A novel structural‐mechanical hypotheses relating costameres and ECM to optimal functional properties of skeletal muscle
Authors: Hodgson John A. , Chen J.S. , Sinha Shantanu , Sinha Usha , Edgerton V. Reggie 
Published: April 2020

The objective of this work is to understand how passive structural components in skeletal muscle provide effective load transmission as the dimensions of the muscle change.

In addition to forces transmitted along muscle fibers, there is a growing recognition that other structural components may transmit contractile loads laterally from myofibrils to the muscle sarcolemma and even between muscle fibers. This loading path is presumed to be mediated by several structural molecules which link myofibrils to the sarcolemma and endomysium and even link across the extracellular space to other muscle fibers. A challenging question is how such forces can be transmitted along the muscle by passive structures such as the endomysium as the dimensions of the muscle change. Corresponding changes in the dimensions of passive materials will influence their ability to transmit mechanical loading due to their force/length properties. One dimension which may not experience significant changes as a muscle changes length is an oblique fiber cross section aligned with the aponeurosis of the muscle (y axis of figure & Huijing, 1998, J. Electromyogr. Kinesiol. 8:61–77). We simulated muscle contractions with a stiff tensile material oriented along this axis and found an increased force output relative to other muscle models. The unchanging dimension of this material means that the force it may transmit is not affected by changes of muscle length.

Additionally, the constant area of the x‐y muscle plane illustrated in the lower part of the figure at all muscle lengths requires that the z dimension perpendicular to that plane must remain constant to maintain constant muscle volume. We concluded that a further critical component of passive muscle structure is a high tensile modulus along the z‐axis. These requirements for high tensile modulus along both the z and y axes suggest the presence of high tensile modulus over the y‐z plane, further suggesting that intra‐ and extracellular structural molecules, known to be anisotropic, must be specifically oriented to optimize muscle function. Costameres seem highly suited for this function. It is significant to note that our hypothesis suggests that critical mechanical properties (structural molecules?) may not be aligned with the long and/or cross‐sectional axes of the muscle fibers as commonly depicted. Furthermore, at least in the longitudinal (y axis) direction, the structural materials must retain similar properties within and across the intra‐ and extracellular regions of the muscle in order to maintain continuity of tensile mudulus.

The figure illustrates a bundle of muscle fibers in the x‐y plane between two constant dimension y‐z planes. The dimension along the z axis remains constant during shortening, constrained by the tensile structure, maximizing the dimensional change along the other cross sectional axis. The longitudinal (y) axis of the plane provides a minimally deformed material to efficiently transmit both lateral and longitudinal force vectors at all muscle lengths without the mechanical consequences of deforming passive materials.

Support or Funding Information

Supported by NIA Grant R01AG056999

Diagram of hypothesized costamere planes traversing muscle fibers

Figure 1