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Erschienen in: European Journal of Applied Physiology 6/2017

27.03.2017 | Invited Review

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

verfasst von: Brian R. MacIntosh

Erschienen in: European Journal of Applied Physiology | Ausgabe 6/2017

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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.
Literatur
Zurück zum Zitat 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 29:627–633CrossRefPubMed 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 29:627–633CrossRefPubMed
Zurück zum Zitat 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):3193–3200CrossRefPubMed 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):3193–3200CrossRefPubMed
Zurück zum Zitat Blix M (1891) Die lange und die spannung des muskels. Skandinavische Archiv fur Physiologie 3 295–318CrossRef Blix M (1891) Die lange und die spannung des muskels. Skandinavische Archiv fur Physiologie 3 295–318CrossRef
Zurück zum Zitat Blix M (1892) Die lange und die spannung des muskels. Skandinavische Archiv fur Physiologie 4:10 Blix M (1892) Die lange und die spannung des muskels. Skandinavische Archiv fur Physiologie 4:10
Zurück zum Zitat Blix M (1894) Die lange und die spannung des muskels. Skandinavische Archiv fur Physiologie 5:57 Blix M (1894) Die lange und die spannung des muskels. Skandinavische Archiv fur Physiologie 5:57
Zurück zum Zitat 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):323–329CrossRefPubMed 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):323–329CrossRefPubMed
Zurück zum Zitat 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):627–643CrossRefPubMed 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):627–643CrossRefPubMed
Zurück zum Zitat 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):1518–1524CrossRefPubMed 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):1518–1524CrossRefPubMed
Zurück zum Zitat 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 81:182–196CrossRefPubMed 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 81:182–196CrossRefPubMed
Zurück zum Zitat Fletcher JR, Esau SP, MacIntosh BR (2010) Changes in tendon stiffness and running economy in highly trained distance runners. Eur J Appl Physiol 110:1037–1046CrossRefPubMed Fletcher JR, Esau SP, MacIntosh BR (2010) Changes in tendon stiffness and running economy in highly trained distance runners. Eur J Appl Physiol 110:1037–1046CrossRefPubMed
Zurück zum Zitat 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 CrossRef 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 CrossRef
Zurück zum Zitat 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):206CrossRefPubMed 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):206CrossRefPubMed
Zurück zum Zitat Gordon AM, Huxley AF, Julian FJ (1966) The variation in isometric tension with sarcomere length in vertebrate muscle fibres. J Physiol 184(1):170–192CrossRefPubMedPubMedCentral Gordon AM, Huxley AF, Julian FJ (1966) The variation in isometric tension with sarcomere length in vertebrate muscle fibres. J Physiol 184(1):170–192CrossRefPubMedPubMedCentral
Zurück zum Zitat Grange RW, Vandenboom R, Houston ME (1993) Physiological significance of myosin phosphorylation in skeletal muscle. Can J Appl Physiol 18(3):229–242CrossRefPubMed Grange RW, Vandenboom R, Houston ME (1993) Physiological significance of myosin phosphorylation in skeletal muscle. Can J Appl Physiol 18(3):229–242CrossRefPubMed
Zurück zum Zitat 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):1289–1296CrossRefPubMed 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):1289–1296CrossRefPubMed
Zurück zum Zitat 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, 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
Zurück zum Zitat Herzog W, Kamal S, Clarke HD (1992) Myofilament lengths of cat skeletal muscle: theoretical considerations and functional implications. J Biomech 25:945–948CrossRefPubMed Herzog W, Kamal S, Clarke HD (1992) Myofilament lengths of cat skeletal muscle: theoretical considerations and functional implications. J Biomech 25:945–948CrossRefPubMed
Zurück zum Zitat Hill AV (1953) The mechanics of active muscle. Proc R Soc Lond Ser B Biol Sci 141:104–117CrossRef Hill AV (1953) The mechanics of active muscle. Proc R Soc Lond Ser B Biol Sci 141:104–117CrossRef
Zurück zum Zitat Huxley AF (1957) Muscle structure and theories of contraction. Prog Biophys Biophys Chem 7:255–318PubMed Huxley AF (1957) Muscle structure and theories of contraction. Prog Biophys Biophys Chem 7:255–318PubMed
Zurück zum Zitat 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):78–83CrossRefPubMed 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):78–83CrossRefPubMed
Zurück zum Zitat Kawakami Y, Fukunaga T (2006) New insights into in vivo human skeletal muscle function. Exerc Sport Sci Rev 34(1):16–21CrossRefPubMed Kawakami Y, Fukunaga T (2006) New insights into in vivo human skeletal muscle function. Exerc Sport Sci Rev 34(1):16–21CrossRefPubMed
Zurück zum Zitat 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):13716–13721CrossRefPubMedPubMedCentral 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):13716–13721CrossRefPubMedPubMedCentral
Zurück zum Zitat Levin A, Wyman J (1927) The viscous elastic properties of muscle. Proc R Soc Lond Ser B Biol Sci 101:218–243CrossRef Levin A, Wyman J (1927) The viscous elastic properties of muscle. Proc R Soc Lond Ser B Biol Sci 101:218–243CrossRef
Zurück zum Zitat 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 71:898–907CrossRefPubMedPubMedCentral 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 71:898–907CrossRefPubMedPubMedCentral
Zurück zum Zitat Lieber RL, Loren GJ, Friden J (1994) In vivo measurement of human wrist extensor muscle sarcomere length changes. J Neurophysiol 71:874–881PubMed Lieber RL, Loren GJ, Friden J (1994) In vivo measurement of human wrist extensor muscle sarcomere length changes. J Neurophysiol 71:874–881PubMed
Zurück zum Zitat 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:612–618CrossRef 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:612–618CrossRef
Zurück zum Zitat MacIntosh BR (2003) Role of calcium sensitivity modulation in skeletal muscle performance. News Physiol Sci 18:222–225PubMed MacIntosh BR (2003) Role of calcium sensitivity modulation in skeletal muscle performance. News Physiol Sci 18:222–225PubMed
Zurück zum Zitat MacIntosh BR, Bryan SN (2002) Potentiation of shortening and velocity of shortening during repeated isotonic tetanic contractions. Pflügers Archiv 443:804–812CrossRefPubMed MacIntosh BR, Bryan SN (2002) Potentiation of shortening and velocity of shortening during repeated isotonic tetanic contractions. Pflügers Archiv 443:804–812CrossRefPubMed
Zurück zum Zitat MacIntosh BR, MacNaughton MB (2005) The length dependence of muscle active force: considerations for parallel elastic properties. J Appl Physiol 98(5):1666–1673CrossRefPubMed MacIntosh BR, MacNaughton MB (2005) The length dependence of muscle active force: considerations for parallel elastic properties. J Appl Physiol 98(5):1666–1673CrossRefPubMed
Zurück zum Zitat MacNaughton MB, MacIntosh BR (2006) Reports of the length dependence of fatigue are greatly exaggerated. J Appl Physiol 101:23–29CrossRefPubMed MacNaughton MB, MacIntosh BR (2006) Reports of the length dependence of fatigue are greatly exaggerated. J Appl Physiol 101:23–29CrossRefPubMed
Zurück zum Zitat 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):271–278CrossRef 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):271–278CrossRef
Zurück zum Zitat Maganaris CN (2001) Force–length characteristics of in vivo human skeletal muscle. Acta Physiol Scand 172(4):279–285CrossRefPubMed Maganaris CN (2001) Force–length characteristics of in vivo human skeletal muscle. Acta Physiol Scand 172(4):279–285CrossRefPubMed
Zurück zum Zitat Maganaris CN (2003) Force–length characteristics of the in vivo human gastrocnemius muscle. Clin Anat 16(3):215–223CrossRefPubMed Maganaris CN (2003) Force–length characteristics of the in vivo human gastrocnemius muscle. Clin Anat 16(3):215–223CrossRefPubMed
Zurück zum Zitat 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):428–445CrossRefPubMed 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):428–445CrossRefPubMed
Zurück zum Zitat 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, 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
Zurück zum Zitat Rassier DE, MacIntosh BR, Herzog W (1999) Length dependence of active force production in skeletal muscle. J Appl Physiol 86(5):1445–1457PubMed Rassier DE, MacIntosh BR, Herzog W (1999) Length dependence of active force production in skeletal muscle. J Appl Physiol 86(5):1445–1457PubMed
Zurück zum Zitat 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 333:637–653CrossRefPubMedPubMedCentral 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 333:637–653CrossRefPubMedPubMedCentral
Zurück zum Zitat ter Keurs HEDJ, Iwazumi T, Pollack GH (1978) The sarcomere length-tension relation in skeletal muscle. J Gen Physiol 72:565–592CrossRefPubMed ter Keurs HEDJ, Iwazumi T, Pollack GH (1978) The sarcomere length-tension relation in skeletal muscle. J Gen Physiol 72:565–592CrossRefPubMed
Zurück zum Zitat 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 46:703–714CrossRefPubMed 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 46:703–714CrossRefPubMed
Zurück zum Zitat 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 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
Zurück zum Zitat 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 122:139–148CrossRefPubMed 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 122:139–148CrossRefPubMed
Metadaten
Titel
Recent developments in understanding the length dependence of contractile response of skeletal muscle
verfasst von
Brian R. MacIntosh
Publikationsdatum
27.03.2017
Verlag
Springer Berlin Heidelberg
Erschienen in
European Journal of Applied Physiology / Ausgabe 6/2017
Print ISSN: 1439-6319
Elektronische ISSN: 1439-6327
DOI
https://doi.org/10.1007/s00421-017-3591-3

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