Skip to main content
SpringerLink
Log in
Book cover

Muscle Biophysics pp 223–246Cite as

Short-Range Mechanical Properties of Skeletal and Cardiac Muscles

  • Chapter
  • First Online:

Part of the book series: Advances in Experimental Medicine and Biology ((AEMB,volume 682))

Abstract

Striated muscles are disproportionately stiff for small movements. This facet of their behavior can be demonstrated by measuring the force produced when the muscle is stretched more than about 1% of its initial length. When this is done, it can be seen that force rises rapidly during the initial phases of the movement and much less rapidly during the latter stages of the stretch. Experiments performed using chemically permeabilized skeletal and cardiac muscles show that the initial stiffness of the preparations increases in proportion with isometric force as the free Ca2+ concentration in the bathing solution is raised from a minimal to a saturating value. This is strong evidence that the short-range mechanical properties of activated muscle result from stretching myosin cross-bridges that are attached between the thick and thin filaments. Relaxed intact muscles also exhibit short-range mechanical properties but the molecular mechanisms underlying this behavior are less clear. This chapter summarizes some of the interesting features of short-range mechanical properties in different types of muscle preparation, describes some of the likely underlying mechanisms and discusses the potential physiological significance of the behavior.

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

Chapter
USD   29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD   169.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD   279.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD   219.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Learn about institutional subscriptions

References

  • 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  PubMed  CAS  Google Scholar 

  • Axelson HW, Hagbarth KE (2001) Human motor control consequences of thixotropic changes in muscular short-range stiffness. J Physiol 535(1):279–288

    Article  PubMed  CAS  Google Scholar 

  • Axelson HW, Hagbarth KE (2003) Human motor compensations for thixotropy-dependent changes in resting wrist joint position after large joint movements. Acta Physiol Scand 179:389–398

    Article  PubMed  CAS  Google Scholar 

  • Bagni MA, Cecchi G, Colombini B, Colomo F (2002) A non-cross-bridge stiffness in activated frog muscle fibers. Biophys J 82:3118–3127

    Article  PubMed  CAS  Google Scholar 

  • Bagni MA, Colombini B, Geiger P, Berlinguer Palmini R, Cecchi G (2004) A non cross-bridge calcium-dependent stiffness in frog muscle fibers. Am J Physiol Cell Physiol 286:C1353–C1357

    Article  PubMed  CAS  Google Scholar 

  • Bers DM (1991) Excitation-contraction coupling and cardiac contractile force. Kluwer, Dordrecht

    Google Scholar 

  • Bianco P, Nagy A, Kengyel A, Szatmári D, Mártonfalvi Z, Huber T, Kellermayer MSZ (2007) Interaction forces between F-actin and titin PEVK domain measured with optical tweezers. Biophys J 93:2102–2109

    Article  PubMed  CAS  Google Scholar 

  • Blair GWS (1969) Elementary rheology, Academic, London

    Google Scholar 

  • Brenner B (1988) Effect of Ca2+ on cross-bridge turnover kinetics in skinned single rabbit psoas fibers: Implications for regulation of muscle contraction. Proc Natl Acad Sci USA 85:3265–3269

    Article  PubMed  CAS  Google Scholar 

  • Buchthal F, Kaiser E (1951) The rheology of the cross striated muscle fibre with particular reference to isotonic conditions. Vol. 21.7. Det Kongelige Danske Videnskabernes Selskab Biologiske Meddelser, Copenhagen

    Google Scholar 

  • Campbell KS (2006) Filament compliance effects can explain tension overshoots during force development. Biophys J 91:4102–4109

    Article  PubMed  CAS  Google Scholar 

  • Campbell KS (2009) Short-range mechanical properties simulated with a mechanical mdoel incorporating multiple half-sarcomeres. Biophys J 96:615a

    Article  Google Scholar 

  • Campbell KS, Holbrook AM (2006) Myocardial stiffness in experimental conditions that mimic ischemia. Biophys J 90:1270A

    Article  Google Scholar 

  • Campbell KS, Lakie M (1995) Tension responses to imposed length changes in isolated relaxed muscle fibre bundles from Rana temporaria. J Physiol 487:155–156P

    Google Scholar 

  • Campbell KS, Lakie M (1998) A cross-bridge mechanism can explain the thixotropic short-range elastic component of relaxed frog skeletal muscle. J Physiol 510.3:941–962

    Article  PubMed  CAS  Google Scholar 

  • Campbell KS, Lakie M (2008) Response to Bianco et al.: Interaction forces between F-actin and titin PEVK domain measured with optical tweezers. Biophys J 94:327–328; 329–330

    Article  PubMed  CAS  Google Scholar 

  • Campbell KS, Moss RL (2000) A thixotropic effect in contracting rabbit psoas muscle: prior movement reduces the initial tension response to stretch. J Physiol 525(2):531–548

    Article  PubMed  CAS  Google Scholar 

  • Campbell KS, Moss RL (2002) History-dependent mechanical properties of permeabilized rat soleus muscle fibers. Biophys J 82:929–943

    Article  PubMed  CAS  Google Scholar 

  • Campbell KS, Moss RL (2003) SLControl: PC-based data acquisition and analysis for muscle mechanics. Am J Physiol Heart Circ Physiol 285:H2857–H2864

    PubMed  CAS  Google Scholar 

  • Campbell KS, Patel JR, Moss RL (2003) Cycling cross-bridges increase myocardial stiffness at sub-maximal levels of Ca2+ activation. Biophys J 84:3807–3815

    Article  PubMed  CAS  Google Scholar 

  • Carnes CA, Geisbuhler TP, Reiser PJ (2004) Age-dependent changes in contraction and regional myocardial myosin heavy chain isoform expression in rats. J Appl Physiol 97:446–453

    Article  PubMed  CAS  Google Scholar 

  • Denny-Brown D (1929) On the nature of postural reflexes. Proc R Soc Lond B Biol Sci 104:252–301

    Article  Google Scholar 

  • Edman KA, Elzinga G, Noble MI (1981) Critical sarcomere extension required to recruit a decaying component of extra force during stretch in tetanic contractions of frog skeletal muscle fibers. J Gen Physiol 78:365–382

    Article  PubMed  CAS  Google Scholar 

  • Endo M (1973) Length dependence of activation of skinned muscle fibres by calcium. Cold Spring Harb Symp Quant Biol 37:505–510

    Article  CAS  Google Scholar 

  • Farman GP, Tachampa K, Mateja R, Cazorla O, Lacampagne A, de Tombe PP (2008) Blebbistatin: use as inhibitor of muscle contraction. Pflugers Arch 455:995–1005

    Article  PubMed  CAS  Google Scholar 

  • Feng TP (1932) The thermo-elastic properties of muscle. J Physiol 74:455–470

    PubMed  CAS  Google Scholar 

  • Ford LE, Huxley AF, Simmons RM (1977) Tension responses to sudden length change in stimulated frog muscle fibres near slack length. J Physiol 269:441–515

    PubMed  CAS  Google Scholar 

  • Fujita H, Labeit D, Gerull B, Labeit S, Granzier HL (2004) Titin isoform-dependent effect of calcium on passive myocardial tension. Am J Physiol Heart Circ Physiol 287:H2528–H2534

    Article  PubMed  CAS  Google Scholar 

  • Gao WD, Backx PH, Azan-Backz M, Marban E (1994) Myofilament Ca2+ sensitivity in intact versus skinned rat ventricular muscle. Circ Res 74:408–415

    Article  PubMed  CAS  Google Scholar 

  • Getz EB, Cooke R, Lehman SL (1998) Phase transition in force during ramp stretches of skeletal muscle. Biophys J 75:2971–2983

    Article  PubMed  CAS  Google Scholar 

  • Granzier HL, Irving TC (1995) Passive tension in cardiac muscles: contribution of collagen, titin, microtubules, and intermediate filaments. Biophys J 68:1027–1044

    Article  PubMed  CAS  Google Scholar 

  • Granzier H, Labeit S (2002) Cardiac titin: an adjustable multi-functional spring. J Physiol 541:335–342

    Article  PubMed  CAS  Google Scholar 

  • Gunst SJ (1983) Contractile force of canine airway smooth muscle during cyclical length changes. J Appl Physiol 55:759–769

    PubMed  CAS  Google Scholar 

  • Harris J (1977) Rheology and non-Newtonian flow. Longman, London and New York

    Google Scholar 

  • Harris SP, Shaffer JF, Bezold KL, Kensler RW (2009) Switching gears with myosin binding protein-C. Biophys J 96:4A

    Article  Google Scholar 

  • Haugen P, Sten-Knudsen O (1981) The dependence of the short-range elasticity on sarcomere length in resting isolated frog muscle fibres. Acta Physiol Scand 112:113–120

    Article  PubMed  CAS  Google Scholar 

  • Herbst M (1976) Studies on the relation between latency relaxation and resting cross-bridges of frog skeletal muscle. Pflugers Arch 364:71–76

    Article  PubMed  CAS  Google Scholar 

  • Hill AV (1965) Trails and trials in physiology. Edward Arnold, London

    Google Scholar 

  • Hill DK (1968) Tension due to interaction between the sliding filaments in resting striated muscle. The effect of stimulation. J Physiol 199:637–684

    PubMed  CAS  Google Scholar 

  • Huxley HE, Stewart A, Sosa H, Irving T (1994) X-ray diffraction measurements of the extensibility of actin and myosin filaments in contracting muscle. Biophys J 67:2411–2421

    Article  PubMed  CAS  Google Scholar 

  • Kellermayer MS, Bianco P, Martonfalvi Z, Nagy A, Kengyel A, Szatmari D, Huber T, Linari M, Caremani M, Lombardi V (2008) Muscle thixotropy: more than just cross-bridges? Biophys J 94:329–330

    Article  CAS  Google Scholar 

  • King NMP, Helmes M, Granzier H (2009) A direct method to measure the restoring force and slack sarcomere length of intact cardiomyocytes. Biophys J 96:498a

    Article  Google Scholar 

  • Lakie M, Walsh EG, Wright GW (1984) Resonance at the wrist demonstrated by the use of a torque motor: an instrumental analysis of muscle tone in man. J Physiol 353:265–285

    PubMed  CAS  Google Scholar 

  • Liddell EGT, Sherrington C (1924) Reflexes in response to stretch (myotatic reflexes). Proc R Soc Lond B Biol Sci 96:212–242

    Article  Google Scholar 

  • Lombardi V, Piazzesi G (1990) The contractile response during steady lengthening of stimulated frog muscle fibres. J Physiol 431:141–171

    PubMed  CAS  Google Scholar 

  • Loram ID, Maganaris CN, Lakie M (2007) The passive, human calf muscles in relation to standing: the short range stiffness lies in the contractile component. J Physiol 584:677–692

    Article  PubMed  CAS  Google Scholar 

  • Meiss RA (1987) Stiffness of active smooth muscle during forced elongation. Am J Physiol Cell Physiol 253:C484–C493

    CAS  Google Scholar 

  • Mitov MI, Holbrook AM, Campbell KS (2009) Myocardial short-range force responses increase with age in F344 rats. J Mol Cell Cardiol 46:39–46

    Article  PubMed  CAS  Google Scholar 

  • Morgan DL (1990) New insights into the behavior of muscle during active lengthening. Biophys J 57:209–221

    Article  PubMed  CAS  Google Scholar 

  • Mutungi G, Ranatunga KW (1996) The viscous, viscoelastic and elastic characteristics of resting fast and slow mammalian (rat) muscle fibres. J Physiol 496.3:827–836

    PubMed  CAS  Google Scholar 

  • Mutungi G, Ranatunga KW (2000) Do cross-bridges contribute to the tension response during stretch of passive muscle? A response. J Muscle Res Cell Motil 21:301–302

    Article  PubMed  CAS  Google Scholar 

  • Proske U, Morgan DL (1999) Do cross-bridges contribute to the tension during stretch of passive muscle? J Muscle Res Cell Motil 20:433–442

    Article  PubMed  CAS  Google Scholar 

  • Proske U, Morgan DL, Gregory JE (1993) Thixotropy in skeletal muscle and in muscle spindles: a review. Prog Neurobiol 41:705–721

    Article  PubMed  CAS  Google Scholar 

  • Rack PMH, Westbury DR (1974) The short range stiffness of active mammalian muscle and its effect on mechanical properties. J Physiol 240:331–350

    PubMed  CAS  Google Scholar 

  • Sandow A (1970) Skeletal muscle. Ann Rev Physiol 32:87–138

    Article  CAS  Google Scholar 

  • Stienen GJ, Versteeg PG, Papp Z, Elzinga G (1992) Mechanical properties of skinned rabbit psoas and soleus muscle fibres during lengthening: effects of phosphate and Ca2+. J Physiol 451:503–523

    PubMed  CAS  Google Scholar 

  • Tikunov BA, Sweeney HL, Rome LC (2001) Quantitative electrophoretic analysis of myosin heavy chains in single muscle fibers. J Appl Physiol 90:1927–1935

    PubMed  CAS  Google Scholar 

  • Vieth E (1989) Fitting piecewise linear regression functions to biological responses. J Appl Physiol 67:390–396

    PubMed  CAS  Google Scholar 

  • Wakabayashi K, Sugimoto Y, Tanaka H, Ueno Y, Takezawa Y, Amemiya Y (1994) X-ray diffraction evidence for the extensibility of actin and myosin filaments during muscle contraction. Biophys J 67:2422–2435

    Article  PubMed  CAS  Google Scholar 

  • Wu Y, Cazorla O, Labeit D, Labeit S, Granzier H (2000) Changes in titin and collagen underlie diastolic stiffness diversity of cardiac muscle. J Mol Cell Cardiol 32:2151–2162

    Article  PubMed  CAS  Google Scholar 

  • Zahalak GI (1997) Can muscle fibers be stable on the descending limbs of their sarcomere length-tension relations? J Biomech 30:1179–1182

    Article  PubMed  CAS  Google Scholar 

  • Zile MR, Baicu CF, Gaasch WH (2004) Diastolic heart failure – abnormalities in active relaxation and passive stiffness of the left ventricle. N Engl J Med 350:1953–1959

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgements

This work was supported by American Heart Association Scientist Development Grant 0630079N, NIH AG021862, NIH HL090749 and the University of Kentucky Research Challenge Trust Fund.

Author information

Authors and Affiliations

  1. Department of Physiology & Center for Muscle Biology, University of Kentucky, Lexington, KY, 40503, USA

    Kenneth S. Campbell

Authors
  1. Kenneth S. Campbell
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Kenneth S. Campbell .

Editor information

Editors and Affiliations

  1. McGill University, Pine Avenue West 475, Montreal, H2W 1S4, Québec, Canada

    Dilson E. Rassier

Rights and permissions

Reprints and permissions

Copyright information

© 2010 Springer Science+Business Media, LLC

About this chapter

Cite this chapter

Campbell, K.S. (2010). Short-Range Mechanical Properties of Skeletal and Cardiac Muscles. In: Rassier, D. (eds) Muscle Biophysics. Advances in Experimental Medicine and Biology, vol 682. Springer, New York, NY. https://doi.org/10.1007/978-1-4419-6366-6_13

Download citation

Publish with us

Policies and ethics

Search

Navigation