Fast muscle in squid (Loligo pealei): contractile properties of a specialized muscle fibre type
1 Department of Biology, CB 3280 Coker Hall, University of North Carolina,
Chapel Hill, NC 27599-3280, USA
2 Biological Structure and Function Section, Division of Biomedical
Sciences, Faculty of Medicine, Fleming Building, Imperial College, London SW7
2AZ, UK
*e-mail: billkier{at}bio.unc.edu
Accepted 19 April 2002
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Summary |
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Key words: cephalopod, muscle, cross-striated muscle, force/velocity relationship, Loligo pealei, muscle contraction, muscle specialization, obliquely striated muscle, prey capture, squid, thick filament length, tentacle
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Introduction |
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The muscles compared in this study include the transverse muscle mass of
the eight arms and the transverse muscle mass of the two tentacles
(Fig. 1). In the arms, this
muscle provides support for the relatively slow and forceful bending and
torsional movements used in swimming, prey handling and behavioural displays.
In the tentacles, the transverse muscle generates the force that causes the
extremely rapid elongation used by squid during the prey-capture strike
(Kier, 1982;
Kier and Smith, 1985
).
Previous work has shown that specialization of the tentacle fibres is not
reflected in differences in biochemistry of the contractile proteins. Sodium
dodecyl sulphate polyacrylamide gel electrophoresis of the proteins of the
myofilament lattice and peptide mapping of the myosin heavy chains revealed no
significant differences between tentacle and arm muscle
(Kier and Schachat, 1992
).
Instead, it is at the level of the ultrastructure that specialization is
observed (Fig. 2). The tentacle
fibres exhibit cross-striations with unusually short thick filaments and short
sarcomeres while the arm fibres show the typical cephalopod obliquely striated
pattern with much longer thick filaments
(Kier, 1985
). The remarkably
short myofilaments and sarcomeres of the tentacle fibres result in more
elements in series per unit length of fibre. Since shortening velocities of
elements in series are additive (Huxley
and Simmons, 1972
; Josephson,
1975
; van Leeuwen,
1991
), this ultrastructural specialization is hypothesized to
increase greatly the shortening velocity of the tentacles fibres relative to
the arm fibres (van Leeuwen and Kier,
1997
). The increase in shortening velocity comes at a price; since
shorter myofilaments have fewer cross-bridges operating in parallel per
half-sarcomere, the tentacle fibres are hypothesized to generate lower
tensions. The goal of the present study was to compare the contractile
properties of the two fibre types in order to test these hypotheses.
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Materials and methods |
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Transmission electron microscopy
Cross-sectional slices of the tentacle and arm transverse muscle were fixed
in 3.0% glutaraldehyde, 0.065 mol l-1 phosphate buffer, 0.5% tannic
acid and 6% sucrose for 6-8 h at 4°C. Following fixation, small blocks of
tissue, approximately 1 mmx1 mmx2 mm were cut from the slabs,
rinsed overnight in chilled 0.065 mol l-1 phosphate buffer and
postfixed for 40 min at 4°C in a 1:1 mixture of 2% osmium tetroxide and 2%
potassium ferrocyanide. The blocks were rinsed in chilled 0.065 mol
l-1 cacodylate buffer for 15 min, and then both dehydrated and
cleared in a graded series of acetone. Acetone was used in place of ethanol
and propylene oxide to minimize dimensional changes in the myofilaments
(Page and Huxley, 1963). The
tissue blocks were embedded in epoxy resin (Epox 812, Ernest R. Fullam,
Latham, NY, USA). During sectioning, special attention was paid to alignment
of the blocks to obtain precisely longitudinal sections of the muscle fibres.
This was achieved through trial and error by examining 0.5-1.0 µm sections
in the light microscope and reorienting the block until individual fibres in
the area of interest remained in the section plane. The block was then trimmed
for ultramicrotomy of the area of interest and sectioned with a diamond knife.
Sections of silver to gold interference colour were stained with saturated
aqueous uranyl acetate and Reynolds lead citrate
(Reynolds, 1963
) and
photographed in a Zeiss EM 10CA electron microscope. Thick filament lengths
were measured on micrographs using morphometrics software.
Muscle mechanics
Small bundles of fibres (1-2 mm diameter and 5-6 mm long) were dissected
from the cross-sectional slices in standard ASW at 4°C while viewing the
slices under a dissecting microscope with transmitted light illumination
(Fig. 1). The dominant axis of
the transverse muscle fibres in a slice was visible using this approach, and
this helped to ensure that the edges of the fibre bundle preparation were cut
parallel to the fibres. A T-shaped aluminium foil clip was attached to each
end of the preparation by applying a small amount of cyanoacrylate adhesive to
the foil clip and then bending the tabs over the ends of the preparation. The
foil clips were aligned and attached in such a way that only transverse muscle
fibres extended between the clips on each end of the preparation
(Fig. 1). A hole in each foil
clip provided the means to attach one end of the preparation to a hook on a
force transducer (AE801 element; SensorOne Technologies Corp., Sausalito, CA,
USA) and the other to a hook on a servomotor arm (model 300B dual-mode lever
arm system; Aurora Scientific, Aurora, Canada). The servomotor controlled the
length and movement of the preparation during the experiments. The preparation
was continuously superfused with aerated standard ASW at 19±0.5°C.
The preparation was stimulated with rectangular current pulses (model DS7A;
Digitimer Ltd, UK) via large platinum plate electrodes. Stimulation,
servomotor lever position and force were controlled and recorded using a
ViewDac (Keithley, UK) data-acquisition and control software sequence and an
A/D board (DAS-1602 Metrabyte, Keithley, UK).
Isometric contractions
The preparation length was increased until a transient passive force was
observed. The stimulus current strength/twitch response relationship was then
recorded using 0.2ms stimuli spaced at intervals of 120s. Control stimulations
of constant current amplitude were used to monitor potential decline of twitch
force during the trial. At the end of the trial, the stimulus current was
adjusted to a level 10-20% higher than that required to elicit the maximum
twitch force.
The length/force relationship of the preparation was investigated using twitches in the tentacle preparations and both twitch and tetanic stimulation (50 Hz, 100ms) in the arm preparations. The length of the preparation was adjusted to that giving peak twitch or tetanic force (L0). The stimulus frequency/force relationship was determined using 200ms tetani at 5-200 Hz with 300s between tetani.
Force/velocity relationship
For the tentacle preparations, the force/velocity relationship was
investigated using isotonic shortening during twitch. The preparation length
was adjusted to that giving peak twitch force as described above. Isotonic
shortening was produced with the servomotor operating in its force-clamp mode.
The velocity of shortening was measured from the recordings of servomotor arm
position. Occasional isometric control stimulations were used to monitor force
decline, and the experiment was terminated if the force decreased by more than
10%. Similar procedures were employed for the arm preparations except that the
small twitch:tetanus ratio observed for these muscle fibres meant that the
twitch force was typically too low for effective force-clamping by the
servomotor. The force/velocity relationship of the arm preparations was
therefore investigated using isotonic shortening during brief tetani (50Hz,
100ms). Perhaps as a result of using tetani rather than twitches, fewer
isotonic shortening trials were possible on a given arm preparation compared
with the tentacle preparations before a decrease in isometric force
occurred.
Curve fitting
Hill's equation (Hill,
1938) was fitted to the force/velocity data using the Solver
function of Microsoft Excel to minimize the sum of the squares of the
deviations of predicted velocity from observed velocity. We used the following
form of Hill's equation:
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Physiological cross section
Upon completion of the experiments, the preparation was tranferred to a
small Sylgard dish and pinned at L0. When a
photomicrograph had been taken (to monitor potential dimensional changes), the
preparation was fixed as described above. The foil clips were cut off, and the
preparation was dehydrated to 95% ethanol and infiltrated and embedded in
glycol methacrylate plastic (JB4, Polysciences, Fort Washington, PA, USA).
Glycol methacrylate embedding was employed because this embedding medium
causes minimal distortion and shrinkage during infiltration and
polymerization. Transverse sections were cut with a glass knife at four evenly
spaced locations along the length of the preparation, and the aggregate area
of cross-sectioned muscle fibre bundles was determined from camera
lucida tracings using morphometrics software (i.e. transverse muscle
fibres oriented in the plane of the section or obviously oblique to the plane
of the section were excluded since these fibres do not contribute to
shortening of the preparation). The specific force was expressed as mN
mm-2 cross-sectional area of the tissue for the transverse section
of minimum area.
Values are presented as means ± S.D.
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Results |
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Relationship between force and velocity of shortening
The relationship between force and velocity was investigated for nine
tentacle and eight arm fibre bundle preparations. Recordings of force and
length from a single tentacle preparation shortening in twitch are shown in
Fig. 3 for several levels of
force-clamp and during an isometric contraction. The force and velocity were
measured as a mean value for a period at the beginning of shortening when the
force and velocity had stabilized. Identical procedures were used for the arm
preparations except that brief (100ms, 50Hz) tetani were employed (see
Materials and methods).
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Force/velocity curves for one tentacle and one arm preparation are shown in
Fig. 4, with force expressed
relative to the isometric force during twitch for the tentacle and relative to
the isometric force during tetanus for the arm. A remarkable difference in the
force/velocity relationship of the two muscle types is observed. In
particular, at 19 °C, the maximum velocity of shortening of the transverse
tentacle muscle was estimated to be as high as 17.2 L0
s-1 (mean ± S.D., 15.4±1.0 L0
s-1, N=9), while the maximum velocity of shortening of the
arm transverse muscle was 1.8 L0 s-1 (mean
± S.D., 1.5±0.2 L0 s-1,
N=8). Table 1 lists
the values of the fitted parameters for Hill's
(1938) equation for the
tentacle and arm preparations.
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Isometric contractile properties
Fig. 5 shows a summary of
the results from investigations of the length/active force relationship for
twitch stimulation of the tentacle fibre bundle preparations (N=10)
and twitch stimulation (N=5) and tetanic stimulation (N=6)
of the arm fibre bundle preparations. No difference was evident in the
length/force relationship between the two fibre types. In addition, no
difference was evident in the length/force relationship during tetanic and
twitch stimulation of the arm fibres. Fig.
6 shows the length/passive force relationship and the
length/active force relationship for an arm preparation and a tentacle
preparation. High levels of resting tension were observed in both the arm and
the tentacle preparations when extended beyond optimal length. Indeed, we were
unable to explore the length/force relationship in this region because of the
damage that occurs to the fibres at these lengths. Near-maximal force is
produced over a range of lengths. The ends of this plateau region are smooth
curves, suggesting heterogeneity similar to that described by Edman and
Reggiani (1987).
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Relationship between stimulus frequency and force
The relationship between stimulus frequency and force was investigated
using 200 ms tetani over a range of frequencies up to 200 Hz. The fusion
frequency was between approximately 40 and 80 Hz for the tentacle and arm
fibres. Multiple stimulation above the fusion frequency produced graded tetani
in both the arm and the tentacle preparations
(Fig. 7).
Fig. 8 shows the relationship
between stimulus frequency and force for fibre bundle preparations of arm
transverse muscle and tentacle transverse muscle. A striking difference in the
response to electrical stimulation in the two fibre types is evident. In
particular, the ratio of twitch force to peak tetanic force (the
twitch:tetanus ratio) was 0.66±0.06 (N=10) in the tentacle
fibres, but only 0.03±0.02 (N=10) in the arm fibres. For the
tentacle fibres, the mean peak tetanic tension of 131±56 mN
mm-2 cross-sectional area (N=12) was observed at a
stimulus frequency of 80 Hz. For the arm fibres, the mean peak tetanic tension
of 468±91 mN mm-2 cross-sectional area (N=5) was
observed at a stimulus frequency of 160 Hz. As can be seen in
Fig. 7B, the force of the arm
preparations was still rising at the end of the 200 ms tetani used in our
experiments. Although we did not investigate the increase in force from longer
tetani in detail, in three arm preparations we used 300, 500 and 700 ms
tetani. The force did not increase after 500 ms of stimulation. The peak force
with 500 ms of stimulation was 28.5±0.5 % higher than with 200 ms of
stimulation. The isometric mechanical properties of the arm and tentacle fibre
bundle preparations are summarized in Table
2.
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Discussion |
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Thick filament length and its implication for peak tension
While the effect of reducing thick filament length is an increase in the
maximum velocity of shortening of the tentacle transverse muscle fibres, this
change in dimension is likely to reduce the tension (stress) produced by these
fibres. This is because shorter thick filaments have fewer myosin
cross-bridges operating in parallel per half-sarcomere. A precise prediction
of the magnitude of the difference in force is not possible at this time
because we need additional information on other aspects of myofilament
structure, including for instance, cross-bridge arrangement, thick:thin
filament ratio, etc. Nevertheless, the results of the isometric experiments
were consistent with the prediction of reduced tension in the tentacle fibres
(approximately 130 mN mm-2) relative to the arm fibres
(approximately 470 mN mm-2). In addition, as described above, the
value of peak tetanic tension reported here for the arm fibres during a 200 ms
tetanus is lower by approximately 28.5% than the peak tetanic tension recorded
with 500 ms tetani. By taking into account this effect of longer stimulation,
we estimate the maximum tension in the arm muscle fibres to be approximately
600 mN mm-2.
Note that the values reported here are likely to be underestimates of the peak tension for both the arm and tentacle muscle because fibres on the cut surfaces of the preparations are likely to have been damaged and thus will not contribute to the force, even though they are included in the measurement of physiological cross-sectional area. Unfortunately, the results of experiments designed to label the damaged fibres of the preparations with horseradish peroxidase or Lucifer Yellow were inconclusive and, thus, we are uncertain of the proportion of damaged fibres on the surface of the preparations. In addition, the estimation of functional cross-sectional area for the bundle preparations is complicated by the more-or-less orthogonal arrangement of the transverse muscle fibres. It was straightforward to recognize and exclude fibres oriented parallel to the section plane (and thus perpendicular to the long axis of the preparation) or fibres aligned at a relatively large angle to the long axis of the preparation. It was more difficult, however, to recognize and exclude fibres oriented at a relatively small angle to the long axis of the preparation. We therefore view the values of peak tension reported here as estimates only and hope that single fibre techniques will be developed in order to provide a definitive measure of tension in these cells.
The estimates of peak tension for the cross-striated tentacle fibres and
the obliquely striated arm fibres are also of interest in the context of the
values of maximum tension reported previously for vertebrate cross-striated
fibres and cephalopod obliquely striated mantle muscle fibres. Curtin and
Woledge (1988) reported a peak
tetanic tension of 255 mN mm-2 for white muscle fibre bundles from
dogfish Scyliorhinus canicula, and Curtin and Edman
(1994
) measured a peak tension
of 287 mN mm-2 for single fast-twitch fibres of the frog Rana
temporaria. The thick filament length of 1.58 µm of vertebrate
cross-striated fibres is relatively invariant
(Offer, 1987
). As described
above, the thick filament length of the cross-striated squid tentacle fibres
was measured to be half as long (0.81 µm) and, thus, the relative tension
of the vertebrate cross-striated fibres and the cross-striated squid tentacle
fibres is also consistent with the difference in thick filament
dimensions.
Milligan et al. (1997)
estimated that the obliquely striated fibres from the mantle of the squid
Alloteuthis subulata (the fibres sampled were from the central,
mitochondria-poor fibres) produce a peak isometric tension of 400 mN
mm-2. We estimate above that the obliquely striated squid arm
fibres from L. pealei may generate 600 mN mm-2.
Unfortunately, measurements of thick filament length from squid mantle muscle
have not yet been reported (Milligan et
al., 1997
). A comparison of peak tension from the arm and the
mantle muscle suggests, however, that the thick filaments of the mantle muscle
are likely to be shorter than those of the arm muscle. It is of interest in
this regard to compare the maximum velocity of shortening of the two obliquely
striated fibre types. Milligan et al.
(1997
) estimate the maximum
velocity of shortening of the squid mantle fibres to be 2.4
L0 s-1 at 11°C. As described above, we
estimate the maximum velocity of shortening of the arm fibres to be 1.5
L0 s-1 at 19°C. Thus, the relative
shortening velocity of the mantle fibres and the arm fibres is consistent with
the prediction of shorter thick filaments in the mantle muscle. Note that,
although the Q10 of cephalopod muscle has not yet been estimated,
it is likely that the maximum velocity of shortening of the mantle fibres
would be even higher if measured at the same temperature as for the arm
fibres.
Functional significance of oblique striation
It is apparent from Fig. 5
that the length/tension relationships of the cross-striated tentacle fibres
and the obliquely striated arm fibres are quite similar within the range of
lengths that could be investigated and are likely to be functionally relevant.
Previous analyses of the structure and function of obliquely striated muscle
fibres suggested that the oblique striation pattern may be important in
allowing a greater range of elongation and shortening than that observed in
cross-striated muscle fibres (Hidaka et
al., 1969; Miller,
1975
). In particular, a superelongation mechanism of `changing
partners' between thick and thin filaments at extreme elongation has been
proposed (Lanzavecchia, 1977
,
1981
;
Lanzavecchia and Arcidiacono,
1981
). We found, however, high levels of resting tension as both
the tentacle and arm fibre bundles were extended beyond optimal length (see
Fig. 6). We were not able to
investigate the length/tension relationship at lengths beyond optimal length
because of the damage that typically occurred to the preparation when
elongated to this extent. Since the preparations used in our study were
bundles of fibres, it is likely that the passive mechanical properties of the
cells are derived in large part from connective tissues surrounding the
fibres. The mechanical properties we measured therefore probably reflect the
properties of the muscle tissue in a whole squid arm and imply that
superelongation is not relevant for the obliquely striated muscle fibres of
the arms. Milligan et al.
(1997
) also found high levels
of resting tension in squid mantle muscle fibres. Thus, the functional
significance of oblique striation for muscle function in squid is unclear.
Constancy of thick filament length as a function of position in the
tentacle
Van Leeuwen and Kier (1997)
proposed a forward dynamics model for the elongation of the tentacular stalk
during prey capture. The model accurately predicts the changing geometry of
the tentacle, the pressure and stress distribution in the tentacle and the
velocity and kinetic energy distribution on the basis of a comparison with
kinematic measurements from high-speed films of prey capture
(Kier and van Leeuwen, 1997
).
In addition, the model demonstrates that the short thick filaments and
sarcomeres of the transverse muscle of the tentacles are necessary for the
observed performance. If thick filament lengths typical of vertebrate
cross-striated muscle sarcomeres were present, a significant reduction in
performance during the strike would result. Further, an analysis employing the
model was used to predict optimal thick filament lengths for the
cross-striated tentacle muscle in two cases: the first case allowed thick
filament length to vary as a function of position from base to tip in the
tentacle; the second case required that thick filament length be constant from
base to tip. In the first case, the model predicts that, to maximize the peak
velocity of the tip of the tentacle during the strike, the thick filaments of
the transverse tentacle muscle should be longer at the base of the tentacle
and shorter at the tip (0.97 µm at the base and 0.50 µm at the tip for
Loligo pealei of similar size to those analyzed here). Longer thick
filaments are predicted at the base of the tentacle because of higher dynamic
loading in this region. (Fibres at the base of the tentacle must accelerate a
larger mass than those at the tip; see Van
Leeuwen and Kier, 1997
.) In the second optimization with
constant-length thick filaments, the model predicts that, to optimize the peak
velocity of the tentacular stalk, the thick filaments should be 0.74 µm
long. The peak velocity of the tentacular strike in the case of constant thick
filament length was predicted to be 99 % of the peak velocity in the case of
variable thick filament lengths (Van
Leeuwen and Kier, 1997
).
The measurements of the thick filament length reported above showed no evidence of differences in thick filament length as a function position in the tentacle, so the situation modelled in the first case of the optimization does not occur in Loligo pealei. Instead, the thick filaments are constant in length as a function of position in the tentacular stalk. It is notable that the thick filament length measured in the present study (0.81 µm) is within 10 % of the value of (0.74 µm) predicted by the theoretical forward dynamics model.
Excitation/contraction coupling
The isometric contraction experiments revealed a striking difference in the
response to electrical stimulation of the two fibre types (see Figs
7,
8). Of particular interest was
the observation that the twitch/tetanus ratio was 0.66 in the tentacle fibres
but only 0.03 in the arm fibres. This difference in response is important in
the context of how these two muscle fibre types function in the animal. The
high speed and acceleration of the tentacles during the prey-capture strike
require a simultaneous and essentially all-or-none contraction of the
transverse muscle. The force produced by the transverse muscle of the arms,
however, must be precisely modulated to provide the support required for the
bending and manipulative movements used for prey handling, behavioural
displays and steering movements while swimming
(Kier and Smith, 1985). The
structural and biochemical differences responsible for this dramatic
difference in response to electrical stimulation have not yet been explored in
detail for these two fibre types. Although the fast-contracting tentacle
fibres include a more extensive sarcoplasmic reticulum than the arm fibres,
additional work on the physiology of the cell membrane and
excitation/contraction coupling mechanisms is needed (see, for example,
Rogers et al., 1997
).
Concluding remarks
Our measurements of the contractile properties of the specialized
cross-striated tentacle fibres of the squid and of the obliquely striated
fibres from the transverse muscle of the arms are consistent with predictions
based on previous ultrastructural and biochemical analyses of the two fibre
types. In the absence of differences in the biochemistry of the proteins of
the myofilament lattice of the two muscle fibre types
(Kier and Schachat, 1992),
specialization of the tentacle transverse muscle fibres for fast contraction
was predicted to be due primarily to shorter thick filaments (Kier,
1985
,
1991
). Since the thick
filament length of the transverse muscle fibres of the tentacles was found to
be one-tenth of that of the transverse muscle fibres of the arm, the velocity
of the tentacle fibres was predicted to be ten times that of the arm fibres,
and our measurements are consistent with this prediction. In addition, because
of the shorter thick filaments of the tentacle fibres, the peak tension of
these cells was predicted to be lower than that of the arm fibres. Our
measurements are also consistent with this prediction.
It appears that modulation of the performance of muscle fibres in the arms
and tentacles of squid has occurred through variation in myofilament and
sarcomere length in the absence of variation in biochemistry. This mechanism
of specialization is thus in stark contrast to that observed in vertebrate
muscle, in which myofilament dimensions are constant but a great diversity of
myofilament protein isoforms exists. It is unclear, however, whether the
similarity in biochemistry observed in the arms and tentacles is an example of
a general phenomenon in cephalopod muscle or whether it reflects the shared
developmental and evolutionary history of the arms and tentacles. Additional
studies of the biochemistry, ultrastructure and mechanics of a wider diversity
of cephalopod muscle are required to determine whether the mechanism of
specialization observed in the arms and tentacles is general for cephalopod
molluscs. Nevertheless, the results presented here, in conjunction with
previous studies of arthropod muscle
(Cochrane et al., 1972;
Costello and Govind, 1983
;
Günzel et al., 1993
;
Gronenberg et al., 1997
;
Jahromi and Atwood, 1969
;
Marden, 2000
; Marden et al.,
1998
,
1999
,
2001
;
Stephens, et al., 1984
;
Stokes et al., 1975
),
demonstrate a greater diversity of mechanisms of specialization of muscle than
is generally recognized.
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Acknowledgments |
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References |
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