Modeling age-related neuromuscular changes in humans

Applied Physiology, Nutrition and Metabolism

Volumn 34, Issue 4, 2009, Pages 732-744

  Webber, Sandra C ^a   Porter, Michelle M ^b   Gardiner, Phillip F ^a  

^a UNIVERSITY OF MANITOBA   (Canada)

^b UNIVERSITY OF MANITOBA   (Canada)

Author keywords

Aging; Effort; Force; Motoneuron; Muscle; Quadriceps; Strength

Indexed keywords

AGE; AGING; ARTICLE; BIOLOGICAL MODEL; HUMAN; INNERVATION; MOTONEURON; MUSCLE CONTRACTION; MUSCLE STRENGTH; NEUROPHYSIOLOGICAL RECRUITMENT; PERCEPTION; PHYSIOLOGY; QUADRICEPS FEMORIS MUSCLE;

AGE FACTORS; AGING; HUMANS; MODELS, NEUROLOGICAL; MOTOR NEURONS; MUSCLE CONTRACTION; MUSCLE STRENGTH; PERCEPTION; QUADRICEPS MUSCLE; RECRUITMENT, NEUROPHYSIOLOGICAL;

EID: 70349935474     PISSN: 17155312     EISSN: None     Source Type: Journal    
DOI: 10.1139/H09-052     Document Type: Article

References (68)

1. Allman, B.L., and Rice, C.L. 2004. An age-related shift in the force-frequency relationship affects quadriceps fatigability in old adults. J. Appl. Physiol. 96(3): 1026-1032. doi:10.1152/japplphysiol.00991.2003. PMID:14594856.
2. Bakels, R., and Kernell, D. 1994. Threshold-spacing in motoneurone pools of rat and cat: possible relevance for manner of force gradation. Exp. Brain Res. 102(1): 69-74. doi:10.1007/BF00232439. PMID:7895800.
3. Baldissera, F., Campadelli, P., and Piccinelli, L. 1987. The dynamic response of cat gastrocnemius motor units investigated by ramp-current injection into their motoneurones. J. Physiol. 387: 317-330. PMID:3656175.
4. Barry, B.K., Pascoe, M.A., Jesunathadas, M., and Enoka, R.M. 2007. Rate coding is compressed but variability is unaltered for motor units in a hand muscle of old adults. J. Neurophysiol. 97(5): 3206-3218. doi:10.1152/jn.01280.2006. PMID:17360826.
5. Brown, W.F., Strong, M.J., and Snow, R. 1988. Methods for estimating numbers of motor units in biceps-brachialis muscles and losses of motor units with aging. Muscle Nerve, 11(5): 423-432. doi:10.1002/mus.880110503. PMID:3374514.
6. Connelly, D.M., Rice, C.L., Roos, M.R., and Vandervoort, A.A. 1999. Motor unit firing rates and contractile properties in tibialis anterior of young and old men. J. Appl. Physiol. 87(2): 843-852. PMID:10444648.
7. Davidson, J.B., Kim, J., Cheng, L.K., Rohrle, O., Shorten, P.R., Soboleva, T.K., et al. 2006. Mathematically modeling the effects of electrically stimulating skeletal muscle. Conf. Proc. IEEE Eng. Med. Biol. Soc. 1: 4635-4638. PMID:17946255.
8. Del Valle A., and Thomas, C.K. 2004. Motor unit firing rates during isometric voluntary contractions performed at different muscle lengths. Can. J. Physiol. Pharmacol. 82(8-9): 769-776. doi:10.1139/y04-084. PMID:15523534.
9. Desmedt, J.E., and Godaux, E. 1977. Ballistic contractions in man: characteristic recruitment pattern of single motor units of the tibialis anterior muscle. J. Physiol. 264(3): 673-693. PMID:845820.
10. Doherty, T.J., Vandervoort, A.A., and Brown, W.F. 1993. Effects of ageing on the motor unit: a brief review. Can. J. Appl. Physiol. 18(4): 331-358. PMID:8275048.
11. Erim, Z., de Luca, C.J., Mineo, K., and Aoki, T. 1996. Rank-ordered regulation of motor units. Muscle Nerve, 19(5): 563-573. doi:10.1002/(SICI)1097-4598(199605)19:5 <563::AID-MUS3> 3.0.CO; 2-9. PMID:8618553.
12. Erim, Z., Beg, M.F., Burke, D.T., and de Luca, C.J. 1999. Effects of aging on motor-unit control properties. J. Neurophysiol. 82(5): 2081-2091. PMID:10561389.
13. Frontera, W.R., Suh, D., Krivickas, L.S., Hughes, V.A., Goldstein, R., and Roubenoff, R. 2000. Skeletal muscle fiber quality in older men and women. Am. J. Physiol. Cell Physiol. 279(3): C611-C618. PMID:10942711.
14. Fuglevand, A.J., Winter, D.A., and Patla, A.E. 1993. Models of recruitment and rate coding organization in motor-unit pools. J. Neurophysiol. 70(6): 2470-2488. PMID:8120594.
15. Gardiner, P.F. 2001. Neuromuscuar aspects of physical activity. Human Kinetics, Champaign, Ill.
16. Grimby, G., Aniansson, A., Zetterberg, C., and Saltin, B. 1984. Is there a change in relative muscle fibre composition with age? Clin. Physiol. 4(2): 189-194. doi:10.1111/j.1475-097X.1984. tb00235.x. PMID:6539189.
17. Heckman, C.J., and Binder, M.D. 1991. Computer simulation of the steady-state input-output function of the cat medial gastrocnemius motoneuron pool. J. Neurophysiol. 65(4): 952-967. PMID:2051212.
18. Hornby, T.G., McDonagh, J.C., Reinking, R.M., and Stuart, D.G. 2002. Motoneurons: A preferred firing range across vertebrate species? Muscle Nerve, 25(5): 632-648. doi:10.1002/mus. 10105. PMID:11994957.
19. Howard, J.E., McGill, K.C., and Dorfman, L.J. 1988. Age effects on properties of motor unit action potentials: ADEMG analysis. Ann. Neurol. 24(2): 207-213 doi:10.1002/ana.410240206. PMID:3178176.
20. Huxley, H.E. 1953. Electron microscope studies of the organisation of the filaments in striated muscle. Biochim. Biophys. Acta, 12(3): 387-394. doi:10.1016/0006-3002(53)90156-5. PMID:13115446.
21. Huxley, A.F., and Niedergerke, R. 1954. Structural changes in muscle during contraction; interference microscopy of living muscle fibres. Nature, 173(4412): 971-973. doi:10.1038/173971a0. PMID:13165697.
22. Kalmar, J.M., Button, D.C., Gardiner, K., Cahill, F., and Gardiner, P.F. 2008. Caloric restriction does not offset age-associated changes in the biophysical properties of motoneurons. J. Neurophysiol. [Epub ahead of print].. PMID:18784275.
23. Kamen, G., and Knight, C.A. 2004. Training-related adaptations in motor unit discharge rate in young and older adults. J. Gerontol. A Biol. Sci. Med. Sci. 59(12): 1334-1338. PMID:15699535.
24. Kamen, G., Sison, S.V., Du, C.C., and Patten, C. 1995. Motor unit discharge behavior in older adults during maximal-effort contractions. J. Appl. Physiol. 79(6): 1908-1913. PMID:8847252.
25. Kanda, K., and Hashizume, K. 1989. Changes in properties of the medial gastrocnemius motor units in aging rats. J. Neurophysiol. 61(4): 737-746. PMID:2656932.
26. Kent-Braun, J.A., Ng, A.V., Doyle, J.W., and Towse, T.F. 2002. Human skeletal muscle responses vary with age and gender during fatigue due to incremental isometric exercise. J. Appl. Physiol. 93(5): 1813-1823. PMID:12381770.
27. Kernell, D. 1979. Rhythmic properties of motoneurones innervating muscle fibres of different speed in m. gastrocnemius medialis of the cat. Brain Res. 160(1): 159-162. doi:10.1016/0006-8993(79) 90612-7. PMID:214206.
28. Kernell, D. 1983. Functional properties of spinal motoneurons and gradation of muscle force. Adv. Neurol. 39: 213-226. PMID:6318530.
29. Kernell, D., Eerbeek, O., and Verhey, B.A. 1983. Relation between isometric force and stimulus rate in cat's hindlimb motor units of different twitch contraction time. Exp. Brain Res. 50(2-3): 220-227. PMID:6227493.
30. Klitgaard, H., Zhou, M., Schiaffino, S., Betto, R., Salviati, G., and Saltin, B. 1990. Ageing alters the myosin heavy chain composition of single fibres from human skeletal muscle. Acta Physiol. Scand. 140(1): 55-62 doi:10.1111/j.1748-1716.1990.tb08975.x. PMID:2275405.
31. Knight, C.A., and Kamen, G. 2008. Relationships between voluntary activation and motor unit firing rate during maximal voluntary contractions in young and older adults. Eur. J. Appl. Physiol. 103(6): 625-630. doi:10.1007/s00421-008-0757-z. PMID:18470532.
32. Lanza, I.R., Russ, D.W., and Kent-Braun, J.A. 2004. Age-related enhancement of fatigue resistance is evident in men during both isometric and dynamic tasks. J. Appl. Physiol. 97(3): 967-975. doi:10.1152/japplphysiol.01351.2003. PMID:15145914.
33. Larsson, L., and Karlsson, J. 1978. Isometric and dynamic endurance as a function of age and skeletal muscle characteristics. Acta Physiol. Scand. 104(2): 129-136. doi:10.1111/j.1748-1716.1978.tb06259.x. PMID:152565.
34. Larsson, L., Grimby, G., and Karlsson, J. 1979. Muscle strength and speed of movement in relation to age and muscle morphology. J. Appl. Physiol. 46(3): 451-456. PMID:438011.
35. Larsson, L., Li, X., and Frontera, W.R. 1997. Effects of aging on shortening velocity and myosin isoform composition in single human skeletal muscle cells. Am. J. Physiol. 272(2 Pt 1): C638-C649 PMID:9124308.
36. Lexell, J., and Downham, D. 1992. What is the effect of ageing on type 2 muscle fibres? J. Neurol. Sci. 107(2): 250-251. doi:10.1016/0022-510X(92)90297-X. PMID:1564525.
37. Lexell, J., Henriksson-Larsen, K., Winblad, B., and Sjostrom, M. 1983. Distribution of different fiber types in human skeletal muscles: effects of aging studied in whole muscle cross sections. Muscle Nerve, 6(8): 588-595. doi:10.1002/mus.880060809. PMID:6646161.
38. Lexell, J., Taylor, C.C., and Sjostrom, M. 1988. What is the cause of the ageing atrophy? Total number, size and proportion of different fiber types studied in whole vastus lateralis muscle from 15to 83-year-old men. J. Neurol. Sci. 84(2-3): 275-294. doi:10.1016/0022-510X(88)90132-3. PMID:3379447.
39. Ling, S.M., Conwit, R.A., Talbot, L., Shermack, M., Wood, J.E., Dredge, E.M., et al. 2007. Electromyographic patterns suggest changes in motor unit physiology associated with early osteoarthritis of the knee. Osteoarthritis Cartilage, 15(10): 1134-1140. doi:10.1016/j.joca.2007.03.024. PMID:17543548.
40. Liu, J.Z., Brown, R.W., and Yue, G.H. 2002. A dynamical model of muscle activation, fatigue, and recovery. Biophys. J. 82(5): 2344-2359. doi:10.1016/S0006-3495(02)75580-X. PMID:11964225.
41. Milner-Brown, H.S., Stein, R.B., and Yemm, R. 1973. The orderly recruitment of human motor units during voluntary isometric contractions. J. Physiol. 230(2): 359-370. PMID:4350770.
42. Morales, F.R., Boxer, P.A., Fung, S.J., and Chase, M.H. 1987. Basic electrophysiological properties of spinal cord motoneurons during old age in the cat. J. Neurophysiol. 58(1): 180-194. PMID:3612223.
43. Moritz, C.T., Barry, B.K., Pascoe, M.A., and Enoka, R.M. 2005. Discharge rate variability influences the variation in force fluctuations across the working range of a hand muscle. J. Neurophysiol. 93(5): 2449-2459. doi:10.1152/jn.01122.2004. PMID:15615827.
44. Munson, J.B., Foehring, R.C., Mendell, L.M., and Gordon, T. 1997. Fast-to-slow conversion following chronic low-frequency activation of medial gastrocnemius muscle in cats. II. Motoneuron properties. J. Neurophysiol. 77(5): 2605-2615. PMID:9163379.
45. Nelson, R.M., Soderberg, G.L., and Urbscheit, N.L. 1984. Alteration of motor-unit discharge characteristics in aged humans. Phys. Ther. 64(1): 29-34. PMID:6691051.
46. Perumal, R., Wexler, A.S., and Binder-Macleod, S.A. 2006. Mathematical model that predicts lower leg motion in response to electrical stimulation. J. Biomech. 39(15): 2826-2836. doi:10.1016/j.jbiomech.2005.09.021. PMID:16307749.
47. Pettigrew, F.P., and Gardiner, P.F. 1987. Changes in rat plantaris motor unit profiles with advanced age. Mech. Ageing Dev. 40(3): 243-259. doi:10.1016/0047-6374(87)90022-4. PMID:3431164.
48. Porter, M.M., Vandervoort, A.A., and Lexell, J. 1995. Aging of human muscle: structure, function and adaptability. Scand. J. Med. Sci. Sports, 5(3): 129-142. PMID:7552755.
49. Pucci, A.R., Griffin, L., and Cafarelli, E. 2006. Maximal motor unit firing rates during isometric resistance training in men. Exp. Physiol. 91(1): 171-178. doi:10.1113/expphysiol.2005.032094. PMID:16210447.
50. Roos, M.R., Rice, C.L., and Vandervoort, A.A. 1997. Age-related changes in motor unit function. Muscle Nerve, 20(6): 679-690. doi: 10.1002/(SICI)1097-4598(199706)20:6<679::AID-MUS4>3. 0.CO;2-5. PMID:9149074.
51. Roos, M.R., Rice, C.L., Connelly, D.M., and Vandervoort, A.A. 1999. Quadriceps muscle strength, contractile properties, and motor unit firing rates in young and old men. Muscle Nerve, 22(8): 1094-1103. doi:10.1002/(SICI)1097-4598(199908) 22:8<1094::AID-MUS14>3.0.CO;2-G. PMID:10417793.
52. Roubenoff, R. 2003. Sarcopenia: effects on body composition and function. J. Gerontol. A Biol. Sci. Med. Sci. 58(11): 1012-1017. PMID:14630883.
53. Rubinstein, S., and Kamen, G. 2005. Decreases in motor unit firing rate during sustained maximal-effort contractions in young and older adults. J. Electromyogr. Kinesiol. 15(6): 536-543. doi:10.1016/j.jelekin.2005.04.001. PMID:16054395.
54. Scott, W.B., Lee, S.C., Johnston, T.E., Binkley, J., and Binder-Macleod, S.A. 2006. Contractile properties and the force-frequency relationship of the paralyzed human quadriceps femoris muscle. Phys. Ther. 86(6): 788-799. PMID:16737404.
55. Stalberg, E., Borges, O., Ericsson, M., Essen-Gustavsson, B., Fawcett, P.R., Nordesjo, L.O., et al. 1989. The quadriceps femoris muscle in 20-70-year-old subjects: relationship between knee extension torque, electrophysiological parameters, and muscle fiber characteristics. Muscle Nerve, 12(5): 382-389. doi:10.1002/mus.880120508. PMID:2725565.
56. Stephens, J.A., and Usherwood, T.P. 1977. The mechanical properties of human motor units with special reference to their fatiguability and recruitment threshold. Brain Res. 125(1): 91-97. doi:10.1016/0006-8993(77)90361-4. PMID:851876.
57. Tax, A.A., Denier van der Gon, J.J., Gielen, C.C., and van den Tempel, C.M. 1989. Differences in the activation of m. biceps brachii in the control of slow isotonic movements and isometric contractions. Exp. Brain Res. 76(1): 55-63. doi:10.1007/BF00253623. PMID:2753109.
58. Taylor, A.M., Steege, J.W., and Enoka, R.M. 2002. Motor-unit synchronization alters spike-triggered average force in simulated contractions. J. Neurophysiol. 88(1): 265-276. PMID:12091552.
59. Thelen, D.G. 2003. Adjustment of muscle mechanics model parameters to simulate dynamic contractions in older adults. J. Biomech. Eng. 125(1): 70-77. doi:10.1115/1.1531112. PMID:12661198.
60. Tomlinson, B.E., and Irving, D. 1977. The numbers of limb motor neurons in the human lumbosacral cord throughout life. J. Neurol. Sci. 34(2): 213-219. doi:10.1016/0022-510X(77)90069-7. PMID:925710.
61. Trappe, S., Gallagher, P., Harber, M., Carrithers, J., Fluckey, J., and Trappe, T. 2003. Single muscle fibre contractile properties in young and old men and women. J. Physiol. 552(Pt 1): 47-58 doi:10.1113/jphysiol.2003.044966. PMID:12837929.
62. Troiani, D., Filippi, G.M., and Bassi, F.A. 1999. Nonlinear tension summation of different combinations of motor units in the anesthetized cat peroneus longus muscle. J. Neurophysiol. 81(2): 771-780. PMID:10036276.
63. Van Cutsem, M., Feiereisen, P., Duchateau, J., and Hainaut, K. 1997. Mechanical properties and behaviour of motor units in the tibialis anterior during voluntary contractions. Can. J. Appl. Physiol. 22(6): 585-597. PMID:9415831.
64. Vandervoort, A.A. 2002. Aging of the human neuromuscular system. Muscle Nerve, 25(1): 17-25. doi:10.1002/mus.1215. PMID:11754180.
65. Vandervoort, A.A., and McComas, A.J. 1986. Contractile changes in opposing muscles of the human ankle joint with aging. J. Appl. Physiol. 61(1): 361-367. PMID:3525504.
66. Wexler, A.S., Ding, J., and Binder-Macleod, S.A. 1997. A mathematical model that predicts skeletal muscle force. IEEE Trans. Biomed. Eng. 44(5): 337-348. doi:10.1109/10.568909. PMID:9125818.
67. Young, A., Stokes, M., and Crowe, M. 1985. The size and strength of the quadriceps muscles of old and young men. Clin. Physiol. 5(2): 145-154. doi:10.1111/j.1475-097X.1985.tb00590.x. PMID:3888498.
68. Yu, F., Hedstrom, M., Cristea, A., Dalen, N., and Larsson, L. 2007. Effects of ageing and gender on contractile properties in human skeletal muscle and single fibres. Acta Physiol. (Oxf.), 190(3): 229 241. doi:10.1111/j.1748-1716.2007.01699.x. PMID:17581136.