The asynchronous muscles of insects are characterized by asynchrony between muscle electrical and mechanical activity, a fibrillar organization with poorly developed sarcoplasmic reticulum, a slow time course of isometric contraction, low isometric force, high passive stiffness and delayed stretch activation and shortening deactivation. These properties are illustrated by comparing an asynchronous muscle, the basalar flight muscle of the beetle Cotinus mutabilis, with synchronous wing muscles from the locust, Schistocerca americana. Because of delayed stretch activation and shortening deactivation, a tetanically stimulated beetle muscle can do work when subjected to repetitive lengthening and shortening. The synchronous locust muscle, subjected to similar stimulation and length change, absorbs rather than produces work.

1. Transient, stretch-evoked force responses of chemically skinned muscle fibers from the cat hindlimb were investigated. The purpose of these experiments was to determine the exent to which short-range stiffness, the apparent stiffness exerted by the fiber over the first 0.5% of length change, is higher in type I than type II muscle fibers. Fibers were obtained from soleus and vastus intermedius muscles, which contain predominantly type I fibers, the LGm, a compartment of the lateral gastrocnemius muscle that contains predominantly type II fibers, and LG3, a compartment of mixed type. 2. Beyond a short range of approximately 1% of muscle length during a 0.5 muscle length/s (ML/s) stretch, most fibers exhibited an abrupt decrease in apparent stiffness or yield. Fibers from the muscles containing predominantly type S (slow twitch, or type I) fibers, soleus and vastus intermedius, exhibited such a pronounced decline in apparent stiffness that force declined as well during continued stretch. Most of the fibers from the LG3 compartment could be divided into two distinct groups depending upon whether or not they showed a force yield at the stretch velocity of 0.5 ML/s. 3. The short-range stiffness measured over the first 0.5% of stretch was greater for fibers showing force yield than for those that did not at matched initial forces and normalized stretch amplitudes. This result is consistent with the hypothesis that the same mechanism that endows the fiber with high short-range stiffness is also responsible for a greater extent of yielding. 4. Fibers from soleus were found to exhibit a force yield over a 200-fold range of velocities (0.01-2 ML/s). In contrast, most fibers from the LGm compartment showed only an increase in extent of yield with stretch velocity. Some of these fibers eventually yielded in force, but only when they were stretched at velocities > 2 ML/s. The proposed relationship between high short-range stiffness and yielding was supported by the finding that short-range stiffness increased sharply in the range of velocities where the fiber showed the greatest increase in extent of yield. 5. After the physiological experiments, fibers were subjected to SDS gel electrophoresis. Two distinct patterns of bands in the low molecular weight range were found to correspond to the two types that were identified on the basis of their dynamic mechanical properties. Fibers that did not yield at 0.5 ML/s showed a band pattern very similar to that of rabbit psoas (type II) fibers. 6. These results support the hypothesis that type I fibers are specialized in presenting a high short-range stiffness for effective postural control in advance of reflex mechanisms and that this property results from intrinsic properties of the fiber and is not due to differences in the dimensions of type I and II fibers. Yielding serves to protect the fiber from damaging levels of force during lengthening contractions. The importance of these transient properties to the mechanical behavior of muscle during ongoing movements is suggested by ...

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The basalar muscle of the beetle Cotinus mutabilis is a large, fibrillar flight muscle composed of approximately 90 fibers. The paired basalars together make up approximately one-third of the mass of the power muscles of flight. Changes in twitch force with changing stimulus intensity indicated that a basalar muscle is innervated by at least five excitatory axons and at least one inhibitory axon. The muscle is an asynchronous muscle; during normal oscillatory operation there is not a 1:1 relationship between muscle action potentials and contractions. During tethered flight, the wing-stroke frequency was approximately 80 Hz, and the action potential frequency in individual motor units was approximately 20 Hz. As in other asynchronous muscles that have been examined, the basalar is characterized by high passive tension, low tetanic force and long twitch duration. Mechanical power output from the basalar muscle during imposed, sinusoidal strain was measured by the work-loop technique. Work output varied with strain amplitude, strain frequency, the muscle length upon which the strain was superimposed, muscle temperature and stimulation frequency. When other variables were at optimal values, the optimal strain for work per cycle was approximately 5%, the optimal frequency for work per cycle approximately 50 Hz and the optimal frequency for mechanical power output 60–80 Hz. Optimal strain decreased with increasing cycle frequency and increased with muscle temperature. The curve relating work output and strain was narrow. At frequencies approximating those of flight, the width of the work versus strain curve, measured at half-maximal work, was 5% of the resting muscle length. The optimal muscle length for work output was shorter than that at which twitch and tetanic tension were maximal. Optimal muscle length decreased with increasing strain. The curve relating work output and muscle length, like that for work versus strain, was narrow, with a half-width of approximately 3 % at the normal flight frequency. Increasing the frequency with which the muscle was stimulated increased power output up to a plateau, reached at approximately 100 Hz stimulation frequency (at 35 degrees C). The low lift generated by animals during tethered flight is consistent with the low frequency of muscle action potentials in motor units of the wing muscles. The optimal oscillatory frequency for work per cycle increased with muscle temperature over the temperature range tested (25–40 degrees C). When cycle frequency was held constant, the work per cycle rose to an optimum with increasing temperature and then declined. We propose that there is a temperature optimum for work output because increasing temperature increases the shortening velocity of the muscle, which increases the rate of positive work output during shortening, but also decreases the durations of the stretch activation and shortening deactivation that underlie positive work output, the effect of temperature on shortening velocity being dominant at lower temperatures and the effect of temperature on the time course of activation and deactivation being dominant at higher temperatures. The average wing-stroke frequency during free flight was 94 Hz, and the thoracic temperature was 35 degrees C. The mechanical power output at the measured values of wing-stroke frequency and thoracic temperature during flight, and at optimal muscle length and strain, averaged 127 W kg(−1)muscle, with a maximum value of 200 W kg(−1). The power output from this asynchronous flight muscle was approximately twice that measured with similar techniques from synchronous flight muscle of insects, supporting the hypothesis that asynchronous operation has been favored by evolution in flight systems of different insect groups because it allows greater power output at the high contraction frequencies of flight.

SUMMARYMechanical power output and metabolic power input were measured from an asynchronous flight muscle, the basalar muscle of the beetle Cotinus mutabilis. Mechanical power output was determined using the work loop technique and metabolic power input by monitoring CO2 production or both CO2 production and O2 consumption. At 35°C, and with conditions that maximized power output (60 Hz sinusoidal strain, optimal muscle length and strain amplitude, 60 Hz stimulation frequency), the peak mechanical power output during a 10 s burst was approximately 140 W kg–1, the respiratory coefficient 0.83 and the muscle efficiency 14–16 %. The stimulus intensity used was the minimal required to achieve a maximal isometric tetanus. Increasing or decreasing the stimulus intensity from this level changed mechanical power output but not efficiency, indicating that the efficiency measurements were not contaminated by excitation of muscles adjacent to that from which the mechanical recordings were made. The CO2 produced during an isometric tetanus was approximately half that during a bout of similar stimulation but with imposed sinusoidal strain and work output, suggesting that up to 50 % of the energy input may go to muscle activation costs. Reducing the stimulus frequency to 30 Hz from its usual value of 60 Hz reduced mechanical power output but had no significant effect on efficiency. Increasing the frequency of the sinusoidal strain from 60 to 90 Hz reduced power output but not CO2 consumption; hence, there was a decline in efficiency. The respiratory coefficient was the same for 10 s and 30 s bursts of activity, suggesting that there was no major change in the fuel used over this time range.The mass-specific mechanical power output and the efficiency of the beetle muscle were each 2–3 times greater than values measured in previous studies, using similar techniques, from locust flight muscles, which are synchronous muscles. These results support the hypothesis that asynchronous flight muscles have evolved in several major insect taxa because they can provide greater power output and are more efficient than are synchronous muscles for operation at the high frequencies of insect flight.