Locomotion as an emergent property of muscle contractile dynamics

Abstract

Skeletal muscles share many common, highly conserved features of organization at the molecular and myofilament levels, giving skeletal muscle fibers generally similar and characteristic mechanical and energetic properties; properties well described by classical studies of muscle mechanics and energetics. However, skeletal muscles can differ considerably in architectural design (fiber length, pinnation, and connective tissue organization), as well as fiber type, and how they contract in relation to the timing of neuromotor activation and in vivo length change. The in vivo dynamics of muscle contraction is, therefore, crucial to assessing muscle design and the roles that muscles play in animal movement. Architectural differences in muscle-tendon organization combined with differences in the phase of activation and resulting fiber length changes greatly affect the time-varying force and work that muscles produce, as well as the energetic cost of force generation. Intrinsic force-length and force-velocity properties of muscles, together with their architecture, also play important roles in the control of movement, facilitating rapid adjustments to changing motor demands. Such adjustments complement slower, reflex-mediated neural feedback control of motor recruitment. Understanding how individual fiber forces are integrated to whole-muscle forces, which are transmitted to the skeleton for producing and controlling locomotor movement, is therefore essential for assessing muscle design in relation to the dynamics of movement.

Keywords: Fascicle strain; In vivo contraction; Muscle activation; Muscle-tendon architecture; Muscle-tendon force.

Fig. 1.

Muscle architecture in relation to functional properties and active muscle volume. (A) Comparison of parallel- versus pinnate-fibered muscle–tendon architecture in relation to functional properties. ΔL, change in length; α, pennation angle; F_t, tendon force; F_m, muscle force; L_F, fascicle length. (B) Influence of muscle–tendon architecture on the cost of force generation (Biewener and Roberts, 2000). Cost of force generation is related to active muscle volume (V′), defined as the volume of muscle activated to generate a given force. Given that skeletal muscles generally produce similar peak isometric stresses (∼200–300 kPa), muscle force generation is generally proportional to the cross-sectional area (A) of activated fibers. Consequently, longer-fibered (L_F) muscles require a larger volume of activated muscle to generate a given force; as shown, a threefold difference in L_F (L_A=3L_B), where L_A and L_B equal the fascicle (or fiber) lengths of muscle A and muscle B, results in proximal muscle A consuming roughly threefold more energy to produce a given force compared with distal muscle B (∼33% recruitment of the muscles is depicted to produce a given force).

Fig. 2.

Comparison of the in vivo force–length behavior and net work done by distal muscle–tendon units under level versus incline conditions. Recordings show muscle forces determined from tendon force measurements, along with normalized fascicle length changes (L/L_r) as determined via sonomicrometry. Data are drawn from the following sources: guinea fowl lateral gastrocnemius (LG) and digital flexor IV (DF-IV) running at 1.3 m s⁻¹ (Daley and Biewener, 2003); wallaby LG and plantaris (PL) hopping at 4.5 m s⁻¹ (Biewener et al., 2004); turkey LG running at 2.5 m s⁻¹ (Biewener and Roberts, 2000; Roberts et al., 1997); and goat medial gastrocnemius (MG), LG, and superficial digital flexor (SDF) trotting at 2.5 m s⁻¹ (McGuigan et al., 2009). Whereas the wallaby LG force–length patterns presented here show positive work during level and incline hopping, with 10–12% shortening strains during active force development, LG shortening strains recorded across four animals averaged −1.0±4.6% for level versus 0.6±4.5% for incline hopping, with net work averaging −8.4±8.4 J kg⁻¹ for level versus −6.8±7.5 J kg⁻¹ for incline hopping (Biewener et al., 2004).

Fig. 3.

Summary statement. In vivo work loops estimated for the wallaby (A) biceps femoris and (B) vastus lateralis muscles during hopping at 4.2 m s⁻¹ on a level versus at an incline. Muscle stress was estimated from inverse dynamics of joint torques to obtain muscle force and muscle fiber cross-sectional area, with fascicle strains recorded via sonomicrometry (McGowan et al., 2007).

Fig. 4.

Qualitative comparison of muscle work in relation to force and energy economy and muscle–tendon architecture based on in vivo results obtained from a variety of animal muscles and locomotor conditions. In general, an inverse relationship exists for muscle work relative to force and energy economy, with long parallel-fibered muscles favoring greater work and shorter pinnate-fibered muscles favoring spring-like muscle–tendon function and low cost of force generation. Results for horse distal limb muscles are inferred from muscle–tendon architecture in relation to joint mechanics (Biewener, 1998b; McGuigan and Wilson, 2003). Other data are drawn from the following sources: wallaby plantaris (PL) and lateral gastrocnemius (LG) (Biewener et al., 1998b, 2004); goat LG, medial gastrocnemius (MG), and superficial digital flexor (SDF) (McGuigan et al., 2009); turkey LG and peroneus longus (PLong) (Gabaldón et al., 2004; Roberts et al., 1997); guinea fowl LG and digital flexor IV (DF-IV) (Daley and Biewener, 2003); mallard LG (Biewener and Corning, 2001); goat biceps femoris (BF) and vastus lateralis (VL) (Gillis et al., 2005); dog VL and semimembranosus (Gregersen et al., 1998); wallaby BF and VL (McGowan et al., 2007); and cockatiel pectoralis (Hedrick et al., 2003).

Fig. 5.

In vivo recordings of the pigeon supracoracoideus and pectoralis during free flight. (A) In vivo fascicle length, muscle force and activation (electromyography [EMG]) of the pigeon supracoracoideus (Supra; upstroke muscle) and pectoralis (Pect; downstroke muscle) during perch take-off and slow level flight to a landing perch. (B) In vivo stress versus normalized length work loops of the Supra and Pect corresponding to the fourth wingbeat cycle shown in grey in A. Insets in B show the muscle anatomy and the location of strain gauges bonded to the proximal humerus in locations where the Pect inserts ventrally on the deltopectoral crest and the tendon of the Supra passes dorsally over the shoulder to insert on the dorsal aspect of the humerus. Pull calibrations were used to calibrate muscle force from voltage recordings of bone strain (see Tobalske and Biewener, 2008 for further details). P′, muscle mass-specific power output.