Linking in vivo muscle dynamics to force-length and force-velocity properties reveals that guinea fowl lateral gastrocnemius operates at shorter than optimal lengths.

The isometric force-length (F-L) and isotonic force-velocity (F-V) relationships characterize the contractile properties of skeletal muscle under controlled conditions, yet it remains unclear how these properties relate to in vivo muscle function. Here, we map the in situ F-L and F-V characteristics of guinea fowl (Numida meleagris) lateral gastrocnemius (LG) to the in vivo operating range during walking and running. We test the hypothesis that muscle fascicles operate on the F-L plateau, near the optimal length for force (L0) and near velocities that maximize power output (Vopt) during walking and running.

Viscoelastic materials are most energy efficient when loaded and unloaded at equal rates.

Biological springs can be used in nature for energy conservation and ultra-fast motion. The loading and unloading rates of elastic materials can play an important role in determining how the properties of these springs affect movements. We investigate the mechanical energy efficiency of biological springs (American bullfrog plantaris tendons and guinea fowl lateral gastrocnemius tendons) and synthetic elastomers.

Architectural gear ratio depends on actuator spacing in a physical model of pennate muscle.

Pennate muscles are defined by the architectural arrangement of their muscle fibers, which run at an angle to the primary axis of muscle shortening. Pennation angles can vary dynamically over the course of individual contractions, influencing the speed and distance of muscle shortening. Despite their relevance to muscle performance, the physical mechanisms that drive dynamic changes in pennation angle remain poorly understood.

Modulation of limb mechanics in alligators moving across varying grades.

Graded substrates require legged animals to modulate their limb mechanics to meet locomotor demands. Previous work has elucidated strategies used by cursorial animals with upright limb posture, but it remains unclear how sprawling species such as alligators transition between grades. We measured individual limb forces and 3D kinematics as alligators walked steadily across level, 15 deg incline and 15 deg decline conditions.

The effects of temperature on elastic energy storage and release in a system with a dynamic mechanical advantage latch.

Changes in temperature alter muscle kinetics and in turn affect whole-organism performance. Some organisms use the elastic recoil of biological springs, structures which are far less temperature sensitive, to power thermally robust movements. For jumping frogs, the use of elastic energy in tendons is facilitated through a geometric latching mechanism that operates through dynamic changes in the mechanical advantage (MA) of the hindlimb.

Adapting small jumping robots to compliant environments.

Jumping animals launch themselves from surfaces that vary widely in compliance from grasses and shrubs to tree branches. However, studies of robotic jumpers have been largely limited to those jumping from rigid substrates. In this paper, we leverage recent work describing how latches in jumping systems can mediate the transition from stored potential energy to kinetic energy.

Hindlimb muscle spindles inform preparatory forelimb coordination prior to landing in toads.

Animals move across a wide range of surface conditions in real-world environments to acquire resources and avoid predation. To effectively navigate a variety of surfaces, animals rely on several mechanisms including intrinsic mechanical responses, spinal-level central pattern generators, and neural commands that require sensory feedback. Muscle spindle Ia afferents play a critical role in providing sensory feedback and informing motor control strategies across legged vertebrate locomotion, which is apparent in cases where this sensory input is compromised.

Tuned muscle and spring properties increase elastic energy storage.

Elastic recoil drives some of the fastest and most powerful biological movements. For effective use of elastic recoil, the tuning of muscle and spring force capacity is essential. Although studies of invertebrate organisms that use elastic recoil show evidence of increased force capacity in their energy loading muscle, changes in the fundamental properties of such muscles have yet to be documented in vertebrates.

Fatigue resistant jaw muscles facilitate long-lasting courtship behaviour in the southern alligator lizard ().

The southern alligator lizard () exhibits a courtship behaviour during which the male firmly grips the female's head in his jaws for many hours at a time. This extreme behaviour counters the conventional wisdom that reptilian muscle is incapable of powering high-endurance behaviours. We conducted experiments in which the jaw-adductor muscles of lizards were stimulated directly while bite force was measured simultaneously.

The Multi-Scale, Three-Dimensional Nature of Skeletal Muscle Contraction.

Muscle contraction is a three-dimensional process, as anyone who has observed a bulging muscle knows. Recent studies suggest that the three-dimensional nature of muscle contraction influences its mechanical output. Shape changes and radial forces appear to be important across scales of organization.

The high speed radular prey strike of a fish-hunting cone snail.

Cone snails are venomous marine gastropods that hydraulically propel a hollow, chitinous radular harpoon into prey [1,2]. This radular harpoon serves both as projectile and conduit for venom delivery. In the fish-hunting cone snail Conus catus, the radular harpoon is also utilized to tether the snail to its prey, rapidly paralyzed by neuroexcitatory peptides [2,3].

Why do Large Animals Never Actuate Their Jumps with Latch-Mediated Springs? Because They can Jump Higher Without Them.

As animals get smaller, their ability to generate usable work from muscle contraction is decreased by the muscle's force-velocity properties, thereby reducing their effective jump height. Very small animals use a spring-actuated system, which prevents velocity effects from reducing available energy. Since force-velocity properties reduce the usable work in even larger animals, why don't larger animals use spring-actuated jumping systems as well? We will show that muscle length-tension properties limit spring-actuated systems to generating a maximum one-third of the possible work that a muscle could produce-greatly restricting the jumping height of spring-actuated jumpers.

Modeling the Determinants of Mechanical Advantage During Jumping: Consequences for Spring- and Muscle-Driven Movement.

Systems powered by elastic recoil need a latch to prevent motion while a spring is loaded but allow motion during spring recoil. Some jumping animals that rely on elastic recoil use the increasing mechanical advantage of limb extensor muscles to accomplish latching. We examined the ways in which limb morphology affects latching and the resulting performance of an elastic-recoil mechanism.

Compliant Substrates Disrupt Elastic Energy Storage in Jumping Tree Frogs.

Arboreal frogs navigate complex environments and face diverse mechanical properties within their physical environment. Such frogs may encounter substrates that are damped and absorb energy or are elastic and can store and release energy as the animal pushes off during take-off. When dealing with a compliant substrate, a well-coordinated jump would allow for the recovery of elastic energy stored in the substrate to amplify mechanical power, effectively adding an in-series spring to the hindlimbs.

Structural Determinants of Muscle Gearing During Dynamic Contractions.

In skeletal muscle, interactions between contractile and connective tissue elements at multiple scales result in emergent properties that determine mechanical performance. One of these phenomena is architectural gearing, which is quantified as the ratio of muscle velocity to muscle fiber velocity. Many pennate muscles operate with a gear ratio greater than one because muscles shorten through a combination of muscle fiber shortening and fiber rotation.

Morphological and kinematic specializations of walking frogs.

The anuran body plan is defined by morphological features associated with saltatory locomotion, but these specializations may have functional consequences for other modes of locomotion. Several frog species use a quadrupedal walking gait as their primary mode of locomotion, characterized by limbs that move in diagonal pairs. Here, we examine how walking species may deviate from the ancestral body plan and how the kinematics of a quadrupedal gait are modified to accommodate the anuran body plan.

The principles of cascading power limits in small, fast biological and engineered systems.

Mechanical power limitations emerge from the physical trade-off between force and velocity. Many biological systems incorporate power-enhancing mechanisms enabling extraordinary accelerations at small sizes. We establish how power enhancement emerges through the dynamic coupling of motors, springs, and latches and reveal how each displays its own force-velocity behavior.

Lowering metabolic rate mitigates muscle atrophy in western fence lizards.

Extended periods of skeletal muscle disuse can cause a significant loss of contractile proteins, which compromises the ability to generate force, mechanical work or power, thus compromising locomotor performance. Several hibernating organisms can resist muscle atrophy despite months of inactivity. This resistance has been attributed to a reduction in body temperature and metabolic rate and activation of physiological pathways that counteract pathways of protein degradation.

Modeling age-related changes in muscle-tendon dynamics during cyclical contractions in the rat gastrocnemius.

Efficient muscle-tendon performance during cyclical tasks is dependent on both active and passive mechanical tissue properties. Here we examine whether age-related changes in the properties of muscle-tendon units (MTUs) compromise their ability to do work and utilize elastic energy storage. We empirically quantified passive and active properties of the medial gastrocnemius muscle and material properties of the Achilles tendon in young (∼6 mo) and old (∼32 mo) rats.

Determinants of aponeurosis shape change during muscle contraction.

Aponeuroses are sheet-like elastic tendon structures that cover a portion of the muscle belly and act as insertion sites for muscle fibers while free tendons connect muscles to bones. During shortening contractions, free tendons are loaded in tension and lengthen due to the force acting longitudinally along the muscle׳s line of action. In contrast, aponeuroses increase in length and width, suggesting that aponeuroses are loaded in directions along and orthogonal to the muscle׳s line of action.

Stuck in gear: age-related loss of variable gearing in skeletal muscle.

Skeletal muscles power a broad diversity of animal movements, despite only being able to produce high forces over a limited range of velocities. Pennate muscles use a range of gear ratios, the ratio of muscle shortening velocity to fiber shortening velocity, to partially circumvent these force-velocity constraints. Muscles operate with a high gear ratio at low forces; fibers rotate to greater angles of pennation, enhancing velocity but compromising force.

Timing matters: tuning the mechanics of a muscle-tendon unit by adjusting stimulation phase during cyclic contractions.

A growing body of research on the mechanics and energetics of terrestrial locomotion has demonstrated that elastic elements acting in series with contracting muscle are critical components of sustained, stable and efficient gait. Far fewer studies have examined how the nervous system modulates muscle-tendon interaction dynamics to optimize 'tuning' or meet varying locomotor demands. To explore the fundamental neuromechanical rules that govern the interactions between series elastic elements (SEEs) and contractile elements (CEs) within a compliant muscle-tendon unit (MTU), we used a novel work loop approach that included implanted sonomicrometry crystals along muscle fascicles.

Passive stiffness of hindlimb muscles in anurans with distinct locomotor specializations.

Anurans (frogs and toads) have been shown to have relatively compliant skeletal muscles. Using a meta-analysis of published data we have found that muscle stiffness is negatively correlated with joint range of motion when examined across mammalian, anuran and bird species. Given this trend across a broad phylogenetic sample, we examined whether the relationship held true within anurans.