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Secrets of the Fly: What Powers Wingbeat? 20 JAN 2005

Yawn. Stretch. Grumble. Retch.
Fruitfly with large red eyes, wings are blurred due to fast motion.No matter. All muscle motion starts with a nerve signal: Move, muscle, now! You know the drill: Brain activates nerve, nerve stimulates muscle cell, and something happens.

A fly is mounted in the flight simulator using glue and a fine wire. Courtesy Steven Frye, Caltech

Things are different in the fruitfly. This mainstay of the compost heap and the biology lab beats its wings 200 times a second. Even Why Filers can do the math: 200 contractions of the muscles that lift the wings, and another 200 in the muscles that pull them back down. All in one second.

That's a problem because it's much faster than nerves can trigger muscles, says Thomas Irving, associate professor of biology at the Illinois Institute of Technology, and director of the Biophysics Collaborative Access Team . "Human muscle needs a nerve impulse, but the insect has got to do it 200 times a second," and so the triggering "has to be done at the molecular level."

Line drawing shows gadget used to hold fly in X-ray stream.
By blasting a fruitfly with X-rays, researchers recorded molecular activity inside its muscles. Courtesy Tom Irving

To explore the molecular level, Irving and colleagues, including fruit-fly flight expert Michael Dickinson of Caltech, triggered some muscular activity of their own. They glued the head of a living fruitfly to a wire and placed it in a bath of X-rays at the Advanced Photon Source at Argonne National Laboratory in Illinois. They put on a light show to force the fly to adopt a steady wingbeat, and aimed brief surges of tightly focused X-rays at the critter's wing muscles. You can read their results in this week's Nature.

Cylinder lined with green and yellow boxes.
This pattern of light and dark confused the fly into thinking it was actually flying. By regulating the timing of the lights, the researchers controlled the rate of wingbeat. Courtesy Michael Reiser, Caltech

X-rays have long been used to probe the structure of molecules, most notably to reveal the peculiar double-helix of DNA more than 50 years ago. The process is called "X-ray diffraction" because molecules bend X-rays as they zoom past... and the amount of bending gives clues to the identity of the molecules. But it's harder to use X-rays to track action in living critters -- for one thing, you can cook the flies if you're not careful. For another, living critters tend to be moving critters...

Minding the muscles
Diagram shows detail of muscles in flexed arm.  Proteins move past each other during contraction.Irving and his colleagues used X-ray diffraction to watch two key muscle proteins, myosin and actin, which slide past each other during contraction. The apparatus was, in effect, an X-ray camera that revealed changing conditions inside muscle cells while the wings were moving. "We were looking at the interaction of motor proteins and filaments when the wings are stretching, being passively lengthened, and when they were being shortened," says Irving. "People had not looked at this before."

Skeletal muscles are made of bundles of fibers, where the proteins myosin and actin interact, causing contraction. Adapted from NIH

When the bicep contracts, the triceps stretches. A similar effect triggers rapid contraction of a fly's wing muscles.

Burly bicep flexes an arm.The result was X-ray data showing how myosin and actin interact during the various stages of muscle contraction. Muscles only contract, exerting a pulling force, so many muscles have to work in tandem: The triceps, for example, extends the arm, while the biceps flexes it.

Fly muscles also work in pairs to move the wing, and the chief finding of the new X-ray study is that this push-me-pull-you interaction is what causes the rapid contractions. (Notice that when you tighten your biceps, the triceps gets longer.) Apparently, as the muscle is stretched, myosin pulls away from the actin, and that triggers contraction.

Such a "length-dependent activity is found in all muscles," says Irving. "It's fairly strong in cardiac muscle, very strong in insect muscle. This may give us an insight into the heart muscle, but it's equally likely that it won't."

Sphere-shaped x-ray of fruitfly in flight, shows muscles flexing.
A new study shows how a fruitfly can beat its wings 200 times a second. The psychedelic background is an X-ray diffraction image of the fly's wing muscles. Courtesy Michael Dickinson, Caltech, and Tom Irving, Illinois Institute of Technology. All photos courtesy Biophysics Collaborative Access Team

Such pessimism aside, Irving describes the wing muscles as a "resonant system," that sustains its own movement. The setup reminds us of a vibrating guitar string, which moves past the center and then is pulled back to the other side.

But if nerves don't play a role in triggering muscle contraction, how does a fly start flapping its wings in the first place? By jumping, Irving says. The moving air catches the wings, the muscles stretch, and contraction is triggered.

And how does the wing stop beating? That remains an open question, says Irving. Don't yawn. Stay tuned.

-- David Tenenbaumlittle fly

Molecular Dynamics of Cyclically Contracting Insect Flight Muscle in Vivo, Michael Dickinson et al, Nature, 20 Jan. 2005.

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