Muscle architecture in relation to function.

Abstract

Animal muscles generate forces and induce movements at desirable rates. These roles are interactive and must be considered together. Performance of the organism and survival of the species also involve potential optimization of control and of energy consumption. Further, individual variability arising partly via ontogeny and partly from phylogenetic history often has pronounced and sometime conflicting effects on structures and their uses. Hence, animal bodies are generally adequate for their tasks rather than being elegantly matched to them. For muscle, matching to role is reflected at all levels of muscular organization, from the nature of the sarcoplasm and contractile filaments to architectural arrangements of the parts and whole of organs. Vertebrate muscles are often analyzed by mapping their placement and then "explaining" this on the basis of currently observed roles. A recent alternative asks the obverse; given a mass of tissue that may be developed and maintained at a particular cost, what predictions do physical principles permit about its placement. Three architectural patterns that deserve discussion are the classical arrangement of fibers in pinnate patterns, the more recent assumption of sarcomere equivalence, and the issue of compartmentation. All have potential functional implications. 1. The assumption of equivalence of the sarcomeres of motor units allows predictions of the fiber length between sites of origin and insertion. In musculoskeletal systems that induce rotation, the observed (but not the pinnation-associated) insertion angle will differ with the radial lines on which the fibers insert. In a dynamic contraction inducing rotation, a shift of moment arm has no effect for muscles of equal mass. 2. Classical pinnate muscles contain many relatively short fibers positioned in parallel but at an angle to the whole muscle, reducing the per fiber force contribution. However, the total physiological cross-section and total muscle force are thus increased relative to arrangements with fibers parallel to the whole muscle. Equivalent muscles may be placed in various volumetric configurations matching other demands of the organism. The loss of fiber force due to (pinnate, not equivalent) angulation is compensated for by the reduced shortening of fibers in multipinnate arrays. 3. Compartmentation, i.e., the subdivision of muscles into independently controlled, spatially discrete volumes, is likely ubiquitous. Differential activation of the columns of radial arrays may facilitate change of vector and with this of function. Compartmentation is apt to be particularly important in strap muscles with short fiber architecture; their motor units generally occupy columnar, rather than transversely stacked, subdivisions; this may affect recovery from fiber atrophy and degeneration.(ABSTRACT TRUNCATED AT 400 WORDS)