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Skeletal muscle adaptations to physical inactivity and subsequent retraining in young men

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Abstract

Skeletal muscle structure and function are markedly affected by chronic disuse. With unloading, muscle mass is lost at rate of about 0.4 %/day but little is known about the recovery of muscle mass and strength following disuse. Here we report an extensive data set describing in detail skeletal muscle adaptations in structure and function in response to both disuse and retraining. Eight young men (23 ± 2.2 years) underwent 3 weeks of unilateral lower limb suspension (ULLS) followed by a 3-week resistance training recovery program. Knee extensor isometric torque, voluntary activation, quadriceps femoris (QF) muscle volume (QFvol), fascicle length (Lf) and pennation angle (θ), physiological cross-sectional area (PCSA) of all four heads of the QF muscle, were measured before, after ULLS, and post-ULLS-resistance training. Needle biopsies were taken from the vastus lateralis muscle of a subgroup (n = 6) of the same subjects and cross sectional area of individual muscle s and myosin content of muscle samples were determined. Following 3 weeks of ULLS, isometric torque decreased by 26 %, PCSA by 3 %, QFvol by 10 %. Lf and θ of all four heads of QF significantly decreased (p ≤ 0.05). Following the 3-week retraining period, isometric torque, PCSA, QFvol, Lf and θ of all four heads of QF were all fully restored to pre ULLS values. CSA of individual muscle fibres and myosin content of muscle samples decreased by 26 and 35 % respectively (post-ULLS) and recovered to almost pre-ULLS values following retraining. There were no significant changes in voluntary activation of the quadriceps muscles in response to either ULLS or subsequent retraining. These results indicate that: (1) the loss of muscle force with 3-week unloading in humans is mostly explained by muscle atrophy and by a decrease in myosin content and, (2) all the neuromuscular changes induced by this model of disuse can be fully restored after a resistance training intervention of equal duration.

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References

  • Adams GR, Caiozzo VJ, Baldwin KM (2003) Skeletal muscle unweighting: spaceflight and ground-based models. J Appl Physiol 95:2185–2201

    PubMed  Google Scholar 

  • Berg HE, Tesch PA (1996) Changes in muscle function in response to 10 days of lower limb unloading in humans. Acta Physiol Scand 157:63–70

    Article  PubMed  CAS  Google Scholar 

  • Berg HE, Dudley GA, Haggmark T, Ohlsen H, Tesch PA (1991) Effects of lower limb unloading on skeletal muscle mass and function in humans. J Appl Physiol 70:1882–1885

    Article  PubMed  CAS  Google Scholar 

  • Berg HE, Larsson L, Tesch PA (1997) Lower limb skeletal muscle function after 6 wk of bed rest. J Appl Physiol 82:182–188

    Article  PubMed  CAS  Google Scholar 

  • Bergström J (1979) Muscle-biopsy needles. Lancet 1(8108):153

    Google Scholar 

  • Bottinelli R, Canepari M, Pellegrino MA, Reggiani C (1996) Force-velocity properties of human skeletal muscle fibres: myosin heavy chain isoform and temperature dependence. J Physiol 495(2):573–586

    Google Scholar 

  • Bruusgaard JC, Johansen IB, Egner IM, Rana ZA, Gundersen K (2010) Myonuclei acquired by overload exercise precede hypertrophy and are not lost on detraining. Proc Natl Acad Sci USA 107(34):15111–15116

    Article  PubMed  CAS  Google Scholar 

  • Capodaglio P, NARICI MV (1998) Muscle atrophy disuse and disease. Adv Occup Med Rehabil 4:83–87

    Google Scholar 

  • Clark BC (2009) In vivo alterations in skeletal muscle form and function after disuse atrophy. Med Sci Sports Exerc 41(10):1869–1875

    Article  PubMed  CAS  Google Scholar 

  • Clark BC, Fernhall B, Ploutz-Snyder LL (2006) Adaptations in human neuromuscular function following prolonged unweighting: I. Skeletal muscle contractile properties and applied ischemia efficacy. J Appl Physiol 101:256–263

    Article  PubMed  Google Scholar 

  • Cutts A (1988) The range of sarcomere lengths in the muscles of the human lower limb. J Anat 160:79–88

    PubMed  CAS  Google Scholar 

  • D’ Antona G, Pellegrino MA, Adami R, Rossi R, Naccari Carlizzi C, Canepari M, Saltin B, Bottinelli R (2003) The effect of ageing and immobilization on structure and function of human skeletal muscle fibres. J Physiol 552:499–511

    Article  Google Scholar 

  • Davies CTM, Rutherford IC, Thomas DO (1987) Electrically evoked contractions of the triceps surae during and following 21 days of voluntary leg immobilization. Eur J Appl Physiol Occup Physiol 56:306–312

    Google Scholar 

  • de Boer MD, Maganaris CN, Seynnes OR, Rennie MJ, Narici MV (2007) Time course of muscular, neural and tendinous adaptations to 23 day unilateral lower-limb suspension in young men. J Physiol 583:1079–1091

    Article  PubMed  Google Scholar 

  • de Boer MD, Seynnes OR, di Prampero PE, Pišot R, Mekjavić IB, Biolo G, Narici MV (2008) Effect of 5 weeks horizontal bed rest on human muscle thickness and architecture of weight bearing and non-weight bearing muscles. Eur J Appl Physiol 104(2):401–407

    Article  PubMed  Google Scholar 

  • Drummond MJ, Dreyer HC, Pennings B, Fry CS, Dhanani S, Dillon EL, Sheffield-Moore M, Volpi E, Rasmussen BB (2008) Skeletal muscle protein anabolic response to resistance exercise and essential amino acids is delayed with aging. J Appl Physiol 104(5):1452–1461

    Article  PubMed  CAS  Google Scholar 

  • Edgerton VR, McCall GE, Hodgson JA, Gotto J, Goulet C, Fleischmann K, Roy RR (2001) Sensorimotor adaptations to microgravity in humans. J Exp Biol 204:3217–3224

    PubMed  CAS  Google Scholar 

  • Erskine RM, Jones DA, Williams AG, Stewart CE, Degens H (2010) Resistance training increases in vivo quadriceps femoris muscle specific tension in young men. Acta Physiol 199:83–89

    Article  CAS  Google Scholar 

  • Gallegly JC, Turesky NA, Strotman BA, Gurley CM, Peterson CA, Dupont-Versteegden EE (2004) Satellite cell regulation of muscle mass is altered at old age. J Appl Physiol 97:1082–1090

    Article  PubMed  Google Scholar 

  • Gans C, Bock WJ (1965) The functional significance of muscle architecture—a theoretical analysis. Ergeb Anat Entwicklungsgesch 38:115–142

    PubMed  CAS  Google Scholar 

  • Glover EI, Phillips SM, Oates BR, Tang JE, Tarnopolsky MA, Selby A, Smith K, Rennie MJ (2008) Immobilization induces anabolic resistance in human myofibrillar protein synthesis with low and high dose amino acid infusion. J Physiol 586(24):6049–6061

    Article  PubMed  CAS  Google Scholar 

  • Hanson AM, Stodieck LS, Cannon CMA, Simske SJ, Ferguson VL (2010) Seven days of muscle re-loading and voluntary wheel running following hindlimb suspension in mice restores running performance, muscle morphology and metrics of fatigue but not muscle strength. J Muscle Res Cell Motil 31:141–153

    Article  PubMed  Google Scholar 

  • Hortobãgyi T, Dempsey L, Fraser D, Zheng D, Hamilton G, Lambert J, Dohm L (2000) Changes in muscle strength, muscle fibre size and myofibrillar gene expression after immobilization and retraining in humans. J Physiol 524:293–304

    Article  PubMed  Google Scholar 

  • Huijing PA (1998) Muscle as a collagen fibre reinforced composite: a review of force transmission in muscle and whole limb. J Biomech 32:329–345

    Article  Google Scholar 

  • Kawakami Y, Abe T, Fukunaga T (1993) Muscle-fibre pennation angles are greater in hypertrophied than in normal muscles. J Appl Physiol 74(6):2740–2744

    PubMed  CAS  Google Scholar 

  • 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 84:7–12

    Article  PubMed  CAS  Google Scholar 

  • Koryak YU (2001) Electrically evoked and voluntary properties of the human triceps surae muscle: effects of long-term spaceflights. Acta Physiologica et Pharmacologica Bulgarica 26(1–2):21–27

    Google Scholar 

  • Larsson L, Li X, Berg HE, Frontera WR (1996) Effects of removal of weight bearing function on contractility and myosin isoform composition in single human skeletal muscle cells. Pflugers Arch 432:320–328

    Article  PubMed  CAS  Google Scholar 

  • Lieber RL, Friden J (2001) Clinical significance of skeletal muscle architecture. Clin Orthop Relat Res 383:140–151

    Article  PubMed  Google Scholar 

  • Narici M, Cerretelli P (1998) Changes in human muscle architecture in disuse-atrophy evaluated by ultrasound imaging. J Gravit Physiol 5:73–74

    Google Scholar 

  • Narici MV, de Boer MD (2011) Disuse of the musculo-skeletal system in space and on earth. Eur J Appl Physiol 111(3):403–420

    Article  PubMed  CAS  Google Scholar 

  • Narici MV, Maganaris CN (2007) Plasticity of the muscle-tendon complex with disuse and aging. Exerc Sport Sci Rev 35:126–134

    Article  PubMed  Google Scholar 

  • Ruegg DG, Kakebeeke TH, Gabriel J-P, Bennefeld M (2003) Conduction velocity of nerve and muscle fiber action potentials after a space mission or a bed rest. Clin Neurophysiol 114(1):86–93

    Google Scholar 

  • Seynnes OR, Maganaris CN, De Boer MD, Di Prampero PE, Narici MV (2008) Early structural adaptations to unloading in the human calf muscles. Acta Physiologica 193(3):265–274

    Google Scholar 

  • Seynnes OR, Erskine RM, Maganaris CN, Longo S, Simoneau EM, Grosset JF, Narici MV (2009) Training-induced changes in structural and mechanical properties of the patellar tendon are related to muscle hypertrophy but not to strength gains. J Appl Physiol 107(2):523–530

    Article  PubMed  CAS  Google Scholar 

  • Seynnes OR, Maffiuletti NA, Horstman AM, Narici MV (2010) Increased H-reflex excitability is not accompanied by changes in neural drive following 24 days of unilateral lower limb suspension. Muscle Nerve 42(5):749–755

    Article  PubMed  Google Scholar 

  • Suetta C, Hvid LG, Justesen L, Christensen U, Neergaard K, Simonsen L, Ortenblad N, Magnusson SP, Kjaer M, AAGAARD P (2009) Effects of aging on human skeletal muscle after immobilization and retraining. J Appl Physiol 107(4):1172–1180

    Article  PubMed  CAS  Google Scholar 

  • Thom JM, Thompson MW, Ruell PA, Bryant GJ, Fonda JS, Harmer AR, De Janse Jonge XAK, Hunter SK (2001) Effect of 10-day cast immobilization on sarcoplasmic reticulum calcium regulation in humans. Acta Physiol Scand 172(2):141–147

    Article  PubMed  CAS  Google Scholar 

  • Urso ML, Scrimgeour AG, Chen Y-W, Thompson PD, Clarkson PM (2006) Analysis of human skeletal muscle after 48 h immobilization reveals alterations in mRNA and protein for extracellular matrix components. J Appl Physiol 101(4):1136–1148

    Google Scholar 

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Correspondence to E. L. Campbell.

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Campbell, E.L., Seynnes, O.R., Bottinelli, R. et al. Skeletal muscle adaptations to physical inactivity and subsequent retraining in young men. Biogerontology 14, 247–259 (2013). https://doi.org/10.1007/s10522-013-9427-6

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  • DOI: https://doi.org/10.1007/s10522-013-9427-6

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