Stimulation frequency history alters length-force characteristics of fully recruited rat muscle.

Effects of stimulation frequency history on length-force characteristics were determined for rat medial gastrocnemius muscle (GM). The peripheral nerve was stimulated supramaximally according to two stimulation protocols. First, a complete set of length-force data were obtained by stimulating the nerve with a decreasing stimulation frequency (DSF) staircase composed of five successive pulse trains (200 ms each) of 100-, 50-, 40-, 30- and 15-Hz stimulation. Then length-force data were obtained using constant stimulation frequency (CSF; during the isometric contraction inter-stimulus interval was constant). The acquisition order of a complete set of length-force data was: first 15-Hz, then 30-, 40-, 50- and finally 100-Hz stimulation. For all DSF conditions, both optimum muscle length as well as active slack length were shifted significantly (P < 0.05) to lower muscle length with respect to CSF. Muscle length range between active slack and optimum length for all DSF conditions was increased significantly with respect to CSF. DSF thus caused a marked shift of the length-force relationship to lower muscle length compared to the CSF-dependent length-force relationship. As a result of this shift, muscle force enhancement (potentiation) was non-linearly related to muscle length; force enhancement decreased exponentially with increasing muscle length. In addition, DSF-dependent length-force characteristics are not scaled and shifted versions of those for CSF. Possible factors affecting these length-force characteristics are higher intracellular calcium concentration, myosin light chain phosphorylation, fatigue during sustained contractions, interaction between aponeurosis and fibre length, distribution of fibre mean sarcomere length with respect to muscle length, and muscle length changes during unfused tetanic contractions. It is concluded that length-force characteristics of rat GM are dependent on both short-term stimulation frequency history as well as stimulation frequency per se.

[1]  J. Desmedt Motor control mechanisms in health and disease , 1983 .

[2]  T. Tsuchiya,et al.  Stiffness changes during enhancement and deficit of isometric force by slow length changes in frog skeletal muscle fibres. , 1988, The Journal of physiology.

[3]  D. Allen,et al.  The influence of intracellular pH on contraction, relaxation and [Ca2+]i in intact single fibres from mouse muscle. , 1993, The Journal of physiology.

[4]  J. Stull,et al.  Myosin light chain phosphorylation and phosphorylase A activity in rat extensor digitorum longus muscle. , 1979, Biochemical and biophysical research communications.

[5]  D. Allen,et al.  Changes of myoplasmic calcium concentration during fatigue in single mouse muscle fibers , 1991, The Journal of general physiology.

[6]  C D Marsden,et al.  "Muscular wisdom" that minimizes fatigue during prolonged effort in man: peak rates of motoneuron discharge and slowing of discharge during fatigue. , 1983, Advances in neurology.

[7]  Guus C. Baan,et al.  Stimulation level-dependent length-force and architectural characteristics of rat gastrocnemius muscle. , 1992, Journal of electromyography and kinesiology : official journal of the International Society of Electrophysiological Kinesiology.

[8]  G. Loeb,et al.  Effect of velocity and mechanical history on the forces of motor units in the cat medial gastrocnemius muscle. , 1992, Journal of neurophysiology.

[9]  S Andreassen,et al.  Regulation of the firing pattern of single motor units. , 1980, Journal of neurology, neurosurgery, and psychiatry.

[10]  D. M. Lewis,et al.  A comparison of isometric contractions of the whole muscle with those of motor units in a fast-twitch muscle of the cat. , 1972, Experimental neurology.

[11]  R. Fitts Cellular mechanisms of muscle fatigue. , 1994, Physiological reviews.

[12]  A J Sargeant,et al.  Physiological characteristics of two extreme muscle compartments in gastrocnemius medialis of the anaesthetized rat. , 1995, Acta physiologica Scandinavica.

[13]  A J van Soest,et al.  The role of series elastic structures in prestretch-induced work enhancement during isotonic and isokinetic contractions. , 1990, The Journal of experimental biology.

[14]  P A Huijing,et al.  Effects of distribution of muscle fiber length on active length‐force characteristics of rat gastrocnemius medialis , 1994, The Anatomical record.

[15]  R. Johansson,et al.  Changes in motoneurone firing rates during sustained maximal voluntary contractions. , 1983, The Journal of physiology.

[16]  D. A. Williams,et al.  Effects of sarcomere length on the force—pCa relation in fast‐ and slow‐twitch skinned muscle fibres from the rat , 1982, The Journal of physiology.

[17]  J. Neter,et al.  Applied linear statistical models : regression, analysis of variance, and experimental designs , 1974 .

[18]  P. Huijing,et al.  Parameter interdependence and success of skeletal muscle modelling , 1995 .

[19]  P A Huijing,et al.  Influence of muscle geometry on shortening speed of fibre, aponeurosis and muscle. , 1992, Journal of biomechanics.

[20]  D. Allen,et al.  Cellular mechanisms of fatigue in skeletal muscle. , 1991, The American journal of physiology.

[21]  F. Zajac Muscle and tendon: properties, models, scaling, and application to biomechanics and motor control. , 1989, Critical reviews in biomedical engineering.

[22]  P Bawa,et al.  Repetitive doublets in human flexor carpi radialis muscle. , 1983, The Journal of physiology.

[23]  J Bagust,et al.  Isometric contractions of motor units in a fast twitch muscle of the cat , 1973, The Journal of physiology.

[24]  S. Binder-Macleod,et al.  Use of a catchlike property of human skeletal muscle to reduce fatigue , 1991, Muscle & nerve.

[25]  J. Stull,et al.  Myosin light chain phosphorylation in vertebrate striated muscle: regulation and function. , 1993, The American journal of physiology.

[26]  J. Stull,et al.  The effect of myosin phosphorylation on the contractile properties of skinned rabbit skeletal muscle fibers. , 1985, The Journal of biological chemistry.

[27]  The course of motor unit twitch in dependence on muscle stretching force. Studies on medial gastrocnemius muscle of the rat. , 1990, Acta neurobiologiae experimentalis.

[28]  J. Hannerz,et al.  The fatigue and voluntary discharge properties of single motor units in man , 1981, The Journal of physiology.

[29]  H P Clamann,et al.  Force output of cat motor units stimulated with trains of linearly varying frequency. , 1989, Journal of neurophysiology.

[30]  Michael J. O'Donovan,et al.  Cat hindlimb motoneurons during locomotion. II. Normal activity patterns. , 1987, Journal of neurophysiology.

[31]  J. Stull,et al.  Myosin light chain phosphorylation in fast and slow skeletal muscles in situ. , 1984, The American journal of physiology.

[32]  P A Huijing,et al.  A comparison of rat extensor digitorum longus and gastrocnemius medialis muscle architecture and length-force characteristics. , 1994, Acta anatomica.

[33]  E. Godaux,et al.  Ballistic contractions in man: characteristic recruitment pattern of single motor units of the tibialis anterior muscle. , 1977, The Journal of physiology.

[34]  T. Lømo,et al.  Gradation of force output in normal fast and slow muscles of the rat. , 1987, Acta physiologica Scandinavica.

[35]  P A Huijing,et al.  Important experimental factors for skeletal muscle modelling: non-linear changes of muscle length force characteristics as a function of degree of activity. , 1996, European journal of morphology.

[36]  G. Cavagna,et al.  Positive work done by a previously stretched muscle. , 1968, Journal of applied physiology.

[37]  J. Winters Hill-Based Muscle Models: A Systems Engineering Perspective , 1990 .

[38]  M D Binder,et al.  Computer simulation of the steady-state input-output function of the cat medial gastrocnemius motoneuron pool. , 1991, Journal of neurophysiology.

[39]  B. C. Abbott,et al.  ABSTRACTS OF MEMOIRS RECORDING WORK DONE AT THE PLYMOUTH LABORATORY THE FORCE EXERTED BY ACTIVE STRIATED MUSCLE DURING AND AFTER CHANGE OF LENGTH , 2022 .

[40]  B Roszek,et al.  Decreasing stimulation frequency-dependent length-force characteristics of rat muscle. , 1994, Journal of applied physiology.

[41]  A. Hill The heat of shortening and the dynamic constants of muscle , 1938 .

[42]  D. Allen,et al.  Relaxation, [Ca2+]i and [Mg2+]i during prolonged tetanic stimulation of intact, single fibres from mouse skeletal muscle. , 1994, The Journal of physiology.

[43]  D. Morgan New insights into the behavior of muscle during active lengthening. , 1990, Biophysical journal.

[44]  P A Huijing,et al.  Effects of growth on architecture and functional characteristics of adult rat gastrocnemius muscle , 1990, Journal of morphology.

[45]  J. Stull,et al.  Phosphorylation of myosin in permeabilized mammalian cardiac and skeletal muscle cells. , 1986, The American journal of physiology.

[46]  J. Stull,et al.  Myosin light chain phosphorylation-dephosphorylation in mammalian skeletal muscle. , 1982, The American journal of physiology.

[47]  J A Stephens,et al.  The motor units of cat medial gastrocnemius: Electrical and mechanical properties as a function of muscle length , 1975, Journal of morphology.

[48]  P. Rack,et al.  The effects of length and stimulus rate on tension in the isometric cat soleus muscle , 1969, The Journal of physiology.

[49]  P. Huijing,et al.  Changes in geometry of activily shortening unipennate rat gastrocnemius muscle , 1993, Journal of morphology.

[50]  K. Edman Mechanical deactivation induced by active shortening in isolated muscle fibres of the frog. , 1975, The Journal of physiology.

[51]  Hubertus F.J.M. Koopman,et al.  The effect of shortening history on the length-force relationship of the muscle , 1995 .

[52]  P A Huijing,et al.  Frequency response to rat gastrocnemius medialis in small amplitude vibrations. , 1994, Journal of biomechanics.

[53]  P. A. Huijing,et al.  Series Elastic Properties of Rat Skeletal Muscle: Distinction of Series Elastic Components and Some Implications , 1992 .

[54]  P A Huijing,et al.  Skeletal muscle stiffness in static and dynamic contractions. , 1994, Journal of biomechanics.

[55]  A. Persechini,et al.  Length‐dependence of isometric twitch tension potentiation and myosin phosphorylation in mouse skeletal muscle , 1990, Journal of cellular physiology.

[56]  R. Moss,et al.  Factors influencing the ascending limb of the sarcomere length‐tension relationship in rabbit skinned muscle fibres. , 1987, The Journal of physiology.

[57]  R. Stein,et al.  Changes in firing rate of human motor units during linearly changing voluntary contractions , 1973, The Journal of physiology.

[58]  Determinants of length range of active force exertion by muscle , 1988, Proceedings of the Annual International Conference of the IEEE Engineering in Medicine and Biology Society.

[59]  T. Lømo,et al.  Firing patterns of motor units in normal rats , 1985, Nature.