Fast muscle in squid (Loligo pealei): contractile properties of a specialized muscle fibre type.

The contractile properties of the transverse muscle of the tentacles and the transverse muscle of the arms of the squid Loligo pealei were investigated using small muscle fibre bundle preparations. In addition, transmission electron microscopy was used to measure the length of the thick myofilaments of the two muscle fibre types. The thick filament length of the cross-striated tentacle fibres was 0.81+/-0.08 microm (mean +/- S.D, N=51) while that of the obliquely striated arm muscle fibres was 7.41+/-0.44 microm (N=58). The difference in thick filament length of the two muscle types was predicted to result in a much higher shortening velocity of the tentacle muscle compared with the arm muscle. This was tested by investigating the force/velocity relationship for isotonic shortening of the two muscle types. Fitting Hill's equation to the results gave a maximum shortening velocity (V(max), the intercept on the velocity axis) of 15.4+/-1.0 L(0) s(-1) (mean +/- S.D., N=9) for the tentacle fibres and of 1.5+/-0.2 L(0) s(-1) (N=8) for the arm fibres, where L(0) is the length at which peak isometric force was recorded. The difference in thick filament length was also predicted to result in lower peak tension in the tentacle versus the arm muscle. For the tentacle, the mean peak tetanic tension during a brief isometric tetanus (0.2s) of 131+/-56 mN mm(-2) cross-sectional area (mean +/- S.D., N=12) was observed at a stimulus frequency of 80 Hz, whereas the mean peak tetanic tension of the arm fibres during a brief isometric tetanus (0.2s) was 468+/-91 mN mm(-2) (N=5) and was observed at a stimulus frequency of 160 Hz. The length/force relationships (expressed relative to L(0)) of the two muscle types were similar. The ratio of twitch force to peak tetanic force was 0.66 in the tentacle fibres, but only 0.03 in the arm fibres.

[1]  E. Reynolds THE USE OF LEAD CITRATE AT HIGH pH AS AN ELECTRON-OPAQUE STAIN IN ELECTRON MICROSCOPY , 1963, The Journal of cell biology.

[2]  H. Huxley,et al.  FILAMENT LENGTHS IN STRIATED MUSCLE , 1963, The Journal of cell biology.

[3]  H. Atwood,et al.  Correlation of structure, speed of contraction, and total tension in fast and slow abdominal muscle fibers of the lobster (Homarus americanus). , 1969, The Journal of experimental zoology.

[4]  T. Yamamoto,et al.  The mechanical properties of the longitudinal muscle in the earthworm. , 1969, The Journal of experimental biology.

[5]  H. Y. Elder,et al.  Physiology and ultrastructure of phasic and tonic skeletal muscle fibres in the locust, Schistocerca gregaria. , 1972, Journal of cell science.

[6]  A. Huxley,et al.  Mechanical Transients and the Origin of Muscular Force , 1973 .

[7]  R. Josephson,et al.  Structural and functional heterogeneity in an insect muscle. , 1975, The Journal of experimental zoology.

[8]  J. Miller The length-tension relationship of the dorsal longitudinal muscle of a leech. , 1975, The Journal of experimental biology.

[9]  R. Josephson Extensive and intensive factors determining the performance of striated muscle. , 1975, The Journal of experimental zoology.

[10]  G. Lanzavecchia Morphological modulations in helical muscles (Aschelminthes and Annelida). , 1977, International review of cytology.

[11]  G. Lanzavecchia Morphofunctional and phylogenetic relations in helical muscles , 1981 .

[12]  W. Kier The functional morphology of the musculature of squid (Loliginidae) arms and tentacles , 1982, Journal of morphology.

[13]  C. Govind,et al.  Contractile responses of single fibers in lobster claw closer muscles: correlation with structure, histochemistry, and innervation , 1983 .

[14]  P. Stephens,et al.  THE DIMORPHIC CLAWS OF THE HERMIT CRAB, PAGURUS POLLICARIS: PROPERTIES OF THE CLOSER MUSCLE. , 1984, The Biological bulletin.

[15]  W. Kier,et al.  The musculature of squid arms and tentacles: Ultrastructural evidence for functional differences , 1985, Journal of morphology.

[16]  W. Kier,et al.  Tongues, tentacles and trunks: the biomechanics of movement in muscular‐hydrostats , 1985 .

[17]  C. Reggiani,et al.  The sarcomere length‐tension relation determined in short segments of intact muscle fibres of the frog. , 1987, The Journal of physiology.

[18]  M. Kushmerick,et al.  Myosin alkali light chain and heavy chain variations correlate with altered shortening velocity of isolated skeletal muscle fibers. , 1988, The Journal of biological chemistry.

[19]  N. Curtin,et al.  Power Output and Force-velocity Relationship of Live Fibres from White Myotomal Muscle of the Dogfish, Scyliorhinus Canicula , 2022 .

[20]  W. Kier Squid cross-striated muscle: The evolution of a specialized muscle fiber type , 1991 .

[21]  J. L. Leeuwen Optimum power output and structural design of sarcomeres , 1991 .

[22]  W. Kier,et al.  Biochemical comparison of fast- and slow-contracting squid muscle. , 1992, The Journal of experimental biology.

[23]  W. Rathmayer,et al.  FIBRE HETEROGENEITY IN THE CLOSER AND OPENER MUSCLES OF CRAYFISH WALKING LEGS , 1993 .

[24]  N A Curtin,et al.  Force‐velocity relation for frog muscle fibres: effects of moderate fatigue and of intracellular acidification. , 1994, The Journal of physiology.

[25]  C. Reggiani,et al.  Molecular diversity of myofibrillar proteins: gene regulation and functional significance. , 1996, Physiological reviews.

[26]  W. Kier Muscle development in squid: Ultrastructural differentiation of a specialized muscle fiber type , 1996, Journal of morphology.

[27]  Wulfila Gronenberg,et al.  Mandible muscle fibers in ants: fast or powerful? , 1997, Cell and Tissue Research.

[28]  W. Kier,et al.  Functional design of tentacles in squid : Linking sarcomere ultrastructure to gross morphological dynamics , 1997 .

[29]  Brown,et al.  Different excitation-contraction coupling mechanisms exist in squid, cuttlefish and octopod mantle muscle , 1997, The Journal of experimental biology.

[30]  W. Kier,et al.  A kinematic analysis of tentacle extension in the squid Loligo pealei , 1997, The Journal of experimental biology.

[31]  Curtin,et al.  Contractile properties of obliquely striated muscle from the mantle of squid (Alloteuthis subulata) and cuttlefish (Sepia officinalis) , 1997, The Journal of experimental biology.

[32]  J. Marden,et al.  From Molecules to Mating Success: Integrative Biology of Muscle Maturation in a Dragonfly , 1998 .

[33]  P. Wigmore,et al.  The generation of fiber diversity during myogenesis. , 1998, The International journal of developmental biology.

[34]  J. Marden,et al.  Alternative splicing, muscle calcium sensitivity, and the modulation of dragonfly flight performance. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[35]  J. Marden,et al.  Variability in the size, composition, and function of insect flight muscles. , 2000, Annual review of physiology.

[36]  J. Marden,et al.  Alternative splicing, muscle contraction and intraspecific variation: associations between troponin T transcripts, Ca(2+) sensitivity and the force and power output of dragonfly flight muscles during oscillatory contraction. , 2001, The Journal of experimental biology.

[37]  F. Schachat,et al.  Molecular heterogeneity of histochemical fibre types: a comparison of fast fibres , 1985, Journal of Muscle Research & Cell Motility.