Fast-start muscle dynamics in the rainbow trout Oncorhynchus mykiss: phase relationship of white muscle shortening and body curvature
1 Marine Biology Research Division, Scripps Institution of Oceanography, La
Jolla, CA 92093-0204, USA
2 Department of Zoology, University of British Columbia, 6270 University
Boulevard, Vancouver, British Columbia V6T 1Z4, Canada
* Author for correspondence (e-mail: jgoldbog{at}ucsd.edu)
Accepted 6 December 2004
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Summary |
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Key words: trout, muscle strain, kinematics, Oncorhynchus mykiss, fast-start
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Introduction |
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The Mauthner cells, a set of reticulospinal neurons that span the length of
the spinal cord, typically mediate fast-starts
(Eaton et al., 1991). Neural
activation causes a nearly simultaneous impulse of muscle activity along the
length of one side of the body (Jayne and
Lauder, 1993
; Wakeling and
Johnston, 1999b
; Ellerby and
Altringham, 2001
; Tytell and
Lauder, 2002
) that results in a concomitant onset of muscle strain
at all axial locations (Ellerby and
Altringham, 2001
). However, some basal actinopterygians exhibit
strong muscle activation on both sides of the body
(Westneat et al., 1998
;
Tytell and Lauder, 2002
).
Despite the simultaneous onset of muscle activity and muscle strain, actual
body bending occurs as a posteriorly traveling wave because of the
morphologically derived axial variation in muscle torque and hydrodynamic
resistance (Wakeling and Johnston,
1999b
). In addition, the faster shortening velocities of the
rostral myotomes function to generate stress more rapidly than at more
posterior locations (James et al.,
1998
; Johnston et al.,
1993
,
1995
;
Wardle et al., 1989
;
Altringham et al., 1993
;
Davies et al., 1995
;
Wardle, 1985
). Consequently,
the fast myotomal muscle produces a net bending moment on the spine, curving
the body to the ipsilateral (concave) side of the body that signifies the
completion of stage 1 in most fast-starts. Stage 2 is associated with a wave
of muscle activity generated on the contralateral (convex) side of the body
(Jayne and Lauder, 1993
;
Wakeling and Johnston, 1999b
;
Hale et al., 2002
), producing
a propulsive flexion and a rapid acceleration away from the stimulus.
Although the muscle activity during fast-starts is relatively well
understood, there are few detailed studies that focus on the changes in muscle
length that produce these rapid bending and propulsive moments. Recent
investigations regarding the muscle dynamics of steady swimming have provided
evidence that the wave of muscle shortening traveling along the body is in
phase with changes in local midline curvature, as in a homogeneous bending
beam (Coughlin et al., 1996;
Shadwick et al., 1998
;
Katz et al., 1999
;
Donley and Shadwick, 2003
).
These results were qualitatively consistent, at an unspecified axial location,
in common carp fast-starts (Wakeling and
Johnston, 1999a
). However, studies involving the deep red muscle
of steady swimming in the shortfin mako shark
(Donley et al., 2004
) and
tunas (Shadwick et al., 1999
;
Katz et al., 2001
) have shown
a temporal decoupling of muscle length and backbone kinematics, such that
muscle shortening in the mid-body region is in phase with curvature at more
posterior locations. The first measurement of muscle length changes during
fish fast-starts (Covell et al.,
1991
) led to a similar conclusion, but the analysis highlighted
muscle dynamics only in relation to total body curvature. Thus, it is not
clear how white muscle shortens to create body bending during maximal
performance.
Since the pioneering study by Covell et al.
(1991), substantial advances
have been made regarding the kinematic analysis of fish locomotion,
particularly aided by digital techniques
(Jayne and Lauder, 1995
;
Katz and Shadwick, 1998
;
Walker, 1998
). In the present
study, we revisit the phase relationship between muscle strain and midline
curvature in the fast-start behavior of Oncorhynchus mykiss to
address the incongruence in our understanding of fish swimming mechanics. We
used sonomicrometry to measure shortening in the lateral myotomal fast fibers
during induced escape responses. Simultaneous high-speed video analysis was
used to calculate local midline curvature and estimate the strain experienced
during the observed body deformation. We compare these data to examine the
phase relationship between local muscle shortening and midline curvature.
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Materials and methods |
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The experimental tank was filled to a depth of 30 cm such that the maneuver was largely within the horizontal plane. Fast-starts were induced from rest by jabbing a meter stick vertically into the experimental tank towards the fish. Over the course of the study, several escape responses were recorded for each individual, which ranged from very strong responses where the head often touched the tail to very weak responses.
Implantation of piezoelectric crystals for in vivo measurement of white muscle strain required that the individual be anesthetized. In preparation for surgery, each fish was exposed to tricane methanesulfonate (MS222; Sigma Chemical Co., St Louis, MO, USA) (0.0001 kg l-1 buffered with Tris HCl) to induce a short period of anesthesia (<30 min). The gills were continuously perfused with anesthetic during surgery and subsequently flushed with fresh water to facilitate recovery. Fish were allowed to recover in isolation chambers for at least 24 h before the experiment was performed.
Sonomicrometry and muscle strain
Two pairs of 1.0 mm diameter piezoelectric crystals were inserted into the
deep, interior white (epaxial lateral) muscle at two axial locations
(0.4L and 0.7L) along one side of each fish. Each pair of
crystals (1 cm apart and parallel to the longitudinal axis of the animal) was
oriented approximately 1020 mm dorsal of the horizontal septum and
49 mm lateral of the spine (approximately centered in the middle of
epaxial cones). Wires leading to the crystals were bundled and sutured to the
skin. Axial locations were highlighted by reflective markers that were glued
to the dorsal surface of the fish (see Fig.
1). Sonometric data were obtained with a digital sonomicrometer at
250 Hz during induced fast-start maneuvers. Muscle length traces allowed for
the calculation of muscle strain (S):
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Kinematic analysis, curvature and predicted strain
Dorsal views of elicited escape responses were captured with a high-speed
video camera (Redlake; San Diego, Ca, USA) at a filming frequency of 250 Hz.
The dorsalventral projected outline of the fish was digitized on each
frame using NIH Image (National Institutes of Health,
http://rsb.info.nih.gov/nih-image).
These outlines were used to calculate a dorsal midline consisting of 51
equidistant coordinates that characterize 50 equally spaced segments (see
Jayne and Lauder, 1995).
Midline coordinates allowed for local curvature (K), the inverse of
the radius of curvature, to be estimated at axial positions corresponding to
each crystal position with QuicKurve
(Walker, 1998
), using a
quintic spline function (M=3) and a smoothing parameter of 25 (MD=1).
Maximum curvature was selected as the maximum curvature experienced at a
particular location along the body over the course of the fast-start maneuver.
Predicted strain, or estimated strain (
K), was calculated as
the product of local curvature (K) and the lateral distance from the
backbone to the piezoelectric crystals (h), just as in a simple beam
(see Rome et al., 1988
;
Van Leeuwen et al., 1990
):
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Phase shift
The sonometric and video data were synchronized by a trigger that produced
a voltage spike on a separate data channel and simultaneously stopped
recording video frames. The temporal relationship between measured strain and
midline curvature (i.e. estimated strain) was quantified using a
cross-correlation analysis. This method involves the calculation of the
coefficient of determination, which describes how closely the measured values
correspond to the estimated values. Profiles were then shifted with respect to
one another to find the time change required to maximize the coefficient of
determination.
Wave velocity
The velocities at which strain and curvature waves propagated along the
body were calculated by dividing the distance between the posterior and
anterior sample sites by the travel time of the corresponding wave minima
(muscle shortening and concave curvature) or maxima (muscle lengthening and
convex curvature).
Turning rate
Turning rate of the head during fast-starts were calculated following the
methods of Domenici et al.
(2004). An angle was formed
between the head, a point on the midline at 0.33L and a reference
axis. Turning rates were calculated by how this angle changed over time.
Total body curvature in relation to strain
For the purposes of analyzing the phase relationship between midline
curvature and muscle shortening under different degrees of strain, the average
strain between the anterior and posterior position was calculated for each
response. The average of this value for all individuals and trials, 12.3%, was
set as the arbitrary boundary between low strain (<12.3%) and high strain
(>12.3%) events. We emphasize that this categorization does not suggest
that O. mykiss exhibits two distinct behavioral response types.
Rainbow trout probably exhibit a continuum of escape responses from weak to
strong, but quantification of this would require a comprehensive behavioral
study. The division used in this study allows us to investigate white muscle
dynamics under different mechanical conditions.
To estimate total body curvature, the minimal distance between the head and
caudal peduncle was recorded over the course of the maneuver (see
Brainerd and Patek, 1998).
Therefore, smaller distances reflected larger total body curvatures. This
parameter is meant to be an index of total body curvature not an absolute
quantity.
Statistics
All statistical analyses were performed using Minitab (version 13; Minitab
Inc., State College, PA, USA) with a significance level of P=0.05.
All parameters failed the Anderson-Darling test for normality
(P<). Thus, the following non-parametric statistical
analyses were warranted.
A Wilcoxon signed rank test was performed to determine if the phase shift between measured strain and estimated strain was different than zero. A P-value <0.05 accepts the hypothesis that the compared values are significantly different than zero. To account for a combined error of one frame for the sonometric and kinematic data, the Wilcoxon point estimate was adjusted to 0.004 s.
A Mann-Whitney U-test was used to test whether the kinematic parameters between high and low strain events were significantly different. A P-value <0.05 accepts the hypothesis that the two parameters are significantly different.
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Results |
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A representative example of an escape response under high and low strain
conditions is shown in Fig. 1.
The midline kinematics over the course of each response type is shown in
Fig. 2. Qualitatively, the
weaker response is similar to the `L-start without a turn' pattern
and the stronger response type is similar to the `L-start
acceleration turn' pattern described previously for the rainbow trout,
Salmo gairdneri (Webb,
1976). For lack of muscle activation data during these
fast-starts, we defined kinematic stages of fast-starts by a change in turning
direction (see Kasapi et al.,
1993
). Low strain responses exhibited a much smaller ipsilateral
bend during stage 1, whereas high strain responses usually involved much
tighter c-shape profiles at the end of stage 1 (Figs
1,
2,
3).
|
|
The calculation of curvature along the backbone revealed a profile that describes the maximum curvature experienced over the course of the maneuver (Fig. 4). Maximum curvature increases sharply between approximately 0.1L and 0.3L and decreases between 0.9L and 1.0L, both of which are a consequence of an anatomical limitation to bending at the extreme ends of the fish. For example, the head lacks vertebrae and the extreme end of the tail is completely devoid of muscle. In the central region of the body (0.3L to 0.9L) maximum curvature generally increases, but includes local minima. It should be noted that calculations of curvature assumed that the long axis of all cross sections of the fish remained vertically orientated. Thus, escape responses may have involved roll moments (see Fig. 1B), which may cause curvature to be slightly under- or over-estimated depending on the direction of rotation.
|
Measured and predicted strain
Measured strain from sonomicrometry and predicted strain from midline
curvature recorded for a high and low strain event are shown in
Fig. 5. Escape responses
occurred with piezoelectric crystals implanted either on the ipsilateral or
contralateral side of the escape response. Thus, our analysis involved either
muscle lengthening (one of nine strong responses, four of 11 weak responses)
or muscle shortening. Since the crystals were too often (eight of nine
responses) on the convex side of the body during strong responses, passive
muscle lengthening in relation to midline curvature could not be analyzed
under high strain.
|
Several kinematic parameters for high and low strain events are listed in Table 1. For all escape responses, peak muscle strains measured by sonomicrometry ranged from 4.620.6% at 0.4L and 5.331.1% at 0.7L, while strain calculated from curvature and chordwise crystal position ranged from 9.713.1% at 0.4L and 7.318.1% at 0.7L (see Table 1 for means and standard deviations). Measured strain was significantly higher for strong responses at both axial positions, whereas predicted strain was not significantly different between responses for either position. The difference between measured and predicted strain was only significantly higher for high strain events at the posterior position. The comparison between measured and estimated strain (including peak, initial and final strain) for both axial positions is shown in Fig. 6. The slope of the regression line through the data is similar to unity, which suggests O. mykiss fast-starts can be generally described as a simple bending beam.
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The onset of muscle length change at both the anterior and posterior locations occurred simultaneously (Fig. 5), but there was a time delay to reach minimum or maximum length yielding an average strain wave speed of 20.6±19.8 L s-1 for all trials. Strain wave velocities were significantly higher for high strain events while curvature wave velocities remained constant (Table 1). Accordingly, changes in midline curvature often lagged behind the onset of muscle shortening (Fig. 5B).
Phase shift
Comparison of measured and predicted strain profiles shows a clear temporal
relationship (Fig. 5), but this
association was not always perfectly in phase. In cases where this phase shift
was not zero, measured strain always preceded curvature. The average phase
shift for the anterior position was 0.006±0.005 s and was significantly
different from zero (Wilcoxon Signed Rank Test, P=0.033). The average
phase shift for the posterior position was 0.012±0.011 s and was
significantly different from zero (Wilcoxon Signed Rank Test,
P=0.002).
The escape response under high strain in Fig. 5B shows a large temporal decoupling between measured and predicted strain at the posterior location. The effect of high strain on phase shift is shown in Fig. 7. High strain significantly increases the phase shift at the posterior location to an average of 0.021±0.009 s (Mann-Whitney U-Test, P<0.005). High strain also affects the magnitude of the measured strain experienced between the anterior and posterior positions such that they are negatively correlated (Fig. 8). In contrast, conditions of high strain fail to affect the anterior phase shift (Mann-Whitney U-Test, P=0.784, Fig. 7). Stronger escape responses appear to be a consequence of rapid strain wave velocities (Table 1), which in effect cause muscle length minima at the anterior and posterior locations to occur closer in time while hydrodynamic resistance causes curvature to lag.
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Discussion |
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Our analysis modifies these conclusions by demonstrating a simultaneous
onset of muscle shortening, as was found in O. mykiss fast-starts
(Ellerby and Altringham, 2001)
and changes in local body curvature. Our results also show a temporal
decoupling of minimum muscle length at different sites along the body,
agreeing with Ellerby and Altringham
(2001
), but disagreeing with
Covell et al. (1991
) who found
no time delay in minimum muscle length across a smaller axial distance of
0.19L. Indeed, comparing muscle length changes between two relatively
close sites will make a rapidly traveling strain wave difficult to detect
(Ellerby and Altringham,
2001
).
Our analysis of fast-start muscle dynamics in O. mykiss
fast-starts shows a temporal decoupling between contractions of white muscle
fibers and changes of local midline curvature. This phase shift was observed
to significantly increase under conditions that yielded high strain at the
posterior axial location (0.7L). The phase shift observed at the
anterior region (0.4L) was not affected by high strain, but a
significant curvature lag was still observed. This dichotomy suggests that
differential hydrodynamic resistance is the primary mechanism underlying this
phase shift. This hypothesis is consistent with the fact that body bending is
increasingly resisted by hydrodynamic resistance along the body in the
posterior direction (Wakeling and
Johnston, 1999b), and that hydrodynamic thrust is imparted to the
water primarily through the caudal region
(Weihs, 1973
;
Webb, 1977
;
Frith and Blake, 1991
).
Regardless of response strength, the tendency of muscle shortening to
precede local midline curvature highlights the significance of external
resistance during fast-starts. For steady swimming, similar effects may not be
significant considering that relatively high strains are rarely observed
during this swimming mode. Katz et al.
(1999) described one instance
during burst swimming in milkfish where curvature lagged behind red anterior
(0.53L) muscle shortening by 16.7 ms under relatively high strain
(approximately 13%). However, red muscle in the same trial at the posterior
location (0.71L) also reached strains of about 13%, but resulted in
muscle shortening lagging behind curvature. All other studies that have
compared local body bending with local muscle length changes have involved
relatively low strain regimes (Coughlin et
al., 1996
; Shadwick et al.,
1999
; Donley and Shadwick,
2003
; Donley et al.,
2004
).
For steady swimming and fast-starts in most fish, axial strain magnitude
from simple beam theory appears to be an accurate predictor of strain measured
by sonomicrometry (Coughlin et al.,
1996; Katz et al.,
1999
; Wakeling and Johnston,
1999a
; Long et al.,
2002
). Beam theory is time independent (steady state) and involves
homogeneous, linearly elastic material
(Stevens, 1987
). Therefore,
this beam-like behavior in swimming fish muscle is unexpected given that the
myotendinous machinery of fishes is incredibly complex
(Gemballa and Vogel, 2002
). In
addition, undulatory swimming relies on reactive forces generated from lateral
accelerations of a given body segment
(Daniel, 1984
). Peak measured
and predicted strains from this study are compared with data from several
species performing various swimming behaviors
(Fig. 9). This comparison shows
that only the posterior position under high strain departs from beam theory
predictions. The deviation is similar to that observed in tunas where strain
from sonomicrometry is greater than strain estimated from beam theory.
Interestingly, this position and condition (posterior, high strain) also
exhibits the highest phase shift (Fig.
7). In this way, beam theory can be used to estimate hydrodynamic
forces along the body by demonstrating incongruence between measured and
predicted strain.
|
The nature of the phase shift in this study is unlike that found in tunas
and the shortfin mako shark where muscle shortening at a given location was
found to be in phase with curvature at a much more posterior location
(Shadwick et al., 1999;
Donley et al., 2004
). These
phase shifts are a mechanical consequence of the highly specialized
myotendinous architecture in these fishes whereas the curvature lag in
fast-starts is probably a result of hydrodynamic forces. Thus, white muscle in
fast-starts of O. mykiss acts locally to generate a posteriorly
directed wave of body bending, but during maximal performance a hydrodynamic
limit to large and rapid lateral deflection is imposed. The mechanism by which
muscle shortens in advance of local bending, as we present here, likely
involves muscle or connective tissue deformation at another location. In some
video sequences the length of the entire body was observed to shorten just
prior to the escape maneuver (Fig.
1B), most notably in the head region; however, the resolution of
our analysis was not sufficient to quantify this change.
Furthermore, localized contraction without body bending could cause
shearing (Alexander, 1969),
which would potentially depress the development of local curvature (see
Fig. 4). Local minima can also
be observed in maximum curvature profiles for several other species performing
fast-starts (Wakeling and Johnston,
1998
; Fernandez et al.,
2002
). When a beam is flexed, the concave side develops
compressive stress while the convex side experiences tensile stress. The
application of these antagonistic forces on each segment of the beam can cause
either rotation or shear (Vogel,
2003
). The angular acceleration of spine bending was shown to
sharply decrease from approximately 0.2FL to 0.4FL in common
carp escape responses (Wakeling and
Johnston, 1999b
). Given this circumstance the body segment must
shear. The proportion of shear to rotation that occurs is likely to be a
function of vertebral length, where few long vertebrae enhance shear and many
small vertebrae are more likely to rotate (J. M. Wakeling, personal
communication). These speculations warrant the investigation of
three-dimensional muscle deformation during fish locomotion.
Our results support Wakeling and Johnston's
(1999b) model that explains
fast-start body bending in terms of muscle torque and hydrodynamic resistance.
The large muscle mass in the anterior region provides high power
(Wakeling and Johnston, 1999b
)
and high stiffness (Blight,
1977
; Wainright et al.,
1978
; Westneat et al.,
1998
), while the reduction of muscle mass in the posterior region
contributes low power and low stiffness
(Blight, 1977
). Strong
bilateral muscle activity may also serve to increase body stiffness in a time
dependent manner (Westneat et al.,
1998
), but this neuromuscular pattern is not observed in O.
mykiss (Hale et al.,
2002
). However, stage 1 body bending is sufficiently explained by
muscle torque alone, even with internal stiffness making no contribution
(Wakeling and Johnston,
1999b
). Additionally, curvature wave velocities along the body
were found to be independent of stage 1 bilateral muscle activity in the
bichir P. senegalus (Tytell and
Lauder, 2002
). Therefore, a more appropriate hybrid oscillator
model for a bending fish would describe the anterior region as torque
dominated rather than stiffness dominated. This hypothesis is reinforced by
the observation in this study that muscle segment shortening rate and head
turning rate maxima at 0.4L are closely associated
(Fig. 10). This suggests that
head turning is a consequence of bending moments driven by torques generated
in the anterior region. It appears as though a stiffer anterior region is
better equipped to turn and cut through the medium. Conversely, a more
flexible posterior region seems aptly designed to impart momentum to the water
by maximizing reactive forces, particularly by effecting the shape dependence
of the acceleration reaction.
|
As torque decreases along the body
(Wakeling and Johnston,
1999b), hydrodynamic resistance to lateral deflection increases
largely due to the presence of a caudal fin, which adds substantial added mass
and increases external resistance to lateral acceleration
(Weihs, 1973
). A robotic
simulation by Ahlborn et al.
(1997
) showed that increasing
the delay between initial and return strokes generates maximal thrust. The
propulsive forces associated with the change in rotational momentum (Albhorn
et al., 1991) may be enhanced by a resistance dominated posterior region. This
mechanical property could passively act as an excellent transmitter of
posteriorly directed forces, especially considering the longitudinal
orientation of posterior muscle fibers and tendinous structures
(Gemballa and Vogel, 2002
). As
force is projected caudally, a sufficient time period is provided for
vorticity to develop around the caudal fin. Clearly, more empirical
hydrodynamic analyses (e.g. Wolfgang et
al., 1999
) of wake structure during fast-starts of real fish are
needed before any firm conclusions can be made.
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Acknowledgments |
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