Muscle function and hydrodynamics limit power and speed in swimming frogs

2017

Journal of Anatomy

The African clawed frog, Xenopus laevis, is one of the most widely used model organisms in biological research. However, the most recent anatomical description of X. laevis was produced nearly a century ago. Compared with other anurans, pipid frogs - including X. laevis - exhibit numerous unusual morphological features; thus, anatomical descriptions of more 'typical' frogs do not detail many aspects of X. laevis skeletal and soft-tissue morphology. The relatively new method of using iodine-based agents to stain soft tissues prior to high-resolution X-ray imaging has several advantages over gross dissection, such as enabling dissection of very small and fragile specimens, and preserving the three-dimensional topology of anatomical structures. Here, we use contrast-enhanced computed tomography to produce a high-resolution three-dimensional digital dissection of a post-metamorphic X. laevis to successfully visualize: skeletal and muscular anatomy; the nervous, respiratory, digestive, excretory and reproductive systems; and the major sense organs. Our digital dissection updates and supplements previous anatomical descriptions of this key model organism, and we present the three-dimensional data as interactive portable document format (PDF) files that are easily accessible and freely available for research and educational purposes. The data presented here hold enormous potential for applications beyond descriptive purposes, particularly for biological researchers using this taxon as a model organism, comparative anatomy and biomechanical modelling.

Section: Introductionmentioning

confidence: 99%

Digital dissection of the model organism Xenopus laevis using contrast‐enhanced computed tomography

Porro

2017

Journal of Anatomy

“…Finally, we address time-varying gearing. Although inlever (r) does not vary over the in vivo range of frog ankle joint motion [27,30,31], the outlever (R) may vary due to (i) the angle of the fluid reaction force vector changing with respect to the foot orientation [8] or (ii) as the foot's position relative to the ankle changes throughout a stroke. To address this, R can be estimated at various points in the foot stroke (see §2).…”

Section: 5mentioning

confidence: 99%

“…body mass; N ¼ 5). The PL inlever, r, value of 0.14 cm was obtained from the tendon travel technique [27]. To calculate R, the foot centroid was located from digital tracings of photographs of the feet (ImageJ, U.S. National Institutes of Health, Bethesda, MD, USA).…”

Section: Estimating In Vivo Gear Ratiosmentioning

confidence: 99%

Built for rowing: frog muscle is tuned to limb morphology to power swimming

Clemente

2013

J. R. Soc. Interface.

Self Cite

Rowing is demanding, in part, because drag on the oars increases as the square of their speed. Hence, as muscles shorten faster, their force capacity falls, whereas drag rises. How do frogs resolve this dilemma to swim rapidly? We predicted that shortening velocity cannot exceed a terminal velocity where muscle and fluid torques balance. This terminal velocity, which is below V max , depends on gear ratio (GR ¼ outlever/inlever) and webbed foot area. Perhaps such properties of swimmers are 'tuned', enabling shortening speeds of approximately 0.3V max for maximal power. Predictions were tested using a 'musculo-robotic' Xenopus laevis foot driven either by a living in vitro or computational in silico plantaris longus muscle. Experiments verified predictions. Our principle finding is that GR ranges from 11.5 to 20 near the predicted optimum for rowing (GR % 11). However, gearing influences muscle power more strongly than foot area. No single morphology is optimal for producing muscle power. Rather, the 'optimal' GR decreases with foot size, implying that rowing ability need not compromise jumping (and vice versa). Thus, despite our neglect of additional forces (e.g. added mass), our model predicts pairings of physiological and morphological properties to confer effective rowing. Beyond frogs, the model may apply across a range of size and complexity from aquatic insects to human-powered rowing.

“…These questions require modelling the physical forces resisting muscle contraction (Marsh, 1999). In some cases, simple modelling can demonstrate how 'environmental feedback' (Aerts and Nauwelaerts, 2009) can reduce the 'volume' of muscle performance space (Richards, 2011;Richards and Clemente, 2013;Clemente and Richards, 2013). In other cases, for example in swimming fish, sophisticated modelling is required to reveal how optimal muscle function is dependent upon the mechanical properties of the body, which governs fluid-structure interactions (Tytell et al, 2010).…”

Section: Resultsmentioning

confidence: 99%

In vitro-virtual-reality: an anatomically explicit musculoskeletal simulation powered by in vitro muscle using closed loop tissue-software interaction

Journal of Experimental Biology

Eberhard

2020

Muscle force-length dynamics are governed by intrinsic contractile properties, motor stimulation and mechanical load. Although intrinsic properties are well characterised, physiologists lack in vitro instrumentation to account for combined effects of limb inertia, musculoskeletal architecture and contractile dynamics. We introduce in vitro virtual reality (in vitro-VR) which enables in vitro muscle tissue to drive a musculoskeletal jumping simulation. In hardware, muscle force from a frog plantaris was transmitted to a software model where joint torques, inertia and ground reaction forces were computed to advance the simulation at 1 kHz. To close the loop, simulated muscle strain was returned to update in vitro length. We manipulated (1) stimulation timing and (2) the virtual muscle's anatomical origin. This influenced interactions among muscular, inertial, gravitational and contact forces dictating limb kinematics and jump performance. We propose that in vitro-VR can be used to illustrate how neuromuscular control and musculoskeletal anatomy influence muscle dynamics and biomechanical performance.