Active lengthening occurs on the ascending limb of the length–tension curve

Routine active lengthening of muscle can potentially damage muscle fibers, and damage is hypothesized to be more likely when active lengthening occurs on the unstable descending limb of the length–tension curve (Proske and Morgan, 2001). Muscles subjected to repeated bouts of active stretch have been shown to add sarcomeres in series, presumably to prevent the fibers from lengthening beyond the plateau of the length–tension curve (Lynn and Morgan, 1994; Lynn et al., 1998; Koh and Herzog, 1998; Butterfield et al., 2005). Consistent with the hypothesis that muscles adjust the number of sarcomeres to avoid lengthening on the descending limb, the maximal length of the ILPO was on the ascending limb of the predicted length–tension curve except when the birds ran up the highest slope (20%) when the maximal length was on the plateau (Fig. 5).

When running uphill, the ILPO increases active shortening and operates at longer lengths

Unlike most major knee extensors in mammals, the biarticular ILPO is also a hip extensor. The ILPO can, therefore, do positive work during both knee and hip extension. However, we predict that the majority of positive work is done at the hip because angular extension is greater at the hip than the knee, and the posterior part of the ILPO, which contains the bulk of the muscle volume, has a larger moment arm at the hip than at the knee (Carr et al., 2011b). Based on what is known about the maximum shortening velocity (V_max) of muscles in turkeys (Nelson et al., 2004) and considering the size difference between the species, the V_max of the ILPO is estimated to be 15 L₀ s^–1. During level and uphill running the ILPO actively shortened by 10–22% while shortening at 1–2 L₀ s^–1, which should allow the active fibers to produce a substantial amount of work.

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Fig. 5.

Estimated mean sarcomere lengths of the ILPO during treadmill exercise at different speeds and slopes. The values at the start of active lengthening varied with slope but not with speed, and thus the mean values across all speeds are plotted as single upward-directed triangles. The mean maximum sarcomere lengths (the values at the end of lengthening and start of shortening) are indicated by closed circles, and values at the end of active shortening by inverted triangles. Treadmill slope is indicated by color: level, black; 10% incline, blue; 15% incline, green; 20% incline, red. Some values are offset on the speed axis for clarity. Error bars indicate ±1 s.e.m. Shaded areas indicate the calculated plateau and ascending limb of guinea fowl ILPO length–tension curve, based on filament lengths.

Roberts et al. found that the turkey ILPO shifted function with changing slope (Roberts et al., 2007). They noted increased lengthening and decreased shortening during downhill running and decreased lengthening and increased shortening when running uphill. They hypothesized that work absorption by the muscle (negative work) predominated when the birds ran downhill and positive work output predominated during uphill running. We did not examine running on a downhill slope, but did demonstrate a decrease in active lengthening and an increase in active shortening when the birds ran uphill (Fig. 3). The shift from negative to positive strain will tend to favor work output when running uphill. However, the net work output of the ILPO will also be influenced by other features of the strain trajectory. A second factor tending to increase work is a shift to longer sarcomere lengths (Fig. 5), placing a portion of the shortening on the plateau of the length–tension curve. However, the increase in positive strain during uphill running is accompanied by an increase in shortening velocity (Fig. 4), which would be predicted to decrease force and thus work. Of course, the net work will also be influenced by altered recruitment, and average EMG per burst and average EMG amplitude increased as incline increased (Fig. 7). On balance it seems probable that positive work per stride increases above the value in level running when the birds run uphill. This conclusion is consistent with the substantial increase in energy use by the ILPO during uphill running (Rubenson et al., 2006).

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Fig. 6.

The period of electromyographic (EMG) activity in the ILPO at different speeds and slopes. Zero time indicates foot-down. The mean start and stop times for the EMG burst are connected with a thick bar, with thin error bars at the ends indicating ±1 s.e.m. Values are grouped by speed on the vertical axis with the slope indicated by color (0%, black; 10%, blue; 15%, green, 20%, red). The thin bars on the right indicate the mean stance times ± 1 s.e.m.

The relationship of energy use to EMG activity changes with mechanical function

EMG amplitude has been used for many years (Inman et al., 1952; Bigland and Lippold, 1954) as the most common in vivo measure of the relative volume of muscle recruited. Thus, intense interest over the years has focused on whether EMG amplitude correlates with muscle force, mechanical power output and metabolic rate (Bigland-Ritchie and Woods, 1976; De Luca, 1997; Kooistra et al., 2006; Disselhorst-Klug et al., 2009). Studies with isolated muscle (Woledge et al., 1985; DeHaan et al., 1989; Beltman et al., 2004; Trinh and Syme, 2007) and in vivo studies (Bigland and Lippold, 1954; Bigland-Ritchie and Woods, 1976; Aura and Komi, 1986; Takarada et al., 1997) predict that the relationship between active fiber volume, as estimated by EMG intensity, and all these variables will vary with the mechanical state of the muscle, including fiber length and shortening velocity. However, in vivo data for individual muscles are limited, particularly with regard to metabolic rate.

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Fig. 7.

Mean values for average EMG per burst (A) and average EMG values per stride (B) in the ILPO on the level (black), 10% incline (blue), 15% incline (green) and 20% incline (red) as a function of speed. Values are offset on the speed axis for clarity. Error bars indicate ±1 s.e.m.

Estimates of energy use based on blood flow for all of the individual muscles in the guinea fowl hindlimb (Marsh et al., 2004; Ellerby et al., 2005; Ellerby and Marsh, 2006; Rubenson et al., 2006) allows us to compare variation in EMG intensity of the ILPO (McGowan et al., 2006) (this study) with the variation in the metabolic rate of this muscle under conditions of varying speed, slope and trunk loading. Because of the tight coupling of increases in blood flow and increases in oxygen consumption in vertebrate skeletal muscle, blood flow can be used as a quantitative measure of metabolic rate (Marsh and Ellerby, 2006). As a measure of EMG intensity, we have used averaged filtered and rectified EMG signals and for metabolic rate we have used the increases in blood flow above the blood flow at rest. To compare EMG intensity with metabolic rate we have recalculated both the EMG values and the increases in muscle blood flow relative to the values obtained in the birds running on the level at 1.5 m s^–1 (see Materials and methods).

Our data, collected during level running, indicate that although measures of EMG intensity are correlated with energy use by the ILPO the quantitative changes in EMG intensity and metabolic rate sometimes differ widely, probably because of differences in mechanical function, and perhaps other factors (Fig. 8). The metabolic rate of the ILPO estimated from blood flow increases dramatically when the birds switch from walking to running and increases further with increasing speed during level running. When the birds walked at 0.5 m s^–1, the metabolic rate of the ILPO was only 4% of the value found during running at 1.5 m s^–1. When the birds increased speed from 1.5 to over 2.4 m s^–1, the metabolic rate increased by 75%. The average EMG intensity per stride also changed substantially with running speed, but the changes were much smaller than the changes in metabolic rate. At 0.5 m s^–1 the average EMG was ∼60% of the value at 1.5 m s^–1, and when running speed was increased to 2.78 m s^–1 the average EMG per stride increased by only 20% over the value at 1.5 m s^–1. The change in the relationship of EMG intensity to muscle metabolic rate with running speed corresponds to major changes in mechanical function with speed and gait. During walking at 0.5 m s^–1 the ILPO lengthens and shortens very slowly while active, only changing length by a few percent (Fig. 3) (also McGowan et al., 2006). Both active lengthening and active shortening velocity and strain increase substantially when the birds switch to a running gait and increase further with increasing running speed (Figs 3 and 4) (McGowan et al., 2006). Isolated muscle and in vivo studies predict that for the same level of activation, metabolic rate will be substantially higher during active shortening than during active lengthening or isometric contractions (Aura and Komi, 1986; Beltman et al., 2004; Bigland-Ritchie and Woods, 1976; Woledge et al., 1985). Nevertheless, the magnitude of the differences between recruitment measured by EMG and muscle metabolic rate are very large, particularly when comparing the EMG intensity found during walking and with that obtained during running at 1.5 m s^–1. Other factors can alter the relationship of EMG intensity to the recruited volume, including the fiber type and motor unit synchrony (Milner-Brown and Stein, 1975; De Luca, 1997; Farina et al., 2004).

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Fig. 8.

Relative changes in blood flow (red) and average EMG amplitude (green) in the ILPO under various exercise conditions. Values are expressed relative to the values measured during level, unloaded running at 1.5 m s^–1. Error bars indicate ±1 s.e.m.

The lack of quantitative correspondence between muscle recruitment measured by EMG intensity and muscle metabolic rate is also evident during uphill running. When the birds ran up a 15% grade at 1.5 m s^–1, the average rectified EMG increased by ∼20% over the value for level running at the same speed, whereas the metabolic rate of the ILPO doubled between level and uphill running on a 15% grade (Fig. 8). For uphill running, two mechanical changes probably contribute to this difference in relative values. First, the ILPO shortens farther and faster during uphill compared with level running. Second, less time is spent in active lengthening, and, therefore, more of the EMG burst serves to activate the muscle during the more costly shortening phase of activity.

Data from guinea fowl carrying trunk loads are also consistent with the hypothesis that the changes in EMG intensity and metabolic rate in the ILPO are quantitatively more similar if similar mechanical conditions are maintained when metabolic effort changes. McGowan et al. measured average EMG intensity in the guinea fowl ILPO during unloaded level running and when birds carried a trunk load of 22% of their body mass (McGowan et al., 2006). This protocol matched that used by Ellerby et al. who measured blood flow under the same conditions. In this case muscle metabolic rate, as indicated by blood flow, increased by 35% in loaded running, whereas average EMG intensity per burst increased by 22% (Ellerby and Marsh, 2006). Given the measurement errors reported in both studies the 13% difference between the relative increase in EMG intensity and the relative increase in metabolic rate is not statistically significant. Correspondingly, the mechanical conditions for the active ILPO, as indicated by the shortening velocity and strain, are similar in loaded and unloaded running (McGowan et al., 2006).

Function of the active lengthening–shortening cycle in the ILPO

The active lengthening during knee flexion in early stance may be functionally similar to that seen in the single joint vastus lateralis of quadrupedal mammals and the femerotibialis of birds (Gillis and Biewener, 2001; Gillis et al., 2005; Hoyt et al., 2005; Roberts et al., 2007). Active lengthening of fascicles in the knee extensors of humans may also occur during stance knee flexion (Cutts, 1989), but in vivo data on this point are lacking. All these knee extensors co-contract with knee flexors during early stance (Ford et al., 2008; Gatesy, 1999; Gillis and Biewener, 2001; Gillis et al., 2005; Mann and Hagy, 1980; Osternig et al., 1995).

Minimizing energy use has usually been considered an important selective force in the evolution of walking and running. In this regard, substantial lengthening of the fascicles in large muscles during level legged locomotion, as occurs in the ILPO and other knee extensors during running, presents a puzzle. McGowan et al. and Roberts et al. suggested that active lengthening of the ILPO in running birds could function to improve the economy of force production and possibly the efficiency of subsequent work production (McGowan et al., 2006; Roberts et al., 2007). However, if the muscle fibers in the ILPO absorb work during early stance knee flexion this mechanical energy will have to be subsequently restored by active muscle shortening leading to an increase in energy cost. When a muscle–tendon unit is stretched, lengthening can occur in the tendon and/or the active muscle fibers. Tendon stretch and elastic recoil can save energy during legged locomotion by decreasing the positive work done by the muscle fibers during a stride (Roberts et al., 1997). However, stretch of the muscle fibers beyond their short-range stiffness results in mechanical energy loss. Small stretches during activation may increase net work output during subsequent shortening (Josephson, 1993), but during longer stretches mechanical energy is lost because muscle force is enhanced during stretch and decreases during shortening (Chapman et al., 1985; Ettema et al., 1990; Ettema, 1996; Takarada et al., 1997).

If the volume of actively stretched muscle is large, supplying the mechanical work to lengthen the active fibers could have a substantial metabolic cost and decrease the economy of locomotion. Although the metabolic rate of the active muscle during stretch is expected to be relatively low (Bigland-Ritchie and Woods, 1976), costly positive muscle work will have to be done to restore the mechanical energy balance during the stride. Positive muscular work will be required either to directly supply the mechanical work during the stretch, or to replace the mechanical work supplied from another source. For example, if work was supplied in early stance from the kinetic energy of the body, this energy would have to be replaced by positive work later in the stride. In the case of the ILPO, fiber lengthening is caused by active knee flexion. During this part of the stride, inverse dynamics calculations in quail (Clark and Alexander, 1975), turkeys (Roberts, 2001) and guinea fowl (R.L.M., unpublished data) indicate that net positive work is required to produce knee flexion. The work to stretch active knee extensors will add to this externally calculated work and thus must be provided directly by the knee flexors, increasing their energy use. The hypothesis that co-contraction increases metabolic cost is supported by evidence from humans (Frost et al., 2002; Mian et al., 2006).

If active lengthening of the knee extensors in early stance costs metabolic energy, it seems likely that this muscle activity has balancing beneficial functions. We hypothesize that the system of co-contracting muscles at the knee, including the ILPO, functions to improve stability by increasing the mechanical impedance (stiffness and damping) of the joint. The ILPO early in stance is actively lengthened by the co-contracting knee flexors, including the flexor cruris lateralis and the posterior iliofibularis (Gatesy, 1999; Hoogendyk, 2005). Impedance control has been identified as a major neural control strategy (Burdet et al., 2001; Full and Kotitschek, 1999; Hogan, 1985) that allows stable kinematic trajectories in the face of externally (Wagner and Blickhan, 2003) or internally (Selen et al., 2005) generated variability in joint moment. Numerous human studies suggest that co-contraction increases in situations that increase loading variability or uncertainty, and thus require higher joint impedance for stable movement (Hewett et al., 2005; Lamontagne et al., 2000).