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Curtin University of Technology
School of Physiotherapy

How Passive Structures Influence the Active Properties of Muscle

Brief Review - by Craig Ranson

Contents

Learning Objectives

Background Information

Passive Structures in Skeletal Muscle

The passive or non-contractile elements of skeletal muscle consist of the connective tissue that houses the contractile elements and the tendinous tissue which connects these sheaths to bone in order to transfer the force of muscular contraction to the bony levers.

Endomysium consists of type III, IV and V collagen. It envelopes each muscle fibre and is intimately associated with the basement membrane of muscle fibres. Continuous with the endomysium is the perimysium. Made up of type I and III collagen, it envelopes bundles of up to 150 fibres, called fascicles. Epimysium is the sheath of type I collagen that encloses entire muscles and forms much of the fascial septa between individual and groups of muscles. This hierarchy of collagenous envelopes are all continuous with each other and should not be considered, as separate independent entities, which is often how they are graphically represented. (Williams & Warwick, 1995).

Endomysium, perimysium and epimysium coalesce and blend into tendon via the aponeurosis, a sheet like intramuscular tendon plate which forms an elaborate muscle /connective tissue interface. At this musculo-tendinous junction their is extensive folding and interdigitation of the intracellular material with the extracellular connective tissue so that this interface acts as a sort of adhesive joint. This folding arrangement decreases the tensile forces placed on the junction due to deformation (stretching) and contraction (Zachezewski, Magee, & Quillen, 1996).

Up until recent years it was thought that the primary function of this harness of connective tissue was to support the muscular elements and transmit the force produced by muscular contraction to the bony levers. Although this is obviously one of the functions of these structures it is now evident that their elastic nature plays a vital role in protecting skeletal muscle from injury and enhancing the efficiency of it's contractions.

New Knowledge

Passive Properties Of Muscle

The Series Elastic Component (SEC) of Muscle

The most simple form of the Hill Model ( Hill, cited in Huijing, 1992b), divides skeletal muscle into contractile elements (CE) and a series elastic component (SEC). The CE provides the basis for the active behaviour of muscle. It is continuous with the passive, SEC which is described as having the characteristics of a spring. The importance of this spring mechanism will be discussed later in the paper.

Obviously, the CE consists of the muscular components of the musculo-tendinous complex. The SEC of skeletal muscle is thought to be located in the tendinous tissue and cross-bridges of muscle fibres. Tendon is the most important part of the SEC of muscle and has been reported to account for approximately 85% of the elastic length changes seen in experiments that stimulated rat muscle to optimal muscle force (Huijing, 1992a).

A change in tension in the SEC is able to substantially influence the force available and produced by muscular contraction (Zachezewski et al, 1996).

Characteristics of the SEC

The effect of loading on tendinous tissue can be explained by it's stress - strain curve. The characteristic crimped structure of tendon tissue provides it with enormous tensile strength. Initial loads (< 4% strain) on the tendon are taken up by straightening of the crimped collagen fibres. In this initial "toe" region of the curve, once the load is removed the elastic properties of the tendon allow it to return to its original length and crimped form, releasing energy that was stored during elongation of the tissue. This area of the curve represents the compliance of tendinous tissue.

Elongation in the next, linear phase, is also within the physiological limits of tendon allowing recovery after lengthening. The slope of the linear phase gives an indication of tendon stiffness, which is said to be approximately half that of steel. This amount of stiffness is necessary to allow efficient transfer of the force of muscular contraction to the bony levers. The stresses in the linear phase of tendon loading are accommodated by the tendons plasticity, if this is exceeded plastic deformation and sequential fibre failure occurs (Butler, Grood, & Noyes, 1978).

Researchers have attempted to develop normalised indices of stiffness and compliance for all of the tendinous tissue within skeletal muscle. It has become evident that these properties differ for aponeurosis (musculo-tendinous junction), tendon proper and the bone - tendon interface (fig 1). These variations can be accounted for by the variation in structure of the different regions of the SEC as outlined previously (Huijing, 1992a; Lieber, 1992).

Fig 1. Stiffness of the different regions of tendon (Lieber, 1992).
Fig 1. Stiffness of the different regions of tendon (Lieber, 1992).

Active Properties Of Muscle

Force-Velocity Characteristics

As a muscle contracts and shortens, the force it can develop falls with the increasing speed of shortening. The velocity of shortening at which the muscle can not produce any force at all in called maximum velocity (Vmax). This relationship between velocity of shortening and force production is proposed to occur because the formation of cross -bridges between actin and myosin filaments within the sarcomeres is rate dependant.

As the myofilaments slide past each other faster and faster there is less time available for cross-bridges to form and thus, less force is produced. (Lieber, 1992).

Fig. 2 Force-Velocity Curve (Lieber, 1992).
Fig. 2 Force-Velocity Curve (Lieber, 1992).

Length-Tension Characteristics

For cross-bridges to be formed between the actin and myosin filaments within individual sarcomeres there must be overlap of the myofilaments. When a muscle is lengthened to it's extreme outer range there is little overlap of the myofilaments and few cross-bridges are formed. As the muscle shortens, the myofilaments begin to overlap further and further, facilitating cross-bridge formation and increased force of contraction of the muscle. This part of the length-tension curve is called the descending limb. The plateau part of the curve occurs where there is optimal overlap of the myofilaments and no further cross-bridges are formed. Subsequently, the amount of force production levels off. In the inner range of muscle contraction the actin filaments begin to overlap on each other reducing the amount of potential binding sites for the myosin filaments. This area of the curve where cross-bridge numbers and force production begins to fall again due to this double-overlap of the actin filaments is termed the ascending limb (Lieber, 1992).

Fig 3. Length Tension Curve (Lieber, 1992).
Fig 3. Length Tension Curve (Lieber, 1992).

Effects of the SEC on Active Properties

Increased Operational Range of Muscle

The ratio of amount of tendon to muscle fibres effectively determines a muscles operating range. This is because as a muscle contracts in a lengthened position, part of the length change that occurs when the muscle is elongated is taken up by lengthening of the compliant tendinous tissue. This elastic lengthening of the musculo-tendinous unit allows the sarcomeres to relatively shorten, thus maintaining a more optimal length-tension relationship and allowing greater force production in the muscles outer range (Lieber, 1992). This effectively increases the operational range of the muscle and is especially important for muscle that must be able to produce strong contractions over a wide range of motion. This is probably why we see two joint muscles such as the biceps brachii, rectus femoris and hamstring muscles having a relatively high tendon to contractile element ratio.

The disadvantage of this system is that there is a delay between contraction of the muscle and initiation of movement as the force produced from muscular contraction will only be transmitted to the bony levers once elastic lengthening of the tendinous tissues has occurred. This produces a situation where there is a trade off between effective muscle range and precise muscular control (Lieber, 1992).

Decreases Muscle Tension During High Impact Motions

The compliance of tendons acts as a protective mechanism against tears when muscle is functioning eccentrically. The force-velocity curve (fig.3) indicates significantly higher levels of tetanic tension within muscle during eccentric activity. The SEC is able to absorb some of this tension, thus protecting the CE from tears that may be caused by high levels of stress (Lieber, 1992).

Effect of the SEC on the Stretch Shortening Cycle

The stretch shortening cycle is described as the positive effect on work output of a musculo-tendinous complex due to pre-stretch. This mechanism is essential in the production of efficient functional movement as isolated muscular contraction without a SEC would not be sufficient to produce the forces required activities such as walking, jumping, throwing or running (Huijing, 1992).

Mechanisms

The negative effects on force production (see fig 2.) of rapid muscular shortening that occur during the concentric phase of the SSC are reduced by the tendon being able to shorten (recoil) quicker than the CE. This relatively slower shortening velocity of the CE allows greater force production.

Clinical Implications

Fusiform muscles with their longer fibres have a larger range of active force production, a higher contractile velocity and a lower maximal force output compared to pennated muscles with their shorter fibres. This is because for a given change in muscle length, the individual sarcomeres lengthen less, with the change in muscle length being distributed over more sarcomeres (Lieber, 1992).

Quadriceps and plantarflexor muscles are designed for high force production because of their low fibre length (FL) to muscle length (ML) ratios and relatively large cross-sectional areas (Lieber, 1992).

Hamstring and dorsiflexor muscles are designed for high contractile velocity due to their relatively high fibre length to muscle length ratio and long muscle fibres (Lieber, 1992).

Hamstring muscles are more susceptible to tearing if a rapid imbalance in force output between the quadriceps and the hamstrings should occur during, for example, forward sprint running (McArdle et al. 1996).

Conclusion

The myosin filament is responsible for the generation of tension during muscle contraction.

The actin filament on the other hand is responsible for the regulation of the tension generated (Lieber, 1992).

In summarising the important points relating to the architecture of skeletal muscle:

It is implicit in this statement that the total excursion (active range) of the muscle is also proportional to the muscle fibre length (Lieber, 1992).

Fusiform muscles with their longer fibres have a larger range of active force production, a higher contractile velocity and a lower maximal force output compared to a pennated muscles with their shorter fibres.

Multipennate muscles, although slower in contractile velocity than fusiform muscles, are capable of generating much greater tension. This is due to the large numbers of sarcomeres that can be arranged in parallel and therefore increased fibre packing. Also the range of excursion through which a pennated muscle acts at an efficient sarcomere length is greater than for a fusiform muscle.

The pennated muscle can utilise the length-tension relationship more effectively in the production of force than can a muscle whose fibres are arranged in parallel.

References

Huijing PA (1992)
Chapter 6C, Mechanical muscle models. In Komi PV (Ed): Strength and Power in Sport.
Lieber R (1992)
Skeletal Muscle and Function: Implications for Rehabilitation and Sports Medicine. Baltimore: Williams and Wilkins.
McArdle WD, Katch FI and Katch VL (1996)
Exercise Physiology: Energy, Nutrition and Human Performance. (4th ed.). Philadelphia: Lea and Febiger.
Nigg BM and Herzog W (Eds) (1994)
Biomechanics of the Musculo-skeletal System. West Sussex: John Wiley & Sons Ltd.
Roy RR, and Edgerton VR (1992)
Chapter 6B, Skeletal muscle architecture and performance. In Komi PV (Ed): Strength and Power in Sport. Oxford.

Short Answer Review Questions

  1. Describe the microscopic structure of the muscle.
  2. Describe the sliding filament theory and how this relates to the cross-bridge cycle.
  3. What is muscle architecture? How is this related to force production and contractile velocity?
  4. What is the PCSA? How does this relate to the index of architecture (i.e. muscle length to fibre length ratio)?
  5. Draw a schematic length-tension relationship for muscles with (i) short fibres and large PCSA's and for (ii) long fibres and small PCSA's.
  6. Describe the process of excitation-contraction coupling.

Exercise Physiology Educational Resources 1997