Filament geometry and the activation of inisect flight muscles

Abstract

HIGH wingbeat frequencies are required for flight in many insects, and have led to striking specialisations¹. The thorax and wings form a resonant system whose oscillation is sustained by alternating contractions of antagonistic muscles. The action of these flight muscles is to produce only a small-amplitude deformation of the thorax, mechanically amplified into wing movements. The muscles are diverse in arrangement¹ and ultrastructure². In several insect orders, they are of a characteristic ‘fibrillar’ type whose very regular architecture is well known³. As recognised largely through the work of Pringle⁴, certain properties of fibrillar muscle permit more rapid wing-beats because the oscillation does not depend on pacemaking neural input: the muscles receive only slow and irregular stimulation, and the contraction of each is triggered, after a delay, directly by the stretch applied to it while its antagonist shortens. Studies of isolated glycerol- extracted fibrillar muscle fibres show that unusual properties underlying this sensitivity to stretch are intrinsic to the contractile apparatus itself⁵. ATPase levels and tension are low in calcium-activated fibres at rest length, but are increased by slight extension (0.1–5%). The muscles exhibit both actin-linked and myosin-linked regulation typical of many invertebrate muscles⁶, and the additional regulatory effects of mechanical conditions are not understood. Stretch has been presumed to modify cross-bridge attachment by some unknown effect on the myosin filamenats⁴ (possibly transmitted through structures which connect them to the Z-line in certain insect muscles⁷). I suggest here that many aspects of stretch–activation in fibrillar muscles may be explained by the particular geometry of their myosin and actin filaments.