DETERMINANTS OF APONEUROSES SHAPE CHANGE DURING MUSCLE CONTRACTION
1
Christopher J. Arellano, 2 Nicholas J. Gidmark, 1 Nicolai Konow, and 1 Thomas J. Roberts
1
Brown University, Providence, RI, USA
University of Washington, Friday Harbor, WA, USA
email: [email protected]
We tested the hypothesis that changes in
aponeurosis width are governed by two forces: 1)
forces resulting from radial expansion (i.e. bulging)
of shortening muscle fibers, and 2) the force acting
along the muscle’s line of action (longitudinal axis).
Fiber bulging due to shortening should increase
aponeurosis
width,
whereas
increases
in
longitudinal force should decrease aponeurosis
width, as expected for a biaxially loaded material.
To test this hypothesis, we measured muscle force,
aponeurosis length, and aponeurosis width during
isotonic muscle contractions.
METHODS
Small (0.8-1.0 mm diameter) radiopaque markers
were surgically implanted along muscle fibers and
into the aponeurosis of the lateral gastrocnemius
(LG) muscle of wild turkeys, Meleagris gallopavo
(Fig. 1A-B; n=3). Following established in-situ
methods [1], the muscle’s distal tendon was rigidly
attached to a lever of a servo-controlled motor that
regulated force and length (Aurora Scientific, Inc).
In-situ measurements of muscle force were
combined with high-speed biplanar x-ray video for
(C)
(N)
f
Force
150
100
50
0
8
0
47.0
Aponeurosis
length (mm)
Aponeuroses are sheet-like tendons that connect in
series with muscle fibers. The mechanical behavior
of aponeuroses differs from that of free tendons
because free tendons are loaded uniaxially, while
aponeuroses experience loads in more than one
direction. During a shortening contraction,
aponeuroses increase in both length and width [1,
2]. It has been proposed that forces generated from
muscle bulging as fibers shorten and expand
radially cause an increase in aponeurosis width [1],
but this idea has not been tested directly.
200
(A)
Volts
(D)
46.5
46.0
(E)
21.0
(B)
X-ray image (one of two)
Proximal fiber
length
Aponeurosis
width (mm)
INTRODUCTION
20.5
20.0
19.5
Muscle
belly
(F)
24
Aponeurosis
Free tendon
Proximal
fiber length (mm)
2
22
20
18
16
14
servo-motor
0
0.2
0.4
0.6
time (sec)
0.8
1.0
1.2
Figure 1: (A) In combination with x-ray video, an in-situ
preparation (B) allowed us to quantify the effects of muscle
fiber shortening on aponeurosis width and length changes (CF) during an isotonic (constant force) contraction at maximal
activation. Blue lines indicate isotonic period used for
analysis.
a series of isotonic contractions. For each
contraction, the positions of the radiopaque markers
were tracked using an established marker-based
workflow (www.xromm.org). Changes in muscle
fiber length, aponeurosis width, and aponeurosis
longitudinal length were quantified from the 3D
marker coordinates (IGOR Pro 6, Wavemetrics).
We isolated the influence of fiber shortening on
aponeurosis width by plotting the two during the
time when the muscle produced a constant force
(Fig. 1C-F; Fig. 2). The linear slope of aponeurosis
width strain versus fiber shortening strain during
each contraction was calculated to give the relative
strain ratio (Fig. 3).
decreased as force increased. As seen in Fig. 3,
increases in aponeurosis width were negligible
when the fibers shortened at the highest constant
force contractions.
20.8
isotonic region
20.6
1.0
20.4
relative strain ratio
( aponeurosis width/ fiber)
Aponeurosis width (mm)
(A)
20.2
20.0
Aponeurosis width (mm)
(B)
21.6
21.2
20.8
0.6
0.4
0.2
0
118 N
0.2
0.4
0.6
relative force (P/Po)
0.8
1.0
Figure 3: Relative strain ratio decreases as relative force
increases indicating that shape change is force dependent (n =
3). Data are fitted with a linear least-square regression analysis
(gray line). Symbols distinguish data from individual birds.
177 N
20.4
0.8
0
12 N
60 N
r2 = 0.92
235 N
20.0
16
17
18
19
20
21
22
23
proximal fiber length (mm)
Figure 2: (A) Data for a single contraction showing the
increase in aponeurosis width as muscle fibers shorten.
Arrowheads indicate direction of fiber shortening during the
contraction. (B) For a series of contractions, increases in
aponeurosis width depend on both magnitude of fiber
shortening and longitudinal muscle force. Representative data
from several isotonic contractions measured from a single LG
muscle.
RESULTS AND DISCUSSION
Influence of muscle fiber shortening and force:
During periods of constant force, aponeurosis width
increased as the muscle fibers shortened (Fig. 2A).
Across contractions, the amount of increase in
aponeurosis width also depended on longitudinal
force. At higher forces, aponeurosis width increases
to a lesser extent with fiber shortening (Fig. 2B).
For example, when the muscle produced 12 N of
constant force, 3 mm of fiber shortening coincided
with a 0.8 mm increase in aponeurosis width (Fig.
2B). At 177 N, the same amount of fiber shortening
coincided with only a 0.3 mm increase in
aponeurosis width.
Relative strain ratio vs. relative force: Aponeurosis
width increases more for a given amount of fiber
shortening at low compared to high force levels.
Overall, the ratio of aponeurosis strain to fiber strain
CONCLUSIONS
Our findings support our hypothesis that
aponeurosis width is governed by two forces. The
radial expansion of fibers associated with muscle
shortening drives increases in aponeurosis width,
while longitudinal forces on the aponeurosis tend to
limit increases in aponeurosis width. The biaxial
strain patterns in aponeuroses depends upon the
relative magnitude of these two forces during a
muscle contraction. These results demonstrate that
muscle shape change influences the mechanical
behavior of aponeuroses and highlight the
mechanism for modulating aponeurosis stiffness.
REFERENCES
1. Azizi and Roberts. J Physiol 17, 4309-4318,
2. Scott and Loeb. J Morph 224, 73-86, 1995.
2009.
ACKNOWLEDGEMENTS
The authors thank Trovoy Walker, Drew
Schmetterling, and Benjamin Scott for their
assistance on this project. The National Institutes of
Health research grant [AR055295] awarded to TJR
supported this research.