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Published in: European Journal of Applied Physiology 12/2017

01-12-2017 | Original Article

Voluntary activation and variability during maximal dynamic contractions with aging

Authors: Vianney Rozand, Jonathon W. Senefeld, Hamidollah Hassanlouei, Sandra K. Hunter

Published in: European Journal of Applied Physiology | Issue 12/2017

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Abstract

Whether reduced supraspinal activation contributes to age-related reductions in maximal torque during dynamic contractions is not known. The purpose was to determine whether there are age differences in voluntary activation and its variability when assessed with stimulation at the motor cortex and the muscle during maximal isometric, concentric, and eccentric contractions. Thirty young (23.6 ± 4.1 years) and 31 old (69.0 ± 5.2 years) adults performed maximal isometric, shortening (concentric) and lengthening (eccentric) contractions with the elbow flexor muscles. Maximal isometric contractions were performed at 90° elbow flexion and dynamic contractions at a velocity of 60°/s. Voluntary activation was assessed by superimposing an evoked contraction with transcranial magnetic stimulation (TMS) or with electrical stimulation over the muscle during maximal voluntary contractions (MVCs). Old adults had lower MVC torque during isometric (− 17.9%), concentric (− 19.7%), and eccentric (− 9.9%) contractions than young adults, with less of an age difference for eccentric contractions. Voluntary activation was similar between the three contraction types when assessed with TMS and electrical stimulation, with no age group differences. Old adults, however, were more variable in voluntary activation than young (standard deviation 0.99 ± 0.47% vs. 0.73 ± 0.43%, respectively) to both the motor cortex and muscle, and had greater coactivation of the antagonist muscles during dynamic contractions. Thus, the average voluntary activation to the motor cortex and muscle did not differ with aging; however, supraspinal activation was more variable during maximal dynamic and isometric contractions in the old adults. Lower predictability of voluntary activation may indicate subclinical changes in the central nervous system with advanced aging.
Literature
go back to reference Babault N, Pousson M, Ballay Y, Van Hoecke J (2001) Activation of human quadriceps femoris during isometric, concentric, and eccentric contractions. J Appl Physiol 91:2628–2634CrossRefPubMed Babault N, Pousson M, Ballay Y, Van Hoecke J (2001) Activation of human quadriceps femoris during isometric, concentric, and eccentric contractions. J Appl Physiol 91:2628–2634CrossRefPubMed
go back to reference Belanger AY, McComas AJ (1981) Extent of motor unit activation during effort. J Appl Physiol 51:1131–1135CrossRefPubMed Belanger AY, McComas AJ (1981) Extent of motor unit activation during effort. J Appl Physiol 51:1131–1135CrossRefPubMed
go back to reference Burnett R a, Laidlaw DH, Enoka RM (2000) Coactivation of the antagonist muscle does not covary with steadiness in old adults. J Appl Physiol 89:61–71CrossRefPubMed Burnett R a, Laidlaw DH, Enoka RM (2000) Coactivation of the antagonist muscle does not covary with steadiness in old adults. J Appl Physiol 89:61–71CrossRefPubMed
go back to reference Devanne H, Lavoie BA, Capaday C (1997) Input-output properties and gain changes in the human corticospinal pathway. Exp Brain Res 114:329–338CrossRefPubMed Devanne H, Lavoie BA, Capaday C (1997) Input-output properties and gain changes in the human corticospinal pathway. Exp Brain Res 114:329–338CrossRefPubMed
go back to reference Dux L (1993) Muscle relaxation and sarcoplasmic reticulum function in different muscle types. Rev Physiol Biochem Pharmacol 122:69–147CrossRefPubMed Dux L (1993) Muscle relaxation and sarcoplasmic reticulum function in different muscle types. Rev Physiol Biochem Pharmacol 122:69–147CrossRefPubMed
go back to reference Enoka RM, Christou EA, Hunter SK et al (2003) Mechanisms that contribute to differences in motor performance between young and old adults. J Electromyogr Kinesiol 13:1–12CrossRefPubMed Enoka RM, Christou EA, Hunter SK et al (2003) Mechanisms that contribute to differences in motor performance between young and old adults. J Electromyogr Kinesiol 13:1–12CrossRefPubMed
go back to reference Gandevia SC (2001) Spinal and supraspinal factors in human muscle fatigue. Physiol Rev 81:1725–1789CrossRefPubMed Gandevia SC (2001) Spinal and supraspinal factors in human muscle fatigue. Physiol Rev 81:1725–1789CrossRefPubMed
go back to reference Gandevia SC, Allen GM, Butler JE, Taylor JL (1996) Supraspinal factors in human muscle fatigue: evidence for suboptimal output from the motor cortex. J Physiol 490(Pt 2):529–536CrossRefPubMedPubMedCentral Gandevia SC, Allen GM, Butler JE, Taylor JL (1996) Supraspinal factors in human muscle fatigue: evidence for suboptimal output from the motor cortex. J Physiol 490(Pt 2):529–536CrossRefPubMedPubMedCentral
go back to reference Hasan Z, Enoka RM (1985) Isometric torque-angle relationship and movement-related activity of human elbow flexors: implications for the equilibrium-point hypothesis. Exp Brain Res 59:441–450PubMed Hasan Z, Enoka RM (1985) Isometric torque-angle relationship and movement-related activity of human elbow flexors: implications for the equilibrium-point hypothesis. Exp Brain Res 59:441–450PubMed
go back to reference Herbert RD, Gandevia SC (1999) Twitch interpolation in human muscles: mechanisms and implications for measurement of voluntary activation. J Neurophysiol 82:2271–2283CrossRefPubMed Herbert RD, Gandevia SC (1999) Twitch interpolation in human muscles: mechanisms and implications for measurement of voluntary activation. J Neurophysiol 82:2271–2283CrossRefPubMed
go back to reference Hermens HJ, Freriks B, Disselhorst-Klug C, Rau G (2000) Development of recommendations for SEMG sensors and sensor placement procedures. J Electromyogr Kinesiol 10:361–374CrossRefPubMed Hermens HJ, Freriks B, Disselhorst-Klug C, Rau G (2000) Development of recommendations for SEMG sensors and sensor placement procedures. J Electromyogr Kinesiol 10:361–374CrossRefPubMed
go back to reference Hortobágyi T, Zheng D, Weidner M et al (1995) The influence of aging on muscle strength and muscle fiber characteristics with special reference to eccentric strength. J Gerontol A Biol Sci Med Sci 50:B399-406PubMed Hortobágyi T, Zheng D, Weidner M et al (1995) The influence of aging on muscle strength and muscle fiber characteristics with special reference to eccentric strength. J Gerontol A Biol Sci Med Sci 50:B399-406PubMed
go back to reference Hunter SK, Thompson MW, Ruell PA et al (1999) Human skeletal sarcoplasmic reticulum Ca2 + uptake and muscle function with aging and strength training. J Appl Physiol 86:1858–1865CrossRefPubMed Hunter SK, Thompson MW, Ruell PA et al (1999) Human skeletal sarcoplasmic reticulum Ca2 + uptake and muscle function with aging and strength training. J Appl Physiol 86:1858–1865CrossRefPubMed
go back to reference Hunter SK, Thompson MW, Adams RD (2000) Relationships among age-associated strength changes and physical activity level, limb dominance, and muscle group in women. J Gerontol A Biol Sci Med Sci 55:B264–B273CrossRef Hunter SK, Thompson MW, Adams RD (2000) Relationships among age-associated strength changes and physical activity level, limb dominance, and muscle group in women. J Gerontol A Biol Sci Med Sci 55:B264–B273CrossRef
go back to reference Inghilleri M, Berardelli A, Cruccu G, Manfredi M (1993) Silent period evoked by transcranial stimulation of the human cortex and cervicomedullary junction. J Physiol 466:521–534PubMedPubMedCentral Inghilleri M, Berardelli A, Cruccu G, Manfredi M (1993) Silent period evoked by transcranial stimulation of the human cortex and cervicomedullary junction. J Physiol 466:521–534PubMedPubMedCentral
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 91:1341–1349CrossRefPubMed Klein CS, Rice CL, Marsh GD (2001) Normalized force, activation, and coactivation in the arm muscles of young and old men. J Appl Physiol 91:1341–1349CrossRefPubMed
go back to reference Krivickas LS, Suh D, Wilkins J et al (2001) Age- and gender-related differences in maximum shortening velocity of skeletal muscle fibers. Am J Phys Med Rehabil 80:447-455-7CrossRef Krivickas LS, Suh D, Wilkins J et al (2001) Age- and gender-related differences in maximum shortening velocity of skeletal muscle fibers. Am J Phys Med Rehabil 80:447-455-7CrossRef
go back to reference Larsson L, Li X, Frontera WR (1997) Effects of aging on shortening velocity and myosin isoform composition in single human skeletal muscle cells. Am J Physiol 272:C638-49CrossRefPubMed Larsson L, Li X, Frontera WR (1997) Effects of aging on shortening velocity and myosin isoform composition in single human skeletal muscle cells. Am J Physiol 272:C638-49CrossRefPubMed
go back to reference Lindle R, Metter E, Lynch N et al (1997) Age and gender comparisons of muscle strength in 654 women and men aged 20–93 year. J Appl Physiol 83:1581–1587CrossRefPubMed Lindle R, Metter E, Lynch N et al (1997) Age and gender comparisons of muscle strength in 654 women and men aged 20–93 year. J Appl Physiol 83:1581–1587CrossRefPubMed
go back to reference Macaluso A, Nimmo MA, Foster JE et al (2002) Contractile muscle volume and agonist-antagonist coactivation account for differences in torque between young and older women. Muscle Nerve 25:858–863. doi: 10.1002/mus.10113 CrossRefPubMed Macaluso A, Nimmo MA, Foster JE et al (2002) Contractile muscle volume and agonist-antagonist coactivation account for differences in torque between young and older women. Muscle Nerve 25:858–863. doi: 10.​1002/​mus.​10113 CrossRefPubMed
go back to reference Molenaar JP, McNeil CJ, Bredius MS, Gandevia SC (2012) Effects of aging and sex on voluntary activation and peak relaxation rate on human elbow flexors studied with motor cortical stimulation. Age (Omaha) 35:1327–1337. doi:10.1037/0022-3514.90.4.644 CrossRef Molenaar JP, McNeil CJ, Bredius MS, Gandevia SC (2012) Effects of aging and sex on voluntary activation and peak relaxation rate on human elbow flexors studied with motor cortical stimulation. Age (Omaha) 35:1327–1337. doi:10.​1037/​0022-3514.​90.​4.​644 CrossRef
go back to reference Porter MM, Vandervoort AA, Kramer JF (1997) Eccentric peak torque of the plantar and dorsiflexors is maintained in older women. J Gerontol A Biol Sci Med Sci 52:B125-31PubMed Porter MM, Vandervoort AA, Kramer JF (1997) Eccentric peak torque of the plantar and dorsiflexors is maintained in older women. J Gerontol A Biol Sci Med Sci 52:B125-31PubMed
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 Sale D, Quinlan J, Marsh E et al (1982) Influence of joint position on ankle plantarflexion in humans. J Appl Physiol 52:1636–1642CrossRefPubMed Sale D, Quinlan J, Marsh E et al (1982) Influence of joint position on ankle plantarflexion in humans. J Appl Physiol 52:1636–1642CrossRefPubMed
go back to reference Simoneau J, Bouchard C (1989) Human variation in skeletal muscle fiber-type proportion and enzyme activities. Am J Physiol 257:E567–E572 Simoneau J, Bouchard C (1989) Human variation in skeletal muscle fiber-type proportion and enzyme activities. Am J Physiol 257:E567–E572
go back to reference Vandervoort AA, McComas AJ (1986) Contractile changes in opposing muscles of the human ankle joint with aging. J Appl Physiol 61:361–367CrossRefPubMed Vandervoort AA, McComas AJ (1986) Contractile changes in opposing muscles of the human ankle joint with aging. J Appl Physiol 61:361–367CrossRefPubMed
go back to reference Venturelli M, Saggin P, Muti E et al (2015) In vivo and in vitro evidence that intrinsic upper- and lower-limb skeletal muscle function is unaffected by ageing and disuse in oldest-old humans. Acta Physiol (Oxf) 215:58–71. doi:10.1111/apha.12524 CrossRef Venturelli M, Saggin P, Muti E et al (2015) In vivo and in vitro evidence that intrinsic upper- and lower-limb skeletal muscle function is unaffected by ageing and disuse in oldest-old humans. Acta Physiol (Oxf) 215:58–71. doi:10.​1111/​apha.​12524 CrossRef
go back to reference Yoon T, Schlinder Delap B, Griffith EE, Hunter SK (2007) Mechanisms of fatigue differ after low- and high-force fatiguing contractions in men and women. Muscle Nerve 36:515–524. doi:10.1002/mus.20844 CrossRefPubMed Yoon T, Schlinder Delap B, Griffith EE, Hunter SK (2007) Mechanisms of fatigue differ after low- and high-force fatiguing contractions in men and women. Muscle Nerve 36:515–524. doi:10.​1002/​mus.​20844 CrossRefPubMed
go back to reference Yue GH, Ranganathan VK, Siemionow V et al (1999) Older adults exhibit a reduced ability to fully activate their biceps brachii muscle. J Gerontol A Biol Sci Med Sci 54:M249–M253CrossRef Yue GH, Ranganathan VK, Siemionow V et al (1999) Older adults exhibit a reduced ability to fully activate their biceps brachii muscle. J Gerontol A Biol Sci Med Sci 54:M249–M253CrossRef
Metadata
Title
Voluntary activation and variability during maximal dynamic contractions with aging
Authors
Vianney Rozand
Jonathon W. Senefeld
Hamidollah Hassanlouei
Sandra K. Hunter
Publication date
01-12-2017
Publisher
Springer Berlin Heidelberg
Published in
European Journal of Applied Physiology / Issue 12/2017
Print ISSN: 1439-6319
Electronic ISSN: 1439-6327
DOI
https://doi.org/10.1007/s00421-017-3737-3

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Acknowledgement to Referees

Acknowledgement to referees