Skip to main content
Top
Published in: European Journal of Applied Physiology 1-2/2004

01-06-2004 | Original Article

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

Authors: Christopher I. Morse, Jeanette M. Thom, Mark G. Davis, Ken R. Fox, Karen M. Birch, Marco V. Narici

Published in: European Journal of Applied Physiology | Issue 1-2/2004

Login to get access

Abstract

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.
Literature
go back to reference Allen GM, Gandevia SC, McKenzie DK (1995) Reliability of measurements of muscle strength and voluntary activation using twitch interpolation. Muscle Nerve 18:593–600PubMed Allen GM, Gandevia SC, McKenzie DK (1995) Reliability of measurements of muscle strength and voluntary activation using twitch interpolation. Muscle Nerve 18:593–600PubMed
go back to reference Behm D, Power K, Drinkwater E (2001) Comparison of interpolation and central activation ratios as measures of muscle inactivation. Muscle Nerve 24:925–934CrossRefPubMed Behm D, Power K, Drinkwater E (2001) Comparison of interpolation and central activation ratios as measures of muscle inactivation. Muscle Nerve 24:925–934CrossRefPubMed
go back to reference 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 70:1882–1885PubMed 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 70:1882–1885PubMed
go back to reference 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 74:359–362PubMed 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 74:359–362PubMed
go back to reference Burnett RA, Laidlaw DH, Enoka RM (2000) Coactivation of the antagonist muscle does not covary with steadiness in old adults. J Appl Physiol 89:61–71PubMed Burnett RA, Laidlaw DH, Enoka RM (2000) Coactivation of the antagonist muscle does not covary with steadiness in old adults. J Appl Physiol 89:61–71PubMed
go back to reference Carolan B, Cafarelli E (1992) Adaptations in coactivation after isometric resistance training. J Appl Physiol 73:911–917PubMed Carolan B, Cafarelli E (1992) Adaptations in coactivation after isometric resistance training. J Appl Physiol 73:911–917PubMed
go back to reference 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 87:843–852 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 87:843–852
go back to reference De Serres SJ, Enoka RM (1998) Older adults can maximally activate the biceps brachii muscle by voluntary command. J Appl Physiol 84:284–291 De Serres SJ, Enoka RM (1998) Older adults can maximally activate the biceps brachii muscle by voluntary command. J Appl Physiol 84:284–291
go back to reference Delbono O, Renganathan M, Messi ML (1997) Excitation-Ca2+ release-contraction coupling in single aged human skeletal muscle fiber. Muscle Nerve [Suppl] 5: S88–92 Delbono O, Renganathan M, Messi ML (1997) Excitation-Ca2+ release-contraction coupling in single aged human skeletal muscle fiber. Muscle Nerve [Suppl] 5: S88–92
go back to reference Doherty TJ, Vandervoort AA, Taylor AW, Brown WF (1993) Effects of motor unit losses on strength in older men and women. J Appl Physiol 74:868–874PubMed Doherty TJ, Vandervoort AA, Taylor AW, Brown WF (1993) Effects of motor unit losses on strength in older men and women. J Appl Physiol 74:868–874PubMed
go back to reference Duchateau J, Enoka RM (2002) Neural adaptations with chronic activity patterns in able-bodied humans. Am J Physiol Med Rehabil 81:S17–27CrossRef Duchateau J, Enoka RM (2002) Neural adaptations with chronic activity patterns in able-bodied humans. Am J Physiol Med Rehabil 81:S17–27CrossRef
go back to reference Duchateau J, Hainaut K (1987) Electrical and mechanical changes in immobilized human muscle. J Appl Physiol 62:2168–2173PubMed Duchateau J, Hainaut K (1987) Electrical and mechanical changes in immobilized human muscle. J Appl Physiol 62:2168–2173PubMed
go back to reference Freedson PS, Melanson E. Sirard J (1998) Calibration of the Computer Science and Applications’ accelerometer. Med Sci Sports Exerc 30:777–781CrossRefPubMed Freedson PS, Melanson E. Sirard J (1998) Calibration of the Computer Science and Applications’ accelerometer. Med Sci Sports Exerc 30:777–781CrossRefPubMed
go back to reference 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–C618 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–C618
go back to reference Fukunaga T, Roy RR, Shellock FG, Hodgson JA, Edgerton VR (1996) Specific tension of human plantar flexors and dorsiflexors. J Appl Physiol 80:158–165 Fukunaga T, Roy RR, Shellock FG, Hodgson JA, Edgerton VR (1996) Specific tension of human plantar flexors and dorsiflexors. J Appl Physiol 80:158–165
go back to reference 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 172:249–255CrossRefPubMed 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 172:249–255CrossRefPubMed
go back to reference Galea V (1996) Changes in motor unit estimates with aging. J Clin Neurophysiol 13:253–260PubMed Galea V (1996) Changes in motor unit estimates with aging. J Clin Neurophysiol 13:253–260PubMed
go back to reference 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 113:1563–1581PubMed 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 113:1563–1581PubMed
go back to reference Harridge SD, Kryger A, Stensgaard A (1999) Knee extensor strength, activation, and size in very elderly people following strength training. Muscle Nerve 22:831–839CrossRefPubMed Harridge SD, Kryger A, Stensgaard A (1999) Knee extensor strength, activation, and size in very elderly people following strength training. Muscle Nerve 22:831–839CrossRefPubMed
go back to reference 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 167:57–68PubMed 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 167:57–68PubMed
go back to reference Jubrias SA, Odderson IR, Esselman PC, Conley KE (1997) Decline in isokinetic force with age: muscle cross-sectional area and specific force. Pflugers Arch 434:246–253CrossRefPubMed Jubrias SA, Odderson IR, Esselman PC, Conley KE (1997) Decline in isokinetic force with age: muscle cross-sectional area and specific force. Pflugers Arch 434:246–253CrossRefPubMed
go back to reference 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 84:7–12CrossRefPubMed 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 84:7–12CrossRefPubMed
go back to reference Kent-Braun JA, Le Blanc R (1996) Quantitation of central activation failure during maximal voluntary contractions in humans. Muscle Nerve 19:861–869CrossRefPubMed Kent-Braun JA, Le Blanc R (1996) Quantitation of central activation failure during maximal voluntary contractions in humans. Muscle Nerve 19:861–869CrossRefPubMed
go back to reference Kent-Braun JA, Ng AV, Young K (2000) Skeletal muscle contractile and noncontractile components in young and older women and men. J Appl Physiol 88:662–668 Kent-Braun JA, Ng AV, Young K (2000) Skeletal muscle contractile and noncontractile components in young and older women and men. J Appl Physiol 88:662–668
go back to reference Klein CS, Rice CL, Marsh GD (2001) Normalized force, activation, and coactivation in the arm muscles of young and old men. J Appl Physiol 91:1341–1349PubMed Klein CS, Rice CL, Marsh GD (2001) Normalized force, activation, and coactivation in the arm muscles of young and old men. J Appl Physiol 91:1341–1349PubMed
go back to reference 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 35:39–44CrossRefPubMed 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 35:39–44CrossRefPubMed
go back to reference 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 83:1581–1587 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 83:1581–1587
go back to reference Loring SH, Hershenson MB (1992) Effects of series compliance on twitches superimposed on voluntary contractions. J Appl Physiol 73:516–521PubMed Loring SH, Hershenson MB (1992) Effects of series compliance on twitches superimposed on voluntary contractions. J Appl Physiol 73:516–521PubMed
go back to reference 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 82:418–424 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 82:418–424
go back to reference 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 25:858–863CrossRefPubMed 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 25:858–863CrossRefPubMed
go back to reference 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 83:843–855PubMed 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 83:843–855PubMed
go back to reference Maganaris CN, Baltzopoulos V, Ball D, Sargeant AJ (2001) In vivo specific tension of human skeletal muscle. J Appl Physiol 90:865–872PubMed Maganaris CN, Baltzopoulos V, Ball D, Sargeant AJ (2001) In vivo specific tension of human skeletal muscle. J Appl Physiol 90:865–872PubMed
go back to reference Magnusson SP, Aagaard P, Dyhre-Poulsen P, Kjaer M (2001) Load-displacement properties of the human triceps surae aponeurosis in vivo. J Physiol (Lond) 531:277–288 Magnusson SP, Aagaard P, Dyhre-Poulsen P, Kjaer M (2001) Load-displacement properties of the human triceps surae aponeurosis in vivo. J Physiol (Lond) 531:277–288
go back to reference 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 82:197–205 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 82:197–205
go back to reference Narici MV, Maganaris CN, Reeves ND, Capodaglio P (2003) Effect of aging on human muscle architecture. J Appl Physiol 95:2229–2234CrossRefPubMed Narici MV, Maganaris CN, Reeves ND, Capodaglio P (2003) Effect of aging on human muscle architecture. J Appl Physiol 95:2229–2234CrossRefPubMed
go back to reference 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 65:438–444 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 65:438–444
go back to reference Narici MV, Maganaris CN, Reeves N (2002) Muscle and tendon adaptations to ageing and spaceflight. J Gravit Physiol 9:137-138 Narici MV, Maganaris CN, Reeves N (2002) Muscle and tendon adaptations to ageing and spaceflight. J Gravit Physiol 9:137-138
go back to reference 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 34:1199–1206 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 34:1199–1206
go back to reference 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 22:1094–1103CrossRefPubMed 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 22:1094–1103CrossRefPubMed
go back to reference 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 92:2292–2302 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 92:2292–2302
go back to reference Stevens J, Binder-Macleod S, Snyder-Mackler L (2001) Characterization of the human quadriceps muscle in active elders. Arch Phys Med Rehabil 82:973–978CrossRefPubMed Stevens J, Binder-Macleod S, Snyder-Mackler L (2001) Characterization of the human quadriceps muscle in active elders. Arch Phys Med Rehabil 82:973–978CrossRefPubMed
go back to reference Stevens JE, Stackhouse SK, Binder-Macleod SA, Snyder-Mackler L (2003) Are voluntary muscle activation deficits in older adults meaningful? Muscle Nerve 27:99–101CrossRefPubMed Stevens JE, Stackhouse SK, Binder-Macleod SA, Snyder-Mackler L (2003) Are voluntary muscle activation deficits in older adults meaningful? Muscle Nerve 27:99–101CrossRefPubMed
go back to reference 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 172:141–147CrossRefPubMed 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 172:141–147CrossRefPubMed
go back to reference 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: B191–197 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: B191–197
go back to reference Vandervoort AA, McComas AJ (1986) Contractile changes in opposing muscles of the human ankle joint with aging. J Appl Physiol 61:361–367 Vandervoort AA, McComas AJ (1986) Contractile changes in opposing muscles of the human ankle joint with aging. J Appl Physiol 61:361–367
go back to reference Young A, Stokes M, Crowe M (1985) The size and strength of the quadriceps muscles of old and young men. Clin Physiol 5:145–154PubMed Young A, Stokes M, Crowe M (1985) The size and strength of the quadriceps muscles of old and young men. Clin Physiol 5:145–154PubMed
go back to reference 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: M249–253 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: M249–253
Metadata
Title
Reduced plantarflexor specific torque in the elderly is associated with a lower activation capacity
Authors
Christopher I. Morse
Jeanette M. Thom
Mark G. Davis
Ken R. Fox
Karen M. Birch
Marco V. Narici
Publication date
01-06-2004
Publisher
Springer-Verlag
Published in
European Journal of Applied Physiology / Issue 1-2/2004
Print ISSN: 1439-6319
Electronic ISSN: 1439-6327
DOI
https://doi.org/10.1007/s00421-004-1056-y

Other articles of this Issue 1-2/2004

European Journal of Applied Physiology 1-2/2004 Go to the issue