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Role of calcium in the regulation of mechanical power in insect flight.

ABSTRACT: Most flying insect species use "asynchronous" indirect flight muscles (A-IFMs) that are specialized to generate high mechanical power at fast contraction frequencies. Unlike individual contractions of "synchronous" muscles, those of A-IFMs are not activated and deactivated in concert with neurogenically controlled cycling of myoplasmic [Ca(2+)] but rather are driven myogenically by oscillatory changes in length. The motor neurons of the A-IFMs, which fire at a rate much slower than contraction frequency, are thought to play the limited role of maintaining myoplasmic [Ca(2+)] above the critical threshold that maintains the muscle in a stretch-activatable state. Despite this asynchronous form of excitation-contraction coupling, animals can actively regulate power output as required for different flight behaviors, although the neurobiological and biophysical basis of this regulation is unknown. While presenting tethered flying fruit flies, Drosophila melanogaster, with visual stimuli, we recorded membrane potential spikes in identified A-IFM fibers. We show that mechanical power output rises and falls in concert with the firing frequency of all A-IFM fibers and cannot be explained by differential recruitment of separately innervated motor units. To explore the hypothesis that myoplasmic [Ca(2+)] might similarly rise and fall in concert with firing frequency, we genetically engineered Drosophila to express the FRET-based Ca(2+) indicator cameleon selectively within A-IFMs. The results show that Ca(2+) levels increase in proportion to muscle firing rate, both during spontaneous flight and when muscle spikes are elicited electrically. Collectively, these experiments on intact animals support an active role for [Ca(2+)] in regulating power output of stretch-activated A-IFM.

SUBMITTER: Gordon S

PROVIDER: S-EPMC1449689 | biostudies-literature | 2006 Mar

REPOSITORIES: biostudies-literature

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Role of calcium in the regulation of mechanical power in insect flight.

Gordon Shefa S Dickinson Michael H MH

Proceedings of the National Academy of Sciences of the United States of America 20060306 11

Most flying insect species use "asynchronous" indirect flight muscles (A-IFMs) that are specialized to generate high mechanical power at fast contraction frequencies. Unlike individual contractions of "synchronous" muscles, those of A-IFMs are not activated and deactivated in concert with neurogenically controlled cycling of myoplasmic [Ca(2+)] but rather are driven myogenically by oscillatory changes in length. The motor neurons of the A-IFMs, which fire at a rate much slower than contraction f ...[more]

PMID: 16537527

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Project description:The application of rapidly applied length steps to actively contracting muscle is a classic method for synchronizing the response of myosin cross-bridges so that the average response of the ensemble can be measured. Alternatively, electron tomography (ET) is a technique that can report the structure of the individual members of the ensemble. We probed the structure of active myosin motors (cross-bridges) by applying 0.5% changes in length (either a stretch or a release) within 2 ms to isometrically contracting insect flight muscle (IFM) fibers followed after 5-6 ms by rapid freezing against a liquid helium cooled copper mirror. ET of freeze-substituted fibers, embedded and thin-sectioned, provides 3-D cross-bridge images, sorted by multivariate data analysis into ~40 classes, distinct in average structure, population size and lattice distribution. Individual actin subunits are resolved facilitating quasi-atomic modeling of each class average to determine its binding strength (weak or strong) to actin. ~98% of strong-binding acto-myosin attachments present after a length perturbation are confined to "target zones" of only two actin subunits located exactly midway between successive troponin complexes along each long-pitch helical repeat of actin. Significant changes in the types, distribution and structure of actin-myosin attachments occurred in a manner consistent with the mechanical transients. Most dramatic is near disappearance, after either length perturbation, of a class of weak-binding cross-bridges, attached within the target zone, that are highly likely to be precursors of strong-binding cross-bridges. These weak-binding cross-bridges were originally observed in isometrically contracting IFM. Their disappearance following a quick stretch or release can be explained by a recent kinetic model for muscle contraction, as behaviour consistent with their identification as precursors of strong-binding cross-bridges. The results provide a detailed model for contraction in IFM that may be applicable to contraction in other types of muscle.

Dataset Information

Role of calcium in the regulation of mechanical power in insect flight.

Publications

Role of calcium in the regulation of mechanical power in insect flight.

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