Vol. 93, Issue 6, 2089-2094, December 2002
Repeated contractions alter the geometry of human skeletal
muscle
Constantinos N.
Maganaris1,
Vasilios
Baltzopoulos1, and
Anthony J.
Sargeant1,2
1 Centre for Biophysical and Clinical Research into
Human Movement, Manchester Metropolitan University, Alsager ST7 2HL,
United Kingdom; and 2 Institute for Fundamental and
Clinical Human Movement Sciences, Vrije University, 10B1 BT Amsterdam,
The Netherlands
 |
ABSTRACT |
The aim of this study was to
investigate the effect of repeated contractions on the geometry of
human skeletal muscle. Six men performed two sets (sets A
and B) of 10 repeated isometric plantarflexion contractions
at 80% of the moment generated during plantarflexion maximal voluntary
contraction (MVC), with a rest interval of 15 min between sets. By use
of ultrasound, the geometry of the medial gastrocnemius (MG) muscle was
measured in the contractions of set A and the displacement
of the MG tendon origin in the myotendinous junction was measured in
the contractions of set B. In the transition from the 1st to
the 10th contractions, the fascicular length at 80% of MVC decreased
from 34 ± 4 (means ± SD) to 30 ± 3 mm
(P < 0.001), the pennation angle increased from
35 ± 3 to 42 ± 3° (P < 0.001), the
myotendinous junction displacement increased from 5 ± 3 to
10 ± 3 mm (P < 0.001), and the average
fascicular curvature remained constant (P > 0.05) at
~4.3 m
1. No changes (P > 0.05) were
found in fascicular length, pennation angle, and myotendinous junction
displacement after the fifth contraction. Electrogoniometry showed that
the ankle rotated by ~6.5° during contraction, but no differences
(P > 0.05) were obtained between contractions. The
present results show that repeated contractions induce tendon creep,
which substantially affects the geometry of the in-series contracting
muscles, thus altering their potential for force and joint moment generation.
ultrasound; in vivo; fascicular length; pennation angle; curvature
| |
INTRODUCTION |
THE FASCICULAR
GEOMETRY IN a muscle is a major determinant of the muscle's
functional capabilities. For identical muscular compositions and
volumes, the longer the fascicles the higher the excursion and velocity
of contraction, and the higher the fascicular insertion angle to the
in-series tendon (pennation angle), the higher the contractile force
potential (3, 18).
Several studies have shown that isometric contraction alters the
length and pennation angle of muscle fascicles (e.g., Refs. 5, 10, 12, 14). The
magnitude of these changes in a single static contraction is determined
by the force elicited in the muscle and the compliance of the in-series
tendon. The higher the contractile force and the more compliant the
tendon, the higher the fascicular shortening and pennation angle
increase with respect to rest (5, 12, 14). If, however,
the same muscle were called on to contract repeatedly, its fascicular
geometry during contraction could also be affected by the tendon's
time-dependent properties. Numerous experiments show that tendons
exhibit creep (i.e., they elongate over time) when loaded in an
oscillating pattern (for review, see Refs. 1,
21), which suggests that repeated contractions might
result in greater fascicular shortening and pennation angle increase
compared with a single contraction, thus altering the muscle's
potential for force and joint moment production. Evidence for this
hypothesis was sought in the present experiment. We studied the
fascicular geometry of the in vivo human medial gastrocnemius (MG) muscle.
| |
METHODS |
Experimental protocol.
Six healthy male volunteers (age: 24 ± 4 yr, height: 172 ± 5 cm, body mass: 72 ± 6 kg; mean ± SD) gave their consent
to participate in this study. The experimental procedures involved were
approved by the institutional ethics committee. The subjects lay prone on the couch of an isokinetic dynamometer (Cybex Norm) set in the
isometric ankle plantarflexion mode. Measurements were taken in the
left leg, with the knee fully extended and the ankle fixed at its
neutral position (the sole of the foot at right angles to the tibial
axis) on the dynamometer footplate with straps. The effectiveness of
this fixation method in preventing ankle rotation was assessed during
the experiments by using an electrogoniometer (Biometrics) with its
ends attached 7 cm above and 3 cm below the lateral malleolus (Fig.
1). The recordings of the goniometer were
collected with a Biopac MP100 system (Biopac Systems) at a sampling
frequency of 500 Hz.
View larger version (13K):
[in this window]
[in a new window]
|
Fig. 1.
Experimental setup. a, Dynamometer; b, footplate; c,
strap; d, lateral malleolus; e; electrogoniometer; f, medial
gastrocnemius (MG) muscle; g, ultrasound probe fixed in position
A for scanning the muscle and in position B for
scanning the myotendinous junction; h, MG tendon.
|
|
Each subject performed 10 successive isometric plantarflexion voluntary
contractions (set A), all at an absolute moment
corresponding to 80% of the moment generated during plantarflexion
maximal voluntary contraction (MVC). We considered that a constancy in
the absolute measured plantarflexion moment between repeated
contractions would correspond to a respective constancy in the force
generated by the MG muscle alone. We will return to this point in the
DISCUSSION. Each contraction was elicited by requesting the
subject to increase the plantarflexion moment gradually over a 3-s
period until reaching the absolute moment targeted. The subject was
then asked to maintain that moment for 1 s before relaxing the
contracting muscles. After 1 s of rest, the next contraction was
elicited. Audiovisual feedback of the plantarflexion moment generated
and time elapsed was provided. The dynamometer signals were collected
(with the acquisition system used for collecting the electrogoniometry
data) at 500 Hz.
Measurements of the MG muscle fascicular geometry were taken in the
contractions of set A by B-mode ultrasonography (5, 9,
10, 12, 14, 19). The accuracy of this method for resting-state
measurements has been confirmed by direct measurements on cadaveric
muscles (9, 12), but further validation is required for
measurements under dynamic conditions. The reproducibility of the
method has also been confirmed previously (12, 14, 19).
Sagittal-plane scans were taken with a 7.5-MHz linear ultrasound probe
(AU5 Esaote Biomedica; axial and lateral resolutions of 0.2 and 0.3 mm,
respectively) placed on the skin at the midlength and midwidth of the
MG muscle. The fascicular geometry in this region has been shown to
represent that along and across the MG muscle belly (10, 12, 14,
19). In the muscle scans produced, fascicular, interfascicular,
and aponeurotic echoes were identified. The probe was then oriented in
the plane over which the fascicles lay, where it was fixed with
adhesive tape. The ultrasound, dynamometer, and electrogoniometer
recordings were synchronized, and the 10 contractions were then
elicited. In the scans recorded, the fascicular length was assumed to
be the length of the curved fascicular path between the two
aponeuroses, and the pennation angle was assumed to the angle between
the fascicular path and the deep aponeurosis (Fig.
2). The results of this measurement
approach depend not only on the positions of the fascicular insertion
and origin in the aponeuroses, but also on the fascicular curvature.
Fascicular curvature values were therefore estimated. The approach we
followed for deriving these estimates assumed that the fascicular path is an arc of a circle (Fig. 3), as
recently described by Muramatsu et al. (19).
View larger version (84K):
[in this window]
[in a new window]
|
Fig. 2.
Left: typical sonographs of the MG muscle at 80% of
maximal voluntary contraction (MVC) in the 1st (A), 3rd
(B), 5th (C), and 10th (D)
contractions of set A. In each scan, the horizontal white
striations are echoes reflected from the superficial and deep
aponeuroses, the oblique white striations are echoes reflected from
interfascicular connective tissue, and the oblique dark striations are
echoes reflected from fascicles. The superimposed black curves show
fascicular orientations. Right: sonographs of the MG
myotendinous junction at 80% of MVC in the 1st (E), 3rd
(F), 5th (G), and 10th (H)
contractions of set B in the same subject. White arrows
point to the end point of the MG tendon origin. Black arrows point to
the shadow generated by a piece of copper wire glued on the skin to
provide a reference marker for the displacements measurements.
|
|
View larger version (18K):
[in this window]
[in a new window]
|
Fig. 3.
Graphical representation of the fascicular geometry
measurements taken. The scan window in the figure encloses the
structures seen in the muscle scans shown in Fig. 2. The length of the
curved fascicular path AB is the fascicular length;  is the
pennation angle formed between the straight line  2
(passing through B and D) and the deep aponeurosis;  is the angle
formed between the straight line 1 (passing through A
and C) and the superficial aponeurosis; and T is the
distance between the 2 aponeuroses. T and were used to
calculate the fascicular curvature, by assuming that the fascicular
length AB is an arc of a circle with radius R. This
assumption has been validated by Muramatsu et al. (19),
who calculated that the fascicular curvature
R1 = (cos2  cos2) · [2T · (cos + cos)]1. The fascicular curvature values in the
present study were derived from the above equation.
|
|
An additional set of 10 contractions (set B) was performed
at the absolute moment reached in the contractions of set A.
Each subject executed set B in the same way as set
A, 15 min after completing set A. This rest period is
much longer than that required to resume the properties of tendon after
loading (~5 min; Ref. 21); therefore, we considered that
set B would yield results independent of the loading applied
in set A. In set B, the scanning probe used
before was shifted toward the distal myotendinous junction of the
muscle, keeping the probe on the axis and plane over which muscle scans
were previously taken. At the myotendinous junction level, an
echoabsorptive marker was glued on the skin underneath the probe. The
probe was then taped on the skin; the ultrasound, dynamometer, and
electrogoniometer recordings were synchronized; and the 10 contractions
were elicited. In the scans recorded, the displacement of the echo
generated by the end point of the MG tendon origin in the myotendinous
junction relative to the position of the echo generated by the external
marker was measured along the MG tendon. Similar protocols to the one
described above have recently shown that ultrasonography provides
reproducible measurements of tendinous displacement during contraction
(11, 15-17).
Data analysis.
The scans recorded when the plantarflexion moment measured was
maintained at 80% of the MVC moment were identified. For each subject
and contraction number in either set, we selected for analysis three
scans with the best available quality in the structures seen. In each
scan, each geometrical characteristic studied was quantified from
measurements in one to three different regions where the fascicular
orientation could be best seen. All morphometric measurements were
carried out by digitization by the same investigator in a randomized
order for contraction number. For each subject and contraction number,
the measurements of each individual geometrical characteristic were
averaged and used for further analysis. One-way ANOVA was used to test
1) differences in fascicular geometry between contractions
(set A) and 2) differences in myotendinous
displacement between contractions (set B). Two-way ANOVA was
used to test differences within and between sets A and
B in the ankle joint rotations corresponding to the scans
examined. Tukey's tests were used for post hoc analysis where
appropriate. Statistical significance was set at P < 0.05. Values are reported as means ± SD.
| |
RESULTS |
The absolute value of plantarflexion moment to which all the
following data refer is 105 ± 6 N · m. In the transition
from the 1st to the 10th contractions in set A, the
fascicular length of the MG muscle decreased from 34 ± 4 to
30 ± 3 mm (P < 0.001), and its pennation angle
increased from 35 ± 3 to 42 ± 3° (P < 0.001). No changes (P > 0.05) were obtained in
fascicular length and pennation angle after the fifth contraction (Fig.
4, A and B). The
average fascicular curvature was ~4.3 m1, with no
differences (P > 0.05) obtained between contractions (Fig. 4C), which indicates lack of artifactual changes in
fascicular length and pennation angle. In the transition from the 1st
to the 10th contractions in set B, the displacement of the
MG myotendinous junction increased from 5 ± 3 to 10 ± 3 mm
(P < 0.001). No displacement changes
(P > 0.05) were obtained after the fifth contraction
(Fig. 4D). The ankle joint rotated in the plantarflexion
direction in all the contractions because of inevitable imperfect
fixation of the foot on the dynamometer. The average rotation
corresponding to the scans examined was ~6.5°, with no differences
(P > 0.05) obtained either within or between
sets A and B (Fig.
5).
View larger version (14K):
[in this window]
[in a new window]
|
Fig. 4.
Summarized results (means ± SD; n = 6) of fascicular length (A), pennation angle (B),
fascicular curvature (C), and myotendinous junction
displacement (D). The resting-state values of fascicular
length and pennation angle before the 1st contraction are also given.
In A, B, and D, P < 0.05 between the 1st and 2nd, 2nd and 3rd, 3rd and 4th, and 4th and 5th
contractions, and P > 0.05 between the 5th, 6th, 7th,
8th, 9th and 10th contractions. In C, P > 0.05 between the contractions.
|
|
View larger version (16K):
[in this window]
[in a new window]
|
Fig. 5.
Summarized results (means ± SD; n = 6) of ankle plantarflexion rotation compared with rest at the time
points corresponding to 80% of MVC moment in sets A
(A) and B (B). P > 0.05 within and between sets.
|
|
| |
DISCUSSION |
The present study was conducted to investigate the effect of
repeated contractions on the fascicular geometry of the human MG
muscle. Our results show that the fascicular behavior during contraction is time dependent.
The use of optic fibers has recently enabled the quantification of in
vivo human tendon forces during muscle contraction (2). However, this technique cannot measure the contractile forces generated
by different muscles ending in one tendon (e.g., the three muscles
comprising the triceps surae complex). Here, we have assumed that the
MG muscle would produce a given force in different contractions
generating the same net plantarflexion moment. (Note that conventional
electromyogram recordings could be misleading in verifying this
assumption because they do not relate to all motor units being active
during a submaximal contraction; hence, we did not record such data.)
However, it may be argued that the MG muscle force could decrease as a
function of contraction number due to fatigue, with the net moment
measured remaining at the constant level required by recruiting more
fibers from fiber type I-predominant and therefore more
fatigue-resistant plantarflexors, e.g., the soleus muscle
(8). Therefore, if the metabolic state of the MG muscle
could be preserved, 1) more pronounced fascicular geometry
changes might be seen, and 2) more contractions might be
required to generate a steady fascicular behavior. On the other hand,
muscle potentiation would produce the opposite effect of fatigue.
However, it is unlikely that potentiation occurred to a substantial
extent in our experiments because the high contractile forces elicited
would not be affected by increases in either Ca2+
sensitivity or myoplasmic Ca2+ concentration (e.g., Ref.
13).
The simultaneous changes in fascicular length and pennation angle found
indicate that these phenomena originated from creep in soft tissue
mediating contractile force transmission from the fascicles to the
dynamometer footplate. The plantarflexion rotations measured were
similar in all contractions, which suggests that any creep in
extraskeletal soft tissue had no measurable effect on the geometry of
the MG muscle in our tests. However, the MG tendon did exhibit creep as
indicated by the increase in the myotendinous junction displacement. In
fact, the MG tendon and the fascicles exhibited very similar
time-dependent behaviors over the same number of contractions (see Fig.
4, A and D), indicating a cause-and-effect relation between the two phenomena. Another structure that could have
exhibited tensile creep in our experiment is the aponeurosis. In an
attempt to assess whether aponeurotic creep occurred to an extent
sufficient to cause a measurable change in muscular geometry, we
calculated the distance traveled by the fascicular insertion in the
aponeurosis in the first five contractions (i.e., the contractions in
which a time-dependent behavior was seen). As shown in Fig.
6, the estimates obtained are similar to
the respective measured differences in the myotendinous junction
displacements, which suggests that the fascicular changes observed were
not affected substantially by creep development in the aponeurotic part
lying between the tendon origin and the fascicular insertion.
View larger version (10K):
[in this window]
[in a new window]
|
Fig. 6.
Triangle ABC represents the effect of creep in the distal
tendon-aponeurosis of the MG muscle on the geometry of a fascicle. A is
the origin of a fascicle, B and C are the insertions of the fascicle in
2 consecutive contractions, and and  are the corresponding
pennation angles. From the law of sines, it follows that (BC) = (AC) · sin · sin1, where = 360 180 + . Application of the above equation in
the first 5 contractions of set A gave the average lengths
illustrated as black bars in the graph at the bottom. The white bars
shown represent the respective average differences in the myotendinous
junction displacement in the first 5 contractions of set B.
The numbers 1-2 to 4-5 in the horizontal axis refer to
transitions from a given contraction number to the next contraction
number.
|
|
The present results are consistent with some of the results reported
recently by Kubo et al. (11) from experiments on the distal tendon-aponeurosis and pennation angle of the human vastus lateralis muscle before and immediately after several
repeated-contraction protocols. In accordance with the present
findings, the repeated loading applied by the above authors increased
the pennation angle of the muscle. Surprisingly, however, this effect
was not always related to an increased tendon-aponeurosis elongation.
The reasons for the above dissociation were neither discussed nor are
readily apparent. It may be the case that certain loading conditions in some muscles induce tensile creep mainly in the proximal tendon aponeurosis. Irrespective, however, of the "contributions" made by
the proximal and distal tendinous components in changing muscular geometry under different loading circumstances, the finding of a
time-dependent fascicular behavior has important biological implications. The fascicular shortening after repeated loading would
correspond to a reduction in the average operating length of the
sarcomeres. In the MG muscle, which operates in the ascending limb of
the force-length relation (6), the shortening induced would shift the average operating sarcomeric length away from that
corresponding to optimal myofilament overlap, thus reducing the
contractile force generated on activation. For an average number of
17,600 in-series sarcomeres in the MG muscle (7), it
follows from our fascicular length measurements that repeated loading
would reduce the length of the average sarcomere from ~1.9 to 1.7 µm, which according to the theoretical force-length relation obtained
by applying the cross-bridge model of contraction (4) to
human myofilament lengths (22) might reduce the
force-generating potential by ~10%. The increased pennation angle in
the muscle would further reduce both the effective vectorial component
of contractile force transmitted along the Achilles tendon and the resultant moment generated about the ankle. Hence, a reduction in the
moment generated in a series of maximal plantarflexion contractions
should not be ascribed to neuromuscular fatigue only. In addition to
changes in force- and moment-generating capabilities, the present
findings could also have implications for proprioceptive control. If
fascicular shortenings of the order obtained in the present study can
be "seen" by the muscle spindles, excitatory and inhibitory
reflexes could be triggered through alterations in the firing of Ia
afferents, introducing potential errors in positional control due to
changes in the activity balance between agonist and antagonist muscles
(e.g., Ref. 20). This would be of no functional relevance
in an experiment involving isometric contractions, but it could
complicate the control of movement generated by physiologically
repeated contractions of high intensity, such as those elicited when running.
| |
FOOTNOTES |
Address for reprint requests and other correspondence:
C. N. Maganaris, Centre for Biophysical and Clinical
Research into Human Movement, Manchester Metropolitan Univ., Alsager
ST7 2HL, UK (E-mail:
c.n.maganaris{at}mmu.ac.uk).
The costs of publication of this
article were defrayed in part by the
payment of page charges. The article
must therefore be hereby marked
"advertisement"
in accordance with 18 U.S.C. Section 1734 solely to indicate this fact.
August 23, 2002;10.1152/japplphysiol.00604.2002
Received 8 July 2002; accepted in final form 21 August 2002.
| |
REFERENCES |
1.
Butler, DL,
Grood ES,
Noyes FR,
and
Zernicke RF.
Biomechanics of ligaments and tendons.
In: Exercise and Sport Science Reviews, edited by Hutton RS.. Philadelphia, PA: Franklin Institute, 1978, vol. 2, p. 125-181.
2.
Finni, T,
Komi PV,
and
Lukkariniemi J.
Achilles tendon loading during walking: application of a novel optic fibre technique.
Eur J Appl Physiol
77:
289-291,
1998.
3.
Gans, C.
Fiber architecture and muscle function.
In: Exercise and Sport Sciences Reviews, edited by Teijung RT.. Philadelphia, PA: Franklin Institute, 1982, vol. 10, p. 160-207.
4.
Gordon, AM,
Huxley AF,
and
Julian FJ.
The variation in isometric tension with sarcomere length in vertebrate muscle fibres.
J Physiol
184:
170-192,
1966[Abstract/Free Full Text].
5.
Herbert, RD,
Moseley AM,
Butler JE,
and
Gandevia SC.
Change in length of relaxed muscle fascicles and tendons with knee and ankle movement in humans.
J Physiol
539:
637-645,
2002[Abstract/Free Full Text].
6.
Herzog, W,
Read LJ,
and
ter Keurs HEDJ
Experimental determination of force-length relations of intact human gastrocnemius muscles.
Clin Biomech
6:
230-238,
1991.
7.
Huijing, PA.
Architecture of the human gastrocnemius muscle and some functional consequences.
Acta Anat (Basel)
123:
101-107,
1985[Web of Science][Medline].
8.
Johnson, MA,
Polgar J,
Weightman D,
and
Appleton D.
Data on the distribution of fibre types in thirty-six human skeletal muscles. An autopsy study.
J Neurol Sci
18:
111-129,
1973[Web of Science][Medline].
9.
Kawakami, Y,
Abe T,
and
Fukunaga T.
Muscle-fiber pennation angles are greater in hypertrophied than in normal muscles.
J Appl Physiol
74:
2740-2744,
1993[Abstract/Free Full Text].
10.
Kawakami, Y,
Ichinose Y,
and
Fukunaga T.
Architectural and functional features of human triceps surae muscles during contraction.
J Appl Physiol
85:
398-404,
1998[Abstract/Free Full Text].
11.
Kubo, K,
Kanehisa H,
Kawakami Y,
and
Fukunaga T.
Influences of repetitive muscle contractions with different modes on tendon elasticity in vivo.
J Appl Physiol
91:
277-282,
2001[Abstract/Free Full Text].
12.
Narici, MV,
Binzoni T,
Hiltbrand E,
Fasel J,
Terrier F,
and
Cerretelli P.
In vivo human gastrocnemius architecture with changing joint angle at rest and during graded isometric contraction.
J Physiol
496:
287-297,
1996[Abstract/Free Full Text].
13.
MacIntosh, BR,
and
Willis JC.
Force-frequency relationship and potentiation in mammalian skeletal muscle.
J Appl Physiol
88:
2088-2096,
2000[Abstract/Free Full Text].
14.
Maganaris, CN,
Baltzopoulos V,
and
Sargeant AJ.
In vivo measurements of the triceps surae architecture in man: implications for muscle function.
J Physiol
512:
604-613,
1998.
15.
Maganaris, CN,
and
Paul JP.
In vivo human tendon mechanical properties.
J Physiol
521:
307-313,
1999[Abstract/Free Full Text].
16.
Maganaris, CN,
and
Paul JP.
In vivo human tendinous tissue stretch upon maximum muscle force generation.
J Biomech
33:
1453-1459,
2000[Web of Science][Medline].
17.
Magnusson, SP,
Aagaard P,
Dyhre-Poulsen P,
and
Kjaer M.
Load-displacement properties of the human triceps surae aponeurosis in vivo.
J Physiol
531:
277-288,
2001[Abstract/Free Full Text].
18.
Muhl, ZF.
Active length-tension relation and the effect of muscle pennation on fibre lengthening.
J Morphol
173:
285-292,
1982[Web of Science][Medline].
19.
Muramatsu, T,
Muraoka T,
Kawakami Y,
Shibayama A,
and
Fukunaga T.
In vivo determination of fascicle curvature in contracting human skeletal muscles.
J Appl Physiol
92:
129-134,
2002[Abstract/Free Full Text].
20.
Rack, PMH,
Ross HF,
Thilmann AF,
and
Walters DKW
Reflex responses at the human ankle: the importance of tendon compliance.
J Physiol
344:
503-524,
1983[Abstract/Free Full Text].
21.
Viidik, A.
Functional properties of collagenous tissues.
Int Rev Connect Tiss Res
6:
127-215,
1973[Medline].
22.
Walker, SM,
and
Schrodt GR.
I-segment lengths and thin filament periods in skeletal muscle fibers of the Rhesus monkey and the human.
Anat Rec
178:
63-82,
1973.
J APPL PHYSIOL 93(6):2089-2094
8750-7587/02 $5.00
Copyright © 2002 the American Physiological Society
TOP
ABSTRACT
INTRODUCTION
