European Journal of Applied Physiology

, Volume 118, Issue 5, pp 1063–1077 | Cite as

The sag response in human muscle contraction

  • Ian C. Smith
  • Jahaan Ali
  • Geoffrey A. Power
  • Walter Herzog
Original Article



We examined how muscle length and time between stimuli (inter-pulse interval, IPI) influence declines in force (sag) seen during unfused tetani in the human adductor pollicis muscle.


A series of 16-pulse contractions were evoked with IPIs between 1 × and 5 × the twitch time to peak tension (TPT) at large (long muscle length) and small (short muscle length) thumb adduction angles. Unfused tetani were mathematically deconstructed into a series of overlapping twitch contractions to examine why sag exhibits length- and IPI-dependencies.


Across all IPIs tested, sag was 62% greater at short than long muscle length, and sag increased as IPI was increased at both muscle lengths. Force attributable to the second stimulus increased as IPI was decreased. Twitch force declined from maximal values across all IPI tested, with the greatest reductions seen at short muscle length and long IPI. At IPI below 2 × TPT, the twitch with highest force occurred earlier than the peak force of the corresponding unfused tetani. Contraction-induced declines in twitch duration (TPT + half relaxation time) were only observed at IPI longer than 1.75 × TPT, and were unaffected by muscle length.


Sag is an intrinsic feature of healthy human adductor pollicis muscle. The length-dependence of sag is related to greater diminution of twitch force at short relative to long muscle length. The dependence of sag on IPI is related to IPI-dependent changes in twitch duration and twitch force, and the timing of peak twitch force relative to the peak force of the associated unfused tetanus.


Force–frequency relationship Length–tension relationship Muscle contraction Summation Unfused tetanus 



Analysis of variance


Electromechanical delay


Half relaxation time


Inter-pulse interval


Maximum voluntary contraction


Peak twitch force


Root mean squared


Time to peak tension


Author contributions

ICS and JA conceived and designed the experiments. ICS, GAP and WH developed the experimental tools and methods. ICS and JA performed the experiments at the University of Calgary and analyzed the data. ICS drafted the manuscript which was revised critically by GAP, JA, and WH. All authors have approved the final version of the manuscript. All designated authors qualify for authorship, and all who qualify for authorship are listed.


Funding for this project was provided by grants from the Canadian Institutes of Health Research (W.H. FDN-143341), the Natural Sciences and Engineering Research Council of Canada (W.H. RGPIN/36674-2013), and the Canada Research Chairs Program (W.H. 950-230603). Additional support was provided by the Killam Foundation (W.H. and G.A.P). I.C.S was supported by a Canadian Institutes of Health Research Fellowship, and G.A.P. was supported by a Canadian Institutes of Health Research Banting Fellowship. Both I.C.S and G.A.P. were supported by postdoctoral fellowships from Alberta Innovates.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no competing interests.


  1. Bakels R, Kernell D (1993) Average but not continuous speed match between motoneurons and muscle units of rat tibialis anterior. J Neurophysiol 70(4):1300–1306CrossRefPubMedGoogle Scholar
  2. Bigland-Ritchie B, Fuglevand AJ, Thomas CK (1998) Contractile properties of human motor units: Is man a cat? Neuroscientist 4(4):240–249CrossRefGoogle Scholar
  3. Binder-Macleod SA, Lee SC, Fritz AD, Kucharski LJ (1998) New look at force–frequency relationship of human skeletal muscle: effects of fatigue. J Neurophysiol 79(4):1858–1868CrossRefPubMedGoogle Scholar
  4. Booth J, McKenna MJ, Ruell PA, Gwinn TH, Davis GM, Thompson MW, Harmer AR, Hunter SK, Sutton JR (1997) Impaired calcium pump function does not slow relaxation in human skeletal muscle after prolonged exercise. J Appl Physiol 83:511–521CrossRefPubMedGoogle Scholar
  5. Brown IE, Loeb GE (2000) Measured and modeled properties of mammalian skeletal muscle: IV. Dynamics of activation and deactivation. J Mus Res Cell Motil 21(1):33–47CrossRefGoogle Scholar
  6. Brown IE, Satoda T, Richmond FJ, Loeb GE (1998) Feline caudofemoralis muscle. Muscle fibre properties, architecture, and motor innervation. Exp Brain Res 121(1):76–91CrossRefPubMedGoogle Scholar
  7. Burke RE (1990) Motor unit types: some history and unsettled issues. In: Binder MD, Mendell LM (eds) The Segmental motor system. Oxford University Press, New York, pp 207–221Google Scholar
  8. Burke RE, Levine DN, Tsairis P, Zajac FE (1973) Physiological types and histochemical profiles in motor units of the cat gastrocnemius. J Physiol 234:723–748CrossRefPubMedPubMedCentralGoogle Scholar
  9. Burke RE, Levine DN, Salcman M, Tsairis P (1974) Motor units in cat soleus muscle: physiological, histochemical and morphological characteristics. J Physiol 238(3):503–514CrossRefPubMedPubMedCentralGoogle Scholar
  10. Burke RE, Rudomin P, Zajac Iii FE (1976) The effect of activation history on tension production by individual muscle units. Brain Res 109:515–529CrossRefPubMedGoogle Scholar
  11. Carp JS, Herchenroder PA, Chen XY, Wolpaw JR (1999) Sag during unfused tetanic contractions in rat triceps surae motor units. J Neurophysiol 81(6):2647–2661CrossRefPubMedGoogle Scholar
  12. Celichowski J, Grottel K (1995) The relationship between fusion index and stimulation frequency in tetani of motor units in rat medial gastrocnemius. Arch Ital Biol 133:81–87PubMedGoogle Scholar
  13. Celichowski J, Grottel K, Bichler E (1999) Differences in the profile of unfused tetani of fast motor units with respect to their resistance to fatigue in the rat medial gastrocnemius muscle. J Mus Res Cell Motil 20:681–685CrossRefGoogle Scholar
  14. Celichowski J, Pogrzebna M, Raikova RT (2005) Analysis of the unfused tetanus course in fast motor units of the rat medial gastrocnemius muscle. Arch Ital Biol 143:51–63PubMedGoogle Scholar
  15. Cooper S, Eccles JC (1930) The isometric responses of mammalian muscles. J Physiol 69(4):377–385CrossRefPubMedPubMedCentralGoogle Scholar
  16. Debold EP, Romatowski J, Fitts RH (2006) The depressive effect of Pi on the force–pCa relationship in skinned single muscle fibers is temperature dependent. Am J Physiol Cell Physiol 290:C1041–C1050CrossRefPubMedGoogle Scholar
  17. Desmedt JE, Hainaut K (1968) Kinetics of myofilament activation in potentiated contraction: staircase phenomenon in human skeletal muscle. Nature 217(5128):529–532CrossRefPubMedGoogle Scholar
  18. Drzymała-Celichowska H, Krutki P (2015) Slow motor units in female rat soleus are slower and weaker than their male counterparts. J Muscle Res Cell Motil 36(3):287–295. CrossRefPubMedGoogle Scholar
  19. Duchateau J, Hainaut K (1986) Nonlinear summation of contractions in striated muscle. I. Twitch potentiation in human muscle. J Muscle Res Cell Motil 7(1):11–17CrossRefPubMedGoogle Scholar
  20. Fortuna R, Groeber M, Seiberl W, Power GA, Herzog W (2017) Shortening-induced force depression is modulated in a time- and speed-dependent manner following a stretch-shortening cycle. Physiol Rep. PubMedPubMedCentralCrossRefGoogle Scholar
  21. Fowles JR, Green HJ (2003) Coexistence of potentiation and low-frequency fatigue during voluntary exercise in human skeletal muscle. Can J Physiol Pharmacol 181:1092–1100CrossRefGoogle Scholar
  22. Fritz N, Schmidt C (1992) Contractile properties of single motor units in two multi-tendoned muscles of the cat distal forelimb. Exp Brain Res 88(2):401–410CrossRefPubMedGoogle Scholar
  23. Fuglevand AJ, Macefield VG, Bigland-Ritchie B (1999) Force–frequency and fatigue properties of motor units in muscles that control digits of the human hand. J Neurophysiol 81(4):1718–1729CrossRefPubMedGoogle Scholar
  24. Fukuda N, O-Uchi J, Sasaki D, Kajiwara H, Ishiwata S, Kurihara S (2001) Acidosis or inorganic phosphate enhances the length dependence of tension in rat skinned cardiac muscle. J Physiol 536(1):153–160CrossRefPubMedPubMedCentralGoogle Scholar
  25. Gardiner PF, Olha AE (1987) Contractile and electromyographic characteristics of rat plantaris motor unit types during fatigue in situ. J Physiol 385:13–34CrossRefPubMedPubMedCentralGoogle Scholar
  26. González E, Delbono O (2001) Age-dependent fatigue in single intact fast- and slow fibers from mouse EDL and soleus skeletal muscles. Mech Ageing Dev 122(10):1019–1032CrossRefPubMedGoogle Scholar
  27. Green HJ, Duhamel TA, Ferth S, Holloway GP, Thomas MM, Tupling AR, Rich SM, Yau JE (2004) Reversal of muscle fatigue during 16 h of heavy intermittent cycle exercise. J Appl Physiol 97:2166–2175CrossRefPubMedGoogle Scholar
  28. Grottel K, Celichowski J (1990) Division of motor units in medial gastrocnemius muscle of the rat in light of variability of their principal properties. Acta Neurobiol Exp 50:571–588Google Scholar
  29. Hwang K, Huan F, Kim DJ (2013) Muscle fibre types of the lumbrical, interossei, flexor, and extensor muscles moving the index finger. J Plast Surg Hand Surg 47(4):268–272. CrossRefPubMedGoogle Scholar
  30. Jones AA, Power GA, Herzog W (2016) History dependence of the electromyogram: implications for isometric steady-state EMG parameters following a lengthening or shortening contraction. J Electromyogr Kinesiol 27:30–38. CrossRefPubMedGoogle Scholar
  31. Kanda K, Hashizume K (1992) Factors causing difference in force output among motor units in the rat medial gastrocnemius muscle. J Physiol 448:677–695CrossRefPubMedPubMedCentralGoogle Scholar
  32. Kerrick WGL, Xu Y (2004) Inorganic phosphate affects the pCa-force relationship more than the pCa-ATPase by increasing the rate of dissociation of force generating cross-bridges in skinned fibers from both EDL and soleus muscles of the rat. J Mus Res Cell Motil 25:107–117CrossRefGoogle Scholar
  33. Krutki P, Celichowski J, Kryściak K, Sławińska U, Majczyński H, Redowicz MJ (2008) Division of motor units into fast and slow of the basis of profile of 20 Hz unfused tetanus. J Physiol Pharmacol 59(2):353–363PubMedGoogle Scholar
  34. Krutki P, Mrówczyński W, Raikova R, Celichowski J (2014) Concomitant changes in afterhyperpolarization and twitch following repetitive stimulation of fast motoneurones and motor units. Exp Brain Res 232(2):443–452. CrossRefPubMedGoogle Scholar
  35. Lee H-D, Herzog W (2002) Force enhancement following muscle stretch of electrically stimulated and voluntarily activated human adductor pollicis. J Physiol 545(Pt 1):321–330CrossRefPubMedPubMedCentralGoogle Scholar
  36. Lev-Tov A, Pratt CA, Burke RE (1988) The motor-unit population of the cat tenuissimus muscle. J Neurophysiol 59(4):1128–1142CrossRefPubMedGoogle Scholar
  37. Luo Y, Davis JP, Smillie LB, Rall JA (2002) Determinants of relaxation rate in rabbit skinned skeletal muscle fibres. J Physiol 545(3):887–901CrossRefPubMedPubMedCentralGoogle Scholar
  38. Macefield VG, Fuglevand AJ, Bigland-Ritchie B (1996) Contractile properties of single motor units in human toe extensors assessed by intraneural motor axon stimulation. J Neurophysiol 75(6):2509–2519CrossRefPubMedGoogle Scholar
  39. MacIntosh BR, Jones D, Devrome AN, Rassier DE (2007) Prediction of summation in incompletely fused tetanic contractions of rat muscle. J Biomech 40(5):1066–1072. CrossRefPubMedGoogle Scholar
  40. McDonagh JC, Binder MD, Reinking RM, Stuart DG (1980) Tetrapartite classification of motor units of cat tibialis posterior. J Neurophysiol 44(4):696–712CrossRefPubMedGoogle Scholar
  41. Merton PA (1954) Voluntary strength and fatigue. J Physiol 123(3):553–564CrossRefPubMedPubMedCentralGoogle Scholar
  42. Nocella M, Colombini B, Benelli G, Cecchi G, Bagni MA, Bruton J (2011) Force decline during fatigue is due to both a decrease in the force per individual cross-bridge and the number of cross-bridges. J Physiol 589:3371–3381CrossRefPubMedPubMedCentralGoogle Scholar
  43. Nocella M, Cecchi G, Colombini B (2017) Phosphate increase during fatigue affects crossbridge kinetics in intact mouse muscle at physiological temperature. J Physiol 595(13):4317–4328. CrossRefPubMedPubMedCentralGoogle Scholar
  44. Parmiggiani F, Stein RB (1981) Nonlinear summation of contractions in cat muscles. II. Later facilitation and stiffness changes. J Gen Physiol 78(3):295–311CrossRefPubMedGoogle Scholar
  45. Raikova R, Celichowski J, Pogrzebna M, Aladjov H, Krutki P (2007) Modeling of summation of individual twitches into unfused tetanus for various types of rat motor units. J Electromyogr Kinesiol 17(2):121–130. CrossRefPubMedGoogle Scholar
  46. Raikova R, Pogrzebna M, Drzymała H, Celichowski J, Aladjov H (2008) Variability of successive contractions subtracted from unfused tetanus of fast and slow motor units. J Electromyogr Kinesiol 18(5):741–751. CrossRefPubMedGoogle Scholar
  47. Rassier DE, MacIntosh BR (2002) Length-dependent twitch contractile characteristics of skeletal muscle. Can J Physiol Pharmacol 80(10):993–1000CrossRefPubMedGoogle Scholar
  48. Rassier DE, Tubman LA, MacIntosh BR (1997) Length-dependent potentiation and myosin light chain phosphorylation in rat gastrocnemius muscle. Am J Physiol 273(1 Pt 1):C198-204PubMedGoogle Scholar
  49. Round JM, Jones DA, Chapman SJ, Edwards RH, Ward PS, Fodden DL (1984) The anatomy and fibre type composition of the human adductor pollicis in relation to its contractile properties. J Neurol Sci 66(2–3):263–272CrossRefPubMedGoogle Scholar
  50. Smith IC, Gittings W, Huang J, McMillan EM, Quadrilatero J, Tupling AR, Vandenboom R (2013) Potentiation in mouse lumbrical muscle without myosin light chain phosphorylation: is resting calcium responsible? J Gen Physiol 141:297–308CrossRefPubMedPubMedCentralGoogle Scholar
  51. Smith IC, Vandenboom R, Tupling AR (2014) Juxtaposition of the changes in intracellular calcium and force during staircase potentiation at 30 and 37 °C. J Gen Physiol 144(6):561–570CrossRefPubMedPubMedCentralGoogle Scholar
  52. Smith IC, Bellissimo C, Herzog W, Tupling AR (2016) Can inorganic phosphate explain sag during unfused tetanic contractions of skeletal muscle? Physiol Rep 4(22):e13043CrossRefPubMedPubMedCentralGoogle Scholar
  53. Smith IC, Vandenboom R, Tupling AR (2017) Contraction-induced enhancement of relaxation during high force contractions of mouse lumbrical muscle at 37 °C. J Exp Biol 220(Pt 16):2870–2873. CrossRefPubMedGoogle Scholar
  54. Stein RB, Parmiggiani F (1981) Nonlinear summation of contractions in cat muscles. I. Early depression. J Gen Physiol 78(3):277–293CrossRefPubMedGoogle Scholar
  55. Stephenson DG, Wendt IR (1984) Length dependence of changes in sarcoplasmic calcium concentration and myofibrillar calcium sensitivity in striated muscle fibres. J Muscle Res Cell Motil 5(3):243–272CrossRefPubMedGoogle Scholar
  56. Tesi C, Piroddi N, Colomo F, Poggesi C (2002) Relaxation kinetics following sudden Ca2+ reduction in single myofibrils from skeletal muscle. Biophys J 83:2142–2151CrossRefPubMedPubMedCentralGoogle Scholar
  57. Thomas CK, Johansson RS, Westling G, Bigland-Ritchie B (1990) Twitch properties of human thenar motor units measured in response to intraneural motor-axon stimulation. J Neurophysiol 64(4):1339–1346CrossRefPubMedGoogle Scholar
  58. Thomas CK, Johansson RS, Bigland-Ritchie B (1991) Attempts to physiologically classify human thenar motor units. J Neurophysiol 65(6):1501–1508CrossRefPubMedGoogle Scholar
  59. Tötösy de Zepetnek JE, Zung HV, Erdebil S, Gordon T (1992) Motor-unit categorization based on contractile and histochemical properties: a glycogen depletion analysis of normal and reinnervated rat tibialis anterior muscle. J Neurophysiol 67(5):1404–1415CrossRefPubMedGoogle Scholar
  60. Troiani D, Filippi GM, Bassi FA (1999) Nonlinear tension summation of different combinations of motor units in the anesthetized cat peroneus longus muscle. J Neurophysiol 81(2):771–780CrossRefPubMedGoogle Scholar
  61. Vollestad NK, Sejersted I, Saugen E (1997) Mechanical behavior of skeletal muscle during intermittent voluntary isometric contractions in humans. J Appl Physiol 83(5):1557–1565CrossRefPubMedGoogle Scholar
  62. Westling G, Johansson RS, Thomas CK, Bigland-Ritchie B (1990) Measurement of contractile and electrical properties of single human thenar motor units in response to intraneural motor-axon stimulation. J Neurophysiol 64(4):1331–1338CrossRefPubMedGoogle Scholar
  63. Zajac FE, Young JL (1980) Properties of stimulus trains producing maximum tension-time area per pulse from single motor units in medial gastrocnemiu muscle of the cat. J Neurophysiol 43(5):1206–1220CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Human Performance Lab, Faculty of KinesiologyUniversity of CalgaryCalgaryCanada
  2. 2.Human Health and Nutritional Sciences, College of Biological SciencesUniversity of GuelphGuelphCanada

Personalised recommendations