The sarcomere length-tension relation in skeletal muscle

Tension development during isometric tetani in single fibers of frog semitendinosus muscle occurs in three phases: (a) in initial fast-rise phase; (b) a slow-rise phase; and (c) a plateau, which lasts greater than 10 s. The slow-rise phase has previously been assumed to rise out of a progressive increase of sarcomere length dispersion along the fiber (Gordon et al. 1966. J. Physiol. [Lond.]. 184:143--169;184:170-- 192). Consequently, the "true" tetanic tension has been considered to be the one existing before the onset of the slow-rise phase; this is obtained by extrapolating the slowly rising tension back to the start of the tetanus. In the study by Gordon et al. (1966. J. Physiol. [Lond.] 184:170--192), as well as in the present study, the relation between this extrapolated tension and sarcomere length gave the familiar linear descending limb of the length-tension relation. We tested the assumption that the slow rise of tension was due to a progressive increase in sarcomere length dispersion. During the fast rise, the slow rise, and the plateau of tension, the sarcomere length dispersion at any area along the muscle was less than 4% of the average sarcomere length. Therefore, a progressive increase of sarcomere length dispersion during contraction appears unable to account for the slow rise of tetanic tension. A sarcomere length-tension relation was constructed from the levels of tension and sarcomere length measured during the plateau. Tension was independent of sarcomere length between 1.9 and 2.6 microgram, and declined to 50% maximal at 3.4 microgram. This result is difficult to reconcile with the cross-bridge model of force generation.

[1]  M. Noble,et al.  Enhancement of mechanical performance by stretch during tetanic contractions of vertebrate skeletal muscle fibres. , 1978, The Journal of physiology.

[2]  F. Julian,et al.  Sarcomere length non-uniformity in relation to tetanic responses of stretched skeletal muscle fibres , 1978, Proceedings of the Royal Society of London. Series B. Biological Sciences.

[3]  R. Baskin,et al.  Light diffraction studies of sarcomere dynamics in single skeletal muscle fibers. , 1977, Biophysical journal.

[4]  H. E. Keurs,et al.  Sarcomere shortening in striated muscle occurs in stepwise fashion , 1977, Nature.

[5]  R. Baskin,et al.  Sarcomere length dispersion in single skeletal muscle fibers and fiber bundles. , 1976, Biophysical journal.

[6]  M. Noble,et al.  Proceedings: Force enhancement induced by stretch of contracting single isolated muscle fibres of the frog. , 1976, The Journal of physiology.

[7]  Pollack Gh,et al.  Sarcomere dynamics in intact cardiac muscle. , 1976 .

[8]  P. Mason,et al.  Sarcomere length changes during stimulation of frog semitendinosus muscle. , 1976, Journal of mechanochemistry & cell motility.

[9]  H. Rahn,et al.  Hydrogen ion regulation, temperature, and evolution. , 1975, The American review of respiratory disease.

[10]  Jay E. Mrrrenthal A sliding filament model for skeletal muscle: dependence of isometric dynamics on temperature and sarcomere length. , 1975 .

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

[12]  L. Teichholz,et al.  Ionic Strength and the Contraction Kinetics of Skinned Muscle Fibers , 1974, The Journal of general physiology.

[13]  M Kawai,et al.  Optical diffraction studies of muscle fibers. , 1973, Biophysical journal.

[14]  K. Edman,et al.  Changes in sarcomere length during isometric tension development in frog skeletal muscle , 1972, The Journal of physiology.

[15]  H. Sugi,et al.  Tension changes during and after stretch in frog muscle fibres , 1972, The Journal of physiology.

[16]  R. J. Podolsky,et al.  Length-Force Relation of Calcium Activated Muscle Fibers , 1972, Science.

[17]  R. Reeves,et al.  An imidazole alphastat hypothesis for vertebrate acid-base regulation: tissue carbon dioxide content and body temperature in bullfrogs. , 1972, Respiration physiology.

[18]  R. Close,et al.  The relations between sarcomere length and characteristics of isometric twitch contractions of frog sartorius muscle , 1972, The Journal of physiology.

[19]  F. D. Carlson,et al.  Transient Phases of the Isometric Tetanus in Frog's Striated Muscle , 1971, The Journal of general physiology.

[20]  J. Goodman Introduction to Fourier optics , 1969 .

[21]  K. Edman,et al.  Laser Diffraction Studies on Single Skeletal Muscle Fibers , 1969, Science.

[22]  A. Huxley,et al.  The variation in isometric tension with sarcomere length in vertebrate muscle fibres , 1966, The Journal of physiology.

[23]  A. Huxley,et al.  Tension development in highly stretched vertebrate muscle fibres , 1966, The Journal of physiology.

[24]  K. Edman,et al.  The relation between sarcomere length and active tension in isolated semitendinosus fibres of the frog , 1966, The Journal of physiology.

[25]  M. Hass,et al.  Sheet Infrared Transmission Polarizers , 1965 .

[26]  F. Buchthal,et al.  ULTRASTRUCTURE OF THE RESTING AND CONTRACTED STRIATED MUSCLE FIBER AT DIFFERENT DEGREES OF STRETCH , 1961, The Journal of biophysical and biochemical cytology.

[27]  J. Délèze,et al.  The mechanical properties of the semitendinosus muscle at lengths greater than its length in the body , 1961, The Journal of physiology.

[28]  A. Huxley,et al.  The maximum length for contraction in vertebrate striated muscle , 1961, The Journal of physiology.

[29]  A. Hill The mechanics of active muscle , 1953, Proceedings of the Royal Society of London. Series B - Biological Sciences.

[30]  R. Ramsey,et al.  The isometric length‐tension diagram of isolated skeletal muscle fibers of the frog , 1940 .

[31]  G. Pollack,et al.  Sarcomere dynamics in intact cardiac muscle. , 1976, European journal of cardiology.

[32]  J. Mittenthal A sliding filament model for skeletal muscle: dependence of isometric dynamics on temperature and sarcomere length. , 1975, Journal of theoretical biology.

[33]  P. Paolini,et al.  Length-dependent optical diffraction pattern changes in frog sartorius muscle. , 1975, Physiological chemistry and physics.

[34]  M. Endo,et al.  Length Dependence of Activation of Skinned Muscle Fibers by Calcium , 1973 .

[35]  V. Marikhin,et al.  [Light diffraction by muscle fibers. I. Analysis of the geometrical pattern of diffraction]. , 1970, Tsitologiia.

[36]  A. Huxley Muscle structure and theories of contraction. , 1957, Progress in biophysics and biophysical chemistry.