European Journal of Applied Physiology

, Volume 92, Issue 1–2, pp 219–226 | Cite as

Reduced plantarflexor specific torque in the elderly is associated with a lower activation capacity

  • Christopher I. Morse
  • Jeanette M. Thom
  • Mark G. Davis
  • Ken R. Fox
  • Karen M. Birch
  • Marco V. Narici
Original Article


Previous studies have reported a decrease in muscle torque per cross-sectional area in old age. This investigation aimed at determining the influence of agonists muscle activation and antagonists co-activation on the specific torque of the plantarflexors (PF) in recreationally active elderly males (EM) and, for comparison, in young men (YM). Twenty-one EM, aged 70–82 years, and 14 YM, aged 19–35 years, performed isometric maximum voluntary contractions (MVC). Activation was assessed by comparing the amplitude of interpolated supramaximal twitch doublets at MVC, with post-tetanic doublet peak torque. Co-activation of the tibialis anterior (TA) was evaluated as the ratio of TA-integrated EMG (IEMG) activity during PF MVC compared to TA IEMG during maximal voluntary dorsiflexion. Triceps surae muscle volume (VOL) was assessed using magnetic resonance imaging (MRI), and PF peak torque was normalised to VOL (PT/VOL) since the later approximates physiological cross-sectional area (CSA) more closely than anatomical CSA. Also, physical activity level, assessed by accelerometry, was significantly lower (21%) in the elderly males. In comparison to the YM group, a greater difference in PT (39%) than VOL (19%) was found in the EM group. PT/VOL and activation capacity were respectively lower by 25% and 21% in EM compared to YM, whereas co-activation was not significantly different. In EM PT/VOL correlated with activation (R 2=0.31, P<0.01). In conclusion, a reduction in activation capacity may contribute significantly to the decline in specific torque in the plantar flexors of elderly males. The hypothesis is put forward that reduced physical activity is partialy responsible for the reduced activation capacity in the elderly.


Activation capacity Ageing Coactivation Plantarflexion Specific torque 



Supported by European Commission Framework V funding (‘Better-Ageing’ Project, No. QLRT-2001-00323). The authors wish to thank Dr. G. Onambele, Mr. I.J. Rothwell and Mr. T. McKee for assistance during preparation of this manuscript.


  1. Allen GM, Gandevia SC, McKenzie DK (1995) Reliability of measurements of muscle strength and voluntary activation using twitch interpolation. Muscle Nerve 18:593–600PubMedGoogle Scholar
  2. Behm D, Power K, Drinkwater E (2001) Comparison of interpolation and central activation ratios as measures of muscle inactivation. Muscle Nerve 24:925–934CrossRefPubMedGoogle Scholar
  3. Berg HE, Dudley GA, Haggmark T, Ohlsen H, Tesch PAIDGA (1991) Effects of lower limb unloading on skeletal muscle mass and function in humans. J Appl Physiol 70:1882–1885PubMedGoogle Scholar
  4. Bruce SA, Newton D, Woledge RC (1989) Effect of age on voluntary force and cross-sectional area of human adductor pollicis muscle. Q J Exp Physiol 74:359–362PubMedGoogle Scholar
  5. 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
  6. Carolan B, Cafarelli E (1992) Adaptations in coactivation after isometric resistance training. J Appl Physiol 73:911–917PubMedGoogle Scholar
  7. Connelly DM, Rice CL, Roos MR, Vandervoort AA (1999) Motor unit firing rates and contractile properties in tibialis anterior of young and old men. J Appl Physiol 87:843–852Google Scholar
  8. De Serres SJ, Enoka RM (1998) Older adults can maximally activate the biceps brachii muscle by voluntary command. J Appl Physiol 84:284–291Google Scholar
  9. Delbono O, Renganathan M, Messi ML (1997) Excitation-Ca2+ release-contraction coupling in single aged human skeletal muscle fiber. Muscle Nerve [Suppl] 5: S88–92Google Scholar
  10. Doherty TJ, Vandervoort AA, Taylor AW, Brown WF (1993) Effects of motor unit losses on strength in older men and women. J Appl Physiol 74:868–874PubMedGoogle Scholar
  11. Duchateau J, Enoka RM (2002) Neural adaptations with chronic activity patterns in able-bodied humans. Am J Physiol Med Rehabil 81:S17–27CrossRefGoogle Scholar
  12. Duchateau J, Hainaut K (1987) Electrical and mechanical changes in immobilized human muscle. J Appl Physiol 62:2168–2173PubMedGoogle Scholar
  13. Freedson PS, Melanson E. Sirard J (1998) Calibration of the Computer Science and Applications’ accelerometer. Med Sci Sports Exerc 30:777–781CrossRefPubMedGoogle Scholar
  14. Frontera WR, Suh D, Krivickas LS, Hughes VA, Goldstein R, Roubenoff R (2000) Skeletal muscle fiber quality in older men and women. Am J Physiol 279:C611–C618Google Scholar
  15. Fukunaga T, Roy RR, Shellock FG, Hodgson JA, Edgerton VR (1996) Specific tension of human plantar flexors and dorsiflexors. J Appl Physiol 80:158–165Google Scholar
  16. Fukunaga T, Miyatani M, Tachi M, Kouzaki M, Kawakami Y, Kanehisa H (2001) Muscle volume is a major determinant of joint torque in humans. Acta Physiol Scand 172:249–255CrossRefPubMedGoogle Scholar
  17. Galea V (1996) Changes in motor unit estimates with aging. J Clin Neurophysiol 13:253–260PubMedGoogle Scholar
  18. Gandevia SC, Macefield G, Burke D, McKenzie DK (1990) Voluntary activation of human motor axons in the absence of muscle afferent feedback. The control of the deafferented hand. Brain 113:1563–1581PubMedGoogle Scholar
  19. Harridge SD, Kryger A, Stensgaard A (1999) Knee extensor strength, activation, and size in very elderly people following strength training. Muscle Nerve 22:831–839CrossRefPubMedGoogle Scholar
  20. 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 167:57–68PubMedGoogle Scholar
  21. Jubrias SA, Odderson IR, Esselman PC, Conley KE (1997) Decline in isokinetic force with age: muscle cross-sectional area and specific force. Pflugers Arch 434:246–253CrossRefPubMedGoogle Scholar
  22. Kawakami Y, Akima H, Kubo K, Muraoka Y, Hasegawa H, Kouzaki M, Imai M, Suzuki Y, Gunji A, Kanehisa H, Fukunaga T (2001) Changes in muscle size, architecture, and neural activation after 20 days of bed rest with and without resistance exercise. Eur J Appl Physiol 84:7–12CrossRefPubMedGoogle Scholar
  23. Kent-Braun JA, Le Blanc R (1996) Quantitation of central activation failure during maximal voluntary contractions in humans. Muscle Nerve 19:861–869CrossRefPubMedGoogle Scholar
  24. Kent-Braun JA, Ng AV, Young K (2000) Skeletal muscle contractile and noncontractile components in young and older women and men. J Appl Physiol 88:662–668Google Scholar
  25. 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
  26. Kubo K, Kanehisa H, Azuma K, Ishizu M, Kuno SY, Okada M, Fukunaga T (2003) Muscle architectural characteristics in women aged 20–79 years. Med Sci Sports Exerc 35:39–44CrossRefPubMedGoogle Scholar
  27. Lindle RS, Metter EJ, Lynch NA, Fleg JL, Fozard JL, Tobin J, Roy TA, Hurley BF (1997) Age and gender comparisons of muscle strength in 654 women and men aged 20–93 years. J Appl Physiol 83:1581–1587Google Scholar
  28. Loring SH, Hershenson MB (1992) Effects of series compliance on twitches superimposed on voluntary contractions. J Appl Physiol 73:516–521PubMedGoogle Scholar
  29. Macaluso A, De Vito G, Felici F, Nimmo MA (2000) Electromyogram changes during sustained contraction after resistance training in women in their 3rd and 8th decades. Eur J Appl Physiol 82:418–424Google Scholar
  30. 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 25:858–863CrossRefPubMedGoogle Scholar
  31. Maganaris CN, Baltzopoulos V, Sargeant AJ (1998) Differences in human antagonistic ankle dorsiflexor coactivation between legs; can they explain the moment deficit in the weaker plantarflexor leg? Exp Physiol 83:843–855PubMedGoogle Scholar
  32. Maganaris CN, Baltzopoulos V, Ball D, Sargeant AJ (2001) In vivo specific tension of human skeletal muscle. J Appl Physiol 90:865–872PubMedGoogle Scholar
  33. Magnusson SP, Aagaard P, Dyhre-Poulsen P, Kjaer M (2001) Load-displacement properties of the human triceps surae aponeurosis in vivo. J Physiol (Lond) 531:277–288Google Scholar
  34. Milesi S, Capelli C, Denoth J, Hutchinson T, Stussi E (2000) Effects of 17 days bedrest on the maximal voluntary isometric torque and neuromuscular activation of the plantar and dorsal flexors of the ankle. Eur J Appl Physiol 82:197–205Google Scholar
  35. Narici MV, Maganaris CN, Reeves ND, Capodaglio P (2003) Effect of aging on human muscle architecture. J Appl Physiol 95:2229–2234CrossRefPubMedGoogle Scholar
  36. Narici M, Landoni L, Minetti A (1992) Assessment of human knee extensor muscles stress from in vivo physiological cross-sectional area and strength measurements. Eur J Appl Physiol 65:438–444Google Scholar
  37. Narici MV, Maganaris CN, Reeves N (2002) Muscle and tendon adaptations to ageing and spaceflight. J Gravit Physiol 9:137-138Google Scholar
  38. Pearson SJ, Young A, Macaluso A, Devito G, Nimmo MA, Cobbold M, Harridge SD (2002) Muscle function in elite master weightlifters. Med Sci Sports Exerc 34:1199–1206Google Scholar
  39. Roos MR, Rice CL, Connelly DM, Vandervoort AA (1999) Quadriceps muscle strength, contractile properties, and motor unit firing rates in young and old men. Muscle Nerve 22:1094–1103CrossRefPubMedGoogle Scholar
  40. Scaglioni G, Ferri A, Minetti AE, Martin A, Van Hoecke J, Capodaglio P, Sartorio A, Narici MV (2002) Plantar flexor activation capacity and H reflex in older adults: adaptations to strength training. J Appl Physiol 92:2292–2302Google Scholar
  41. Stevens J, Binder-Macleod S, Snyder-Mackler L (2001) Characterization of the human quadriceps muscle in active elders. Arch Phys Med Rehabil 82:973–978CrossRefPubMedGoogle Scholar
  42. Stevens JE, Stackhouse SK, Binder-Macleod SA, Snyder-Mackler L (2003) Are voluntary muscle activation deficits in older adults meaningful? Muscle Nerve 27:99–101CrossRefPubMedGoogle Scholar
  43. Thom JM, Thompson MW, Ruell PA, Bryant GJ, Fonda JS, Harmer AR, De Jonge XA, Hunter SK (2001) Effect of 10-day cast immobilization on sarcoplasmic reticulum calcium regulation in humans. Acta Physiol Scand 172:141–147CrossRefPubMedGoogle Scholar
  44. Urbanchek MG, Picken EB, Kalliainen LK, Kuzon WM Jr (2001) Specific force deficit in skeletal muscles of old rats is partially explained by the existence of denervated muscle fibers. J Gerontol A 56: B191–197Google Scholar
  45. Vandervoort AA, McComas AJ (1986) Contractile changes in opposing muscles of the human ankle joint with aging. J Appl Physiol 61:361–367Google Scholar
  46. Young A, Stokes M, Crowe M (1985) The size and strength of the quadriceps muscles of old and young men. Clin Physiol 5:145–154PubMedGoogle Scholar
  47. Yue GH, Ranganathan VK, Siemionow V, Liu JZ, Sahgal V (1999) Older adults exhibit a reduced ability to fully activate their biceps brachii muscle. J Gerontol A 54: M249–253Google Scholar

Copyright information

© Springer-Verlag 2004

Authors and Affiliations

  • Christopher I. Morse
    • 1
  • Jeanette M. Thom
    • 1
  • Mark G. Davis
    • 3
  • Ken R. Fox
    • 3
  • Karen M. Birch
    • 2
  • Marco V. Narici
    • 1
  1. 1.Centre for Biophysical and Clinical Research into Human Movement (CRM)Manchester Metropolitan UniversityAlsager UK
  2. 2.University of Leeds Institute of Sport and Exercise ScienceUniversity of LeedsLeeds UK
  3. 3.Department of Exercise and Health Sciences, Centre for Sport, Exercise and HealthUniversity of BristolBristol UK

Personalised recommendations