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How Animals Move: Comparative Lessons on Animal Locomotion

Paul J. Schaeffer, Stan L. Lindstedt

10.1002/cphy.c110059

Source: Volume 3, Issue 1, January 2013

Published online: January 2013

Full Article on Wiley Online Library



Abstract

Comparative physiology often provides unique insights in animal structure and function. It is specifically through this lens that we discuss the fundamental properties of skeletal muscle and animal locomotion, incorporating variation in body size and evolved difference among species. For example, muscle frequencies in vivo are highly constrained by body size, which apparently tunes muscle use to maximize recovery of elastic recoil potential energy. Secondary to this constraint, there is an expected linking of skeletal muscle structural and functional properties. Muscle is relatively simple structurally, but by changing proportions of the few muscle components, a diverse range of functional outputs is possible. Thus, there is a consistent and predictable relation between muscle function and myocyte composition that illuminates animal locomotion. When animals move, the mechanical properties of muscle diverge from the static textbook force‐velocity relations described by A. V. Hill, as recovery of elastic potential energy together with force and power enhancement with activation during stretch combine to modulate performance. These relations are best understood through the tool of work loops. Also, when animals move, locomotion is often conveniently categorized energetically. Burst locomotion is typified by high‐power outputs and short durations while sustained, cyclic, locomotion engages a smaller fraction of the muscle tissue, yielding lower force and power. However, closer examination reveals that rather than a dichotomy, energetics of locomotion is a continuum. There is a remarkably predictable relationship between duration of activity and peak sustainable performance. © 2013 American Physiological Society. Compr Physiol 3:289‐314, 2013.

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Figure 1. Figure 1.

The volume of a muscle fiber is composed of three (space occupying) structural components: myofibrils, mitochondria, and sarcoplasmic reticulum (SR). Because these structures collectively fill the fiber volume, on this three‐dimensional graph every muscle fiber must fall somewhere on a single plane. As the contractile proteins compose the myofibrils, any increase in mitochondria or SR (i.e., demand for sustained performance or high‐frequency muscle use) must be at the cost of reduced force (and power) production. The wide range of muscle functions, from posture to ballistic use to noise making are all possible not because of unique structures, but rather a rearrangement of these structural elements. We have included a selection of vertebrate muscle examples that occupy different regions of this three‐dimensional space; see text for discussion [modified, with permission, from reference (130)].
Figure 2. Figure 2.

For muscles to function at different operating frequencies calcium cycling kinetics must be tuned to frequency of muscle use. As a consequence, there is a consistent and predictable relationship between frequency of muscle use and the volume of the muscle fiber devoted to sarcoplasmic reticulum (SR). In this figure, when necessary we have normalized data to a muscle temperature of 40°C using the Q10 reported for these specific animals. Data are from human limb muscle (92), guinea pig limb muscle [(56,62); both mammals open triangles], hummingbird flight muscle [filled circle, (236)], cicada noisemaker muscle [open circle, (107)], and rattlesnake noisemaker muscle [filled triangle, (188)]. In contrast, asynchronous insect muscle achieves high frequencies with a low volume density of SR [square, (107)].
Figure 3. Figure 3.

Maximum ATP synthetic capacity (and thus oxygen uptake) in skeletal muscle is a direct function of mitochondrial capacity to process reducing equivalents. In mammals, this seems to be a simple function of muscle mitochondrial volume. With variation in cristae density across all taxa, oxygen uptake most closely correlates with the total quantity of inner mitochondrial membrane surface area. The maximum rate of oxygen uptake per unit of inner mitochondrial membrane area is nearly constant when all data are normalized to a common temperature of 40°C (using a Q10 of 2.2) in rattlesnakes (square) mammals (circles) and hummingbirds (triangle).
Figure 4. Figure 4.

Much of our knowledge of muscle mechanics is traceable to the pioneering experiments by A. V. Hill which form the basis of our understanding of how force, velocity, and power are related in skeletal muscle. In the Hill model, experiments were performed using an afterloaded isotonic contraction model in which maximally activated, isolated muscle contracted against a constant external load. Thus, contraction was isometric until sufficient force was developed, but isotonic thereafter. Using this approach, it can be observed that as the load is reduced, muscles contract at increasing velocity to generate a characteristic force‐velocity curve (panel A). The load and velocity of each point that generates this curve demonstrate how as load is reduced, the period during which an isometric contraction occurs is extended before movement begins and the rate of length change increases with reduced load (panel B). The characteristics of this relationship are unchanged when force and velocity are replaced with stress and strain rate (size‐independent measures of each variable; panel A). The product of force and velocity are power and the relationship between power and velocity reveals that muscle generates maximal power at about one third of maximal velocity (panel C). While muscles of identical cross‐sectional area generate nearly identical force, the rate at which those muscles develop force may greatly affect power generation. The isocline demonstrates the increase in maximal power resulting from increasing maximal contraction velocity (panel C). Panels A and B modified, with permission, from reference (33).
Figure 5. Figure 5.

Locomotor muscles are used cyclically. During steady‐state locomotion, each stride, wing‐beat, or tail‐beat re‐enacts a stereotyped series of muscle movements with nearly identical force production. Because the product of force and distance is work, the simultaneous tracing of muscle force and length changes during one muscle cycle results in the production of a work loop (107). The work loop reveals insights into in vivo muscle mechanics beyond those of traditional Hill mechanics. Likewise, we can also envision the trajectory of power generation in vivo, which also departs from a steady‐state Hill model. As power is the product of force and velocity, we can determine the power generated at any point during muscle activation. By following a single muscle cycle, it is possible to follow the trajectory of power production. (A, left) If a hypothetical work loop is created for an isolated contraction (as in Figure 4), it appears as a rectangle. Force must increase isometrically (i) until sufficient force is generated for the muscle to shorten isotonically (ii). When the muscle relaxes, force will fall, also isometrically (iii), until the muscle is returned (e.g., by an antagonist) to the starting position. The area of this rectangle is the work done by the muscle. (A, right) For the same contraction, the power generated by the muscle is depicted. A power trajectory for the same isolated contraction is overlaid on a Hill plot of force and velocity. Again, force must increase at zero velocity until the muscle shortens isotonically, generating power at a constant point on the force velocity curve. Finally, the muscle returns to the starting point of zero force and velocity when it relaxes. (B, left) This hypothetical work loop is modified when the contraction is repeated cyclically during locomotion. Any moving object (like an animal in motion) has kinetic energy. This energy can be captured as work done on the muscle to extend a muscle prior to shortening. Thus, while the muscle does the same (F‐D) work on the environment, part of this work is derived from recovered strain energy stored in the muscle. The work loop is thus modified as the lengthening phase of the work loop is accomplished by the conversion of kinetic energy to work done on the muscle, as labeled, which reduces the work done by the muscle. (B, right) Once again, we can view this contraction as a power trajectory on the force‐velocity plot. In this case, as the muscle is stretched (velocity is negative because it is in the opposite direction as the force produced) force increases until it reaches a magnitude sufficient for shortening to occur. From this point on, the power trajectory is similar to that seen above. (C, left) An in vivo work loop is indeed a loop that demonstrates characteristics not revealed in a force‐velocity depiction. First, muscle fibers that have been lengthened during activation generate enhanced force and thus work production. In addition, shortening is not isotonic, both force and velocity vary during shortening. (C, right panel) If we examine the power trajectory of this in vivo cyclic contraction, as force enhancement leads to increase in the work done by the muscle, the power produced during that part of the contraction similarly extends beyond the maximum power that a muscle can generate in an isolated (Hill) contraction.
Figure 6. Figure 6.

When animals run each stride represents an active and passive cycle of muscle lengthening and shortening. If we view one stride starting with foot‐fall (A), the extensor muscles (quadriceps) are initially short as the knee is extended. During running, the center of mass remains relatively constant, thus the knee is slightly bent when beneath the center of mass (B) and thus has been actively lengthened in this portion of the stride, reflected in the accompanying work loop. The extensors are actively shortened until the foot leaves the ground (C and D) completing the active phase of the work loop. The recovery phase when the foot is off the ground is characterized by little work done but relatively longer muscle excursions, the flat phase of the work loop (E).
Figure 7. Figure 7.

Maximum running speed in humans has been plotted using current world running records. (A) When these record times are plotted as a function of race duration, it seems to represent a dichotomous function; speed drops steeply over durations up to about 100 s and there is a nearly constant speed beyond that. (B) When the same data are plotted on logarithmic coordinates, different patterns emerge. First, because all races are from a standing start, the shortest duration events reflect this acceleration. Top speed is reached between 10 to 20 s. However, above 100 s, the relationship is linear (r2 = 0.98). The arrow on this graph depicts the predicted speed (6.4 m s−1) at a of 82 mL kg−1 min−1, corresponding to an elite runner.
Figure 8. Figure 8.

Mitochondria are localized in two compartments, subsarcolemmal and intermyofibrillar. It is commonly supposed that these compartments serve different functions, although these functions have not been identified. As smaller animals possess higher mass‐specific metabolic rates, they also possess higher overall volume densities of mitochondria. However, the proportion of those mitochondria located in the subsarcolemmal compartment remains nearly constant across a wide range of body sizes. All data [from rat (3200,220), guinea pig (56), rabbit (1076), cat (91), dog, goat, calf, and pony (901)] are from a variety of skeletal muscles, with variation in oxidative phenotype; however, when data from only the diaphragm are examined the outcome is nearly identical. Thus, increased metabolic demand is not met by increasing the proportion of mitochondria localized in the subsarcolemmal compartment.


Figure 1.

The volume of a muscle fiber is composed of three (space occupying) structural components: myofibrils, mitochondria, and sarcoplasmic reticulum (SR). Because these structures collectively fill the fiber volume, on this three‐dimensional graph every muscle fiber must fall somewhere on a single plane. As the contractile proteins compose the myofibrils, any increase in mitochondria or SR (i.e., demand for sustained performance or high‐frequency muscle use) must be at the cost of reduced force (and power) production. The wide range of muscle functions, from posture to ballistic use to noise making are all possible not because of unique structures, but rather a rearrangement of these structural elements. We have included a selection of vertebrate muscle examples that occupy different regions of this three‐dimensional space; see text for discussion [modified, with permission, from reference (130)].



Figure 2.

For muscles to function at different operating frequencies calcium cycling kinetics must be tuned to frequency of muscle use. As a consequence, there is a consistent and predictable relationship between frequency of muscle use and the volume of the muscle fiber devoted to sarcoplasmic reticulum (SR). In this figure, when necessary we have normalized data to a muscle temperature of 40°C using the Q10 reported for these specific animals. Data are from human limb muscle (92), guinea pig limb muscle [(56,62); both mammals open triangles], hummingbird flight muscle [filled circle, (236)], cicada noisemaker muscle [open circle, (107)], and rattlesnake noisemaker muscle [filled triangle, (188)]. In contrast, asynchronous insect muscle achieves high frequencies with a low volume density of SR [square, (107)].



Figure 3.

Maximum ATP synthetic capacity (and thus oxygen uptake) in skeletal muscle is a direct function of mitochondrial capacity to process reducing equivalents. In mammals, this seems to be a simple function of muscle mitochondrial volume. With variation in cristae density across all taxa, oxygen uptake most closely correlates with the total quantity of inner mitochondrial membrane surface area. The maximum rate of oxygen uptake per unit of inner mitochondrial membrane area is nearly constant when all data are normalized to a common temperature of 40°C (using a Q10 of 2.2) in rattlesnakes (square) mammals (circles) and hummingbirds (triangle).



Figure 4.

Much of our knowledge of muscle mechanics is traceable to the pioneering experiments by A. V. Hill which form the basis of our understanding of how force, velocity, and power are related in skeletal muscle. In the Hill model, experiments were performed using an afterloaded isotonic contraction model in which maximally activated, isolated muscle contracted against a constant external load. Thus, contraction was isometric until sufficient force was developed, but isotonic thereafter. Using this approach, it can be observed that as the load is reduced, muscles contract at increasing velocity to generate a characteristic force‐velocity curve (panel A). The load and velocity of each point that generates this curve demonstrate how as load is reduced, the period during which an isometric contraction occurs is extended before movement begins and the rate of length change increases with reduced load (panel B). The characteristics of this relationship are unchanged when force and velocity are replaced with stress and strain rate (size‐independent measures of each variable; panel A). The product of force and velocity are power and the relationship between power and velocity reveals that muscle generates maximal power at about one third of maximal velocity (panel C). While muscles of identical cross‐sectional area generate nearly identical force, the rate at which those muscles develop force may greatly affect power generation. The isocline demonstrates the increase in maximal power resulting from increasing maximal contraction velocity (panel C). Panels A and B modified, with permission, from reference (33).



Figure 5.

Locomotor muscles are used cyclically. During steady‐state locomotion, each stride, wing‐beat, or tail‐beat re‐enacts a stereotyped series of muscle movements with nearly identical force production. Because the product of force and distance is work, the simultaneous tracing of muscle force and length changes during one muscle cycle results in the production of a work loop (107). The work loop reveals insights into in vivo muscle mechanics beyond those of traditional Hill mechanics. Likewise, we can also envision the trajectory of power generation in vivo, which also departs from a steady‐state Hill model. As power is the product of force and velocity, we can determine the power generated at any point during muscle activation. By following a single muscle cycle, it is possible to follow the trajectory of power production. (A, left) If a hypothetical work loop is created for an isolated contraction (as in Figure 4), it appears as a rectangle. Force must increase isometrically (i) until sufficient force is generated for the muscle to shorten isotonically (ii). When the muscle relaxes, force will fall, also isometrically (iii), until the muscle is returned (e.g., by an antagonist) to the starting position. The area of this rectangle is the work done by the muscle. (A, right) For the same contraction, the power generated by the muscle is depicted. A power trajectory for the same isolated contraction is overlaid on a Hill plot of force and velocity. Again, force must increase at zero velocity until the muscle shortens isotonically, generating power at a constant point on the force velocity curve. Finally, the muscle returns to the starting point of zero force and velocity when it relaxes. (B, left) This hypothetical work loop is modified when the contraction is repeated cyclically during locomotion. Any moving object (like an animal in motion) has kinetic energy. This energy can be captured as work done on the muscle to extend a muscle prior to shortening. Thus, while the muscle does the same (F‐D) work on the environment, part of this work is derived from recovered strain energy stored in the muscle. The work loop is thus modified as the lengthening phase of the work loop is accomplished by the conversion of kinetic energy to work done on the muscle, as labeled, which reduces the work done by the muscle. (B, right) Once again, we can view this contraction as a power trajectory on the force‐velocity plot. In this case, as the muscle is stretched (velocity is negative because it is in the opposite direction as the force produced) force increases until it reaches a magnitude sufficient for shortening to occur. From this point on, the power trajectory is similar to that seen above. (C, left) An in vivo work loop is indeed a loop that demonstrates characteristics not revealed in a force‐velocity depiction. First, muscle fibers that have been lengthened during activation generate enhanced force and thus work production. In addition, shortening is not isotonic, both force and velocity vary during shortening. (C, right panel) If we examine the power trajectory of this in vivo cyclic contraction, as force enhancement leads to increase in the work done by the muscle, the power produced during that part of the contraction similarly extends beyond the maximum power that a muscle can generate in an isolated (Hill) contraction.



Figure 6.

When animals run each stride represents an active and passive cycle of muscle lengthening and shortening. If we view one stride starting with foot‐fall (A), the extensor muscles (quadriceps) are initially short as the knee is extended. During running, the center of mass remains relatively constant, thus the knee is slightly bent when beneath the center of mass (B) and thus has been actively lengthened in this portion of the stride, reflected in the accompanying work loop. The extensors are actively shortened until the foot leaves the ground (C and D) completing the active phase of the work loop. The recovery phase when the foot is off the ground is characterized by little work done but relatively longer muscle excursions, the flat phase of the work loop (E).



Figure 7.

Maximum running speed in humans has been plotted using current world running records. (A) When these record times are plotted as a function of race duration, it seems to represent a dichotomous function; speed drops steeply over durations up to about 100 s and there is a nearly constant speed beyond that. (B) When the same data are plotted on logarithmic coordinates, different patterns emerge. First, because all races are from a standing start, the shortest duration events reflect this acceleration. Top speed is reached between 10 to 20 s. However, above 100 s, the relationship is linear (r2 = 0.98). The arrow on this graph depicts the predicted speed (6.4 m s−1) at a of 82 mL kg−1 min−1, corresponding to an elite runner.



Figure 8.

Mitochondria are localized in two compartments, subsarcolemmal and intermyofibrillar. It is commonly supposed that these compartments serve different functions, although these functions have not been identified. As smaller animals possess higher mass‐specific metabolic rates, they also possess higher overall volume densities of mitochondria. However, the proportion of those mitochondria located in the subsarcolemmal compartment remains nearly constant across a wide range of body sizes. All data [from rat (3200,220), guinea pig (56), rabbit (1076), cat (91), dog, goat, calf, and pony (901)] are from a variety of skeletal muscles, with variation in oxidative phenotype; however, when data from only the diaphragm are examined the outcome is nearly identical. Thus, increased metabolic demand is not met by increasing the proportion of mitochondria localized in the subsarcolemmal compartment.

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Article Title: How Animals Move: Comparative Lessons on Animal Locomotion
 

How to Cite

Paul J. Schaeffer, Stan L. Lindstedt. How Animals Move: Comparative Lessons on Animal Locomotion. Compr Physiol 2013, 3: 289-314. doi: 10.1002/cphy.c110059