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
Powering the large variety of motor activities in which animals engage has required the evolution of different muscle types with widely varying contraction speeds. Hill showed as early as 1938 that the rate at which an active muscle uses energy is proportional to its isometric twitch speed (Hill, 1938(Hill, , 1950. The mechanisms underlying this relationship appear to be that both the rates of SR-Ca¥ pumping and crossbridge cycling increase to permit faster twitch speeds. Because both processes require ATP, there must be an increase in the rate of ATP utilization. Researchers have been able to partition the energy used during contraction into its two constituent parts by stretching muscle beyond myofilament overlap. In muscles from diverse species representing a large range of twitch speeds, it was found that a constant proportion (•25-40%) of the total energy during contraction is used by SR-Ca¥ pumps and nearly all of the remainder by the crossbridges (reviewed in Homsher & Kean, 1978). This finding is consistent with the notion that, as twitch speed of the muscle increases, the crossbridge kinetics and the Ca¥ pumping rate increase in unison. However, it is unclear if this must necessarily be the case. If the Ca¥ transient duration were the rate limiting step of relaxation, it seems possible that, in muscles adapted for very high frequency contractions, the SR-Ca¥ pumping rate might have increased far more dramatically than the crossbridge cycling rate. This in turn would increase the proportion of energy used by SR-Ca¥ pumps. Also, in these high frequency contraction muscles, the relative myofibrillar volume is known to be reduced (e.g. to 50% in toadfish swimbladder) as the space is taken up by increasing volume of SR (Rome & Lindstedt, 1998). This should increase further the proportion of the total energy utilization by the SR-Ca¥ pumps. To test this hypothesis, we determined the ATP utilization rate and partitioned it between SR-Ca¥ pumps and crossbridges in the swimbladder muscle of toadfish. The swimbladder has the fastest isometric relaxation rate of any vertebrate muscle (e.g. at 15°C it takes only •10 ms for force to fall from 90 to 10% in swimbladder compared with 1. The rate at which an isometrically contracting muscle uses energy is thought to be proportional to its twitch speed. In both slow and fast muscles, however, a constant proportion (25-40%) of the total energy has been found to be used by SR-Ca¥ pumps and the remainder by crossbridges. We examined whether SR-Ca¥ pumps account for a larger proportion of the energy in the fastest vertebrate muscle known (the toadfish swimbladder), and whether the swimbladder muscle utilizes energy at the superfast rate one would predict from its mechanics. 2. The ATP utilization rates of the SR-Ca¥ pumps and crossbridges were measured using a coupled assay system on fibres skinned with saponin. Surprisingly, despite its superfast twitch speed, the ATP utilization rate of swimbladder was no higher than that of much slower fast-twitch amphibian muscles. 3. Th...
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