Isometric and isovelocity contractile performance of red musle fibres from the dogfish Scyliorhinus canicula
1 Biological Structure and Function, Division of Biomedical Sciences,
Faculty of Medicine, Sir Alexander Fleming Building, Imperial College of
Science, Technology and Medicine, London SW7 2AZ
2 UCL Institute of Human Performance, Royal National Orthopaedic Hospital
Trust, Brockley Hill, Stanmore, Middlesex HA7 4LP, UK
* Present address: Department of Biosciences, Faculty of Natural Sciences,
University of Hertfordshire, College Lane, Hatfield, Hertfordshire AL10 9AB,
UK
Author for correspondence (e-mail:
n.curtin{at}ic.ac.uk
)
Accepted 19 March 2002
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Summary |
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Key words: red muscle, fish, muscle, contraction, power, isometric force, P0, force/velocity, force, series elasticity, V0, Vmax, Scyliorhinus canicula, dogfish
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Introduction |
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In this study, two questions are addressed about the contractile performance of red fibres from dogfish. Are they as strong as white fibres during isometric contraction? How much force is produced during constant-velocity movement (shortening and lengthening) at full activation?
Red fibres are small and held together by extensive connective tissue; consequently, some are damaged during dissection of the small bundles of fibres required for in vitro experiments. Thus, to answer the question about strength accurately, force must be expressed relative to the cross-sectional area of undamaged fibres. A simple method for identifying damaged and intact fibres has been developed, and quantitative validation of the method is reported.
The mechanical and energetic performance of red fibres during a brief
period of sinusoidal movement have also been investigated
(Curtin and Woledge, 1993b).
In these `work-loop' contractions, which are like those that power swimming,
the stimulation is brief and not long enough to activate the fibres fully.
Here, we report the mechanical properties of fully active red fibres during
constant-velocity shortening and lengthening. Although we recognize that these
contractions are unlike those powering swimming, they are of value. They give
direct information about contractile performance under conditions in which the
cross-bridges are not limited or influenced by variations in activation
(proportion of cross-bridges that are cycling, etc.). In other words, under
conditions in which all variations in force and movement are due solely to
cross-bridge properties and none is due to changes in the degree of
activation. As we have demonstrated for white fibres, force and power during
work loops that mimic swim-like contractions can be predicted by taking
account of the behaviour of cross-bridges and the series elasticity (from
experiments such as those reported here) and a reasonable assumption about the
time course of activation (Curtin et al.,
1998
).
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Materials and methods |
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Histology of red fibre bundles
Nine bundles of red fibres were dissected from three fish and stained with
0.005% Evans Blue, but without any stimulation. After staining and a rinse in
saline, these fibre bundles were prepared for cryostat sectioning. The
preparation was mounted in gelatine (15% w/v in saline) while the myosepta
were held in forceps to keep the fibres as straight as possible while the
gelatine set. After hardening in the refrigerator, the gelatine blocks were
trimmed and fixed to cork discs with OCT embedding compound (Histological
Equipment Ltd, UK). The blocks were frozen by immersion in partially frozen
isopentane for 10 s and stored at -40°C. Transverse sections of 10 µm
thickness were cut on a cryostat (Bright Instrument Company, UK) at -18°C.
Sections were taken at various points along the length of each fibre bundle.
They were placed on microscope slides and covered with glycerol and a
coverslip.
The sections were examined under a fluorescent microscope (Olympus Provis) using a green filter that made the Evans-Blue-stained fibres appear bright red and unstained fibres appear dark. Images were recorded and measured with a Photonic Science Olympus video camera operated by the program PhotoLite (Image-Pro). A graticule slide (Graticules Ltd, Kent, England) was recorded and measured in the same series to give the calibration scale.
Contractile properties
In the experiments on contractile properties, the myosepta at the ends of
the fibre bundle were held in T-shaped platinum foil clips. The preparation
was mounted in a Perspex bath between a combined motor and force transducer
(Cambridge Technology, Inc., model 300B) and a fixed hook. The saline was
circulated continuously through the bath and was maintained at approximately
12°C. The muscle fibre bundle was electrically stimulated (Digitimer,
MultiStim System-D330) from end to end through the platinum clips. A program
written in TestPoint (Keithley Instruments, UK) controlled stimulation and
motor arm position and recorded force, length and stimulation. A DAS-1800AO
Series A/D board (Keithley Instruments, UK) was used.
The relationship between force and stimulus strength during tetanic stimulation was investigated in each fibre bundle to establish the supra-maximal stimulus strength. For red fibres, the stimulus strength was varied by changing both the duration (range 0.5-8 ms) and the voltage (0-6 V) of the stimulus pulses. Some fibre bundles produced two responses to stimulation. The first, faster response was produced by every fibre bundle and was the object of interest here. The later response was much slower to develop and could last well over a minute. Increasing stimulus strength by increasing pulse duration rather than voltage was usually effective at producing maximal fast responses, without eliciting a slow response also. The fibre bundle was discarded if a slow response was produced with all stimulus conditions. For white fibres, pulse duration was always brief (0.2 or 0.5 ms), and stimulus strength was varied by changing stimulus voltage. The length/tension relationship was investigated in each fibre bundle to identify the fibre length (L0) at which tetanic force was maximal.
At the end of the experiment, the fibre length at L0
was measured under a dissecting microscope. Red fibre bundles were stained
with Evans Blue, which does not cross intact surface membranes, to distinguish
intact from damaged fibres. Bundle were stained with 0.005% Evans Blue in
dogfish saline overnight, then rinsed in saline and transferred to 100%
alcohol for 20 min and then to 5% formaldehyde. The stained fibres were
removed and discarded, and the others were dried and weighed on a Cahn
microbalance. White fibre bundles were fixed in alcohol, and damaged fibres,
which can be identified without staining, and non-fibre material were removed
before the intact fibres were dried and weighed. The cross-sectional area
(CSA) was calculated as:
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The sarcomere length in red fibres at L0 was 2.32±0.02 µm (mean ± S.E.M., N=8 fibres from two fibre bundles from different fish) as measured by laser diffraction.
Red and white fibres: maximum isometric force
The maximum force, P0, during a tetanus at
L0 was measured in purely isometric experiments on 35
bundles of red fibres from 17 fish and 25 bundles of white fibres from 13
fish. The tetanus duration was sufficient for force to reach a plateau value
(of at least 0.4 s), indicating that the fibres had been stimulated long
enough to become fully active. The stimulation frequency was 29.5 Hz for the
red fibre bundles and within the range 25-35 Hz for the white fibre bundles;
these frequencies gave fused, maximal tetanic force. The stimulus pulse
duration was within the range 1.5-4 ms for red fibres (see above) and was 0.2
ms for white fibres.
V0 for red fibres
The slack test method (Edman,
1979) was used to determine the shortening velocity at zero load
(V0). The muscle preparation was released by different
distances (
L) from the plateau of an isometric tetanic
contraction at L0 (see
Fig. 4A). Regression lines were
fitted to the early part of force redevelopment, and the time interval
(
t) from the release to the start of force redevelopment was
measured (see Fig. 4C). The
slope of the regression line of
L versus
t
gives V0 (see Fig.
4D).
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Force/velocity experiments on red fibres
The muscle fibres were stimulated tetanically at approximately 29.5 Hz
every 5 min. For the experiments on both shortening and stretch, movement
started during the plateau of the tetanus (0.75 s after the beginning of
stimulation). In experiments on shortening, the muscle was released from
L0 by a step reduction in length (0.02-0.2 mm complete in
2 ms) followed by a constant-velocity ramp shortening (at 1-8 mm
s-1). The size of the step was adjusted so that the force remained
constant during the first part of the ramp shortening. The duration of tetanus
(1.8-3 s) was set so that stimulation continued after the end of shortening.
In experiments on stretch, the fibre bundle was stretched at a constant
velocity starting from a length less than L0; force was
measured when length reached L0. Control recordings were
made of passive force during movement without stimulation. The control
recording was subtracted from the total force recorded during stimulation to
give the active force.
Curve-fitting for shortening
The following equation was used to fit the force/velocity data for
shortening for each muscle bundle:
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Characteristics of the series elastic component in red fibre
bundles
The recordings of force during step-and-ramp shortening in force/velocity
experiments were also analyzed to give the stress/strain characteristics of
the series elastic component of the fibre bundles. The analysis was based on
A. V. Hill's (1938)
two-component model of muscle consisting of a contractile element, in which
force depends on the velocity of movement, and an elastic component in series
(SEC) with the contractile component. The force in the SEC is assumed to be
dependent on the length of the SEC and to be independent of velocity
(Curtin et al., 1998
). The step
size that is followed by a constant force during subsequent ramp shortening
was measured and plotted versus force during shortening to give the
strain versus stress relationship of the series elasticity.
Curve-fitting
The following relationship was fitted to the data points. Strain,
Y, is the sum of a constant, k, a linear component,
a(x), and a saturating component, b(x),
where x is stress (see Fig.
7A):
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Results |
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Our impression during dissection was that fibres on the surface of the bundle were easily damaged because they are of small diameter and held together tightly by connective tissue. The image in Fig. 1A gives some support for this idea in that the damaged fibres are on the surface or clustered near the surface; none is deep within the bundle. To test this further, we calculated the cross-sectional area that would be intact if all the damaged fibres were confined to a continuous layer of fibres at the surface of the bundle. For this calculation, we assumed that fibre diameter was uniform at 81.1 µm (based on the median value for intact fibres, see above). The total area of intact fibres and total area of damaged fibres were calculated for two conditions: one layer of damaged fibres and two layers of damaged fibres. Fig. 2 shows the area of the intact fibres expressed as a fraction of the total area (intact + damaged fibres) for a range of bundle sizes covering that used in the histology experiments. The observations from the histology experiments are also shown; they match the prediction based on one layer of damaged fibres much better than that for two layers of damaged fibres. These results support the idea that most damaged fibres are on the surface of the bundle and that the fraction of the total area that is therefore intact increases with total area in a non-linear manner.
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Isometric force and area of red and white fibre bundles
The relationship between maximum isometric force at L0
and the cross-sectional area (based on intact fibres) of red and white fibres
is shown in Fig. 3. For red
fibre bundles, the force per cross-sectional area (stress) was
142.4±10.3 kN m-2 (N=35). For white fibre bundles,
it was considerably greater, 289.2±8.4 kN m-2
(N=25).
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V0 for red fibre bundles
Fig. 4 shows sample
recordings from the slack test measurement of V0
(Edman, 1979). The recordings
of force after release are shown on an expanded time scale in
Fig. 4C with straight lines
fitted through the early part of force recovery. The fitted line was
extrapolated to the time axis to give a value for the time interval from the
step to the start of force recover. Fig.
4D shows these times versus the size of the release. The
slope is V0, the velocity of shortening under zero load,
and the intercept is the amount of shortening by the series elastic component
(SEC) during the step itself. For this bundle, V0 was
1.503 L0 s-1 and the SEC shortening was
0.053L0. The mean value of unloaded shortening velocity
from six muscle preparations was 1.693±0.108 L0
s-1 and SEC shortening was
0.067±0.006L0.
Force/velocity relationship for red fibre bundles
Shortening
Fig. 5A shows three
superimposed recordings of active force for different step sizes and
velocities of ramp shortening. Fig.
5B,C shows the force and length changes on an expanded time scale.
On each force recording, a horizontal line shows the value that was measured.
This is the force produced by the contractile element as it shortens at
constant velocity and by the SEC at the length to which it was released during
the step. The length of the SEC is constant when force is constant.
For all seven fibre bundles, the relationship between force and the
velocity of shortening was hyperbolic, and Hill's equation was fitted for each
fibre bundle as described in Materials and methods. The mean values of the
fitted parameters, expressed in various units, are included in
Table 3A.
Fig. 6A shows the results for
all the fibre bundles; each fibre bundle's force is expressed relative to its
own isometric force at L0, and velocity is expressed
relative to its own fitted Vmax. Note that the isometric
force, P/P0=1.0, is considerably less than
, the intercept of the fitted
line on the force axis. The line in Fig.
6A is the average of the fitted lines for the seven fibre
bundles.
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Fig. 6B shows the power during shortening, which was calculated as the product of force and the velocity values shown in Fig. 6A. The line in Fig. 6B is the average of the power for the seven fibre bundles, where power was calculated for each bundle from its fitted force/velocity curve. Table 1 lists the maximum power values found in this way.
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Stiffness and compliance of the series elasticity
Fig. 7A,B shows the
characteristics of the SEC of one fibre bundle. The lines were fitted through
the points as described in the Materials and methods section
(Fig. 7A). The total strain was
calculated as if it were due to two structures acting in series: a linear
compliance (red line) and another more compliant element with a limited strain
range (green line). The results are also plotted as stress versus
strain in Fig. 7B, showing the
typical relationship for a tendon-like structure; the stiffness is low at
small stresses and increases to a constant value at higher stresses. For the
example shown in Fig. 7, the
stiffness of the steep part of the curve was
26.2[(P/P0)/(
L/L0)]
[compliance
0.038(
L/L0)/(
P/P0)] and
the stiffness in the less steep part was
9.94[(
P/P0)/(
L/L0)]
[compliance 0.101
(
L/L0)/(
P/P0)]. The size
of step required to remove completely the strain produced by stress equal to
the isometric force was 0.050L0, which is the intercept of
the fitted line on the strain axis. Similar results were obtained for the
seven fibre bundles used in the force/velocity experiments, and the mean
values are given in Table
2.
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Stretch
In three of the experiments, the fibre bundle was stretched at a constant
velocity to investigate the negative velocity part of the force/velocity
relationship. Fig. 8A shows
three superimposed recordings for different velocities of stretch.
Fig. 8B,C shows the force and
length changes on an expanded time scale. On each force recording, a
horizontal line shows the value of force that was measured. The force/velocity
results are shown in Fig. 6A.
All the velocities were within the range where force is relatively independent
of velocity. The mean force was 1.519±0.032P0
(N=3 fibre bundles) during stretch at velocities in the range -0.28
to -0.63 Vmax. The power absorbed by the fibre bundles
during stretch is shown in Fig.
6C, where its magnitude can be compared with the power output
during shortening.
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Discussion |
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Are red fibres as strong as white fibres?
Table 3 shows the force per
cross-sectional area produced by white fibres from dogfish in experiments in
which only live fibres are included in the cross-sectional area. The value,
289.2±8.4 kN m-2 (N=25), is considerably greater
than that produced by intact red fibres, 142.4±10.3 kN m-2
(N=35).
At least part of the difference between white and red fibres of dogfish is
because a larger fraction of the cross-sectional area consists of myofibrils
in white fibres than in red fibres, as discussed by Altringham and Johnston
(1982). Bone et al.
(1986
; their
Table 1) found that
mitochondria occupy only 0.99±0.16% (mean ± S.E.M.) of the
volume of white fibres, but 21.55±3.39% (mean ± S.E.M.) of the
volume of red fibres in fully grown dogfish (as were used in the present
study). These results can be used to express the force relative to the
cross-sectional area not occupied by mitochondria. Using this ratio and the
isometric force values in Table
3 gives the following values: 292.1 kN m-2
(=289.2/0.99) for white fibres and 180.2 kN m-2 (=142.4/0.79) for
intact red fibres. Therefore, the evidence indicates that red fibres are not
as strong as white fibres, even after effects due to damaged fibres and the
difference in mitochondrial volume have been taken into account.
Force/velocity characteristics and power output for red fibres
Comparison with red fibres from other species of fish
Table 4 summarizes the
force/velocity characteristics and maximum power output of red fibres from
other species of fish. In all cases, the fish had been acclimated to the
temperature at which the acute experiments were carried out. There is a
threefold range in maximum power output (26.5-70.9 W kg-1), with
dogfish and carp (Cyprinus carpio) fin muscle producing very similar
low values and scup (Stenotomus chrysops L.) producing the highest.
The low power from dogfish and carp fin muscle reflects their low
Vmax. In addition, both muscle have a low value for
maximum power, approximately
0.11P0Vmax, which indicates that they
produce relatively little power given their capacity to produce isometric
force and their maximum velocity of shortening. In other words, their
force/velocity relationships are more curved than those of carp and scup
myotomal muscle. There is no clear pattern in the relationship between
isometric force and maximum power output.
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Comparison of red and white fibres from dogfish
The results reported here can be used to compare the performance of red and
white fibres from the same species of fish.
Fig. 9 and
Table 3 compare the fitted
force/velocity and power/velocity curves for red and white fibres from
dogfish. In Fig. 9A,B, force is
expressed as a fraction of isometric force and velocity as a fraction of the
maximum velocity of shortening to remove variations between these fibre types
that are due to differences in intrinsic isometric strength and the maximum
velocity of filament sliding. The curves for red and white fibres are very
similar. For both fibre types, the maximum power output is
0.111P0Vmax and is produced during
shortening at 0.30Vmax in red fibres and
0.31Vmax in white fibres. In terms of muscle function,
this means that the red and white fibres have equal capacities to produce
power within the limits set by the isometric force and maximum velocity of
shortening of each fibre type.
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Fig. 9C shows the force/velocity relationships for red and white fibres calculated from the mean values of the constants found by fitting the hyperbolic Hill equation to the data and the value of P0 (in kN m-2). The isometric force of red fibres is approximately 49 % of that for white fibres; the difference in maximum velocity of shortening is very similar, the value for red fibres being 48 % of that of white fibres. Fig. 9D shows the corresponding power/velocity relationships with power (in W kg-1). From the fitted curves, the maximum power output of the red fibres, 28.6 W kg-1, is only 23 % of that of the white fibres, 122.2 W kg-1. Clearly, both the red fibres' lower capacity to produce force and the slower intrinsic velocity of filament sliding contribute to making their power output less than that of white fibres (see Table 3A).
How do these differences in power output of red and white fibres compare
with those of mammalian fibres? The dogfish fibres are like mammalian fibre
types in that the maximum power output of mouse soleus (red) fibres,
23.6±1.8 W kg-1 (mean ± S.E.M., N=6), is
less than that of mouse extensor digitorum (white) fibres, 57.2±4.2 W
kg-1 (mean ± S.E.M., N=6)
(Barclay et al., 1993).
However, there is an important difference; whereas dogfish red and white fibre
power is the same when expressed relative to
P0Vmax (see above), in mouse the red
fibres' maximum power expressed relative to
P0Vmax is only 86 % of the
corresponding value for white fibres
(Barclay et al., 1993
). Thus,
the dogfish red fibres are more effective than mouse red fibres at translating
their intrinsic strength (P0) and intrinsic shortening
speed (Vmax) into power output.
Force/velocity relationship during stretch
We report here that red fibres produce a force of
1.519±0.017P0 (N=3) during isovelocity
stretch. This is very similar to the results of an earlier study of white
muscle fibres from dogfish, 1.569 ±0.031P0, (mean
± S.E.M., N=3; see Fig.
1D in Curtin et al.,
1998). The velocity ranges used in the two studies were different,
but it has been clearly established from many studies of muscle from other
species (for example, Aubert,
1956
; Lombardi and Piazzesi,
1990
) that the force during stretch is independent of velocity
except in the very low velocity range. Thus, it seems that red and white
fibres of dogfish are very similar both during stretch and during shortening,
two conditions in which there are important difference in the cross-bridge
cycle (Lombardi and Piazzesi,
1990
; Piazzesi and Lombardi,
1995
) and energy (Curtin and
Davies, 1973
) turnover.
Comparison of isovelocity shortening and sinusoidal movement
Although maximum power output during sinusoidal movement of red fibres has
been investigated previously (Curtin and
Woledge, 1993b), the value is not comparable with that reported
here. In these two studies, different methods were used to normalize for the
amount of live fibre in the preparation (maximum rate of energy output and
mass of live fibres) and, consequently, maximum power is reported in different
units. However, it is possible to compare the velocities of movement at which
power was maximal. In the experiments reported here on fully active red
fibres, maximum power was produced during isovelocity shortening at
0.3Vmax, which is equivalent to
0.544L0 s-1
(Table 3). This can be compared
with maximum power output during sinusoidal movement, which resembles that
during swimming. Power output has been measured at movement frequencies in the
range 0.61-1.67 Hz with a stimulus duty cycle of 0.3. The stimulus phase was
optimized to give maximum power at each movement frequency. Maximum power
output occurred at a movement frequency of 1.02±0.066 Hz
(N=9). At this frequency, the maximum instantaneous velocity was 0.31
L0 s-1 and the mean velocity was 0.147
L0 s-1; both are considerably lower than the
velocity (0.544 L0 s-1) giving maximum power
during isovelocity shortening of fully active red fibres. This difference is
probably due to the time required for the relatively slow rise in force and,
perhaps more importantly, the slow relaxation of force in the sinusoidal
experiments, where stimulation is intermittent. If relaxation of force is not
completed during the shortening part of the sinusoidal movement, this results
in negative power during stretch and a reduction in the net power for the
complete cycle of movement.
Stress/strain characteristics of the series elastic component
There is reasonable agreement between the two estimates of the size of
release required to reduce isometric force to zero. The slack test experiments
gave a mean value of 0.067±0.006L0 (N=6)
and the value from the force/velocity experiments
(Fig. 7) is
0.050±0.003L0 (N=7).
As stated in the Results, the shape of the stress/strain curve shown in
Fig. 7B is typical for tendon
(Ker et al., 1986;
Alexander, 1988
) in that
stiffness is low at small stresses and increases to a constant value at higher
stresses. The stiffness of the steep part of the curve is 4.09 MPa, which is
considerably less than that expected for tendon, approximately 1500 MPa
(Alexander, 1988
). However, a
large discrepancy is expected because our value uses the stress expressed as
force per cross-sectional area of the muscle fibres, an area that is much
larger than the cross-sectional area of the pieces of myosepta. It is also
relevant that, although the myosepta are the major determinant of the observed
stiffness, other structures in addition to the myosepta are likely to
contribute to the elastic characteristics we measure. These structures include
the thick and thin contractile filaments within the muscle fibres themselves,
which act in series with the cross-bridges to transmit force to the ends of
the fibres.
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Acknowledgments |
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References |
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