684 IEEE JOURNAL OF OCEANIC ENGINEERING, VOL. 29, NO. 3, JULY 2004 Force Generation for Locomotion of Vertebrates: Skeletal Muscle Overview Angie M. King, Denis S. Loiselle, and Peter Kohl Abstract—Locomotion is essential for vertebrate survival. Forces required for movement are generated by skeletal muscle. Skeletal muscle shortening and/or force generation occur via parallel sliding of two protein filaments: actin and myosin. This is driven by the cycling of cross-bridges, whose unitary nanometer length change and picoNewton force output are fueled by conversion of chemical energy, stored in the form of adenosine triphosphate, into a change in myosin protein configuration. The range of force and length changes of a muscle is determined by factors such as muscle cross section, fiber angle, tendon attachment, and lever ge- ometry, but also by the metabolic pathways available for adenosine triphosphate synthesis and by enzymes involved in cross-bridge cycling. In addition, muscle mechanical activity is affected by the extent of actin and myosin filament overlap. Force output can be graded by selective recruitment of motor units and/or by variation of force output from individual units. The cost of locomotion is subject to species differences and is affected by the environment and form of movement, with an energy efficiency of up to 0.4. Overall, design principles of vertebrate skeletal muscle may serve as an interesting reference point for novel actuator technologies. Index Terms—Force regulation, muscle function, muscle struc- ture. I. INTRODUCTION L OCOMOTION is a vital function for vertebrates, required for systems maintenance, reproduction and protection. This includes not only translocation, but also the postural basis for stance and stability. The foundation for the buildup and regulation of force for locomotion is provided by skeletal muscle. Other muscle types, such as smooth and cardiac, are not addressed here. Likewise, we do not discuss, in any detail, the enormous variation across species in molecular structure or innervation of skeletal muscle. II. STRUCTURE OF SKELETAL MUSCLE Skeletal musculature is made up of anatomically distinct units, which are attached to bones (via tendons) or other mus- Manuscript received July 25, 2003; revised December 12, 2003. This work was supported by the U.K. Medical Research Council and by the Biotechnology and Biological Sciences Research Council. P. Kohl is a Royal Society Research Fellow. A. M. King was with the Cardiac Mechano-Electric Feedback Group, Uni- versity Laboratory of Physiology, Oxford OX1 3PT, U.K. She is now with the Diagnostic Medical Sonography Program, Division of Diagnostic Ultrasound, University of Colorado Hospital, Denver, CO 80262 USA. D. S. Loiselle was with the Cardiac Mechano-Electric Feedback Group, Ox- ford, OX1 3PT, U.K. He is now with the Bioengineering Institute and Depart- ment of Physiology, University of Auckland, Auckland 1001, New Zealand. P. Kohl is with the Cardiac Mechano-Electric Feedback Group, Uni- versity Laboratory of Physiology, Oxford, OX1 3PT, U.K. (e-mail: peter.kohl@physiol.ox.ac.uk). Digital Object Identifier 10.1109/JOE.2004.833205 cles (via ligaments) to support specialized movement. In the human, there are 630 individual muscles, which make up 40% of total body weight. Individual muscles are composed of fascicles—assemblies of muscle fibers that are surrounded by a connective tissue sheath that can span the entire length of a muscle [Fig. 1(A)–(C)] [1]. Each fiber (diameter between 10 and 100 m) is one single cell, which is usually multinucleated, whose cytosol is confined by a single membrane called the sarcolemma. Glycogen, a chief en- ergy provider for skeletal muscle contraction, is stored in con- junction with this membrane. The sarcolemma protrudes into the muscle fiber at regular intervals forming transverse tubules (t-tubules). T-tubules provide an important pathway for elec- trical signals from the surface to the core of the cell, where they abut the cisterns of the sarcoplasmic reticulum (SR), the intra- cellular Ca store of muscle cells. Fibers contain densely packed regular bundles of myofibrils, the contractile units of muscle. Myofibrils are made up of thick (myosin, diameter 15 nm) and thin (actin, diameter 5 nm) pro- tein myofilaments. These myofilaments are arranged in a hexag- onal pattern and interdigitate [Fig. 1(F)]. In man, each myofibril contains approximately 1500 myosin and 3000 actin filaments [2]. Myofibrils (and, therefore, myofilaments) are organized in highly structured sarcomeres [Figs. 1(E) and 2]. The regular packing of myofibrils in the sarcomere gives rise to the typical cross striation of skeletal muscle, as skeletal muscle is birefringent, where the region of the sarcomere that contains the (thick) myosin filaments is optically more dense (anisotropic: A-band) than the remainder of the sarcomere that contains only the (thin) actin filaments (isotropic: I-band). The center of the I-band is marked by a narrow dark line, referred to as the Z-line (zwischen, German for “in between”). The distance between two Z-lines is the sarcomere length ( m at rest). Z-lines provide the anchor point for actin filaments, which extend on both sides of each Z-line. It is important to note that, functionally, sarcomeres consist of two half-sarcomeres whose force generators have opposite polarity. Actin filaments (each m long) consist of two inter- twined pearl-necklace-like chains composed of globular actin molecules (the pearls, where myosin will bind), tropomyosin (the chain, which covers the binding sites for myosin), and tro- ponin (where Ca will bind to displace tropomyosin and en- able actin–myosin bonding) [3]. Myosin filaments ( m long) consist of several hundred myosin molecules that are each around 0.15 m long [4] and have the appearance of a daffodil (before flowering). Individual molecules are connected by their “stems,” with the bud “head” sticking out to the sides of the assembled filament, as in a tightly 0364-9059/04$20.00 © 2004 IEEE