedel LJ, Luff AR. Alterations in the contactile properties of motor units within the ageing rat medial gastrocnemius. J Neurol Sci 1992 : 112 : 170 177.
36. Eisen A, Siejka S, Schulzer M, Calne D. Age-dependent decline in motor evoked potential (MEP) amplitude: with a comment on changes in Parkinson's disease. Electroencephalogr Clin Neurophysiol 1991 : 81 : 209 215.
37. Enoka RM, Christou EA, Hunter SK, Kornatz KW, Semmler JG, Taylor AM, Tracy BL. Mechanisms that contribute to differences in motor performance between young and old adults. J Electromyogr Kinesiol 2003 : 13 : 1 12.
38. Esmarck B, Andersen JL, Olsen S, Mizuno M, Kjaer M. Timing of protein intake after resistance exercise bouts is paramount for muscle hypertrophy over a 12-week training period in elderly. J Physiol 2001 : 535 : 301 311.
39. Essén-Gustavsson B, Borges O. Histochemical and metabolic characteristics of human skeletal muscle in relation to age. Acta Physiol Scand 1986 : 126 : 107 114.
40. Ferri A, Scaglioni G, Pousson M, Capodaglio P, Van Hoecke J, Narici MV. Strength and power changes of the human plantar flexors and knee extensors in response to resistance training in old age. Acta Physiol Scand 2003 : 177 : 69 78.
41. Fiatarone MA, O'Neill EF, Ryan ND, Clements KM, Solares GR, Nelson ME, Roberts SB, Kehayias JJ, Lipsitz LA, Evans WJ. Exercise training and nutritional supplementation for physical frailty in very elderly people. New Engl J Med 1994 : 330 : 1769 1775.
42. Fiatarone Singh MA, Ding W, Manfredi TJ, Solares GS, O'Neill EF, Clements KM, Ryan ND, Kehayias JJ, Fielding RA, Evans WJ. Insulin-like growth factor I in skeletal muscle after weight lifting exercise in frail elders. Am J Physiol 1999 : 277 : E135 E143.
43. Fielding RA, LeBrasseur NK, Cuoco A, Bean J, Mizer K, Fiatarone Singh MA. High-velocity resistance training increases skeletal muscle peak power in older women. J Am Geriatr Soc 2002 : 50 : 655 662.
44. Foldvari M, Clark M, Laviolette LC, Bernstein MA, Kaliton D, Castaneda C, Pu CT, Hausdorff JM, Fielding RA, Singh MA. Association of muscle power with functional status in community dwelling elderly women. J Gerontol A Biol Sci Med Sci 2000 : 55 : M192 M199.
45. Frontera WR, Meredith CN, O'Reilly KP, Knuttgen HG, Evans WJ. Strength conditioning in older men: skeletal muscle hypertrophy and improved function. J Appl Physiol 1988 : 64 : 1038 1044.
46. Galea V. Changes in motor unit estimates with aging. J Clin Neurophysiol 1996 : 13 : 253 260.
47. Gallegly JC, Turesky NA, Strotman BA, Gurley CM, Peterson CA, Dupont-Versteegden EE. Satellite cell regulation of muscle mass is altered at old age. J Appl Physiol 2004 : 97 : 1082 1090.
48. Garland SJ, Griffin L. Motor unit double discharges: statistical anomaly or functional entity? Can J Appl Physiol 1999 : 24 : 113 130.
49. Grounds MD. Reasons for the degeneration of ageing skeletal muscle: a central role for IGF-1 signalling. Biogerontology 2002 : 3 : 19 24.
50. Grounds MD, Radley HG, Gebski BL, Bogoyevitch MA, Shavlakadze T. Implications of cross-talk between tumor necrosis factor and insulin-like growth factor-1 signalling in skeletal muscle. Clin Exp Pharmacol Physiol 2008 : 35 : 846 851.
51. Häkkinen K, Alén M, Kallinen M, Newton RU, Kraemer WJ. Neuromuscular adaptation during prolonged strength training, detraining and re-strength-training in middle-aged and elderly people. Eur J Appl Physiol 2000 : 83 : 51 62.
52. Häkkinen K, Kallinen M, Izquierdo M, Jokelainen K, Lassila H, Mälkiä E, Kraemer WJ, Newton RU, Alén M. Changes in agonist-antagonist EMG, muscle CSA, and force during strength training in middle-aged and older people. J Appl Physiol 1998a : 84 : 1341 1349.
53. Häkkinen K, Kraemer WJ, Newton RU, Alen M. 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.
54. Häkkinen K, Newton RU, Gordon SE, McCormick M, Volek JS, Nindl BC, Gotshalk LA, Campbell WW, Evans WJ, Häkkinen A, Humphries BJ, Kraemer WJ. Changes in muscle morphology, electromyographic activity, and force production characteristics during progressive strength training in young and older men. J Gerontol A Biol Sci Med Sci 1998b : 53 : B415 B423.
55. Hantai D, Akaaboune M, Lagord C, Murawsky M, Houenou LJ, Festoff BW, Vaught JL, Rieger F, Blondet B. Beneficial effects of insulin-like growth factor-I on wobbler mouse motoneuron disease. J Neurol Sci 1995 : 129 (Suppl.) : 122 126.
56. Harridge DR, Kryger A, Stensgaard A. Knee extensor activation and size in very elderly people following strength training. Muscle Nerve 1999 : 22 : 831 839.
57. Hashizume K, Kanda K. Differential effects of aging on motoneurons and peripheral nerves innervating the hindlimb and forelimb muscles of rats. Neurosci Res 1995 : 22 : 189 196.
58. Heuser JE, Reese TS. Evidence for recycling of synaptic vesicle membrane during transmitter release at the frog neuromuscular junction. J Cell Biol 1973 : 57 : 315 344.
59. Hikida RS, Staron RS, Hagerman FC, Walsh S., Kaiser E., Shell S, Hervey S. Effects of high-intensity resistance training on untrained older men> II. Muscle fiber characteristics and nucleo-cytoplasmic relationships. J Gerontol A Biol Sci Med Sci 2000 : 55 : B347 B354.
60. Hikida RS, Walsh S, Barylski N, Campos G, Hagerman FC, Staron RS. Is hypertrophy limited in elderly muscle fibers? A comparison of elderly and young strength-trained men. Basic Appl Myol 1998 : 8 : 419 427.
61. Hortobagyi T, DeVita P. Muscle pre- and coactivity during downward stepping are associated with leg stiffness in aging. J Electromyogr Kinesiol 2000 : 10 : 117 126.
62. Hortobagyi T, Tunnel D, Moody J, Beam S, DeVita P. Low- or high-intensity strength training partially restores impaired quadriceps force accuracy and steadiness in aged adults. J Gerontol Biol Sci 2001 : 56A : B38 B47.
63. Inokuchi S, Ishikawa H, Iwamoto S, Kimura T. Age-related changes in the histological composition of the rectus abdominis muscle of the adult human. Hum Biol 1975 : 47 : 231 249.
64. Izquierdo M, Aguado X, Gonzalez R, Lopez JL, Häkkinen K. Maximal and explosive force production capacity and balance performance in men of different ages. Eur J Appl Physiol Occup Physiol 1999 : 79 : 260 267.
65. Janssen I, Heymsfield SB, Ross R. Low relative skeletal muscle mass (sarcopenia) in older persons is associated with functional impairment and physical disability. J Am Geriatr Soc 2002 : 50 : 889 896.
66. Johnson H, Mossberg K, Arvidsson U, Piehl F, Hökfelt T, Ulfhake B. Increase in alpha-CGRP and GAP-43 in aged motoneurons: a study of peptides, growth factors, and ChAT mRNA in the lumbar spinal cord of senescent rats with symptoms of hindlimb incapacities. J Comp Neurol 1995 : 359 : 69 89.
67. Kadi F, Charifi N, Denis C, Lexell J. Satellite cells and myonuclei in young and elderly women and men. Muscle Nerve 2004 : 29 : 120 127.
68. Kamen G, Knight CA. Training-related adaptations in motor unit discharge rate in young and older adults. J Gerontol Med Sci 2004 : 59A : 1334 1338.
69. Kanda K, Hashizume K, Miwa T, Miwa Y. Overloading a muscle does not alter the rate of motoneuronal loss in aged rats. Neurobiol Aging 1996 : 17 : 613 617.
70. Kawamura Y, O'Brien PC, Okazaki H, Dyck PJ. Lumbar motoneurons of man. II. Numbers and diameter distributions of large- and intermediate-diameter cytons in motoneuron columns of spinal cord of man. J Neuropathol Exp Neurol 1977b : 36 : 861 870. (Pubitemid 8191198)
71. Kawamura Y, Okazaki H, O'Brien PC, Dyck PJ. Lumbar motoneurons of man. I. Numbers and diameter histograms of alpha and gamma axons and ventral roots. J Neuropathol Exp Neurol 1977a : 36 : 853 860.
72. Kido A, Tanaka N, Stein RB. Spinal excitation and inhibition decrease as humans age. Can J Physiol Pharmacol 2004 : 82 : 238 248.
73. Klass M, Baudry S, Duchateau J. Voluntary activation during maximal contraction with advancing age: a brief review. Eur J Appl Physiol 2007 : 100 : 543 551.
74. 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 2008 : 104 : 739 746.
75. Klein CS, Marsh GD, Petrella RJ, Rice CL. Muscle fiber number in the biceps brachii muscle of young and old men. Muscle Nerve 2003 : 28 : 62 68.
76. Klein CS, Rice CL, Marsh GD. Normalized force, activation, and coactivation in the arm muscles of young and old men. J Appl Physiol 2001 : 91 : 1341 1349.
77. Klitgaard H, Mantoni M, Schiaffino S, Ausoni S, Gorza L, Laurent-Winter C, Schnohr P, Saltin B. Function, morphology and protein expression of ageing skeletal muscle: a cross-sectional study of elderly men with different training backgrounds. Acta Physiol Scand 1990 : 140 : 41 54.
78. Koceja DM, Markus CA, Trimble MH. Postural modulation of the soleus H reflex in young and old subjects. Electroencephalogr Clin Neurophysiol 1995 : 97 : 387 393.
79. Koceja DM, Mynark RG. Comparison of heteronymous monosynaptic Ia facilitation in young and elderly subjects in supine and standing positions. Int J Neurosci 2000 : 103 : 1 17.
80. Korhonen MT, Cristea A, Alén M, Häkkinen K, Sipilä S, Mero A, Viitasalo JT, Larsson L, Suominen H. Aging, muscle fiber type, and contractile function in sprint-trained athletes. J Appl Physiol 2006 : 101 : 906 917.
81. Kosek DJ, Kim J-S, Petrella JK, Cross JM, Bamman MM. Efficacy of 3 days/wk resistance training on myofiber hypertrophy and myogenic mechanisms in young vs. older adults. J Appl Physiol 2006 : 101 : 531 544.
82. Kromer LF. Nerve growth factor treatment after brain injury prevents neuronal death. Science 1987 : 235 : 214 216.
83. Kryger AI, Andersen JL. Resistance training in the oldest old: consequences for muscle strength, fiber types, fiber size, and MHC isoforms. Scand J Med Sci Sports 2007 : 17 : 422 430.
84. Larsen AH, Puggaard L, Hämäläinen U, Aagaard P. Comparison of ground reaction forces and antagonist muscle coactivation during stair walking with ageing. J Electromyogr Kinesiol 2008 : 18 : 568 580.
85. Larsson L, Sjödin B, Karlsson J. Histochemical and biochemical changes in human skeletal muscle with age in sedentary males, age 22-65 years. Acta Physiol Scand 1978 : 103 : 31 39.
86. Lascelles RG, Thomas PK. Changes due to age in internodal length in the sural nerve in man. J Neurol Neurosurg Psychiatry 1966 : 29 : 40 44.
87. Lexell J, Downham DY. The occurrence of fibre type grouping in healthy human muscle: a quantitative study of cross-sections of whole vastus lateralis from men between 15 and 83 years. Acta Neuropathol 1991 : 81 : 377 381.
88. Lexell J, Henriksson-Larsen K, Sjostrom M. Distribution of different fibre types in human skeletal muscles - 2. A study of cross-sections of whole m. vastus lateralis. Acta Physiol Scand 1983 : 117 : 115 122. (Pubitemid 13142146)
89. Lexell J, Taylor T, Sjostrom M. What is the cause of the ageing atrophy? Total number, size, and proportion of different fibre types studied in whole vastus lateralis muscle from 15- to 83-year-old men. J Neurol Sci 1988 : 84 : 275 294.
90. Luff AR. Age-associated changes in the innervation of muscle fibers and changes in the mechanical properties of motor units. Ann NY Acad Sci 1998 : 854 : 92 101.
91. Macaluso A, Nimmo MA, Foster JE, Cockburn M, McMillan NC, De Vito G. Contractile muscle volume and agonist-antagonist coactivation account for differences in torque between young and older women. Muscle Nerve 2002 : 25 : 858 863.
92. Martel GF, Roth SM, Ivey FM, Lemmer JT, Tracy BL, Hurlbut DE, Metter EJ, Hurley BF, Rogers MA. Age and sex affect human muscle fibre adaptations to heavy-resistance strength training. Exp Physiol 2006 : 91 (2) : 457 464.
93. Masakado Y, Noda Y, Nagata MA, Kimura A, Chino N, Akaboshi K. Macro-EMG and motor unit recruitment threshold: differences between the young and the aged. Neurosci Lett 1994 : 179 : 1 4.
94. McNeil CJ, Doherty TJ, Stashuk DW, Rice CL. Motor unit number estimates in the tibialis anterior muscle of young, old, and very old men. Muscle Nerve 2005 : 31 : 461 467.
95. 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 2007 : 102 : 1962 1968.
96. Metter EJ, Conwit R, Metter B, Pacheco T, Tobin J. The relationship of peripheral motor nerve conduction velocity to age-associated loss of grip strength. Aging (Milano) 1998 : 10 : 471 478.
97. Mittal KR, Logmani FH. Age-related reduction in 8th cervical ventral nerve root myelinated fiber diameters and numbers in man. J Gerontol 1987 : 42 : 8 10.
98. Morita H, Shindo M, Yanagawa S, Yoshida T, Momoi H, Yanagisawa N. Progressive decrease in heteronymous monosynaptic Ia facilitation with human ageing. Exp Brain Res 1995 : 104 : 167 170.
99. Morse CI, Thom JM, Mian OS, Birch KM, Narici MV. Gastrocnemius specific force is increased in elderly males following a 12-month physical training programme. Eur J Appl Physiol 2007 : 100 : 563 570.
100. Narici MV, Reeves ND, Morse CI, Maganaris CN. Muscular adaptations to resistance exercise in the elderly. J Musculoskel Neuron Interact 2004 : 4 : 161 164.
101. Pearson SJ, Young A, Macaluso A, Devito G, Nimmo MA, Cobbold M, Harridge SD. Muscle function in elite master weightlifters. Med Sci Sports Exerc 2002 : 34 : 1199 1206.
102. Ramirez-Leon V, Kullberg S, Hjelle OP, Ottersen OP, Ulfhake B. Increased glutathione levels in neurochemically identified fibre systems in the aged rat lumbar motor nuclei. Eur J Neurosci 1999 : 11 : 2935 2948.
103. Raue U, Slivka D, Jemiolo B, Hollon C, Trappe S. Proteolytic gene expression differs at rest and after resistance exercise between young and old women. J Gerontol Med Sci 2007 : 62A : 1407 1412.
104. Raue U, Slivka D, Minchev K, Trappe S. Improvements in whole muscle and myocellular function are limited with high-intensity resistance training in octogenarian women. J Appl Physiol 2009 : 106 : 1611 1617.
105. Reeves ND, Narici MV, Maganaris CN. Effect of resistance training on skeletal muscle-specific force in elderly humans. J Appl Physiol 2004a : 96 : 885 892.
106. Reeves ND, Narici MV, Maganaris CN. In vivo human muscle structure and function: adaptations to resistance training in old age. Exp Physiol 2004b : 89 : 675 689.
107. Rosenheimer JL. Ultraterminal sprouting in innervated and partially denervated adult and aged rat muscle. Neurosci 1990 : 38 : 763 770.
108. Roth SM, Martel GF, Ivey FM, Lemmer JT, Metter EJ, Hurley BF, Rogers MA. Skeletal muscle satellite cell populations in healthy young and older men and women. Anat Rec 2000 : 260 : 351 358.
109. Sajko S, Kubinova L, Cvetko E, Kreft M, Wernig A, Erzen I. Frequency of M-Cadherin-stained satellite cells declines in human muscles during aging. J Histochem Cytochem 2004 : 52 : 179 185.
110. Sale MV, Semmler JG. Age-related differences in corticospinal control during functional isometric contractions in left and right hands. J Appl Physiol 2005 : 99 : 1483 1493.
111. Scaglioni G, Ferri A, Minetti AE, Martin A, Van Hoecke J, Capodaglio P, Sartorio A, Narici MV. Plantar flexor activation capacity and H reflex in older adults: adaptations to strength training. J Appl Physiol 2002 : 92 : 2292 2302.
112. Sica RE, McComas AJ, Upton AR, Longmire D. Motor unit estimations in small muscles of the hand. J Neurol Neurosurg Psychiatry 1974 : 37 : 55 67.
113. Simoneau E, Martin A, Van Hoecke J. Muscular performances at the ankle joint in young and elderly men. J Gerontol A Biol Sci Med Sci 2005 : 60 : 439 447.
114. Skelton DA, Greig CA, Davies JM, Young A. Strength, power and related functional ability of healthy people aged 65-89 years. Age Ageing 1994 : 23 : 371 377.
115. Slivka D, Raue U, Hollon C, Minchev K, Trappe S. Single muscle fiber adaptations to resistance training in old (80 yr) men: evidence for limited skeletal muscle plasticity. Am J Physiol Regul Integr Comp Physiol 2008 : 295 : R273 R280.
116. Stålberg E, Borges O, Ericsson M, Essén-Gustavsson B, Fawcett PR, Nordesjö LO, Nordgren B, Uhlin R. The quadriceps femoris muscle in 20-70-year-old subjects: relationship between knee extension torque, electrophysiological parameters, and muscle fiber characteristics. Muscle Nerve 1989 : 12 : 382 389.
117. Stålberg E, Fawcett PR. Macro EMG in healthy subjects of different ages. J Neurol Neurosurg Psychiatry 1982 : 45 : 870 878.
118. Suetta C, Aagaard P, Magnusson SP, Andersen LL, Sipilä S, Rosted A, Jakobsen AK, Duus B, Kjaer M. Muscle size, neuromuscular activation, and rapid force characteristics in elderly men and women: effects of unilateral long-term disuse due to hip-osteoarthritis. J Appl Physiol 2007 : 102 : 942 948.
119. Suetta C, Aagaard P, Rosted A, Jakobsen AK, Duus B, Kjaer M, Magnusson SP. Training-induced changes in muscle CSA, muscle strength, EMG, and rate of force development in elderly subjects after long-term unilateral disuse. J Appl Physiol 2004a : 97 : 1954 1961.
120. Suetta C, Andersen JL, Dalgas U, Berget J, Koskinen S, Aagaard P, Magnusson SP, Kjaer M. Resistance training induces qualitative changes in muscle morphology, muscle architecture, and muscle function in elderly postoperative patients. J Appl Physiol 2008 : 105 : 180 186.
121. Suetta C, Hvid LG, Justesen L, Christensen U, Neergaard K, Simonsen L, Ortenblad N, Magnusson SP, Kjaer M, Aagaard P. Effects of aging on human skeletal muscle after immobilization and retraining. J Appl Physiol 2009 : 107 : 1172 1180.
122. Suetta C, Magnusson SP, Rosted A, Aagaard P, Jakobsen AK, Larsen LH, Duus B, Kjaer M. Resistance training in the early post-operative phase reduces hospitalization and leads to muscle hypertrophy in elderly hip surgery patients - a controlled randomized study. J Am Geriatr Soc 2004b : 52 : 2016 2022.
123. Tam SL, Gordon T. Mechanisms controlling axonal sprouting at the neuromuscular junction. J Neurocytol 2003a : 32 : 961 974.
124. Tam SL, Gordon T. Neuromuscular activity impairs axonal sprouting in partially denervated muscles by inhibiting bridge formation of perisynaptic Schwann cells. J Neurobiol 2003b : 57 : 221 234.
125. Tinetti ME, Speechley M, Ginter SF. Risk factors for falls among elderly persons living in the community. N Engl J Med 1988 : 319 : 1701 1707.
126. Tomlinson BE, Irving D. The numbers of limb motor neurons in the human lumbosacral cord throughout life. J Neurol Sci 1977 : 34 : 213 219.
127. Tracy BL, Byrnes WC, Enoka RM. Strength training reduces force fluctuations during anisometric contractions of the quadriceps femoris muscles in old adults. J Appl Physiol 2004 : 96 : 1530 1540.
128. Tracy BL, Enoka RM. Older adults are less steady during submaximal isometric contractions with the knee extensor muscles. J Appl Physiol 2002 : 92 : 1004 1012.
129. Tracy BL, Enoka RM. Steadiness training with light loads in the knee extensors of elderly adults. Med Sci Sports Exerc 2006 : 38 : 735 745.
130. Van Cutsem M, Duchateau J. Preceding muscle activity influences motor unit discharge and rate of torque development during ballistic contractions in humans. J Physiol 2005 : 562 : 635 644.
131. Van Cutsem M, Duchateau J, Hainaut K. Changes in single motor unit behavior contribute to the increase in contraction speed after dynamic training in humans. J Physiol 1998 : 513 (1) : 295 305.
132. Vandervoort AA. Aging of the human neuromuscular system. Muscle Nerve 2002 : 25 : 17 25.
133. Vandervoort AA, McComas AJ. Contractile changes in opposing muscles of the human ankle joint with aging. J Appl Physiol 1986 : 61 : 361 367.
134. Ward NS, Frackowiak RSJ. Age-related changes in the neural correlates of motor performance. Brain 2003 : 126 : 873 888.
135. Ward NS, Swayne OB, Newton JM. Age-dependent changes in the neural correlates of force modulation: an fMRI study. Neurobiol Aging 2008 : 29 : 1434 1446.
136. Welle S, Thornton C. Insulin-like growth factor-1, actin and myosin heavy chain messenger mRNAs in skeletal muscle after an injection of growth hormone in subjects over 60 years old. J Endocrinol 1997 : 155 : 93 97.
137. Whitman SA, Wacker MJ, Richmond SR, Godard MP. Contributions of the ubiquitin-proteasome pathway and apoptosis to human skeletal muscle wasting with age. Pflugers Arch 2005 : 450 : 437 446.