Vertebrate sound producing muscles often operate at frequencies exceeding 100 Hz, making them the fastest vertebrate muscles. Like other vertebrate muscle, these sonic muscles are "synchronous," necessitating that calcium be released and resequestered by the sarcoplasmic reticulum during each contraction cycle. Thus to operate at such high frequencies, vertebrate sonic muscles require extreme adaptations. We have found that to generate the "boatwhistle" mating call , the swimbladder muscle fibers of toadfish have evolved (i) a large and very fast calcium transient, (ii) a fast crossbridge detachment rate, and (iii) probably a fast kinetic off-rate of Ca2+ from troponin. The fi'bers of the shaker muscle of rattlesnakes have independently evolved similar traits, permitting tail rattling at '90 Hz.sients-in fact the largest and fastest ever recorded. However, our results showed that a fast Ca2+ transient alone is not sufficient for high frequency operation. By measuring Vmax, an index of crossbridge detachment rate, and the force-pCa relationship in skinned fibers, a possible index of troponin kinetics, we found that rapid activation and relaxation likely also require a modification of the crossbridge kinetic rate, and probably a modification of the kinetics of Ca2+-troponin binding. In reaching these conclusions, we first compared the above measurements in three fiber types from toadfish, ranging from slow twitch swimming fibers to the superfast twitch swimbladder fibers. We then compared the properties of rattlesnake shaker fibers with those of swimbladder.Skeletal muscle fibers perform a wide range of activities, and different fiber types are accordingly designed to operate at different speeds and frequencies (1). A number of modifications appear to underlie this diversity. For example, in locomotory muscle, compared with slow twitch fibers, fast twitch fibers have a faster myosin with a higher maximum velocity of shortening (Vm,,) (2, 3), a greater content of sarcoplasmic reticulum (SR), and its associated Ca2+ pumps (4, 5), a different isoform of the SR Ca2+ pump (SERCAl in fast versus SERCA2 in slow) (6, 7) and a greater concentration of parvalbumin (a soluble protein that binds both calcium and magnesium) (5, 8). There is also evidence that fast fibers have a briefer myoplasmic free Ca2+ concentration ([Ca2+]) transient (9, 10) and less sensitive force-pCa relationship (11,12).To understand the physiological modifications that underlie very rapid contractions, we have studied two of the fastest vertebrate muscles known. Both of these "sonic" muscles are used to produce sounds at the frequency at which the muscle contracts. The "boatwhistle" mating call of the male toadfish (Opsanus tau) is generated by '200 Hz contractions (25°C) of the muscles encircling the fish's gas-filled swimbladder (13-15). The familiar "rattle" of the venomous western diamondback rattlesnake (Crotalus atrox) is generated by "90 Hz contractions (35°C) of the shaker muscles at the base of the tail (16-19). The operational frequ...
Contractile abilities of normal and "mini" triceps surae muscles from mice (Mus domesticus) selectively bred for high voluntary wheel running. J Appl Physiol 99: 1308 -1316, 2005. First published June 9, 2005; doi:10.1152/japplphysiol.00369.2005.-As reported previously, artificial selection of house mice caused a 2.7-fold increase in voluntary wheel running of four replicate selected lines compared with four random-bred control lines. Two of the selected lines developed a high incidence of a small-muscle phenotype ("mini muscles") in the plantar flexor group of the hindlimb, which apparently results from a simple Mendelian recessive allele. At generations 36 -38, we measured wheel running and key contractile characteristics of soleus and medial gastrocnemius muscles from normal and mini muscles in mice from these selected lines. Mice with mini muscles ran faster and a greater distance per day than normal individuals but not longer. As expected, in minimuscle mice the medial and lateral gastrocnemius muscles were ϳ54 and 45% the mass of normal muscles, respectively, but the plantaris muscles were not different in mass and soleus muscles were actually 30% larger. In spite of the increased mass, contractile characteristics of the soleus were unchanged in any notable way between mini and normal mice. However, medial gastrocnemius muscles in mini mice were changed markedly toward a slower phenotype, having slower twitches; demonstrated a more curved force-velocity relationship; produced about half the massspecific isotonic power, 20 -50% of the mass-specific cyclic work and power (only 10 -25% the absolute power if the loss in mass is considered); and fatigued at about half the rate of normal muscles. These changes would promote increased, aerobically supported running activity but may compromise activities that require high power, such as sprinting. experimental evolution; fatigue; muscle mechanics; power; selective breeding; work SWALLOW ET AL. (34) describe an artificial selection experiment using a base population of outbred, Hsd:ICR house mice (Mus domesticus) in which four replicate lines were subject to selective breeding for high levels of voluntary wheel running whereas another four lines were random bred as controls. Compared with mice from the control lines, mice from the selected lines ran ϳ70% more revolutions/day after 10 generations of selection (34), 100% more after 14 generations (17), and 170% more revolutions and about double the average running speed after 23 generations (5, 11, 13). These mice have been the focus of anatomical, behavioral, physiological, and psychological investigations on the correlated effects of such selection (e.g., Refs. 7,11,[23][24][25]28,29,[35][36][37].More recently it has been noted that some individuals in both the selected and control lines express a small-muscle phenotype in which the plantar flexor muscle group (soleus, gastrocnemius, and plantaris) is 44 -50% lighter than normal for the body mass (5, 12, 17). Evidence suggests that this smallmuscle phenotype, coine...
Superfast muscles power high-frequency motions such as sound production and visual tracking. As a class, these muscles also generate low forces. Using the toadfish swimbladder muscle, the fastest known vertebrate muscle, we examined the crossbridge kinetic rates responsible for high contraction rates and how these might affect force generation. Swimbladder fibers have evolved a 10-fold faster crossbridge detachment rate than fast-twitch locomotory fibers, but surprisingly the crossbridge attachment rate has remained unchanged. These kinetics result in very few crossbridges being attached during contraction of superfast fibers (only Ϸ1͞6 of that in locomotory fibers) and thus low force. This imbalance between attachment and detachment rates is likely to be a general mechanism that imposes a tradeoff of force for speed in all superfast fibers.The superfast fiber type is found where high-frequency contractions are required, such as in vertebrate eye muscles and in both vertebrate and invertebrate synchronous soundproducing muscles. These muscles have a series of modifications for speed, including a large volume of sarcoplasmic reticulum (SR) (1-7) to produce very rapid calcium transients (8) and low-affinity troponin to speed myofilament deactivation after [Ca 2ϩ
Effects of temperature on muscle contraction and powering movement are profound, outwardly obvious, and of great consequence to survival. To cope with the effects of environmental temperature fluctuations, endothermic birds and mammals maintain a relatively warm and constant body temperature, whereas most fishes and other vertebrates are ectothermic and conform to their thermal niche, compromising performance at colder temperatures. However, within the fishes the tunas and lamnid sharks deviate from the ectothermic strategy, maintaining elevated core body temperatures that presumably confer physiological advantages for their roles as fast and continuously swimming pelagic predators. Here we show that the salmon shark, a lamnid inhabiting cold, north Pacific waters, has become so specialized for endothermy that its red, aerobic, locomotor muscles, which power continuous swimming, seem mammal-like, functioning only within a markedly elevated temperature range (20-30 degrees C). These muscles are ineffectual if exposed to the cool water temperatures, and when warmed even 10 degrees C above ambient they still produce only 25-50% of the power produced at 26 degrees C. In contrast, the white muscles, powering burst swimming, do not show such a marked thermal dependence and work well across a wide range of temperatures.
In animals, muscles are the most common effectors that translate neuronal activity into behavior. Nowhere is behavior more restricted by the limits of muscle performance than at the upper range of high-frequency movements. Here, we see new and multiple designs to cope with the demands for speed. Extremely rapid oscillations in force are required to power cyclic activities such as flight in insects or to produce vibrations for sound. Such behaviors are seen in a variety of invertebrates and vertebrates, and are powered by both synchronous and asynchronous muscles. In synchronous muscles, each contraction/relaxation cycle is accompanied by membrane depolarization and subsequent repolarization, release of activator calcium, attachment of cross-bridges and muscle shortening, then removal of activator calcium and cross-bridge detachment. To enable all of these to occur at extremely high frequencies a suite of modifications are required, including precise neural control, hypertrophy of the calcium handling machinery, innovative mechanisms to bind calcium, and molecular modification of the cross-bridges and regulatory proteins. Side effects are low force and power output and low efficiency, but the benefit of direct, neural control is maintained. Asynchronous muscles, in which there is not a 1:1 correspondence between neural activation and contraction, are a radically different design. Rather than rapid calcium cycling, they rely on delayed activation and deactivation, and the resonant characteristics of the wings and exoskeleton to guide their extremely high-frequency contractions. They thus avoid many of the modifications and attendant trade-offs mentioned above, are more powerful and more efficient than high-frequency synchronous muscles, but are considerably more restricted in their application.
The purpose of this study was to identify the frequency, conduction velocity, and wavelength of fast and slow motor unit action potentials (MUAPs) from mixed mammalian muscle. Stimulation and blocking pulses to the sciatic nerve produced varying recruitment patterns (confirmed by force measurements) of fast and slow motor units of the medial gastrocnemius of six rats. Myoelectric signals from the muscle were resolved into their intensity in time and frequency space. Slow MUAPs had a mean frequency (+/- SEM) of 183 +/- 8 Hz, conduction velocity of 3.5 +/- 0.6 m s(-1), and wavelength of 19 mm. Fast MUAPs had a mean frequency of 369 +/- 11 Hz, conduction velocity of 6.7 +/- 0.5 m s(-1), and wavelength of 18 mm. Frequency and conduction velocity, but not wavelength, were significantly different between the fast and slow MUAPs. The distinct wave properties of fast and slow MUAPs can thus be used to distinguish action potentials from these motor units, and could be used to determine patterns of motor unit recruitment during locomotion.
We recorded electromyograms of slow-twitch (red) muscle fibers and videotaped swimming in the largemouth bass (Micropterus salmoides) during cruise, burst-and-glide, and C-start maneuvers. By use of in vivo patterns of stimulation and estimates of strain, in vitro power output was measured at 20 degrees C with the oscillatory work loop technique on slow-twitch fiber bundles from the midbody area near the soft dorsal fin. Power output increased slightly with cycle frequency to a plateau of approximately 10 W/kg at 3-5 Hz, encompassing the normal range of tail-beat frequencies for steady swimming (approximately 2-4 Hz). Power output declined at cycle frequencies simulating unsteady swimming (burst-and-glide, 10 Hz; C-start, 15 Hz). However, activating the muscle at 10 Hz did significantly increase the net work done compared with the work produced by the inactive muscle (work done by the viscous and elastic components). Thus this study provides further insight into the apparently paradoxical observation that red muscle can contribute little or no power and yet continues to show some recruitment during unsteady swimming. Comparison with published values of power requirements from oxygen consumption measurements indicates a limit to steady swimming speed imposed by the maximum power available from red muscle.
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