Skeletal muscle design to meet functional demands

Abstract

Skeletal muscles are length- and velocity-sensitive force producers, constructed of a vast array of sarcomeres. Muscles come in a variety of sizes and shapes to accomplish a wide variety of tasks. How does muscle design match task performance? In this review, we outline muscle's basic properties and strategies that are used to produce movement. Several examples are provided, primarily for human muscles, in which skeletal muscle architecture and moment arms are tailored to a particular performance requirement. In addition, the concept that muscles may have a preferred sarcomere length operating range is also introduced. Taken together, the case is made that muscles can be fine-tuned to perform specific tasks that require actuators with a wide range of properties.

Figures

Figure 1.

Basic biomechanical properties of skeletal muscle. (a) The isometric sarcomere length–tension curve defined for frog skeletal muscle obtained using sequential isometric contractions in single muscle fibres (solid line). Dotted line represents passive muscle tension borne by the muscle without activation. Numbers shown above the active curve represent the three main regions of the length–tension curve: the ascending limb (1), plateau (2) and descending limb (3). (b) The isotonic muscle force–velocity curve for skeletal muscle obtained using sequential isotonic contractions. The circled numbers represent the force and velocity data from two concentric contractions (1,2) and one eccentric contraction (3). Note that force increases dramatically upon forced muscle lengthening and drops precipitously upon muscle shortening. Figures modified from Lieber [4].

Figure 2.

Generalized picture of muscle architectural types. Skeletal muscle fibres may be oriented parallel to the muscle's force-generating axis (a; known as ‘longitudinal’ architecture), at a fixed angle relative to the force-generating axis (b; known as ‘pennate’ architecture), or at multiple angles relative to the force-generating axis (c; known as ‘multi-pennate’ architecture). Each of these drawings represents an idealized view of muscle architecture and probably does not adequately describe any single muscle. (ML, muscle length; FL, fibre length.) Figure modified from Lieber [4].

Figure 3.

Skeletal muscle length–tension properties are well-approximated by the length–tension relationship. The active theoretical length–tension curve (black line) and experimental (grey circles) muscle length–tension relation are shown for three rabbit muscles of different architectures: (a) TA, tibialis anterior; (b) EDL, extensor digitorum longus; (c) ED II, second toe digital extensor. Theoretical and experimental data were highly correlated for all muscles (TA: r2 = 0.81, intraclass correlation coefficient: ICC = 0.84; EDL: r2 = 0.90, ICC = 0.86; ED II: r2 = 0.87, ICC = 0.89). Relative tension (muscle tension normalized to maximum tension) was plotted on the ordinate to facilitate comparison between muscles. Data replotted from Winters et al. [27].

Figure 4.

Scatter graph of fibre length and physiological cross-sectional areas (PCSAs) of muscles in the human lower limb. Fibre length is proportional to muscle excursion while PCSA is proportional to maximum muscle force. Thus, this graph can be used to compare the relative forces and excursions of leg muscles. Similar colours are used for the same functional groups. Data from Ward et al. [34]. (AdB, adductor brevis; AdL, adductor longus; AM, adductor magnus; BFL, biceps femoris, long head; BFS, biceps femoris, short head; EDL, extensor digitorum longus; EHL, extensor hallucis longus; FDL, flexor digitorum longus; GMAX, gluteus maximus; GMED, gluteus medius; GR, gracilis; FHL, flexor hallucis longus; ILPS, iliopsoas; LG, lateral gastrocnemius; MG, medial gastrocnemius; PEC, pectineus; PB, peroneus brevis; PL, peroneus longus; RF, rectus femoris; SAR, sartorius; SM, semimembranosus; SOL, soleus; ST, semitendinosus; TA, tibialis anterior; TP, tibialis posterior; VI, vastus intermedius; VL, vastus lateralis; VM, vastus medialis.)

Figure 5.

Ultrasonic measurement of muscle fibre shortening and tendon lengthening during ‘isometric’ dorsiflexion of the tibialis anterior. (a) Sagittal plane image of anterior compartment prior to contraction. (b) Sagittal plane image of anterior compartment during contraction. Note the shift in an individual muscle fascicle that is followed in the image during this process and the change in length (ΔL) and pennation angle calculated. Data from Ito et al. [36]. Images courtesy of Dr Yasuo Kawakami, Waseda University, Japan.

Figure 6.

Magnetic resonance imaging (MRI) used to render and calculate muscle volume for a human semitendinosus (ST). (a) Serial contiguous slices are acquired in the transverse plane. ST is highlighted in yellow. (b) Serial images are registered to reconstruct the entire thigh. (c) Muscles are distinguished from other tissues to calculate total muscle volume. (d) ST muscle is isolated from the entire thigh and the PCSA calculated. (e) Comparative photograph of dissected human ST.

Figure 7.

(a) Theoretical relationship between muscle fibre length and isometric force for a muscle with constant mass. (b) Theoretical relationship between muscle fibre length and dynamic muscle force for a muscle shortening at a constant velocity. (c) Tension calculated as fibre length is altered based on the isometric and isotonic effects shown in (a) and (b). Optimal fibre length results from a tradeoff between decreasing sarcomere shortening velocity (which increases force) and decreasing muscle isometric force capacity as fibre length increases. Data replotted from Lieber [42].

Figure 8.

(a) Change in sarcomere length with changing wrist joint angle (dSL/dϕ) for the extensor carpi radialis brevis (ECRB) and extensor carpi radialis longus (ECRL) muscles. Values are actually calculated directly from intraoperative sarcomere length values measured during hand surgery. (b) Calculated force–velocity relationships for the ECRB and ECRL muscles based on muscle architecture and wrist joint moment arms. The two curves cross at an angular velocity of approximately 240° s−1 which, on the basis of the muscle moment arms, corresponds to a muscle velocity of approximately 80 mm s−1. These data demonstrate that architectural ‘design’ can be used to favour isometric or isotonic force production and that synergists often have distinct architectural properties. Data from Lieber et al. [46].

Figure 9.

Operating ranges of the wrist motors on the isometric sarcomere length–tension relation. Note that wrist extensors operated primarily on the plateau region while the flexors operated predominantly along the ascending and steep ascending limbs. (Data are presented for flexion-extension in neutral forearm rotation.) Data from Loren & Lieber [48]. (FCU, flexor carpi ulnaris; FCR, flexor carpi radialis; ECRB, extensor carpi radialis brevis; ECRL, extensor carpi radialis longus; ECU, extensor carpi ulnaris.)

Figure 10.

Sarcomere length operating range of the human multifidus muscle plotted on the human skeletal muscle sarcomere length tension curve (black line). Grey circles represent average sarcomere length obtained via biopsy in lumbar extension (n = 8) or lumbar flexion (n = 5), as reported by Ward et al. [51]. These data demonstrate that the multifidus muscle operates on the ascending limb of the length tension curve and becomes intrinsically stronger as the spine in flexed (arrow). Schematic sarcomeres are shown on the ascending and descending limb to scale, based on the quantification of actin and myosin filament lengths reported previously in Lieber et al. [39].