Person:

Biewener, Andrew

Hummingbirds (Trochilidae) are widely known for their insect-like flight strokes characterized by high wing beat frequency, small muscle strains and a highly supinated wing orientation during upstroke that allows for lift production in both halves of the stroke cycle. Here, we show that hummingbirds achieve these functional traits within the limits imposed by a vertebrate endoskeleton and muscle physiology by accentuating a wing inversion mechanism found in other birds and using long-axis rotational movement of the humerus. In hummingbirds, long-axis rotation of the humerus creates additional wing translational movement, supplementing that produced by the humeral elevation and depression movements of a typical avian flight stroke. This adaptation increases the wing-to-muscle-transmission ratio, and is emblematic of a widespread scaling trend among flying animals whereby wing-to-muscle-transmission ratio varies inversely with mass, allowing animals of vastly different sizes to accommodate aerodynamic, biomechanical and physiological constraints on muscle-powered flapping flight.

The supracoracoideus (SUPRA) is the primary upstroke muscle for avian flight and is the antagonist to the downstroke muscle, the pectoralis (PECT). We studied in vivo contractile properties and mechanical power output of both muscles during take-off, level and landing flight. We measured muscle length change and activation using sonomicrometry and electromyography, and muscle force development using strain recordings on the humerus. Our results support a hypothesis that the primary role of the SUPRA is to supinate the humerus. Antagonistic forces exerted by the SUPRA and PECT overlap during portions of the wingbeat cycle, thereby offering a potential mechanism for enhancing control of the wing. Among flight modes, muscle strain was approximately the same in the SUPRA (33–40%) and the PECT (35–42%), whereas peak muscle stress was higher in the SUPRA ((85–126 N m^{–2})) than in the PECT ((50–58 N m^{–2})). The SUPRA mainly shortened relative to resting length and the PECT mainly lengthened. We estimated that elastic energy storage in the tendon of the SUPRA contributed between 28 and 60% of the net work of the SUPRA and 6–10% of the total net mechanical work of both muscles. Mechanical power output in the SUPRA was congruent with the estimated inertial power required for upstroke, but power output from the PECT was only 42–46% of the estimated aerodynamic power requirements for flight. There was a significant effect of flight mode upon aspects of the contractile behavior of both muscles including strain, strain rate, peak stress, work and power.

To relate in vivo behavior of fascicle segments within a muscle to their in vitro force-length relationships, we examined the strain behavior of paired segments within each of three vertebrate muscles. After determining in vivo muscle activity patterns and length changes of in-series segments within the semimembranosus muscle (SM) in the American Toad (Bufo americanus) during hopping and within the sternohyoid (SH) muscle in the rat (Rattus rattus) during swallowing, and of spatially separated fascicles within the medial gastrocnemius (MG) muscle in the rat during trotting, we measured their corresponding in vitro (toad) or in situ (rat) force–length relationships (FLRs). For all three muscles, in vivo strain heterogeneity lasted for about 36–57% of the behavior cycle, during which one segment or fascicle shortened while the other segment or fascicle simultaneously lengthened. In the toad SM, the proximal segment shortened from the descending limb across the plateau of its FLR from 1.12 to 0.91 of its optimal length (Lo), while the distal segment lengthened (by 0.04 ± 0.04 Lo) before shortening down the ascending limb from 0.94 to 0.83 Lo. In the rat SH muscle, the proximal segment tended to shorten on its ascending limb from 0.90 to 0.85 Lo while the distal segment tended to lengthen across Lo (0.96–1.12 Lo). In the rat MG muscle, in vivo strains of proximal fascicles ranged from 0.72 to 1.02 Lo, while the distal fascicles ranged from 0.88 to 1.11 Lo. Even though the timing of muscle activation patterns were similar between segments, the heterogeneous strain patterns of fascicle segments measured in vivo coincided with different operating ranges across their FLRs simultaneously, implying differences in force–velocity behavior as well. The three vertebrate skeletal muscles represent a diversity of fiber architectures and functions and suggest that patterns of in vivo contractile strain and the operating range over the FLR in one muscle region does not necessarily represent other regions within the same muscle.

Muscle function changes to meet the varying mechanical demands of locomotion across different gait and grade conditions. A muscle's work output is determined by time-varying patterns of neuromuscular activation, muscle force and muscle length change, but how these patterns change under different conditions in small animals is not well-defined. Here we report the first integrated in vivo force-length and activation patterns in rats, a commonly used small animal model, to evaluate the dynamics of two distal hindlimb muscles (medial gastrocnemius, MG and plantaris, PL) across a range of gait (walk, trot, and gallop) and grade (level versus incline) conditions. We use these data to explore how the pattern of force production, muscle activation and muscle length changes across conditions in a small quadrupedal mammal. As hypothesized, we found that the rat muscles show limited fascicle strains during active force generation in stance across gaits and grades, indicating that these distal rat muscles generate force economically but perform little work, similar to patterns observed in larger animals during level locomotion. Additionally, given differences in fiber type composition and variation in motor unit recruitment across the gait and grade conditions examined here for these muscles, the in vivo force-length behavior and neuromuscular activation data reported here can be used to validate improved two-element Hill-type muscle models.