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Ultrasonography was used to measure changes in length of muscle fascicles in relaxed human tibialis anterior and gastrocnemius during passively imposed changes in joint angle. Changes in the length of muscle fascicles were compared to changes in the length of the whole muscle-tendon units calculated from joint angles and anthropometric data. Relaxed muscle fascicles underwent much smaller changes in length than their muscle-tendon units. On average, muscle fascicles in tibialis anterior [saw] 55 ± 13 % (mean ±s.d.) of the total change in muscle-tendon length. This indicates nearly half of the total change in muscle-tendon length was taken up by stretch of tendon. In gastrocnemius, which has relatively long tendons, only 27 ± 9 % of the total change in muscle-tendon length was transmitted to muscle fascicles. Thus, the tendency for passive movement to be taken up by the tendon was greater for gastrocnemius than tibialis anterior (P = 0.002). For these muscles, the relatively large changes in tendon length across much of the physiological range of muscle-tendon lengths could not wholly be explained by tendon slackness, changes in fibre pennation, or stretch or contraction history of the muscle. Our data confirm that when joints are moved passively, length changes [seen] by muscle fascicles can be much less than changes in the distance between muscle origin and insertion. This occurs because tendons undergo significant changes in length, even at very low forces.
Relatively few studies have directly measured the elongation of tendons at the low levels of tension typically experienced by relaxed muscles. Stolov & Weillep (1966) measured elongation of the muscle belly and of the extramuscular part of the tendon as the relaxed rat gastrocnemius muscle was extended over a physiological range of lengths. They reported that the tendon lengthened only slightly and that most of the increase in length occurred in the muscle belly. However, the tendon of the rat gastrocnemius extends into the belly of the muscle (e.g. Woittiez et al. 1984), so this does not rule out the possibility that the intramuscular tendon increased in length. In a more recent study, resting rabbit soleus muscles were passively extended through a physiological range of lengths, and the lengths of muscle fascicles and tendons (both the extramuscular and intramuscular parts) were measured with markers placed on the ends of muscle fascicles (Herbert & Crosbie, 1997). Muscle fascicles experienced strains that were about four times greater than strains in tendons but, because the tendon was nearly four times longer than the muscle fascicles, muscle fascicles [saw] only about half of the total change in length imposed on the muscle-tendon unit. That is, in the rabbit soleus, changes in tendon length accounted for nearly half of the total change in muscle-tendon length.
Refshauge and colleagues (1998) were able to measure how movements at the human ankle and toe were transmitted to the bellies of the relaxed tibialis anterior and extensor hallicis longus muscles. By surgical exposure of the tendons in one subject they showed that, when the ankle was in a dorsiflexed position, movement at the ankle joint produced little change in the length of the muscle bellies. This suggests that the extramuscular part of the tendons is either slack or very compliant when the ankle is passively dorsiflexed. When, however, the ankle was plantarflexed, there was faithful transmission of joint movement to the muscle belly, suggesting that when this muscle is relaxed and held at relatively stretched lengths the extramuscular part of the tendons is not slack and does not undergo significant elongation. It was not possible in that study to determine how much movement was taken up by the long intramuscular tendons, or how much change in length of the muscle belly was transmitted to muscle fascicles.
Changes in the length and pennation of human muscle fascicles can be measured directly, reliably and non-invasively with ultrasonography (e.g. Rutherford & Jones, 1992; Herbert & Gandevia, 1995; Narici et al. 1996; Kawakami et al. 1998; Ito et al. 1998; Maganaris et al. 1998). In the present study, ultrasonography was used to examine length changes in muscle fascicles of two relaxed, human, lower limb muscles with changes in joint angle. The two muscles differed in the relative lengths of their tendons. The aim was to determine, in a passive muscle, how much of the total increase in muscle-tendon length is transmitted to the muscle fascicles and how much is taken up by elongation of the tendons. Ultrasonography was used to determine change in length of muscle fascicle and, by inference, change in length of the whole tendon; that is, both its extramuscular and intramuscular parts.
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Estimates of the rest lengths of muscle fascicles and tendons were obtained by assuming that rest lengths lay close to the shortest in vivo lengths. With this assumption, rest lengths of muscle fascicles were, on average, about one-third greater in tibialis anterior than in gastrocnemius (39 ± 8 mm in tibialis anterior; 29 ± 7 mm in medial gastrocnemius). In contrast, the tendon is about one-third shorter in tibialis anterior (230 ± 31 mm in tibialis anterior; 302 ± 28 mm in medial gastrocnemius). Thus the proportion of tendon, as measured by the ratio of rest lengths of tendon and muscle fascicles, is 77 % greater in the medial gastrocnemius (5.9 in tibialis anterior; 10.4 in medial gastrocnemius).
A summary of the five studies designed to look at muscle and tendon compliance is given in Table 1. The key finding is that much less of the passive change in whole muscle-tendon length is taken up by muscle fascicles than would occur if the tendons were inextensible. This finding holds irrespective of the[history] of the muscle.
Expt 1. Change in length of medial gastrocnemius muscle fascicles and tendon
The relationship between muscle fascicle length and change in muscle-tendon length for the medial gastrocnemius of one subject is shown in Fig. 2A. The relationship is approximately linear (see below). Thus, even though the stiffness of both tendon and muscle fascicles increases with tension (Alexander & Bennet-Clark, 1977), the ratio of their stiffnesses remains nearly constant. The slope of the linear regression is less than one, indicating that muscle fascicles do not lengthen as much as the muscle-tendon unit. For this subject, the slope was 0.28, meaning that 28 % of the total change in muscle-tendon length occurred in the muscle fascicles; the remaining 72 % of the total change in muscle-tendon length is presumed to have occurred primarily in the tendon (see below). The mean slope for all nine subjects was 0.27 (s.d.= 0.09; mean r = 0.77; Fig. 3A). This indicates that in the passive muscle, just over one-quarter of the total change in muscle-tendon length was transmitted to muscle fascicles.
Figure 3. Linear regressions of muscle fascicle length on change in muscle-tendon length
Each line is the linear regression through all data for one subject (mean of 22 measurements per subject; see Fig. 2). The regression line for each subject has been extended from the smallest to the largest muscle-tendon length measured. A, medial gastrocnemius. B, tibialis anterior. (Note that scales and ratio of horizontal and vertical scales differ in A and B.)
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Expt 2. Change in length of tibialis anterior muscle fascicles and tendon
The relationship between muscle fascicle length and change in muscle-tendon length for the tibialis anterior of one subject is shown in Fig. 2B. For this subject, the slope of the regression was 0.52. Similar results were obtained for all six subjects. The mean slope for all subjects was 0.55 ± 0.13 (mean r = 0.89; Fig. 3B), indicating that, on average, approximately one-half of the total change in muscle-tendon length was transmitted to muscle fascicles. This slope was significantly greater than the slope for the medial gastrocnemius (P= 0.002).
We considered several potential sources of error in our measurements. First, tendon length was estimated by subtracting change in muscle fascicle length from change in muscle-tendon length. This ignores the pennation of muscle fascicles. At rest, pennation of tibialis anterior varies from 13 deg at short lengths to 9 deg at stretched lengths, and pennation of medial gastrocnemius varies from 45 deg at short lengths to 22 deg at stretched lengths (Kawakami et al. 1998; Maganaris & Baltzopoulos, 1999). Neglecting pennation produces errors in estimates of tendon length that are approximately:
where lf is fascicle length, lmt is muscle-tendon length, and θ is the angle of pennation. Consequently, actual tendon length is of the order of 0.4 % (tibialis anterior, shortest length) to 2.7 % (medial gastrocnemius, shortest length) greater than estimated by subtracting fascicle length from muscle-tendon length. These errors are of little practical significance. Ignoring change in pennation, however, produces larger errors in estimates of change in length. The error is approximately
where the subscripts [max] and [min] refer to the stretched and shortened lengths, respectively, and lmt is muscle-tendon length. Thus change in tendon length has been overestimated (in relative terms) by approximately 2.1 % for tibialis anterior and 14.4 % for medial gastrocnemius. The slope of the relationship between muscle fascicle length (y axis) and change in muscle-tendon length (x axis) is underestimated by:
which equates to an underestimation of slope of approximately 0.009 for tibialis anterior and 0.091 for medial gastrocnemius. This does not materially change the interpretation of the results (see Discussion).
Although a linear regression was fitted to the data, we also considered the possibility that the relationship between changes in muscle fascicle and muscle-tendon lengths is actually non-linear. If the relationship curved upwards this would indicate that the contribution of tendon was greatest at short lengths and became progressively smaller at longer lengths. To investigate this possibility we pooled the data from the medial gastrocnemius muscles of nine subjects and, separately, the tibialis anterior muscles of six subjects by expressing both change in muscle fascicle length and change in muscle-tendon length as a percentage of the shortest muscle-tendon length (this provided greater statistical precision in the subsequent analysis). For the medial gastrocnemius, the slope appeared to increase slightly with increasing muscle-tendon length, but for the tibialis anterior the slope appeared to decrease slightly. When the data were analysed with polynomial regression, second and third order terms increased the proportion of explained variance by less than 2 % for tibialis anterior and 5 % for medial gastrocnemius, suggesting that curved regression lines do not provide better fits to the data and that there was no flattening of the curve at short lengths.
If the tendon fell fully slack at short lengths, the relationship between muscle fascicle length and change in muscle-tendon length would have a zero slope at short lengths and a positive slope only at lengths greater than slack length. In that case, the slope we estimated with linear regression would underestimate the true slope above slack length. The failure of curvilinear regression to provide a better fit to the pooled data argues against this possibility. A further test was provided by fitting a linear regression to the data obtained at the shortest muscle lengths (initially just the shortest five measurements). The slope of this regression was not significant (this might occur either because there the slope of the regression was truly zero or because the small number of data points provided insufficient statistical precision to detect a true positive slope). Then the regression was fitted to progressively longer lengths until the slope became significant. This provided an approximate upper limit to the range of lengths over which the muscle could possibly be slack. A second linear regression was fitted to the remaining data, which must have been obtained at lengths greater than slack length. The slope of this regression was 0.37 for medial gastrocnemius (95 % confidence interval 0.28 to 0.46) and 0.44 for tibialis anterior (95 % confidence interval 0.37 to 0.51) indicating that the slope was clearly less than 1 even at lengths that must be greater than slack length, if indeed the muscles fall slack at short lengths.
Expt 3. Effect of prior contraction at the test angle (part A)
In three subjects who performed isometric contractions of the medial gastrocnemius at the test angle prior to measurement of medial gastrocnemius muscle fascicle length, the relationship between muscle fascicle length and change in muscle-tendon length was, again, approximately linear. The mean slope of the relationship was 0.21 (range 0.19 to 0.23), just a little less than the slope of 0.27 obtained when muscles were not pre-conditioned by prior contraction. Thus essentially the same findings were obtained when the muscle was pre-conditioned with a contraction at the test angle.
Expt 4. Effect of prior contraction at the test angle (part B)
A second experiment, on the tibialis anterior muscle, also investigated whether prior contraction at the test angle influenced the slope of the relationship between muscle fascicle length and change in muscle-tendon length. When the muscle was stretched prior to measurement the mean slope was 0.44 (range 0.41 to 0.47), but when the muscle was first stretched and then contracted at the test angle prior to measurement the mean slope was 0.61 (range 0.34 to 0.80). This difference was not significant (P = 0.50), but as the sample was small we cannot rule out the possibility that prior contraction does produce small increases in the slope of the relationship. Nonetheless, the slope is still clearly much less than 1.
Expt 5. Effect of ongoing contraction
In nine subjects, when the tibialis anterior muscle contracted (even to only 5 % MVC), the contribution of muscle fascicles to total change in length (as reflected in the slope of the regression of muscle fascicle length on change in muscle-tendon length) tended to increase (Fig. 4). The mean slope of the regression was 0.44 ± 0.19 at rest (cf. 0.55 ± 0.13 in Expt 2 above), 0.66 ± 0.26 at 5 % MVC, and 0.60 ± 0.22 with MVC (Friedman's test, P = 0.06).
Figure 4. Effect of muscle contraction on relationship between muscle fascicle length and change in muscle-tendon length for tibialis anterior
Data from one subject. A, subject relaxed. B, subject contracting the ankle dorsiflexor muscles to 5 % of the maximal isometric torque that could be produced with the ankle dorsiflexed to 90 deg. C, subject contracting the ankle dorsiflexor muscles to 100 % of the maximal isometric torque that could be produced with the ankle dorsiflexed to 90 deg. The slope of the regressions is greater during contraction than at rest, indicating that muscle fascicles undergo relatively greater changes in length during contraction.
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Ultrasonographs of relaxed human tibialis anterior and medial gastrocnemius muscles were used to quantify changes in muscle fascicle length produced by movement of the ankle and knee. With passive movement, muscle fascicles underwent much smaller changes in length than whole muscle-tendon units (i.e. origin-to-insertion length). Muscle fascicles lengthened only half as much (in the tibialis anterior) or one-quarter as much (in the gastrocnemius) as their muscle-tendon units. Thus when resting muscles are stretched (e.g. by contraction of their antagonists) much of the increase in muscle-tendon length occurs in the tendon.
These findings rely on the accuracy of estimations of changes in muscle-tendon length with joint angle. This has been carefully evaluated (Methods, see Fig. 1). The five sources of data on change in muscle-tendon length with joint angle (Grieve et al. 1978; Spoor et al. 1990; Visser et al. 1990; Spoor & van Leeuwen, 1992; Klein et al. 1996) gave similar estimates of change in muscle-tendon length, and this justifies their use here. Even large errors in these estimates would not alter substantially our main finding.
There are several possible explanations for the observation that muscle fascicles appear to contribute surprisingly little to total changes in resting muscle-tendon length. First, muscles may fall slack at short lengths. Indeed some passive muscles may be slack across major parts of their physiological range, as assessed by ultrasonography in humans (e.g. Herbert & Gandevia 1995) and by recordings of the discharge of primary muscle spindle endings in cats (Burgess et al. 1982). Slack would produce a horizontal region in the relationship between muscle fascicle length and change in muscle-tendon length at short lengths, although it may have been obscured by scatter in our data. While we cannot rule out the possibility that there is slack at very short lengths, particularly in medial gastrocnemius, slack would not wholly explain why changes in muscle fascicle length are less than changes in muscle-tendon length. Even if we assume the largest possible slack length that could be consistent with our data, the slope of the relationship at longer lengths is still less than 0.45 for both muscles.
A small part of the total change in muscle-tendon length is due to changes in muscle pennation. Pennation decreases with increasing muscle-tendon unit length, increasing the effective length of muscle fascicles. Our calculations, based on published data of changes in pennation in these muscles, suggest this mechanism accounts for only 9 % of the total change in length of relaxed medial gastrocnemius and only 1 % for relaxed tibialis anterior.
The remainder of the total change in length (∼44 % of total change in muscle-tendon length for medial gastrocnemius and 56 % for tibialis anterior) must be due to elongation of the tendon. At the low tensions in relaxed muscles, both muscle fascicles and tendons are highly compliant. Tendons are intrinsically less compliant than muscle (i.e. tendon experiences smaller strains than muscle fascicles at a given tension) but, because the tendons of tibialis anterior and medial gastrocnemius are much longer than their muscle fascicles (by about 10-fold for medial gastrocnemius), the tendons experience relatively large changes in length.
The need for compliant tendons is illustrated in Fig. 2A. Medial gastrocnemius muscle fascicles are ∼29 mm long when the ankle is plantarflexed and the knee is flexed. Dorsiflexion by 77 deg increases muscle-tendon length by 65 mm. The muscle fascicles could not lengthen from 29 mm to (29 + 65 =) 94 mm without being damaged. If muscle fascicle strain is to be less than 100 %, muscle fascicles must contribute less than 45 % of change in muscle-tendon length. As pennation may contribute ∼9 % of the total length change (see above), tendon must contribute more than 46 % of total change in muscle-tendon length.
Significant tendon compliance at resting tensions is consistent with data from a study on rabbit soleus muscle (Herbert & Crosbie, 1997). In the rabbit soleus, muscle fascicle strains are about four times greater than tendon strains, but because the tendons are about four times as long as the muscle fascicles, approximately half of the increase in muscle-tendon length occurs in muscle fascicles and half in tendon. The present study extends these findings to passive human muscles in vivo. However, the present data are difficult to reconcile with a recent study on cat medial gastrocnemius, in which an indirect estimate of muscle fibre length was used (Whitehead et al. 2001). The authors argued that for lengths beyond optimum, their data favoured the muscle fibres rather than the tendon as the site of lengthening when the muscle was passively extended. The cause of these important discrepancies requires further investigation.
The present data are similar to some, but not all, ultrasound data on resting human ankle muscles. Three studies have described resting fascicle lengths of medial gastrocnemius at short and stretched lengths (Narici et al. 1996; Kawakami et al. 1998; Maganaris et al. 1998). Our analysis of these data gives slopes of 0.46 (Narici et al. 1996), 0.43 (Kawakami et al. 1998) and 0.46 (Maganaris et al. 1998). These values are higher than our value of 0.27, but still much less than 1.0. The smaller slope could be explained if there was slack at short lengths, as we measured fascicle lengths over a greater range. In contrast, Maganaris & Baltzopoulos (1999) report a slope of 0.92 for tibialis anterior, higher than that of 0.55 in our study. It is not clear why these data differ from our data and from the medial gastrocnemius data of Narici et al., Kawakami et al. and Maganaris et al. but failure to obtain full relaxation could be critical. Several ultrasonographic studies on human muscles have attempted to estimate length-tension properties of tendon by measuring muscle fascicle length changes during isometric contraction (e.g. Fukashiro et al. 1995). While this approach may provide estimates of tendon length changes induced by contraction, the data in such studies may not be comparable with the present data if, as has been suggested, contraction changes the mechanical properties of the intramuscular tendon (Ettema & Huijing, 1989; Lieber et al. 2000).
Elek et al. (1990) performed elegant experiments to determine the extent of [extramysial displacement ] (primarily elongation of tendon) in cat medial gastrocnemius during gait. They recorded spindle discharge while the passive muscle-tendon unit was subjected to gait-like changes in length. Subsequently, the muscle was contracted by selectively stimulating alpha motoneurones, and changes in muscle-tendon length were adjusted until the same pattern of spindle discharge was obtained under passive and active conditions, whereupon it was assumed that muscle fascicles were undergoing the length changes. Elek et al. estimated that extramysial displacements were small (∼0.5 % of total muscle-tendon length), which suggests there was little elongation of tendon in the transition from passive to active conditions. However, this method could underestimate the extramysial (or tendon) displacement with contraction because some spindles lie partly or wholly in series with extrafusal muscle fibres (Binder & Stuart, 1980; Cameron et al. 1983).
In one subject, who had also participated in an experiment in which the tendon of tibialis anterior was surgically exposed, we were able to compare estimates of changes in muscle-tendon length with direct measures of displacement of the extramuscular tendon of tibialis anterior (Refshauge et al. 1998). Displacement of a marker on the extramuscular tendon (∼10 cm proximal to the distal insertion) was measured when the ankle was moved passively during relaxation. At ankle angles of ≥−10 deg (i.e. at all but the most dorsiflexed positions) the marker moved 0.60 mm deg−1 (calculated from Fig. 5 in Refshauge et al. 1998), a value that is exactly equal to the estimated change in tibialis anterior muscle-tendon length for this subject. This indicates that there is little stretch in the most distal 10 cm of the tendon of tibialis anterior and that most stretch occurs in more proximally in the tendon. Perhaps this is not surprising, as strains in the intramuscular tendons of isolated muscles greatly exceed those in extramuscular tendon (Lieber et al. 1991; Trestik & Lieber, 1993; Zuurbier et al. 1994; cf. Scott & Loeb, 1995). In contrast, at high tensions, strains in the intramuscular and extramuscular tendon are nearly identical (cat soleus muscle; Morgan, 1977).
There was a tendency, albeit not quite significant (P = 0.06), for ankle displacement to produce larger changes in muscle fascicle length at higher forces. The slope remains less than one, which probably indicates that the contribution of synergistic muscles to the dorsiflexion torque is not constant across joint angles. Regardless of the mechanism, an intriguing consequence is that the stretch [seen] by muscle fascicles and their spindles might be modulated by muscle contraction. Contraction of only 5 % MVC increases the change in muscle fascicle length associated with a change in joint angle by about 50 %, suggesting even this low level of muscle contraction increases the [sensitivity] of tibialis anterior muscle spindles to changes in ankle angle by half. This provides an additional mechanism which would alter the sensitivity of muscle spindles. Furthermore, this adds extra complexity to central [interpretation] of spindle afferent discharge, as is required for proprioceptive judgements; for tibialis anterior, the sensitivity of muscle spindles to joint displacement can be increased indirectly by excitation of alpha motoneurones as well as by fusimotor neurones.
In summary, this study suggests that for a range of movement and contraction [histories] the tendon of long human muscles acting across the ankle (and in particular its intramuscular portion) may undergo surprisingly large changes in length.