Transfer of mechanical energy between ankle and knee joints by gastrocnemius and plantaris muscles during cat locomotion

2005

SUMMARY Measurements of joint work and power were determined using inverse dynamics analysis based on ground reaction force and high-speed video recordings of tammar wallabies as they decelerated and accelerated while hopping over a force platform on level ground. Measurements were obtained over a range of accelerations ranging from -6 m s-2 to 8 m s-2. The goal of our study was to determine which joints are used to modulate mechanical power when tammar wallabies change speed. From these measurements, we also sought to determine which hind limb muscle groups are the most important for producing changes in mechanical work. Because our previous in vivoanalyses of wallaby distal muscle function indicated that these muscle-tendon units favor elastic energy savings and perform little work during steady level and incline hopping, we hypothesized that proximal muscle groups operating at the hip and knee joint are most important for the modulation of mechanical work and power. Of the four hind limb joints examined, the ankle joint had the greatest influence on the total limb work, accounting for 89% of the variation observed with changing speed. The hip and metatarsophalageal (MP) joints also contributed to modulating whole limb work, but to a lesser degree than the ankle, accounting for 28% (energy production) and -24% (energy absorption) of the change in whole limb work versus acceleration, respectively. In contrast, the work produced at the knee joint was independent of acceleration. Based on the results of our previous in vivo studies and given that the magnitude of power produced at the ankle exceeds that which these muscles alone could produce, we conclude that the majority of power produced at the ankle joint is likely transferred from the hip and knee joints viaproximal bi-articular muscles, operating in tandem with bi-articular ankle extensors, to power changes in hopping speed of tammar wallabies. Additionally, over the observed range of performance, peak joint moments at the ankle (and resulting tendon strains) did not increase significantly with acceleration, indicating that having thin tendons favoring elastic energy storage does not necessarily limit a tammar wallaby's ability to accelerate or decelerate.

Section: Discussionmentioning

confidence: 99%

Joint work and power associated with acceleration and deceleration in tammar wallabies (Macropus eugenii)

McGowan

Baudinette

2005

“…Similar patterns are also observed in the dog forelimb biarticular Tr LONG , which shortens when active early in stance during level trotting (−15.0%) and galloping (−16.3%; Gregersen et al, 1998). Thus, counter to biomechanical analyses of humans (Lichtwark and Wilson, 2006;Prilutsky and Zatsiorsky, 1994;van Ingen Schenau, 1990) and in vivo measurements of cat (Prilutsky et al, 1996), turkey, wallaby, and goat distal hind limb muscles (discussed above), indicating that biarticular muscles primarily transfer energy between adjacent joints rather than performing net work, the fascicle strain and activation patterns of goat and dog Tr LONG indicate that this forelimb biarticular muscle contributes significant positive work during level locomotion. In contrast, the mono-articular goat Tr LAT likely absorbs and then produces energy during stance.…”

Section: Introductionmentioning

confidence: 86%

Locomotion as an emergent property of muscle contractile dynamics

2016

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 forcevelocity 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.

“…Most of the distal limb muscles are multiarticular; thus, the high sensitivity of distal joint mechanics to limb posture supports this idea (Daley et al, 2007). Multiarticular muscles also transfer energy between joints (Bobbert et al, 1986;Prilutsky et al, 1996;McGowan et al, 2007).…”

Section: Regional Patterns Of Muscle Work In Relation To Joint Workmentioning

confidence: 95%

“…Transfer of energy via biarticular muscles has been demonstrated during jumping or sprinting actions (Bobbert et al, 1986;van Ingen Schenau et al, 1994;Jacobs et al, 1996). However, it also occurs during steady locomotion in cats (Prilutsky et al, 1996) and wallabies (McGowan et al, 2007), and likely other animals. In cats and wallabies considerable net work appears at the ankle joint during .…”

Section: Regional Patterns Of Muscle Work In Relation To Joint Workmentioning

confidence: 99%

“…Conversely, body, limb and joint dynamics alone cannot predict or explain the mechanical role played by individual muscles. This is because multiple muscles often operate agonistically at a joint and biarticular muscles may transfer energy between joints, so that mechanical work performed by muscles at one joint appears as energy at a different joint (Bobbert et al, 1986;Prilutsky et al, 1996). Muscle-tendon architecture and choice of synergist muscle activation for a task can dramatically influence how an animal's neuro-musculoskeletal system responds to perturbations (e.g.…”

Section: Introductionmentioning

confidence: 99%

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Unsteady locomotion: integrating muscle function with whole body dynamics and neuromuscular control

Daley

2007

138

143

SUMMARY By integrating studies of muscle function with analysis of whole body and limb dynamics, broader appreciation of neuromuscular function can be achieved. Ultimately, such studies need to address non-steady locomotor behaviors relevant to animals in their natural environments. When animals move slowly they likely rely on voluntary coordination of movement involving higher brain centers. However, when moving fast, their movements depend more strongly on responses controlled at more local levels. Our focus here is on control of fast-running locomotion. A key observation emerging from studies of steady level locomotion is that simple spring-mass dynamics, which help to economize energy expenditure, also apply to stabilization of unsteady running. Spring-mass dynamics apply to conditions that involve lateral impulsive perturbations, sudden changes in terrain height, and sudden changes in substrate stiffness or damping. Experimental investigation of unsteady locomotion is challenging, however, due to the variability inherent in such behaviors. Another emerging principle is that initial conditions associated with postural changes following a perturbation define different context-dependent stabilization responses. Distinct stabilization modes following a perturbation likely result from proximo-distal differences in limb muscle architecture, function and control strategy. Proximal muscles may be less sensitive to sudden perturbations and appear to operate, in such circumstances, under feed-forward control. In contrast, multiarticular distal muscles operate, via their tendons, to distribute energy among limb joints in a manner that also depends on the initial conditions of limb contact with the ground. Intrinsic properties of these distal muscle–tendon elements, in combination with limb and body dynamics, appear to provide rapid initial stabilizing mechanisms that are often consistent with spring-mass dynamics. These intrinsic mechanisms likely help to simplify the neural control task, in addition to compensating for delays inherent to subsequent force- and length-dependent neural feedback. Future work will benefit from integrative biomechanical approaches that employ a combination of modeling and experimental techniques to understand how the elegant interplay of intrinsic muscle properties, body dynamics and neural control allows animals to achieve stability and agility over a variety of conditions.