Abstract
Defining variations in skeletal muscle passive mechanical properties at different size scales ranging from single muscle fibers to whole muscles is required in order to understand passive muscle function. It is also of interest from a muscle structural point-of-view to identify the source(s) of passive tension that function at each scale. Thus, we measured passive mechanical properties of single fibers, fiber bundles, fascicles, and whole muscles in three architecturally diverse muscles from New Zealand White rabbits (n = 6) subjected to linear deformation. Passive modulus was quantified at sarcomere lengths across the muscle’s anatomical range. Titin molecular mass and collagen content were also quantified at each size scale, and whole muscle architectural properties were measured. Passive modulus increased non-linearly from fiber to whole muscle for all three muscles emphasizing extracellular sources of passive tension (p < 0.001), and was different among muscles (p < 0.001), with significant muscle by size-scale interaction, indicating quantitatively different scaling for each muscle (p < 0.001). These findings provide insight into the structural basis of passive tension and suggest that the extracellular matrix (ECM) is the dominant contributor to whole muscle and fascicle passive tension. They also demonstrate that caution should be used when inferring whole muscle properties from reduced muscle size preparations such as muscle biopsies.
Highlights
Passive tension is borne by a muscle when it is lengthened beyond slack length
The ED2 fascicles were intermediate in their stressstrain relationship between the fiber, bundle and whole muscle scales (Figure 2C). These relationships became more obvious upon examining the passive modulus, which increased with increasing size scale (p < 0.0001; Figure 3) and was significantly different among muscles (p < 0.0001)
Magid and Law (1985) first demonstrated that frog muscle fibers and whole muscles have the same passive modulus, demonstrating that passive tension was mediated intracellularly across scale in frog muscle. This finding led to spectacular experiments that have elucidated the nature of the intracellular titin protein
Summary
Passive tension is borne by a muscle when it is lengthened beyond slack length. This increased tension resists further stretch, even in the absence of muscle activation. Muscle ECM, which is dominated by collagen in terms of mass, is organized into three interconnected levels – epimysium surrounds whole muscles, perimysium surrounds fascicles, and endomysium surrounds individual fibers (Borg and Caulfield, 1980; Trotter et al, 1995) These distinctions represent anatomical definitions with very little structural or functional basis. These various connective tissue layers provide structural support and play an important role in force transmission between fibers and tendon (Trotter and Purslow, 1992) Another passive load bearing structure is titin (Wang, 1985; Maruyama, 1986), which is a large (∼4 MDa) protein that spans from the sarcomere M-line to the Z-disk (Maruyama et al, 1985) and bears tension with increased sarcomere strain (Trombitas et al, 1995)
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