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Functional and Clinical Significance of Skeletal Muscle Architecture

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Functional and Clinical Significance of Skeletal Muscle Architecture INVITED REVIEW ABSTRACT: Skeletal muscle architecture is the structural property of whole muscles that dominates their function. This review describes the basic architectural properties of human upper and lower extremity muscles. The designs of various muscle groups in humans and other species are analyzed from the point of view of optimizing function. Muscle fiber arrangement and motor unit arrangement is discussed in terms of the control of movement. Finally, the ability of muscles to change their architecture in response to immobilization, eccentric exercise, and surgical tendon transfer is reviewed. Future integrative physiological studies will provide insights into the mecha- nisms by which such adaptations occur. It is likely that muscle fibers trans- duce both stress and strain and respond by modifying sarcomere number in a way more suited to the new biomechanical environment. © 2000 John Wiley & Sons, Inc. Muscle Nerve 23: 1647–1666, 2000 FUNCTIONAL AND CLINICAL SIGNIFICANCE OF SKELETAL MUSCLE ARCHITECTURE RICHARD L. LIEBER, PhD,1,2 and JAN FRIDE´ N, MD, PhD3 1 Veterans Affairs Medical Center and University of California, Department of Orthopaedics, U.C. San Diego School of Medicine and V.A. Medical Center, 3350 La Jolla Village Drive, San Diego, California 92161, USA 2 Veterans Affairs Medical Center and University of California, Department of Bioengineering, San Diego, California, USA 3 Department of Hand Surgery, Go¨teborg University, Go¨teborg, Sweden Accepted 5 June 2000 Structure–function relationships in skeletal muscle provides guidelines for electrode placement during have been described and examined for over a cen- electromyographic measures of muscle activity, ex- tury. Classic studies have elucidated the microscopic plains the mechanical basis of muscle injury during and ultrastructural properties of skeletal muscle fi- normal movement, and aids in the interpretation of bers, yielding great insights into their function. How- histological specimens obtained from muscle biop- ever, less attention has been paid to the studies of sies. The purpose of this review is to describe the the macroscopic properties of skeletal muscle tissues theoretical significance of muscle architecture, to dating back to the 1600s (see discussion and refer- describe the basic architectural properties of human ences in Kardel27). This macroscopic arrangement upper and lower extremity muscles, and to intro- of muscle fibers is known as a muscle’s architec- duce advanced topics that represent current issues ture.20 Because muscle architecture is a primary de- not yet resolved in the literature. terminant of muscle function, understanding this structure–function relationship is of great practical BASIC ARCHITECTURAL DEFINITIONS importance. This understanding not only clarifies the physiological basis of force production and It is well-known that skeletal muscle is highly orga- movement but also provides a scientific rationale for nized at the microscopic level, as witnessed by the surgery that may involve tendon-transfer procedures, incredible number and diversity of electron micro- graphs and schematics of muscle sarcomeres that Abbreviations: CT, computed tomography; dSL/d␻, sarcomere length have been published in review articles and text- change during joint rotation; ECRB, extensor carpi radialis brevis; ECRL, books. However, with few exceptions, the arrange- extensor carpi radialis longus; EMG, electromyography; Lf, muscle fiber length; Lm, muscle length; Lo, optimal length; MRI, magnetic resonance ment of muscle fibers within and between muscles imaging; MTU, muscle tendon unit; PCSA, physiological cross-sectional ␳ has received much less attention. Muscle fibers are area; Po, maximum tetanic tension; , muscle density; r, moment arm; ␪ ROM, range of motion; , muscle fiber pennation angle; Vmax, maximum often depicted as projecting in bundles (fascicles) contraction velocity from an origin on a proximal tendon plate to an Key words: architecture; muscle design; muscle fiber; skeletal muscle; tendon transfer surgery insertion more distally. This simply does not do jus- Correspondence to: R.L. Lieber; e-mail: [email protected] tice to the wide array of muscle “designs” that are © 2000 John Wiley & Sons, Inc. apparent throughout the animal kingdom. The ar- Skeletal Muscle Architecture MUSCLE & NERVE November 2000 1647 chitecture of a given muscle is extremely consistent Muscles composed of fibers that extend parallel between individuals of the same species, giving rise to the muscle’s force-generating axis are described to the concept that certain constraints that deter- as having a parallel or longitudinal architecture (Fig. mine muscle architectural properties are pres- 1A). Although the fibers may project along a line ent.5,26,34,36,41,55,58,59,65 Although much attention has parallel to the force-generating axis, experimental been paid to factors such as fiber-type distribution in studies of mammalian muscle suggest that muscle determining muscle function, there is no question fibers do not extend the entire muscle length. In that function is also strongly determined by a mus- fact, detailed studies of muscle fiber lengths demon- cle’s architecture.7 strate that muscle fibers may not even extend the Skeletal muscle architecture can be defined as entire length of a fascicle.41,47 Muscles with fibers “the arrangement of muscle fibers within a muscle that are oriented at a single angle relative to the relative to the axis of force generation.”31 Whereas force-generating axis are described as having uni- muscle fibers have a relatively consistent fiber diam- pennate architecture (Fig. 1B). The angle between eter between muscles of different sizes and fiber size the fiber and the force-generating axis has been is directly proportional to fiber force generation, ar- measured at resting length in mammalian muscles of chitectural differences between muscles demon- very different designs and varies from about 0° to strate much more variability and more strongly affect 30°. It becomes obvious when performing muscle function. Although it might be proposed that differ- dissections that most muscles fall into the third and ent muscles produce different amounts of force most general category, multipennate muscles— based on differences in fiber size, fiber size between muscles constructed of fibers that are oriented at muscles actually varies little. Architectural differ- several angles relative to the axis of force generation ences between muscles are the best predictors of (Fig. 1C). Although these three designations are force generation. The various types of architectural oversimplified, they provide a vocabulary with which arrangements are as numerous as the number of to describe muscle designs. Because fiber orienta- muscles themselves. For discussion purposes, how- tion may have nothing to do with classic anatomical ever, we describe three general classes of muscle fi- axes, determination of muscle architecture is impos- ber architecture. sible from a single biopsy or even a magnetic reso- FIGURE 1. Artist’s conception of three general types of skeletal muscle architecture. (A) Longitudinal architecture in which muscle fibers run parallel to the muscle’s force-generating axis, as in the biceps brachii. (B) Unipennate architecture in which muscle fibers run at a fixed angle relative to the muscle’s force-generating axis, as in the vastus lateralis muscle. (C) Multipennate architecture in which muscle fibers run at several angles relative to the muscle’s force-generating axis (gluteus medius muscle). Lf, muscle fiber length; Lm, muscle length. 1648 Skeletal Muscle Architecture MUSCLE & NERVE November 2000 nance imaging (MRI), computerized tomography angles may vary from superficial to deep and even (CT), or ultrasound image, as these methods cannot from proximal to distal (Fig. 1). Although more so- account for variations in fiber length and orientation phisticated methods could be developed for mea- that occur along the muscle length. Thus, experi- surement of pennation angle, it is doubtful they mental methods have been developed to character- would provide a great deal more insight into muscle ize the architectural properties of skeletal muscle. function, because variations in pennation angle may not strongly affect function20 (see below). EXPERIMENTAL DETERMINATION OF SKELETAL Muscle length L is defined as “the distance from MUSCLE ARCHITECTURE m the origin of the most proximal muscle fibers to the Quantitative studies of muscle architecture were pio- insertion of the most distal fibers.”31 This is not the neered by Gans and Bock20 and Gans and De Vries,21 same as Lf because of the variable degree of “stagger” who developed precise methodology for defining seen in muscle fibers as they arise from and insert muscle architecture based on microdissection of onto tendon plates. To date, muscle fiber length can whole muscles. The usual parameters included in be determined only by microdissection of individual an architectural analysis are muscle length (Lm), fibers from fixed tissues or by laborious identifica- fiber length (Lf), pennation angle (i.e., the fiber tion of fibers by glycogen depletion on serial sections ␪ angle relative to the force-generating axis, ), and along the length of the muscle.47 Unless investiga- physiological cross-sectional area (PCSA). Typically, tors are explicit, when they refer to muscle fiber muscles are chemically fixed in 10% buffered forma- length, they are probably referring to muscle fiber lin in order
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