Comparative Vertebrate Muscle Physiology


Although all vertebrate skeletal twitch fibres share the same basic structure and operate by the same contractile mechanism, they are called upon to perform a host of different functions ranging from slow speed locomotion to high speed sound production. There are a number of important qualitative modifications (protein isoforms with different kinetic rates) as well as quantitative modifications (different densities of important structures) which permit this wide range of activities and form the comparative aspects of muscle physiology.

Keywords: muscle; mechanics; locomotion; sound production

Figure 1.

Cross‐section of typical mammalian muscle histochemically stained to show different fibre types. Darkly stained fibres are type I, unstained fibres are type IIa, and intermediate stained fibres are type IIb. Note the fibre type can vary from one cell to the next.

Figure 2.

Three views of carp. The red muscle forms a thin sheet just under the skin (its thickness is exaggerated for illustrative purposes in part (c)). The red fibres run parallel to the body axis (a, b). The white fibres run in a helical fashion with respect to the backbone (c). Consequently, white fibres need shorten by only ∼; as much as the red ones to produce a given curvature change of the body. By placing (EMG) electrodes as shown, one can monitor the activity of different fibre types during swimming. EMGs reveal that at low swimming speeds only the red fibres are used, whereas at high swimming speeds and the escape response, the white muscle fibres are used as well. (Reprinted from Rome et al., 1988.)

Figure 3.

High speed motion picture frames during steady swimming with red muscle (left, five film frames separated by 0.1 s) and escape response with white muscle (right, six frames at 5 ms intervals). When fish swim, the muscle on the concave side actively shortens and the muscle on the convex side is being passively lengthened by action of the contralateral muscle. To a first approximation, the sarcomere length change is proportional to the curvature of the backbone. Note the extreme curvature of the backbone during the escape response compared to very little curvature during steady swimming. Note also the relative time scales: one full tail beat of steady swimming takes 0.4 s whereas it takes only 0.025 s for the fish to complete bending during the escape response.

Figure 4.

Myofilament overlap in swimming carp. During sustained swimming (top) only the red muscle is active. The dotted lines and arrows show the SL excursion (1.91–2.23 μm). Note that the force does not drop below 96%. If the red muscle had to power the more extreme escape response (bottom), it would have to shorten to 1.4 μm where it generates little tension. Instead the white muscle which has a 4× greater gear ratio is used. In the posterior region of the fish, the white muscle shortens to only 1.75 μm (arrows and dotted line), where at least 85% maximal tension is generated. In the rest of the fish the excursion is smaller and the force higher. Note because carp myofilament lengths are the same as those of frog, the frog SL–tension curve is used to describe the SL–tension curves for carp red and white muscles.

Figure 5.

V/Vmax in swimming carp. Force–velocity (dashed) and power–velocity (solid) curves of the red muscle (upper) and white muscle (lower). During steady swimming (upper) the red muscle shortens at a V of 0.7–1.5 (ML) per second (shaded region) corresponding to a V/Vmax of 0.17–0.38 where maximum power is generated with optimal efficiency. The red fibres cannot power the escape response because they would have to shorten at 20 ML s−1 (upper) or 4× their Vmax. The escape response is powered by the white muscle which, because of its 4× higher gear ratio, needs to shorten at only 5 ML s−1, which corresponds to a V/Vmax of 0.38 where maximum power is generated (lower). The white muscle would not be well suited to power steady swimming movements (shaded, lower panel), as it would have to shorten at a V/Vmax of 0.01–0.03, where power and efficiency are low.

Figure 6.

Major kinetic steps in muscle activation and relaxation. Activation: step 1, Ca2+ is released from the SR into the myoplasm; step 2, Ca2+ binds to troponin, releasing inhibition of the thin filament; step 3, crossbridges then attach. Relaxation: step 4, Ca2+ is resequestered from the myoplasm by the Ca2+ pumps; step 5, Ca2+ comes off troponin, thereby preventing further crossbridge attachment; step 6, crossbridges then detach. For a muscle to relax rapidly, steps 4–6 must all be very fast.

Figure 7.

Twitch tension (upper) and calcium transients (lower) of three fibre types from toadfish at 15°C. In each case, the force and the calcium records have been normalized to their maximum value. The twitch and calcium transient become briefer, going from the slow‐twitch red fibre (r), to the fast‐twitch white fibre (w), to the superfast‐twitch swim bladder fibre (s). (Adapted from Rome et al., 1996.)

Figure 8.

Force production and calcium transients during repetitive stimulation. (a) Slow‐twitch red fibre stimulated at 3.5 Hz. The threshold [Ca2+] for force generation was derived by force–pCa experiment on skinned fibres and is shown with a dotted line. (b) Swim bladder fibre stimulated at 67 Hz. Note that the [Ca2+] threshold for force production is much higher for the swim bladder than for the red fibre and the different scale for the ordinate. (Adapted from Rome et al., 1996.)


Further Reading

Lutz G and Rome LC (1994) Built for jumping: the design of frog muscular system. Science 263: 370–372.

Rome LC, Funke RP, Alexander RM et al. (1988) Why animals have different muscle fibre types. Nature 355: 824–827.

Rome LC and Sosnicki AA (1991) Myofilament overlap in swimming carp. II. Sarcomere length changes during swimming. American Journal of Physiology (Cell Physiology) 260: C289–C296.

Rome LC, Swank D and Corda D (1993) How fish power swimming. Science 261: 340–343.

Rome LC, Syme DA, Hollingworth S, Lindstedt SL and Baylor SM (1996) The whistle and the rattle: the design of sound producing muscles. Proceedings of the National Academy of Sciences of the USA 93: 8095–8100.

Rome LC (1997) Testing a muscle's design. American Scientist 85: 356–363.

Rome LC (1997) Muscle and Movement. Eckert's Animal Physiology, 4th edn, pp. 351–395. San Francisco, CA: W. H. Freeman.

Rome LC and Lindstedt SL (1997) Mechanical and metabolic design of the muscular system in vertebrates. In: Dantzler W (ed.) Handbook of Physiology. Comparative Physiology, pp. 1587–1651. New York: Oxford University Press.

Rome LC and Lindstedt SL (1998) The quest for speed: muscles built for high frequency contractions. News in Physiological Sciences 13: 261–268.

Rome LC, Cook C, Syme D et al. (1999) Trading force for speed: Crossbridge kinetics of super‐fast muscle fibers. Proceedings of the National Academy of Sciences of the USA 96: 5826–5831.

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Rome, Lawrence C(Apr 2001) Comparative Vertebrate Muscle Physiology. In: eLS. John Wiley & Sons Ltd, Chichester. [doi: 10.1038/npg.els.0001862]