Structural and Functional Gradients with Temperature in the Flight Muscle of Manduca Sexta

Abstract

The force/extension curve of the flight muscle of the Hawkmoth, Manduca sexta is remarkably similar to that of mammalian cardiac muscle suggesting that it may serve as a useful model system for certain aspects of cardiac muscle structure and function ( J Exp Biol. 2004;207:2455). More recently, it was discovered that these animals maintain an astonishing thermal gradient of 8.8 C in the 5 mm distance dorsal to ventral in their dorso-longitudinal flight muscles (DLMs). Does the existence of this thermal gradient necessarily imply a functional gradient? Do these changes in function have, as their basis, changes in structure? Twitch dynamics of individual fibers within the DLM in intact animals are temperature dependent so that mechanical power output (and it's phase dependence) varies with depth in the tissue. A surprising observation was that all five sub-units in the DLM were simultaneously activated. Cooler muscles subjected to 25 hz stimulation (flight frequency) are partially fused with (likely) little crossbridge turnover. To assess the structural correlates of temperature gradients, we performed small-angle x-ray fiber diffraction measurements as a function of position along the dorsal-ventral thermal gradient in intact moth thoraces. The equatorial intensity ratio (I20/I10) in unstimulated muscle increased by ∼25% in the first 1 −1.5 mm traversing from dorsal to ventral, implying that increased temperature was associated with increased association of the myosin heads with the thin filaments presumably predisposing them towards more productive acto-myosin interaction. Interestingly, X-ray patterns from skinned muscle preparations improved with increasing temperature indicating better structural order. Together, these observations suggest that cooler, superficial muscles may act mainly as elastic energy storage, whereas warmer deeper muscles may do the bulk of the mechanical work.