Molecular dynamics of cyclically contracting insect flight muscle in vivo.
Flight in insects--which constitute the largest group of species in the animal kingdom--is powered by specialized muscles located within the thorax. In most insects each contraction is triggered not by a motor neuron spike but by mechanical stretch imposed by antagonistic muscles. Whereas 'stretch activation' and its reciprocal phenomenon 'shortening deactivation' are observed to varying extents in all striated muscles, both are particularly prominent in the indirect flight muscles of insects. Here we show changes in thick-filament structure and actin-myosin interactions in living, flying Drosophila with the use of synchrotron small-angle X-ray diffraction. To elicit stable flight behaviour and permit the capture of images at specific phases within the 5-ms wingbeat cycle, we tethered flies within a visual flight simulator. We recorded images of 340 micros duration every 625 micros to create an eight-frame diffraction movie, with each frame reflecting the instantaneous structure of the contractile apparatus. These time-resolved measurements of molecular-level structure provide new insight into the unique ability of insect flight muscle to generate elevated power at high frequency.
Dickinson
Michael
M
Department of Bioengineering, California Institute of Technology, Pasadena, California 91125, USA.
Farman
Gerrie
G
Frye
Mark
M
Bekyarova
Tanya
T
Gore
David
D
Maughan
David
D
Irving
Thomas
T
D000818:Animals; D004330:Drosophila / Q000033:anatomy & histology / Q000502:physiology*; D004331:Drosophila melanogaster / Q000033:anatomy & histology / Q000502:physiology; D005260:Female; D005426:Flight, Animal / Q000502:physiology*; D009119:Muscle Contraction / Q000502:physiology*; D018485:Muscle Fibers, Skeletal / Q000502:physiology; D018482:Muscle, Skeletal / Q000033:anatomy & histology / Q000502:physiology*; D013997:Time Factors; D014921:Wings, Animal / Q000502:physiology; D014961:X-Ray Diffraction