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Recent developments in understanding the length dependence of contractile response of skeletal muscle

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Abstract

Maximal active force of skeletal muscle contraction occurs at a sarcomere length where overlap of thick and thin filaments is optimal. However, the interaction of muscle length and active force is complicated. Active force, is the force generated by energy-requiring processes. To calculate active force, passive force provided by in-parallel structures must be subtracted from total force. Sarcomere length will change during a contraction with constant muscle–tendon length, due to tendon stretch. Passive force therefore changes during the contraction. Taking this into account, it has been demonstrated that there is less length dependence of fatigue than previously thought. The remaining difference may be associated with length dependence of activation, a property that is evident with submaximal activation. The sarcomere length at which peak contraction occurs is longer than the length that gives optimal overlap of the filaments and this shift of optimal length appears to be due to increased Ca2+ sensitivity. The increased Ca2+ sensitivity occurs because at longer lengths, the myofilaments are closer together allowing greater force than expected. However, the potential for length-dependent activation has been challenged. Submaximal contractions obtained by recruitment of fewer motor units but with maximal stimulation across different muscle lengths still demonstrate length-dependent activation. In contrast, contractions with similar absolute electromyographic signal magnitude at different lengths do not demonstrate length-dependent activation. Recent work has improved our understanding of how sarcomere length impacts the force of contraction but also reveals inadequacies in our knowledge that need to be addressed by additional research.

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Fig. 1
Fig. 2
Fig. 3
Fig. 4

Source: MacNaughton et al. 2007 with permission of the author. Muscle length is presented as mm difference from the original optimal length determined with double pulse stimulation at high frequency. Optimal length for 50 Hz contractions occurs at a length longer than the optimum for double-pulse stimulation at 200 Hz

Fig. 5

Source: MacNaughton et al. 2007 with permission of the author

Fig. 6
Fig. 7

Source: MacNaughton et al. 2007 with permission of the author. (Color figure online)

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Abbreviations

%:

Percent

Ca2+ :

Calcium ion

mM:

Millimolar (millimoles per liter)

Nm:

Nanometer

µm:

Micrometer

References

  • Abbott BC, Aubert XM (1952) The force exerted by active striated muscle during and after change of length. J Physiol 117:77–86

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Allinger TL, Epstein M, Herzog W (1996) Stability of muscle fibers on the descending limb of the force–length relation. A theoretical consideration. J Biomech 29:627–633

    Article  CAS  PubMed  Google Scholar 

  • Arampatzis A, Mademli L, De Monte G, Walsh M (2007) Changes in fascicle length from rest to maximal voluntary contraction affect the assessment of voluntary activation. J Biomech 40(14):3193–3200

    Article  PubMed  Google Scholar 

  • Azizi E, Roberts TJ (2010) Muscle performance during frog jumping: influence of elasticity on muscle operating lengths. Proc R Soc B Biol Sci 277(1687):1523–1530. doi:10.1098/rspb.2009.2051

    Article  Google Scholar 

  • Bagni MA, Cecchi G, Colomo F (1990) Myofilament spacing and force generation in intact frog muscle fibres. J Physiol 430:61–75

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Blix M (1891) Die lange und die spannung des muskels. Skandinavische Archiv fur Physiologie 3 295–318

    Article  Google Scholar 

  • Blix M (1892) Die lange und die spannung des muskels. Skandinavische Archiv fur Physiologie 4:10

    Google Scholar 

  • Blix M (1894) Die lange und die spannung des muskels. Skandinavische Archiv fur Physiologie 5:57

    Google Scholar 

  • Bobbert MF, Ettema GC, Huijing PA (1990) The force–length relationship of a muscle-tendon complex: experimental results and model calculations. Eur J Appl Physiol Occup Physiol 61(3–4):323–329

    Article  CAS  PubMed  Google Scholar 

  • Brown IE, Cheng EJ, Loeb GE (1999) Measured and modeled properties of mammalian skeletal muscle. II. The effects of stimulus frequency on force–length and force–velocity relationships. J Muscle Res Cell Motil 20(7):627–643

    Article  CAS  PubMed  Google Scholar 

  • Bullimore SR, Leonard TR, Rassier DE, Herzog W (2007) History-dependence of isometric muscle force: effect of prior stretch or shortening amplitude. J Biomech 40(7):1518–1524

    Article  PubMed  Google Scholar 

  • Edman KAP, Kiessling A (1971) The time course of the active state in relation to sarcomere length and movement studied in single skeletal muscle fibres of the frog. Acta Physiol Scand 81:182–196

    Article  CAS  PubMed  Google Scholar 

  • Fletcher JR, Esau SP, MacIntosh BR (2010) Changes in tendon stiffness and running economy in highly trained distance runners. Eur J Appl Physiol 110:1037–1046

    Article  PubMed  Google Scholar 

  • Fontana HdB, Herzog W (2016) Vastus lateralis maximum force-generating potential occurs at optimal fascicle length regardless of activation level. Eur J Appl Physiol 116:1267–1277. doi:10.1007/s00421-016-3381-3

    Article  Google Scholar 

  • Gerritsen KGM, van den Bogert AJ, Hulliger M, Zernicke RF (1998) Intrinsic muscle properties facilitate locomotor control—a computer simulation study. Motor Control 2(3):206

    Article  CAS  PubMed  Google Scholar 

  • Gordon AM, Huxley AF, Julian FJ (1966) The variation in isometric tension with sarcomere length in vertebrate muscle fibres. J Physiol 184(1):170–192

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Grange RW, Vandenboom R, Houston ME (1993) Physiological significance of myosin phosphorylation in skeletal muscle. Can J Appl Physiol 18(3):229–242

    Article  CAS  PubMed  Google Scholar 

  • Herzog W, Guimaraes AC, Anton MG, Carter-Erdman KA (1991) Moment-length relations of rectus femoris muscles of speed skaters/cyclists and runners. Med Sci Sports Exerc 23(11):1289–1296

    Article  CAS  PubMed  Google Scholar 

  • Herzog W, Abrahamse SK, ter Keurs HEDJ (1990) Theoretical determination of force-length relations of intact human skeletal muscles using the cross-bridge model. Pflugers Archiv 416(1-2):113-119

  • Herzog W, Kamal S, Clarke HD (1992) Myofilament lengths of cat skeletal muscle: theoretical considerations and functional implications. J Biomech 25:945–948

    Article  CAS  PubMed  Google Scholar 

  • Hill AV (1953) The mechanics of active muscle. Proc R Soc Lond Ser B Biol Sci 141:104–117

    Article  CAS  Google Scholar 

  • Holt NC, Azizi E (2014) What drives activation-dependent shifts in the force–length relationship. Biol Lett 10:4. doi:10.1098/rsbl.2014.0651

    Article  Google Scholar 

  • Huxley AF (1957) Muscle structure and theories of contraction. Prog Biophys Biophys Chem 7:255–318

    CAS  PubMed  Google Scholar 

  • Ichinose Y, Kawakami Y, Ito M, Fukunaga T (1997) Estimation of active force–length characteristics of human vastus lateralis muscle. Acta Anat 159(0001–5180):78–83

    Article  CAS  PubMed  Google Scholar 

  • Jewell BR, Wilkie DR (1958) An analysis of the mechanical components in frog’s striated muscle. J Physiol 143:515–540

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kawakami Y, Fukunaga T (2006) New insights into in vivo human skeletal muscle function. Exerc Sport Sci Rev 34(1):16–21

    Article  PubMed  Google Scholar 

  • Labeit D, Watanabe K, Witt C, Fujita H, Wu Y, Lahmers S, Funck T, Labeit S, Granzier H (2003) Calcium-dependent molecular spring elements in the giant protein titin. Proc Natl Acad Sci 100(23):13716–13721

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Levin A, Wyman J (1927) The viscous elastic properties of muscle. Proc R Soc Lond Ser B Biol Sci 101:218–243

    Article  Google Scholar 

  • Levine RJC, Kensler RW, Yang ZH, Stull JT, Sweeney HL (1996) Myosin light chain phosphorylation affects the structure of rabbit skeletal muscle thick filaments. Biophys J 71:898–907

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lieber RL, Loren GJ, Friden J (1994) In vivo measurement of human wrist extensor muscle sarcomere length changes. J Neurophysiol 71:874–881

    CAS  PubMed  Google Scholar 

  • Lieber RL, Ponten E, Burkholder TJ, Friden J (1996) Sarcomere length changes after flexor carpi ulnaris to extensor digitorum communis tendon transfer. J Hand Surg [Am] 21A:612–618

    Article  Google Scholar 

  • MacIntosh BR (2003) Role of calcium sensitivity modulation in skeletal muscle performance. News Physiol Sci 18:222–225

    CAS  PubMed  Google Scholar 

  • MacIntosh BR, Bryan SN (2002) Potentiation of shortening and velocity of shortening during repeated isotonic tetanic contractions. Pflügers Archiv 443:804–812

    Article  CAS  PubMed  Google Scholar 

  • MacIntosh BR, MacNaughton MB (2005) The length dependence of muscle active force: considerations for parallel elastic properties. J Appl Physiol 98(5):1666–1673

    Article  PubMed  Google Scholar 

  • MacIntosh BR, Rassier DE (2002) What is fatigue? Can J Appl Physiol 27(1):42–55

    Article  CAS  PubMed  Google Scholar 

  • MacNaughton MB, MacIntosh BR (2006) Reports of the length dependence of fatigue are greatly exaggerated. J Appl Physiol 101:23–29

    Article  CAS  PubMed  Google Scholar 

  • MacNaughton MB, Campbell JJ, MacIntosh BR (2007) Dantrolene, like fatigue, has a length-dependent effect on submaximal force–length relationships of rat gastrocnemius muscle. Acta Physiol (Oxf) 189(3):271–278

    Article  CAS  Google Scholar 

  • Maganaris CN (2001) Force–length characteristics of in vivo human skeletal muscle. Acta Physiol Scand 172(4):279–285

    Article  CAS  PubMed  Google Scholar 

  • Maganaris CN (2003) Force–length characteristics of the in vivo human gastrocnemius muscle. Clin Anat 16(3):215–223

    Article  PubMed  Google Scholar 

  • Martyn DA, Gordon AM (1988) Length and myofilament spacing-dependent changes in calcium sensitivity of skeletal fibres: effects of pH and ionic strength. J Muscle Res Cell Motil 9(5):428–445

    Article  CAS  PubMed  Google Scholar 

  • Rack PMH, Westbury DR (1969) The effects of length and stimulus rate on tension in the isometric cat soleus muscle. J Physiol 204(2):443–460

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ramsey RW, Street SF (1940) The isometric length-tension diagram of isolated skeletal muscle fibers of the frog. J Cell Comp Physiol 15(1):11–34. doi:10.1002/jcp.1030150103

    Article  CAS  Google Scholar 

  • Rassier DE, MacIntosh BR (2002) Length-dependent twitch contractile characteristics of skeletal muscle. Can J Physiol Pharmacol 80(10):993–1000. doi:10.1139/Y02-127

    Article  CAS  PubMed  Google Scholar 

  • Rassier DE, Tubman LA, MacIntosh BR (1997) Length-dependent potentiation and myosin light chain phosphorylation in rat gastrocnemius muscle. Am J Physiol Cell Physiol 273(1 Pt 1):C198–C204

  • Rassier DE, MacIntosh BR, Herzog W (1999) Length dependence of active force production in skeletal muscle. J Appl Physiol 86(5):1445–1457

    CAS  PubMed  Google Scholar 

  • Scott SH, Brown IE, Loeb GE (1996) Mechanics of feline soleus: I. Effect of fascicle length and velocity on force output. J Muscle Res Cell Motil 17(2):207–219. doi:10.1007/BF00124243

    Article  CAS  PubMed  Google Scholar 

  • Spector SA, Simard CP, Fournier M, Sternlicht E, Edgerton VR (1982) Architectural alterations of rat hind-limb skeletal muscles immobilized at different lengths. Exp Neurol 76(1):94–110. doi:10.1016/0014-4886(82)90104-2

    Article  CAS  PubMed  Google Scholar 

  • Stephenson DG, Williams DA (1982) Effects of sarcomere length on the force–pCa relation in fast- and slow-twitch skinned muscle fibres from the rat. J Physiol 333:637–653

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • ter Keurs HEDJ, Iwazumi T, Pollack GH (1978) The sarcomere length-tension relation in skeletal muscle. J Gen Physiol 72:565–592

    Article  CAS  PubMed  Google Scholar 

  • ter Keurs HEDJ, Rijnsburger WH, van Heuningen R, Nagelsmit MJ (1980) Tension development and sarcomere length in rat cardiac trabeculae: evidence of length-dependent activation. Circ Res 46:703–714

    Article  CAS  PubMed  Google Scholar 

  • Walker SM, Schrodt GR (1974) I segment lengths and thin filament periods in skeletal muscle fibers of the rhesus monkey and the human. Anat Rec 178(1):63-81

  • Wakahara T, Kanehisa H, Kawakami Y, Fukunaga T (2007) Fascicle behavior of medial gastrocnemius muscle in extended and flexed knee positions. J Biomech 40(10):2291–2298. doi:10.1016/j.jbiomech.2006.10.006

    Article  PubMed  Google Scholar 

  • Yang Z, Stull JT, Levine RJ, Sweeney HL (1998) Changes in interfilament spacing mimic the effects of myosin regulatory light chain phosphorylation in rabbit psoas fibers. J Struct Biol 122:139–148

    Article  CAS  PubMed  Google Scholar 

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Authors and Affiliations

  1. Faculty of Kinesiology, University of Calgary, Calgary, AB, Canada

    Brian R. MacIntosh

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  1. Brian R. MacIntosh
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Correspondence to Brian R. MacIntosh.

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Communicated by Nigel A. S. Taylor.

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MacIntosh, B.R. Recent developments in understanding the length dependence of contractile response of skeletal muscle. Eur J Appl Physiol 117, 1059–1071 (2017). https://doi.org/10.1007/s00421-017-3591-3

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