European Journal of Applied Physiology

, Volume 100, Issue 5, pp 543–551 | Cite as

Voluntary activation during maximal contraction with advancing age: a brief review

  • Malgorzata Klass
  • Stéphane Baudry
  • Jacques Duchateau
Original Article

Abstract

It is well established that the loss of muscle mass (i.e. sarcopenia) is the primary factor contributing to the reduction in muscle force with ageing. Based on the observation that force declines at a faster rate than muscle mass, neural alterations are also thought to contribute to muscle weakness by reducing central drive to the agonist muscles and by increasing coactivation of the antagonist muscles. Researchers have attempted to quantify the contribution of impaired voluntary drive to the decline in muscle force using superimposed electrical stimulation during maximal voluntary contractions (MVCs) and by recording surface electromyographic (EMG) activity. Although reduced voluntary activation of agonist muscles and increased coactivation of antagonist muscles during a MVC have been reported with advancing age, such changes are not supported by all studies. These discrepancies may be explained by differences in sensitivity between the methods used to assess voluntary activation, as well as differences between the characteristics of the study population, the muscle group that is tested, and the type of contraction that is performed. The objective of this review is to summarize current knowledge regarding the activation of agonist and antagonist muscles during MVC in elderly and to try to clarify the disparities in literature concerning the influence of a possible deficit in voluntary activation on the maximal force capacity of muscles in elderly adults.

Keywords

Ageing Voluntary activation Antagonist coactivation Motor units Electromyography 

Notes

Acknowledgments

The authors are particularly grateful to Dr K. Maluf for useful comments on the paper and to A. Desseir for assistance in the preparation of the manuscript. Some experiments described in this review were performed with support from a grant of the European Community (contract QLK6-CT-2001-00323) and the Fonds National de la Recherche Scientifique of Belgium.

References

  1. Aagaard P, Simonsen EB, Andersen JL, Magnusson P, Dyhre-Poulsen P (2002) Increased rate of force development and neural drive of human skeletal muscle following resistance training. J Appl Physiol 93:1318–1326PubMedGoogle Scholar
  2. Allen GM, McKenzie DK, Gandevia SC (1998) Twitch interpolation of the elbow flexor muscles at high forces. Muscle Nerve 21:318–328PubMedCrossRefGoogle Scholar
  3. Baratta R, Solomonow M, Zhou M, Letson D, D’Ambrosia R (1988) Muscular coactivation. The role of antagonist musculature in maintaining knee joint stability. Am J Sports Med 16:113–122PubMedCrossRefGoogle Scholar
  4. Baudry S, Klass M, Duchateau J (2005) Post-activation potentiation influences differently the nonlinear summation of contractions in young and elderly adults. J Appl Physiol 98:1243–1250PubMedCrossRefGoogle Scholar
  5. Behm DG, St-Pierre DMM, Perez D (1996) Muscle inactivation: assessment of interpolated twitch technique. J Appl Physiol 81:2267–2273PubMedGoogle Scholar
  6. Behm D, Power K, Drinkwater E (2001) Comparison of interpolation and central activation ratios as measures of muscle inactivation. Muscle Nerve 24:925–934PubMedCrossRefGoogle Scholar
  7. Belanger AY, McComas AJ (1981) Extent of motor unit activation during effort. J Appl Physiol 51:1131–1135PubMedGoogle Scholar
  8. Bigland-Ritchie B, Johansson R, Lippold OC, Woods JJ (1983) Contractile speed and EMG changes during fatigue of sustained maximal voluntary contractions. J Neurophysiol 50:313–324PubMedGoogle Scholar
  9. Bilodeau M, Erb MD, Nichols JM, Joiner KL, Weeks J (2001) Fatigue of elbow flexor muscles in younger and older adults. Muscle Nerve 24:98–106PubMedCrossRefGoogle Scholar
  10. Burnett RA, Laidlaw DH, Enoka RM (2000) Coactivation of the antagonist muscle does not covary with steadiness in old adults. J Appl Physiol 89:61–71PubMedGoogle Scholar
  11. Campbell MJ, McComas AJ, Petito F (1973) Physiological changes in ageing muscles. J Neurol Neurosurg Psychiatry 36:174–182PubMedCrossRefGoogle Scholar
  12. Carolan B, Cafarelli E (1992) Adaptations in coactivation after isometric resistance training. J Appl Physiol 73:911–917PubMedGoogle Scholar
  13. Chan KM, Doherty TJ, Brown WF (2001) Contractile properties of human motor units in health, aging, and disease. Muscle Nerve 24:1113–1133PubMedCrossRefGoogle Scholar
  14. Connelly DM, Rice CL, Roos MR, Vandervoort AA (1999) Motor unit firing rate and contractile properties in tibialis anterior of young and old men. J Appl Physiol 87:843–852PubMedGoogle Scholar
  15. Crone C, Nielsen J (1989) Spinal mechanisms in man contributing to reciprocal inhibition during voluntary dorsiflexion of the foot. J Physiol 416:255–272PubMedGoogle Scholar
  16. D’Antona G, Pellegrino MA, Adami R, Rossi R, Carlizzi CN, Canepari M, Saltin B, Bottinelli R (2003) The effect of ageing and immobilization on structure and function of human skeletal muscle fibres. J Physiol 552:499–511PubMedCrossRefGoogle Scholar
  17. De Serres SJ, Enoka RM (1998) Older adults can maximally activate the biceps brachii muscle by voluntary command. J Appl Physiol 84:284–291PubMedCrossRefGoogle Scholar
  18. Doherty TJ, Brown WF (1993) The estimated numbers and relative sizes of thenar motor units as selected by multiple point stimulation in young and older adults. Muscle Nerve 16:355–366PubMedCrossRefGoogle Scholar
  19. Doherty TJ, Brown WF (1997) Age-related changes in the twitch contractile properties of human thenar motor units. J Appl Physiol 82:93–101PubMedGoogle Scholar
  20. Eisen A, Siejka S, Schulzer M, Calne D (1991) Age-dependent decline in motor evoked potential (MEP) amplitude: with a comment on changes in Parkinson’s disease. Electroencephalogr Clin Neurophysiol 81:209–215PubMedCrossRefGoogle Scholar
  21. Esposito F, Malgrati D, Veicsteinas A, Orizio C (1996) Time and frequency domain analysis of electromyogram and sound myogram in the elderly. Eur J Appl Physiol 73:503–510Google Scholar
  22. Farina D, Merletti R, Enoka R (2004) The extraction of neural strategies from the surface EMG. J Appl Physiol 96:1486–1495PubMedCrossRefGoogle Scholar
  23. Frontera WR, Hughes VA, Lutz KJ, Evans WJ (1991) A cross-sectional study of muscle strength and mass in 45- to 78-yr-old men and women. J Appl Physiol 71:644–650PubMedGoogle Scholar
  24. Galganski ME, Fuglevand AJ, Enoka RM (1993) Reduced control of motor output in a human hand muscle of elderly subjects during submaximal contractions. J Neurophysiol 69:2108–2115PubMedGoogle Scholar
  25. Hakkinen K, Alen M, Kallinen M, Izquierdo M, Jokelainen K, Lassila H, Mälkiä E, Kraemer WJ, Newton RU (1998) Muscle CSA, force production, and activation of leg extensors during isometric and dynamic actions in middle-aged and elderly men and women. J Aging Phys Act 6:232–247Google Scholar
  26. Harridge SDR, White MJ (1993) A comparison of voluntary and electrically evoked isokinetic plantar flexor torque in males. Eur J Appl Physiol 66:343–348CrossRefGoogle Scholar
  27. Harridge SDR, Kryger A, Stensgaard A (1999) Knee extensor strength, activation, and size in very elderly people following strength training. Muscle Nerve 22:831–839PubMedCrossRefGoogle Scholar
  28. Herbert RD, Gandevia SC (1999) Twitch interpolation in human muscles: mechanisms and implications for measurement of voluntary activation. J Neurophysiol 82:2271–2283PubMedGoogle Scholar
  29. Höök P, Sriramoju V, Larsson L (2001) Effects of aging on actin sliding speed on myosin from single skeletal muscle cells of mice, rats, and humans. Am J Physiol 280:C782–C788Google Scholar
  30. Hunter SK, Thompson MW, Ruell PA, Harmer AR, Thom JM, Gwinn TH, Adams RD (1999) Human skeletal sarcoplasmic reticulum Ca²+ uptake and muscle function with aging and strength training. J Appl Physiol 86:1858–1865PubMedGoogle Scholar
  31. Hurley MV, Newham DJ (1993) The influence of arthrogenous muscle inhibition on quadriceps rehabilitation of patients with early, unilateral osteoarthritic knees. Br J Rheumatol 32:127–131PubMedCrossRefGoogle Scholar
  32. Izquierdo M, Ibanez J, Gorostiaga E, Garrues M, Zuniga A, Anton A, Larrion JL, Hakkinen K (1999) 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 167:57–68PubMedCrossRefGoogle Scholar
  33. Jakobi JM, Rice CL (2002) Voluntary muscle activation varies with age and muscle group. J Appl Physiol 93:457–462PubMedGoogle Scholar
  34. Kamen G, Sison SV, Du CC, Patten C (1995) Motor unit discharge behavior in older adults during maximal-effort contractions. J Appl Physiol 79:1908–1913PubMedGoogle Scholar
  35. Keenan KG, Farina D, Maluf KS, Merletti R, Enoka RM (2005) Influence of amplitude cancellation on the simulated surface electromyogram. J Appl Physiol 98:120–131PubMedCrossRefGoogle Scholar
  36. Kellis E (1998) Quantification of quadriceps and hamstring antagonist activity. Sports Med 25:37–62PubMedCrossRefGoogle Scholar
  37. Kent-Braun JA, Le Blanc R (1996) Quantitation of central activation failure during maximal voluntary contractions in humans. Muscle Nerve 19:861–869PubMedCrossRefGoogle Scholar
  38. Kent-Braun JA, Ng AV (1999) Specific strength and voluntary muscle activation in young and elderly women and men. J Appl Physiol 87:22–29PubMedGoogle Scholar
  39. Kent-Braun JA, Ng AV, Doyle JW, Towse TF (2002) Human skeletal muscle responses vary with age and gender during fatigue due to incremental isometric exercise. J Appl Physiol 93:1813–1823PubMedGoogle Scholar
  40. Klass M, Baudry S, Duchateau J (2005a) Aging does not affect voluntary activation of the ankle dorsiflexors during isometric, concentric, and eccentric contractions. J Appl Physiol 99:31–38CrossRefGoogle Scholar
  41. Klass M, Baudry S, Duchateau J (2005b) Contractile properties of single motor units in elderly. Comput Methods Biomech Biomed Engin (Suppl. 1):167–168Google Scholar
  42. Klein CS, Rice CL, Marsh GD (2001) Normalized force, activation, and coactivation in the arm muscles of young and old men. J Appl Physiol 91:1341–1349PubMedGoogle Scholar
  43. Lanza IR, Russ DW, Kent-Braun JA (2004) Age-related enhancement of fatigue resistance is evident in men during both isometric and dynamic tasks. J Appl Physiol 97:967–975PubMedCrossRefGoogle Scholar
  44. Lexell J (1993) Ageing and human muscle: observations from Sweden. Can J Appl Physiol 18:2–18PubMedGoogle Scholar
  45. Macaluso A, De Vito G (2004) Muscle strength, power and adaptations to resistant training in older people. Eur J Appl Physiol 91:450–472PubMedCrossRefGoogle Scholar
  46. Macaluso A, Nimmo MA, Foster JE, Cockburn M, McMillan NC, De Vito G (2002) Contractile muscle volume and agonist-antagonist coactivation account for differences in torque between young and older women. Muscle Nerve 25:858–863PubMedCrossRefGoogle Scholar
  47. Masakado Y, Noda Y, Nagata MA, Kimura A, Chino N, Akaboshi K (1994) Macro-EMG and motor unit recruitment threshold: differences between the young and the aged. Neurosci Lett 179:1–4PubMedCrossRefGoogle Scholar
  48. McNeil CJ, Doherty TJ, Stashuk DW, Rice CL (2005) Motor unit number estimates in the tibialis anterior muscle of young, old, and very old men. Muscle Nerve 31:461–467PubMedCrossRefGoogle Scholar
  49. Merton PA (1954) Voluntary strength and muscle fatigue. J Physiol 123:553–564PubMedGoogle Scholar
  50. Miller M, Downham D, Lexell J (1999) Superimposed single impulse and pulse train electrical stimulation: a quantitative assessment during submaximal isometric knee extension in young, healthy men. Muscle Nerve 22:1038–1046PubMedCrossRefGoogle Scholar
  51. Morse CI, Thom JM, Davis MG, Fox KR, Birch KM, Narici MV (2004) Reduced plantarflexor specific torque in the elderly is associated with a lower activation capacity. Eur J Appl Physiol 92:219–226PubMedCrossRefGoogle Scholar
  52. Morse CI, Thom JM, Birch KM, Narici MV (2005) Tendon elongation influences the amplitude of interpolated doublets in the assessment of activation in elderly men. J Appl Physiol 98:221–226PubMedCrossRefGoogle Scholar
  53. Narici MV, Maganaris CN (2006) Adaptability of elderly human muscles and tendons to increased loading. J Anat 208:433–443PubMedCrossRefGoogle Scholar
  54. Narici MV, Maganaris CN, Reeves N (2002) Muscle and tendon adaptations to ageing and spaceflight. J Gravit Physiol 9:137–138Google Scholar
  55. Ochala J, Lambertz D, Pousson M, Goubel F, Van Hoecke J (2004) Changes in mechanical properties of human flexor muscles in ageing. Exp Gerontol 39:349–358PubMedCrossRefGoogle Scholar
  56. Payne AM, Delbono O (2004) Neurogenesis of excitation–contraction uncoupling in aging skeletal muscle. Exerc Sport Sci Rev 32:36–40PubMedCrossRefGoogle Scholar
  57. Philipps SK, Bruce SA, Newton D, Woledge RC (1992) The weakness of old age is not due to failure of muscle activation. J Gerontol 47A:M45–M49Google Scholar
  58. Pitcher JB, Ogston KM, Miles TS (2003) Age and sex differences in human motor cortex input–output characteristics. J Physiol 546:605–613PubMedCrossRefGoogle Scholar
  59. Porter MM, Vandervoort AA, Kramer JF (1997) Eccentric peak torque of the plantar and dorsiflexors is maintained in older women. J Gerontol 52:B125–B131Google Scholar
  60. Pousson M, Lepers R, Van Hoeck J (2001) Changes in isokinetic torque and muscular activity of elbow flexors muscles with age. Exp Gerontol 36:1687–1698PubMedCrossRefGoogle Scholar
  61. Roos MR, Rice CL, Vandervoort AA (1997) Age-related changes in motor unit function. Muscle Nerve 20:679–690PubMedCrossRefGoogle Scholar
  62. Roos MR, Rice CL, Connelly DM, Vandervoort AA (1999) Quadriceps muscle strength, contractile properties, and motor units firing rates in young and old men. Muscle Nerve 22:1094–1103PubMedCrossRefGoogle Scholar
  63. Semmler JG, Steege JW, Kornatz KW, Enoka RM (2000) Motor-unit synchronization is not responsible for lager motor-unit forces in old adults. J Neurophysiol 84:358–366PubMedGoogle Scholar
  64. Simoneau E, Martin A, Van Hoecke J (2005) Muscular performances at the ankle joint in young and elderly men. J Gerontol 60A:439–447Google Scholar
  65. Stackhouse SK, Stevens JE, Lee SCK, Pearce KM, Snyder-Mackler L, Binder-Macleod SA (2001) Maximum voluntary activation in nonfatigued and fatigued muscle of young and elderly individuals. Phys Ther 81:1102–1109PubMedGoogle Scholar
  66. Stevens JE, Binder-Masleod S, Snyder-Mackler L (2001) Characterization of the human quadriceps muscle in active elders. Arch Phys Med Rehabil 82:973–978PubMedCrossRefGoogle Scholar
  67. Stevens JE, Stackhouse SK, Binder-Macleod SA, Snyder-Mackler L (2003) Are voluntary muscle activation deficits in older adults meaningful? Muscle Nerve 27:99–101PubMedCrossRefGoogle Scholar
  68. Thomas DO, White MJ, Sagar G, Davies CT (1987) Electrically evoked isokinetic plantar flexor torque in males. J Appl Physiol 63:1499–1503PubMedGoogle Scholar
  69. Valkeinen H, Ylinen J, Malkia E, Alen M, Hakkinen K (2002) Maximal force, force/time and activation/coactivation characteristics of the neck muscles in extension and flexion in healthy men and women at different ages. Eur J Appl Physiol 88:247–254PubMedCrossRefGoogle Scholar
  70. Van Cutsem M, Duchateau J (2005) Preceding muscle activity influences motor unit discharge and rate of torque development during ballistic contractions in humans. J Physiol 15:635–644Google Scholar
  71. Vandervoort AA, McComas AJ (1986) Contractile changes in opposing muscles of the human ankle joint with aging. J Appl Physiol 61:361–367PubMedGoogle Scholar
  72. Vandervoort AA, Kramer JF, Wharram ER (1990) Eccentric knee strength of elderly females. J Gerontol 45:B125–B128PubMedGoogle Scholar
  73. Wang F-C, De Pasqua V, Delwaide PJ (1999) Age-related changes in fastest and slowest conducting axons of thenar motor units. Muscle Nerve 22:1022–1029PubMedCrossRefGoogle Scholar
  74. White MJ, Harridge SDR (1990) At high angular velocities voluntary activation limits maximal isokinetic torque generation in elderly and young human triceps surae. J Physiol 429:52PGoogle Scholar
  75. Winegard KJ, Hicks AL, Vandervoort AA (1997) An evaluation of the length–tension relationship in elderly human plantarflexor muscles. J Gerontol A Biol Sci Med Sci 52:B337–B343PubMedGoogle Scholar
  76. Yue GH, Ranganathan VK, Siemionov V, Liu JZ, Sahgal V (1999) Older adults exhibit a reduced ability to fully activate their biceps brachii muscle. J Gerontol 54A:249–253Google Scholar

Copyright information

© Springer-Verlag 2006

Authors and Affiliations

  • Malgorzata Klass
    • 1
  • Stéphane Baudry
    • 1
  • Jacques Duchateau
    • 1
  1. 1.Laboratory of Applied BiologyUniversité Libre de BruxellesBrusselsBelgium

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