Skip to main content
Log in

Use it or lose it: multiscale skeletal muscle adaptation to mechanical stimuli

  • REVIEW
  • Published:
Biomechanics and Modeling in Mechanobiology Aims and scope Submit manuscript

Abstract

Skeletal muscle undergoes continuous turnover to adapt to changes in its mechanical environment. Overload increases muscle mass, whereas underload decreases muscle mass. These changes are correlated with, and enabled by, structural alterations across the molecular, subcellular, cellular, tissue, and organ scales. Despite extensive research on muscle adaptation at the individual scales, the interaction of the underlying mechanisms across the scales remains poorly understood. Here, we present a thorough review and a broad classification of multiscale muscle adaptation in response to a variety of mechanical stimuli. From this classification, we suggest that a mathematical model for skeletal muscle adaptation should include the four major stimuli, overstretch, understretch, overload, and underload, and the five key players in skeletal muscle adaptation, myosin heavy chain isoform, serial sarcomere number, parallel sarcomere number, pennation angle, and extracellular matrix composition. Including this information in multiscale computational models of muscle will shape our understanding of the interacting mechanisms of skeletal muscle adaptation across the scales. Ultimately, this will allow us to rationalize the design of exercise and rehabilitation programs, and improve the long-term success of interventional treatment in musculoskeletal disease.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8
Fig. 9
Fig. 10
Fig. 11
Fig. 12
Fig. 13
Fig. 14

Similar content being viewed by others

References

  • Aagaard P, Andersen JL, Dyhre-Poulsen P, Leffers AM, Wagner A et al (2001) A mechanism for increased contractile strength of human pennate muscle in response to strength training: changes in muscle architecture. J Physiol 534:613–623

    Google Scholar 

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

    Google Scholar 

  • Ahtikoski A, Koskinen SO, Virtanen P, Kovanen V, Takala TE (2001) Regulation of synthesis of fibrillar collagens in rat skeletal muscle during immobilization in shortened and lengthened positions. Acta Physiol Scand 172:131–140

    Google Scholar 

  • Akeson W, Amiel D, Mechanic G, Woo S, Harwood F et al (1977) Cross-linking alterations in joint contractures: changes in the reducible cross-links in periarticular connective tissue collagen after nine weeks of immobilization. Connect Tissue Res 5:15–19

    Google Scholar 

  • Akima H, Kubo K, Imai M, Kanehisa H, Suzuki Y et al (2001) Inactivity and muscle: effect of resistance training during bed rest on muscle size in the lower limb. Acta Physiol Scand 172:269–278

    Google Scholar 

  • Allen D, Linderman J (1997) Growth hormone/IGF-I and/or resistive exercise maintains myonuclear number in hindlimb unweighted muscles. J Appl Physiol 83:1857–1861

    Google Scholar 

  • Allen DL, Roy RR, Edgerton VR (1999) Myonuclear domains in muscle adaptation and disease. Muscle Nerve 22:1350–1360

    Google Scholar 

  • Ambrosi D, Ateshian GA, Arruda EM, Cowin SC, Dumais J, Goriely A, Holzapfel GA, Humphrey JD, Kemkemer R, Kuhl E, Olberding JE, Taber LA, Garikipati K (2011) Perspectives on biological growth and remodeling. J Mech Phys Solids 59:863–883

    MATH  MathSciNet  Google Scholar 

  • Andersen J, Aagaard P (2000) Myosin heavy chain IIX overshoot in human skeletal muscle. Muscle Nerve 23:1095–1104

    Google Scholar 

  • Arnold EM, Delp SL (2011) Fibre operating lengths of human lower limb muscles during walking. Phil Trans R Soc B 366:1530–1539

    Google Scholar 

  • Asakawa DS, Pappas GP, Drace JE, Delp SL (2002) Aponeurosis length and fascicle insertion angles of the biceps brachii. J Mech Med Biol 2:449–455

    Google Scholar 

  • Ausoni S, Gorza L, Schiaffino S, Gundersen K, Lomo T (1990) Expression of myosin heavy chain isoforms in stimulated fast and slow rat muscles. J Neurosci 10:153–160

    Google Scholar 

  • Baker JH, Matsumoto DE (1988) Adaptation of skeletal muscle to immobilization in a shortened position. Muscle Nerve 11:231–244

    Google Scholar 

  • Baldwin K, Haddad F (2001) Invited review: effects of different activity and inactivity paradigms on myosin heavy chain gene expression in striated muscle. J Appl Physiol 90:345–357

    Google Scholar 

  • Bamman M, Clarke M (1998) Impact of resistance exercise during bed rest on skeletal muscle sarcopenia and myosin isoform distribution. J Appl Physiol 84:157–163

    Google Scholar 

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

    Google Scholar 

  • Berg HE, Eiken O, Miklavcic L, Mekjavic IB (2007) Hip, thigh and calf muscle atrophy and bone loss after 5-week bedrest inactivity. Eur J Appl Physiol 99:283–289

    Google Scholar 

  • Billeter R, Puntschort A, Vogt M, Wittwer M, Wey E (1997) Molecular biology of human muscle adaptation. Int J Sports Med 18:S300–S301

    Google Scholar 

  • Blazevich AJ, Cannavan D, Coleman DR, Horne S (2007) Influence of concentric and eccentric resistance training on architectural adaptation in human quadriceps muscles. J Appl Physiol 103:1565– 1575

  • Blemker SS, Delp SL (2005) Three-dimensional representation of complex muscle architectures and geometries. Ann Biomed Eng 33:661–673

    Google Scholar 

  • Blemker SS, Pinsky PM, Delp SL (2005) A 3D model of muscle reveals the causes of nonuniform strains in the biceps brachii. J Biomech 38:657–665

    Google Scholar 

  • Blemker SS, Delp SL (2006) Rectus femurs and vast us intermedius fiber excursions predicted by three-dimensional muscle models. J Biomech 39:1383–1391

    Google Scholar 

  • Boakes JL, Foran J, Ward SR, Lieber RL (2007) Muscle adaptation by serial sarcomere addition 1 year after femoral lengthening. Clin Orthop Relat Res 456:250–253

    Google Scholar 

  • Böl M, Reese S (2008) Micromechanical modelling of skeletal muscles based on the finite element method. Comput Methods Biomech Biomed Eng 11:489–504

    Google Scholar 

  • Böl M (2010) Micromechanical modelling of skeletal muscles: from the single fiber to the whole muscle. Arch Appl Mech 80:557–567

    MATH  Google Scholar 

  • Böl M, Leichsenring K, Weichert C, Sturmat M, Schenk P, Blickhan R, Siebert T (2013) Three-dimensional surface geometries of the rabbit soleus muscle during contraction: input for biomechanical modeling and its validation. Biomech Model Mechanobiol 12:1205–1220

    Google Scholar 

  • Booth FW, Thomason DB (1991) Molecular and cellular adaptation of muscle in response to exercise: perspectives of various models. Physiol Rev 71:541–585

    Google Scholar 

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

  • Brockett CL, Morgan DL, Proske U (2001) Human hamstring muscles adapt to eccentric exercise by changing optimum length. Med Sci Sports Exerc 33:783–790

    Google Scholar 

  • Burkholder TJ, Fingado B, Baron S, Lieber RL (1994) Relationship between muscle fiber types and sizes and muscle architectural properties in the mouse hindlimb. J Morphol 221:177–90

    Google Scholar 

  • Burkholder TJ, Lieber RL (1998) Sarcomere number adaptation after retinaculum transection in adult mice. J Exp Biol 201:309–316

    Google Scholar 

  • Bustamante AC, Marko JF, Siggia ED, Smith S (1994) Entropic elasticity of lambda-phage DNA. Science 265:1599–1600

    Google Scholar 

  • Caiozzo V, Haddad F, Baker M, Herrick R, Prietto N et al (1996) Microgravity-induced transformations of myosin isoforms and contractile properties of skeletal muscle. J Appl Physiol 81:123–132

    Google Scholar 

  • Caiozzo V, Baker M, Baldwin K (1997) Modulation of myosin isoform expression by mechanical loading: role of stimulation frequency. J Appl Physiol 82:211–218

    Google Scholar 

  • Caiozzo VJ, Utkan A, Chou R, Khalafi A, Chandra H et al (2002) Effects of distraction on muscle length: mechanisms involved in sarcomerogenesis. Clin Orthop Relat Res 403:S133–S145

    Google Scholar 

  • Caiozzo V (2002) Plasticity of skeletal muscle phenotype: mechanical consequences. Muscle Nerve 26:740–768

    Google Scholar 

  • Campbell EL, Seynnes OR, Bottinelli R, McPhee JS, Atherton PJ et al (2013) Skeletal muscle adaptations to physical inactivity and subsequent retraining in young men. Biogerontology 14:247–259

    Google Scholar 

  • Canon F, Goubel F (1995) Changes in stiffness induced by hindlimb suspension in rat soleus muscle. Pflugers Arch 429:332–337

    Google Scholar 

  • Carson JA, Wei L (2000) Integrin signaling’s potential for mediating gene expression in hypertrophying skeletal muscle. J Appl Physiol 88:337–343

    Google Scholar 

  • Cromie MJ, Sanchez GN, Schnitzer MJ, Delp SL (2013) Sarcomere lengths in human extensor carpi radials brevis measured by microendoscropy. Muscle Nerve 48:286–292

    Google Scholar 

  • Csapo R, Maganaris CN, Seynnes OR, Narici MV (2010) On muscle, tendon and high heels. J Exp Biol 213:2582–2588

    Google Scholar 

  • D’Antona G, Pellegrino MA, Adami R, Rossi R, Carlizzi CN et al (2003) The effect of ageing and immobilization on structure and function of human skeletal muscle fibres. J Physiol 552:499–511

    Google Scholar 

  • D’Antona G, Lanfranconi F, Pellegrino MA, Brocca L, Adami R et al (2006) Skeletal muscle hypertrophy and structure and function of skeletal muscle fibres in male body builders. J Physiol 570:611– 627

  • Dash RK, Dibella Ja, Cabrera ME (2007) A computational model of skeletal muscle metabolism linking cellular adaptations induced by altered loading states to metabolic responses during exercise. Biomed Eng Online 6:14

    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

    Google Scholar 

  • DeFreitas JM, Beck TW, Stock MS, Dillon MA, Kasishke PR (2011) An examination of the time course of training-induced skeletal muscle hypertrophy. Eur J Appl Physiol 111:2785–2790

    Google Scholar 

  • Delp SL, Zajac FE (1992) Force- and moment-generating capacity of lower-extremity muscles before and after tendon lengthening. Clin Orthop Relat Res 284:247–259

    Google Scholar 

  • Deschenes M (2001) A comparison of the effects of unloading in young adult and aged skeletal muscle. Med Sci Sports Exerc 33:1477– 1483

    Google Scholar 

  • Deschenes MR, Kraemer WJ (2002) Performance and physiologic adaptations to resistance training. Am J Phys Med Rehabil 81:S3–16

    Google Scholar 

  • De Deyne PG, Hayatsu K, Meyer R, Paley D, Herzenberg JE (1999) Muscle regeneration and fiber-type transformation during distraction osteogenesis. J Orthop Res 17:560–570

    Google Scholar 

  • De Deyne P (2002) Lengthening of muscle during distraction osteogenesis. Clin Orthop Relat Res 403S:S171–S177

    Google Scholar 

  • Edgerton V, Zhou M, Ohira Y, Klitgaard H, Jiang B et al (1995) Human fiber size and enzymatic properties after 5 and 11 days of spaceflight. J Appl Physiol 78:1733–1739

    Google Scholar 

  • Ehler E, Gautel M (2008) The sarcomere and sarcomerogenesis. In: Laing NG (ed) Sarcomere Skelet Muscle Disease. Landes Biosience and Springer+Business Media, pp 1–14

  • Elsalanty M, Makarov M, Cherkashin A, Birch J, Samchukov M (2007) Changes in pennate muscle architecture after gradual tibial lengthening in goats. Anat Rec 290:461–467

    Google Scholar 

  • Eriksson A, Kadi F, Malm C, Thornell LE (2005) Skeletal muscle morphology in power-lifters with and without anabolic steroids. Histochem Cell Biol 124:167–175

    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

    Google Scholar 

  • Farup J, Kjølhede T, Sørensen H, Dalgas U, Møller AB et al (2012) Muscle morphological and strength adaptations to endurance vs. resistance training. J Strength Cond Res 26:398–407

    Google Scholar 

  • Fitts RH, Trappe SW, Costill DL, Gallagher PM, Creer A et al (2010) Prolonged space flight-induced alterations in the structure and function of human skeletal muscle fibres. J Physiol 588:3567–3592

    Google Scholar 

  • Fournier M, Roy R, Perham H, Simard C, Edgerton V (1983) Is limb immobilization a model of muscle disuse? Exp Neurol 80:147–156

    Google Scholar 

  • Fowles J, MacDougall J, Tarnopolsky M, Sale D, Roy B et al (2000) The effects of acute passive stretch on muscle protein synthesis in humans. Can J Appl Physiol 25:165–180

    Google Scholar 

  • Fry AC (2004) The role of resistance exercise intensity on muscle fibre adaptations. Sports Med 34:663–679

    MathSciNet  Google Scholar 

  • Gajdosik RL (2001) Passive extensibility of skeletal muscle: review of the literature with clinical implications. Clin Biomech 16:87–101

    Google Scholar 

  • Gajdosik RL, Allred JD, Gabbert HL, Sonsteng BA (2007) A stretching program increases the dynamic passive length and passive resistive properties of the calf muscle-tendon unit of unconditioned younger women. Eur J Appl Physiol 99:449–454

    Google Scholar 

  • Gautel M (2011) Cytoskeletal protein kinases: titin and its relations in mechanosensing. Pflugers Arch 462:119–134

    Google Scholar 

  • Gibson JNA, Halliday D, Morrison WL, Stoward PJ, Hornsby GA et al (1987) Decrease in human quadriceps muscle protein turnover consequent upon leg immobilization. Clin Sci 72:503–509

    Google Scholar 

  • Gillies AR, Lieber RL (2011) Structure and function of the skeletal muscle extracellular matrix. Muscle Nerve 44:318–331

    Google Scholar 

  • Göktepe S, Abilez OJ, Kuhl E (2010) A generic approach towards finite growth with examples of athlete’s heart, cardiac dilation, and cardiac wall thickening. J Mech Phys Solids 58:1661–1680

    MATH  MathSciNet  Google Scholar 

  • Göktepe S, Abilez OJ, Parker KK, Kuhl E (2010a) A multiscale model for eccentric and concentric cardiac growth through sarcomerogenesis. J Theor Biol 265:433–442

    Google Scholar 

  • Goldspink D (1978) The influence of passive stretch on the growth and protein turnover of the denervated extensor digitorum longus muscle. Biochem J 174:595–602

    Google Scholar 

  • Goldspink G, Scutt A (1992) Gene expression in skeletal muscle in response to stretch and force generation. Am J Physiol Integr Comp Physiol 262:R356–R363

    Google Scholar 

  • Goldspink G (1999) Changes in muscle mass and phenotype and the expression of autocrine and systemic growth factors by muscle in response to stretch and overload. J Anat 194:323–334

    Google Scholar 

  • Goldspink G, Yang SY (2001) Gene expression associated with muscle adaptation in response to physical signals. Cell Mol Response Stress 2:87–96

    Google Scholar 

  • Gordon A, Huxley A, Julian F (1966) The variation in isometric tension with sarcomere length in vertebrate muscle fibres. J Physiol 184:170–192

    Google Scholar 

  • Gossman MR, Sahrmann SA, Rose SJ (1982) Review of length-associated changes in muscle. Experimental evidence and clinical implications. Phys Ther 62:1799–1808

    Google Scholar 

  • Goto K, Okuyama R, Honda M, Uchida H, Akema T et al (2003) Profiles of connecting (titin) in atrophied soleus muscle induced by unloading of rats. J Appl Physiol 94:897–902

    Google Scholar 

  • Granzier H, Helmes M, Cazorla O, McNabb M, Labeit D et al (2000) Mechanical properties of titin isoforms. Elast Filam Cell 481:283–304

    Google Scholar 

  • Gregory P, Low RB, Stirewalt WS (1986) Changes in skeletal-muscle myosin isoenzymes with hypertrophy and exercise. Biochem J 238:55–63

    Google Scholar 

  • Grossman EJ, Roy RR, Talmadge RJ, Zhong H, Edgerton VR (1998) Effects of inactivity on myosin heavy chain composition and size of rat soleus fibers. Muscle Nerve 21:375–389

    Google Scholar 

  • Gruther W, Benesch T, Zorn C, Paternostro-Sluga T, Quittan M et al (2008) Muscle wasting in intensive care patients: ultrasound observation of the M. quadriceps femoris muscle layer. J Rehabil Med 40:185–189

    Google Scholar 

  • Hackney KJ, Ploutz-Snyder LL (2012) Unilateral lower limb suspension: integrative physiological knowledge from the past 20 years (1991–2011). Eur J Appl Physiol 112:9–22

    Google Scholar 

  • Haddad F, Roy R (2003) Atrophy responses to muscle inactivity. II. Molecular markers of protein deficits. J Appl Physiol 95:791–802

    Google Scholar 

  • Haddad F, Roy RR, Zhong H, Edgerton VR, Baldwin KM (2003) Atrophy responses to muscle inactivity. I. Cellular markers of protein deficits. J Appl Physiol 95:781–790

    Google Scholar 

  • Hanson AM, Harrison BC, Young MH, Stodieck LS, Ferguson VL (2012) Longitudinal characterization of functional, morphologic, and biochemical adaptations in mouse skeletal muscle with hindlimb suspension. Muscle Nerve 48:393–402

    Google Scholar 

  • Hedayatpour N, Falla D (2012) Non-uniform muscle adaptations to eccentric exercise and the implications for training and sport. J Electromyogr Kinesiol 22:329–333

    Google Scholar 

  • Heslinga JW, te Kronnie G, Huijing PA (1995) Growth and immobilization effects on sarcomeres: a comparison between gastrocnemius and soleus muscles of the adult rat. Eur J Appl Physiol Occup Physiol 70:49–57

    Google Scholar 

  • Hill AV (1938) The heat of shortening and dynamics constants of muscles. Proc R Soc Lond B 126:136–195

    Google Scholar 

  • Hoang PD, Herbert RD, Gandevia SC (2007) Effects of eccentric exercise on passive mechanical properties of human gastrocnemius in vivo. Med Sci Sports Exerc 39:849–857

    Google Scholar 

  • Holzapfel GA (2000) Nonlinear solid mechanics: a continuum approach for engineering John Wiley & Sons, Chichester. Q11

  • Holzapfel GA, Gasser TC, Ogden RW (2000) A new constitutive framework for anterial wall mechanics and a comparative study of material models. J Elast 61:1–48

    MATH  MathSciNet  Google Scholar 

  • Hubbard R, Ianuzzo C, Linduska J (1975) Compensatory adaptation of skeletal muscle composition to a long term functional overload. Growth 39:85–93

    Google Scholar 

  • Huijing PA (1999) Muscle as a collagen fiber reinforced composite: a review of force transmission in muscle and whole limb. J Biomech 32:329–345

    Google Scholar 

  • Huxley HE, Hanson J (1954) Changes in the cross-striations of muscle during contraction and stretch and their structural interpretation. Nature 173:973–976

    Google Scholar 

  • Ianuzzo C, Gollnick P, Armstrong R (1976) Compensatory adaptations of skeletal muscle fiber types to a long-term functional overload. Life Sci 19:1517–1524

    Google Scholar 

  • Janecki D, Jarocka E, Jaskólska A (2011) Muscle passive stiffness increases less after the second bout of eccentric exercise compared to the first bout. J Sci Med Sport 14:338–343

    Google Scholar 

  • Johnson T, Klueber K (1991) Skeletal muscle following tonic overload: functional and structural analysis. Med Sci Sports Exerc 23:49– 55

  • Joo ST, Kim GD, Hwang YH, Ryu YC (2013) Control of fresh meat quality through manipulation of muscle fiber characteristics. Meat Sci 95:828–836

    Google Scholar 

  • Jürimäe J, Abernethy PJ, Blake K, McEniery MT (1996) Changes in the myosin heavy chain isoform profile of the triceps brachii muscle following 12 weeks of resistance training. Eur J Appl Physiol Occup Physiol 74:287–292

    Google Scholar 

  • Kasper CE, Xun L (2000) Expression of titin in skeletal muscle varies with hind-limb unloading. Biol Res Nurs 2:107–115

    Google Scholar 

  • Kawakami Y (1993) Muscle-fiber pennation angles are greater in hypertrophied than in normal muscles. J Appl Physiol 74: 2740–2744

  • Kawakami Y, Abe T, Kuno SY, Fukunaga T (1995) Training-induced changes in muscle architecture and specific tension. Eur J Appl Physiol Occup Physiol 72:37–43

    Google Scholar 

  • Kho AL, Perera S, Alexandrovich A, Gautel M (2012) The sarcomeric cytoskeleton as a target for pharmacological intervention. Curr Opin Pharmacol 12:347–354

    Google Scholar 

  • Kirby TJ, McCarthy JJ (2013) MicroRNAs in skeletal muscle biology and exercise adaptation. Free Radic Biol Med 64:95–105

    Google Scholar 

  • Kjaer M (2004) Role of extracellular matrix in adaptation of tendon and skeletal muscle to mechanical loading. Physiol Rev 84:649–698

    Google Scholar 

  • Komi PV, Karlsson J (1979) Physical performance, skeletal muscle enzyme activities, and fibre types in monozygous and dizygous twins of both sexes. Acta Physiol Scand Suppl 462:1

    Google Scholar 

  • Kovanen V, Suominen H, Peltonen L (1987) Effects of aging and life-long physical training on collagen in slow and fast skeletal muscle in rats. A morphometric and immuno-histochemical study. Cell Tissue Res 248:247–255

    Google Scholar 

  • Kraemer WJ, Nindl BC, Ratamess NA, Gotshalk LA, Volek JS et al (2004) Changes in muscle hypertrophy in women with periodized resistance training. Med Sci Sport Exerc 36:697–708

    Google Scholar 

  • Kraus W, Torgan C, Taylor D (1994) Skeletal muscle adaptation to chronic low-frequency motor nerve stimulation. Exerc Sport Sci Rev 22:313–360

    Google Scholar 

  • Kubo K, Kanehisa H (2001) Influence of static stretching on viscoelastic properties of human tendon structures in vivo. J Appl Physiol 90:520–527

    Google Scholar 

  • Kubo K, Ikebukuro T, Yata H (2010) Time course of changes in muscle and tendon properties during strength training and detraining. J Strength Cond Res 24:322–331

    Google Scholar 

  • Kuhl E, Holzapfel GA (2007) A continuum model for remodeling in living structures. J Math Sci 42:8811–8823

    Google Scholar 

  • Kuhl E (2014) Growing matter—a review of growth in living systems. J Mech Behav Biomed Mat 29:529–543

    Google Scholar 

  • LaRoche DP, Connolly DAJ (2006) Effects of stretching on passive muscle tension and response to eccentric exercise. Am J Sports Med 34:1000–1007

    Google Scholar 

  • Lee SJ, McPherron AC (2001) Regulation of muscle activity and muscle growth. Proc Natl Acad Sci 98:9306–9311

    Google Scholar 

  • Lemos RR, Epstein M, Herzog W, Wyvill B (2004) A framework for structured modeling of skeletal muscle. Comput Methods Biomech Biomed Eng 7:305–317

    Google Scholar 

  • Lieber RL (2009) Skeletal muscle structure, function, and plasticity: the physiological basis of rehabilitation. M—medicine series. Wolters Kluwer Health/Lippincott Williams & Wilkins, Philadelphia

  • Lieber R, Friden J (2000) Functional and clinical significance of skeletal muscle architecture. Muscle Nerve 23:1647–1666

    Google Scholar 

  • Lindsey CA, Makarov MR, Shoemaker S, Birch JG, Buschang PH et al (2002) The effect of the amount of limb lengthening on skeletal muscle. Clin Orthop Relat Res 402:278–287

    Google Scholar 

  • Llewellyn ME, Barretto RPJ, Delp SL, Schnitzer MJ (2008) Minimally invasive high-speed imaging of sarcomere contractile dynamics in mice and humans. Nature 454:784–788

    Google Scholar 

  • Lynn R, Morgan D (1994) Decline running produces more sarcomeres in rat vastus intermedius muscle fibers than does incline running. J Appl Physiol 77:1439–1444

    Google Scholar 

  • MacDougall J, Sale D, Elder G, Sutton J (1982) Physiology of elite powerlifters and bodybuilders. Eur J Appl Physiol Occup Physiol 48:117–126

    Google Scholar 

  • Mackey A, Holm L, Reitelseder S, Pedersen TG, Doessing S et al (2011) Myogenic response of human skeletal muscle to 12 weeks of resistance training at light loading intensity. Scand J Med Sci Sports 21:773–782

    Google Scholar 

  • Magid A, Law D (1985) Myofibrils bear most of the resting tension in frog skeletal muscle. Science 230:1280–1282

    Google Scholar 

  • Magnusson SP, Narici MV, Maganaris CN, Kjaer M (2008) Human tendon behaviour and adaptation, in vivo. J Physiol 586:71–81

    Google Scholar 

  • Makarov M, Birch J, Samchukov M (2009) The role of variable muscle adaptation to limb lengthening in the development of joint contractures: an experimental study in the goat. J Pediatr Orthop 29:175–181

    Google Scholar 

  • Matano T, Tamai K, Kurokawa T (1994) Adaptation of skeletal muscle in limb lengthening: a light diffraction study on the sarcomere length in situ. J Orthop Res 12:193–196

    Google Scholar 

  • Maxwell LC, Faulkner JA, Hyatt GJ (1974) Estimation of number of fibers in guinea pig skeletal muscles. J Appl Physiol 37:259–264

    Google Scholar 

  • McDonagh MJN, Davies CTM (1984) Adaptive response of mammalian skeletal muscle to exercise with high loads. Eur J Appl Physiol 52:139–155

    Google Scholar 

  • Millard M, Uchida T, Seth A, Delp SL (2013) Flexing computational muscle: modeling and simulation of musculotendon dynamics. J Biomech Eng 135:021005

    Google Scholar 

  • Miller BF, Olesen JL, Hansen M, Døssing S, Crameri RM et al (2005) Coordinated collagen and muscle protein synthesis in human patella tendon and quadriceps muscle after exercise. J Physiol 567:1021–1033

  • Moore DR, Phillips SM, Babraj JA, Smith K, Rennie MJ (2005) Myofibrillar and collagen protein synthesis in human skeletal muscle in young men after maximal shortening and lengthening contractions. Am J Physiol Endocrinol Metab 288:E1153–E1159

    Google Scholar 

  • Münster S, Jawerth LM, Ba Leslie, Weitz JI, Fabry B et al (2013) Strain history dependence of the nonlinear stress response of fibrin and collagen networks. Proc Natl Acad Sci 110:12197–202

    Google Scholar 

  • Murtada SC, Arner A, Holzapfel GA (2012) Experiments and mechanochemical modeling of smooth muscle contraction: significance of filament overlap. J Theor Biol 297:176–186

    MathSciNet  Google Scholar 

  • Mutungi G, Ranatunga KW (1996) The viscous, viscoelastic and elastic characteristics of resting fast and slow mammalian (rat) muscle fibres. J Physiol 496:827–836

    Google Scholar 

  • Nakamura M, Ikezoe T, Takeno Y, Ichihashi N (2012) Effects of a 4-week static stretch training program on passive stiffness of human gastrocnemius muscle-tendon unit in vivo. Eur J Appl Physiol 112:2749–2755

    Google Scholar 

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

    Google Scholar 

  • Neagoe C, Opitz CA, Makarenko I, Linke WA (2003) Gigantic variety: expression patterns of titin isoforms in striated muscles and consequences for myofibrillar passive stiffness. J Muscle Res Cell Motil 24:175–189

    Google Scholar 

  • Nordez A, Cornu C, McNair P (2006) Acute effects of static stretching on passive stiffness of the hamstring muscles calculated using different mathematical models. Clin Biomech 21:755–760

    Google Scholar 

  • Nordez A, Casari P, Mariot JP, Cornu C (2009) Modeling of the passive mechanical properties of the musculo-articular complex: acute effects of cyclic and static stretching. J Biomech 42:767–773

    Google Scholar 

  • Ogneva IV (2010) Transversal stiffness of fibers and desmin content in leg muscles of rats under gravitational unloading of various durations. J Appl Physiol 109:1702–1709

    Google Scholar 

  • Oliveira Milani J, Matheus J, Gomide L, Volpon J, Shimano A (2008) Biomechanical effects of immobilization and rehabilitation on the skeletal muscle of trained and sedentary rats. Ann Biomed Eng 36:1641–1648

    Google Scholar 

  • Oomens C, Maenhout M, van Oijen C, Drost M, Baaijens F (2003) Finite element modelling of contracting skeletal muscle. Philos Trans R Soc Lond B Biol Sci 358:1453–1460

    Google Scholar 

  • Pansarasa O, Rinaldi C, Parente V, Miotti D, Capodaglio P et al (2009) Resistance training of long duration modulates force and unloaded shortening velocity of single muscle fibres of young women. J Electromyogr Kinesiol 19:e290–e300

    Google Scholar 

  • Patel T, Lieber R (1996) Force transmission in skeletal muscle: from actomyosin to external tendons. Exerc Sport Sci Rev 25:321– 363

  • Pattullo MC, Cotter MA, Cameron NE, Barry JA (1992) Effects of lengthened immobilization on functional and histochemical properties of rabbit tibialis anterior muscle. Exp Physiol 77:433– 442

  • Peters D, Barash IA, Burdi M, Yuan PS, Mathew L et al (2003) Asynchronous functional, cellular and transcriptional changes after a bout of eccentric exercise in the rat. J Physiol 553:947–957

    Google Scholar 

  • Pette D, Staron RS (2000) Myosin isoforms, muscle fiber types, and transitions. Microsc Res Tech 50:500–509

    Google Scholar 

  • Pontén E, Fridén J (2008) Immobilization of the rabbit tibialis anterior muscle in a lengthened position causes addition of sarcomeres in series and extra-cellular matrix proliferation. J Biomech 41:1801–1804

    Google Scholar 

  • Potier TG, Alexander CM, Seynnes OR (2009) Effects of eccentric strength training on biceps femoris muscle architecture and knee joint range of movement. Eur J Appl Physiol 105:939–944

    Google Scholar 

  • Prado LG, Makarenko I, Andresen C, Krüger M, Opitz C et al (2005) Isoform diversity of giant proteins in relation to passive and active contractile properties of rabbit skeletal muscles. J Gen Physiol 126:461–480

    Google Scholar 

  • Psatha M, Wu Z, Gammie FM, Ratkevicius A, Wackerhage H et al (2012) A longitudinal MRI study of muscle atrophy during lower leg immobilization following ankle fracture. J Magn Reson Imaging 35:686–695

    Google Scholar 

  • Purslow PP, Trotter JA (1994) The morphology and mechanical properties of endomysium in series-fibred muscles: variations with muscle length. J Muscle Res Cell Motil 15:299–308

    Google Scholar 

  • Rausch MK, Dam A, Göktepe S, Abilez OJ, Kuhl E (2011) Computational modeling of growth: systemic and pulmonary hypertension in the heart. Biomech Model Mechanobiol 10:799–811

    Google Scholar 

  • Reeves ND, Maganaris CN, Longo S, Narici MV (2009) Differential adaptations to eccentric versus conventional resistance training in older humans. Exp Physiol 94:825–833

    Google Scholar 

  • Reid DA, Mcnair PJ (2004) Passive Force, Angle, and Stiffness Changes after Stretching of Hamstring Muscles. Med Sci Sport Exerc 36:1944–1948

    Google Scholar 

  • Ricoy JR, Encinas AR, Cabello A, Madero S, Arenas J (1998) Histochemical study of the vastus lateralis muscle fibre types of athletes. J Physiol Biochem 54:41

    Google Scholar 

  • Röhrle O, Davidson J, Pullan A (2008) Bridging scales: a three-dimensional electromechanical finite element model of skeletal muscle. SIAM J Sci Comput 30:2882–2904

    MATH  MathSciNet  Google Scholar 

  • Röhrle O (2010) Simulating the electro-mechanical behavior of skeletal muscles. Comput Sci Eng 12:48–58

    Google Scholar 

  • Röhrle O, Davidson JB, Pullan A (2012) A physiologically based, multi-scale model of skeletal muscle structure and function. Front Physiol 3:1–14

  • Roig M, O’Brien K, Kirk G, Murray R, McKinnon P et al (2009) The effects of eccentric versus concentric resistance training on muscle strength and mass in healthy adults: a systematic review with meta-analysis. Br J Sports Med 43:556–568

    Google Scholar 

  • Roy RR, Baldwin KM, Edgerton VR (1991) The plasticity of skeletal muscle: effects of neuromuscular activity. Exerc Sport Sci Rev 19:269–312

    Google Scholar 

  • Saez P, Pena E, Martinez MA, Kuhl E (2013) Mathematical modeling of collagen turnover in biological tissue. J Math Biol 67:1765–1793

    MATH  MathSciNet  Google Scholar 

  • Sandler H (1986) Inactivity: physiological effects. Access Online via Elsevier

  • Schenk P, Siebert T, Hiepe P, Güllmar D, Reichenbach JR, Wick C, Blickhan R, Böl M (2013) Determination of three-dimensional muscle architectures: validation of the DTI-based fiber tractgraphy method by manual digitization. J Anatomy 223: 61–68

  • Scott W, Stevens J, BinderMacleod S (2001) Human skeletal muscle fiber type classifications. Phys Ther 81:1810–1816

    Google Scholar 

  • Seger JY, Arvidsson B, Thorstensson A (1998) Specific effects of eccentric and concentric training on muscle strength and morphology in humans. Eur J Appl Physiol Occup Physiol 79:49–57

    Google Scholar 

  • Seynnes OR, de Boer M, Narici MV (2007) Early skeletal muscle hypertrophy and architectural changes in response to high-intensity resistance training. J Appl Physiol 102:368–373

    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 Physiol 193:265–274

    Google Scholar 

  • Shah SB, Su FC, Jordan K, Milner DJ, Fridén J et al (2002) Evidence for increased myofibrillar mobility in desmin-null mouse skeletal muscle. J Exp Biol 205:321–325

    Google Scholar 

  • Sherwood L (2010) Human physiology: from cells to systems Cengage Learning, Belmont, USA.

  • Shoepe TC, Stelzer JE, Garner DP, Widrick JJ (2003) Functional adaptability of muscle fibers to long-term resistance exercise. Med Sci Sports Exerc 35:944–951

    Google Scholar 

  • Simoneau JA, Lortie G, Boulay MR, Marcotte M, Thibault MC et al (1985) Human skeletal muscle fiber type alteration with high-intensity intermittent training. Eur J Appl Physiol Occup Physiol 54:250–253

    Google Scholar 

  • Simpson A, Williams P (1995) The response of muscle to leg lengthening. J Bone Joint Surg 77:630–636

    Google Scholar 

  • Smith LR, Lee KS, Ward SR, Chambers HG, Lieber RL (2011) Hamstring contractures in children with spastic cerebral palsy result from a stiffer extracellular matrix and increased in vivo sarcomere length. J Physiol 589:2625–2639

    Google Scholar 

  • Storm C, Pastore JJ, MacKintosh FC, Lubensky TC, Janmey PA (2005) Nonlinear elasticity in biological gels. Nature 435:191–194

    Google Scholar 

  • Tabary J, Tabary C, Tardieu C (1972) Physiological and structural changes in the cat’s soleus muscle due to immobilization at different lengths by plaster casts. J Physiol 224:231–244

    Google Scholar 

  • Taber LA (1995) Biomechanics of growth, remodeling, and morphogenesis. Appl Mech Rev 48:487–545

    Google Scholar 

  • Taber LA (1998) Biomechanical growth laws for muscle tissue. J Theor Biol 193:201–213

    Google Scholar 

  • Talmadge R, Roy R (1996) MHC and sarcoplasmic reticulum protein isoforms in functionally overloaded cat plantaris muscle fibers. J Appl Physiol 80:1296–1303

    Google Scholar 

  • Tardieu C, Tabary JC, Tabary C, Tardieu G (1982) Adaptation of connective tissue length to immobilization in the lengthened and shortened positions in cat soleus muscle. J Physiol 78:214–220

    Google Scholar 

  • Tesch P (1988) Skeletal muscle adaptations consequent to long-term heavy resistance exercise. Med Sci Sports Exerc 20:S132–S134

    Google Scholar 

  • Thelen DG (2003) Adjustment of muscle mechanics model parameters to simulate dynamic contractions in older adults. J Biomech Eng 125:70–77

    Google Scholar 

  • Thomason D, Booth F (1990) Atrophy of the soleus muscle by hindlimb unweighting. J Appl Physiol 68:1–12

    Google Scholar 

  • Tidball JG (2005) Mechanical signal transduction in skeletal muscle growth and adaptation. J Appl Physiol 98:1900–1908

    Google Scholar 

  • Toursel T, Stevens L, Granzier H, Mounier Y (2002) Passive tension of rat skeletal soleus muscle fibers: effects of unloading conditions. J Appl Physiol 92:1465–1472

    Google Scholar 

  • Trappe S (2002) Effects of spaceflight, simulated spaceflight and countermeasures on single muscle fiber physiology. J Gravit Physiol 9:P323–P326

    Google Scholar 

  • Trappe S, Trappe T, Gallagher P, Harber M, Alkner B et al (2004) Human single muscle fibre function with 84 day bed-rest and resistance exercise. J Physiol 557:501–513

    Google Scholar 

  • Tskhovrebova L, Trinick J, Sleep JA, Simmons R (1997) Elasticity and unfolding of single molecules of the giant muscle protein titin. Nature 387:308–312

    Google Scholar 

  • Wang K, Ramirez-Mitchell R (1983) A network of transverse and longitudinal intermediate filaments is associated with sarcomeres of adult vertebrate skeletal muscle. J Cell Biol 96:562–570

    Google Scholar 

  • Wickiewicz T, Roy R (1983) Muscle architecture of the human lower limb. Clin Orthop Relat Res 179:275–283

    Google Scholar 

  • Widrick J, Romatowski J, Bain J, Trappe S, Trappe T et al (1997) Effect of 17 days of bed rest on peak isometric force and unloaded shortening velocity of human soleus fibers. Am J Physiol Physiol 273:C1690–C1699

    Google Scholar 

  • Widrick JJ, Knuth ST, Norenberg KM, Romatowski JG, Bain JL et al (1999) Effect of a 17 day spaceflight on contractile properties of human soleus muscle fibres. J Physiol 516:915–930

  • Widrick JJ, Trappe SW, Romatowski JG, Da Riley, Costill DL et al (2002) Unilateral lower limb suspension does not mimic bed rest or spaceflight effects on human muscle fiber function. J Appl Physiol 93:354–360

  • Williams PE, Goldspink G (1971) Longitudinal growth of striated muscle fibres. J Cell Sci 9:751–767

    Google Scholar 

  • Williams PE, Goldspink G (1973) The effect of immobilization on the longitudinal growth of striated muscle fibres. J Anat 116:45–55

    Google Scholar 

  • Williams PE, Goldspink G (1978) Changes in sarcomere length and physiological properties in immobilized muscle. J Anat 127:459–468

    Google Scholar 

  • Williams P, Goldspink G (1984) Connective tissue changes in immobilised muscle. J Anat 138:343–350

    Google Scholar 

  • Williams P, Catanese T (1988) The importance of stretch and contractile activity in the prevention of connective tissue accumulation in muscle. J Anat 158:109–114

    Google Scholar 

  • Williams P, Kyberd P, Simpson H, Kenwright J, Goldspink G (1998) The morphological basis of increased stiffness of rabbit tibialis anterior muscles during surgical limb lengthening. J Anat 193:131–138

    Google Scholar 

  • Williamson D (2001) Reduction in hybrid single muscle fiber proportions with resistance training in humans. J Appl Physiol 91:1955–1961

    Google Scholar 

  • Woo S, Matthews J, Akeson W, Amiel D, Convery F (1975) Connective tissue response to immobility. Arthritis Rheum 18:257–264

    Google Scholar 

  • Wren T (2003) A computational model for the adaptation of muscle and tendon length to average muscle length and minimum tendon strain. J Biomech 36:1117–1124

    Google Scholar 

  • Yasuda N, Glover EI, Phillips SM, Isfort RJ, Tarnopolsky MA (2005) Sex-based differences in skeletal muscle function and morphology with short-term limb immobilization. J Appl Physiol 99:1085–1092

    Google Scholar 

  • Ye F, Baligand C, Keener JE, Vohra R, Lim W et al (2013) Hindlimb muscle morphology and function in a new atrophy model combining spinal cord injury and cast immobilization. J Neurotrauma 30:227–235

    Google Scholar 

  • Yokogawa M, Yamazaki T, Inoue K, Inaoka P, Tsuji K et al (2008) Age-associated changes in atrophy of the extensor digitorum longus muscle in hindlimb-suspended rats. J Phys Ther Sci 20:129–133

    Google Scholar 

  • Yu JG, Carlsson L, Thornell LE (2004) Evidence for myofibril remodeling as opposed to myofibril damage in human muscles with DOMS: an ultrastructural and immunoelectron microscopic study. Histochem Cell Biol 121:219–227

    Google Scholar 

  • Yucesoy CA, Koopman BHFJM, Baan GC, Grootenboer HJ, Huijing PA (2003) Effects of inter- and extramuscular myofascial force transmission on adjacent synergistic muscles: assessment by experiments and finite-element modeling. J Biomech 36:1797–1811

  • Zhou M, Klitgaard H, Saltin B, Roy R, Edgerton V et al (1995) Myosin heavy chain isoforms of human muscle after short-term spaceflight. J Appl Physiol 78:1740–1744

    Google Scholar 

  • Zöllner AM, Abilez O, Böl M, Kuhl E (2012) Stretching skeletal muscle: chronic muscle lengthening through sarcomerogenesis. PLoS One 7:e45661

    Google Scholar 

Download references

Acknowledgments

This work was supported by the National Science Foundation Graduate Research Fellowship and by the Stanford Graduate Engineering Fellowship to Katrina Wisdom, by the National Institutes of Health Grants R24 HD065690 and U54 GM072970 to Scott Delp, and by the National Science Foundation CAREER award CMMI 0952021 and INSPIRE grant 1233054 and by the National Institutes of Health Grant U01 HL119578 to Ellen Kuhl. Thank you to Dr Richard Lieber, Alexander Real, Aleksandra Denisin, and Alexander Zöllner for helpful conversations, and to David Delp for the illustrations.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Ellen Kuhl.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Wisdom, K.M., Delp, S.L. & Kuhl, E. Use it or lose it: multiscale skeletal muscle adaptation to mechanical stimuli. Biomech Model Mechanobiol 14, 195–215 (2015). https://doi.org/10.1007/s10237-014-0607-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10237-014-0607-3

Keywords

Navigation