D

inactive downstroke

FIGURE 2 In insects using an asynchronous flight motor, the wing muscles are segregated into two anatomically, physiologically, and functionally distinct groups. (A) The large indirect power muscles, which fill the thorax, are arranged in two antagonistic groups. (B) A cross section through the thorax (as indicated by line in A) showing the action of the power muscles. The laterally placed dorsoventral muscles drive the upstroke, whereas the more medial dorsolongitudinal muscles drive the downstroke. The contraction of each muscle set stretches the antagonist group thereby activating the next phase of oscillation. The motion of the thorax is indicated by black arrows, motion of wings is shown by gray arrows. (C) The arrangement of direct steering muscles. (D) Illustration of how activity of a steering muscle changes wing motion (enlargement of rectangular region in C); as muscle becomes active (dark gray), wing trajectory changes.

of interneurons and motor neurons that pattern the activity of the flight muscles. The phasic, phase-locked nature of this feedback is important because the mechanical properties of steering muscles are extremely sensitive to the precise time at which they are activated within the wingbeat cycle.

Muscles

As with sensory systems, motor systems of insects exhibit many specializations related to flight behavior. Unlike the wings of birds, bats, and pterosaurs, insect wings contain no intrinsic muscles. The wing is attached to the thorax by a complicated hinge structure that amplifies the tiny strains of the flight musculature into the large sweeping motions of the wing. The hinge is composed of a connected set of hard sclerotized elements (the wing sclerites or pteralia) embedded within a matrix of more compliant cuticle. Flight muscles may be segregated into two morphological groups according to how they transmit force to the wing. Direct flight muscles insert upon apodemes connected directly to the wing sclerites. In contrast, indirect flight muscles insert within the thorax some distance from the base of the wing. Odonates are distinct in possessing only direct flight muscles, whereas most insects possess some combination of direct and indirect muscles. In many of the most species-rich orders, including the Coleoptera, Hymenoptera, and Diptera, direct and indirect muscles differ physiologically and serve distinct functions (Fig. 2).

Large indirect "power" muscles provide the mechanical energy to drive the gross up-and-down motion of the wings, whereas a set of small direct "steering" muscles controls the fine changes in wing kinematics during flight. Each contraction in a steering muscle is activated one for one, by action potentials in presynaptic motor neurons, but contractions in the power muscles are asynchronous with motor input. By a molecular mechanism not yet fully understood, rapid stretch activates the crossbridges in asynchronous muscles, causing them to shorten after a brief delay. The low-frequency drive of motor neurons is sufficient to elevate calcium concentration within the sarcoplasm of asynchronous muscle to a level that maintains crossbridges in a stretch-activated state. During flight, contractions within sets of antagonist downstroke and upstroke muscles provide the requisite mechanical stretch to activate each other. Stretch activation frees muscles from the requirement of an extensive sarcoplasmic reticulum (SR), which is necessary in synchronous muscle for the release and subsequent uptake of calcium during twitches.

Asynchronous muscles are capable of generating elevated levels of mechanical power because their internal volume is filled almost exclusively with contractile fibrils and mitochondria. The advantage of stretch activation is especially strong at high frequencies for which typical twitch muscles would require an enormous surface area of SR, severely compromising their ability to generate power. Thus, asynchronous fliers can attain much higher wingbeat frequencies, and thus smaller body size, than can insects using synchronous flight muscles. The mechanical efficiency of asynchronous muscles should also be high because the normal costs associated with cyclic release and uptake of calcium through the SR are not incurred. Because their contraction is only partially controlled by the nervous system, indirect asynchronous muscles are ill-suited to mediating rapid changes in wing motion. The nervous system exerts its control of flight behavior primarily through the action of the direct synchronous steering muscles.

Pattern-Generating Circuits

The motor neurons that innervate insect flight muscles are driven by complex rhythm-generating circuits within the nervous system. Seminal studies by Don Wilson on locust flight led to the discovery of central pattern generators (CPGs), circuits consisting of interneurons and motor neurons capable of generating rhythmic patterns in the complete absence of phasic sensory feedback. Cells within CPGs excite and inhibit the motor neurons of upstroke and downstroke muscles so that they fire antiphasically during the stroke cycle. Even stretch-activated muscles are driven by CPGs, although the firing rate is roughly 10 times lower than wingbeat frequency. Although there is no doubt that insect nervous systems contain CPGs, research pioneered by Kier Pearson and colleagues has demonstrated that sensory feedback from thoracic mechanosensory structures plays an essential role in patterning motor output during flight. For example, electrical stimulation of wing stretch receptor cells can reset the timing of the flight rhythm in locusts—thus fulfilling a strict criterion that is used to test whether a neuron is a member of a CPG. The circuitry underlying flight behavior is best described as a distributed pattern-generating network, consisting of both central and peripheral neurons.

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