Swimming of larval zebrafish: finaxis coordination and implications for function and neural control
1 Department of Organismal Biology and Anatomy, The University of Chicago,
Chicago, IL 60637, USA
2 Committee on Neurobiology, The University of Chicago, Chicago, IL 60637,
USA
3 Committee on Computational Neuroscience, The University of Chicago,
Chicago, IL 60637, USA
* Author for correspondence (e-mail: mhale{at}uchicago.edu)
Accepted 14 September 2004
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Summary |
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Key words: kinematics, biomechanics, gait, Danio rerio, larva, musculature, locomotion, mechanical design, central pattern generator, pectoral fin
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Introduction |
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Many species, including adult zebrafish
(Thorsen et al., 2004), use
axial body bending at all speeds, and the fins to maneuver and stabilize
(Webb, 1994
). When used for
maneuvering, pectoral fins have been shown to alternate out of phase
temporally, such that abduction of one fin coincides with adduction of the
contralateral fin (Drucker and Lauder,
2003
). Other species employ their pectoral fins in synchrony as
their primary mode of locomotion during steady swimming across a wide range of
speeds (Webb, 1973
,
1993
;
Gibb et al., 1994
; Drucker and
Jensen,
1996a
,b
;
Walker and Westneat, 1997
).
The morphologically unusual burrfish (Chilomycterus schoepfi)
alternates the pectoral fins during swimming, which are active simultaneously
with the caudal fin (Arreola and Westneat,
1996
).
Research in locomotion of larval fishes has focused on axial movements
during steady swimming, turning, prey capture
(Budick and O'Malley, 2000;
Borla et al., 2002
), startle
behaviors (Batty, 1981
; Hale,
1996
,
1999
;
Budick and O'Malley, 2000
;
Müller and van Leeuwen,
2004
) and swimming performance
(Fisher et al., 2000
;
Bellwood and Fisher, 2001
;
Fisher and Bellwood, 2003
).
Work by Batty (1981
), and
Müller and van Leeuwen
(2004
), demonstrated that
plaice larvae (Pleuronectes platessa) and zebrafish larvae,
respectively, can swim with simultaneous axial and pectoral fin movements.
However, the detailed kinematics and role of coordinated pectoral fin and body
movements have gone unstudied primarily due to the technical difficulty of
visualizing pectoral fins of larvae
(Budick and O'Malley,
2000
).
The combined movement of the limbs and axis during locomotion has been
studied in depth in tetrapods. Axial bending is often coordinated with limb
rhythms so that a flexionextension limb cycle corresponds to one cycle
of axial bending (Ritter,
1992; Ashley-Ross,
1994
). The limbs within a fore limb or hind limb pair alternate
with each other so that, for most of the stride cycle, one side is in its
swing phase while the other is in its support phase
(Biewener, 2003
). There is a
short period of overlap when both limbs are on the ground with one limb at the
beginning of the support phase and the other at the end during walking. The
production of axial movements via standing or traveling waves of
bending (Williams et al.,
1989
; Frolich and Biewener,
1992
; Ritter,
1992
; Reilly and Delancey,
1997
) varies among species, developmental stage and gait. The
basic temporal pattern of this locomotor activity involves the integrated
activity of central pattern generators (CPGs) in the spinal cord (for reviews,
see: Stein, 1978
;
Grillner, 1981
;
McClellan, 1996
).
Pectoral fin muscles of adult fishes have been studied in many species and
include an array of muscles that control fin adduction and abduction during
different locomotor modes (e.g.
Winterbottom, 1974; Geerlink,
1979
,
1983
,
1989
;
Westneat, 1996
). Several
muscles, including their subdivisions and individual bundles, perform various
roles in actuating the fin during locomotion
(Thorsen and Westneat, in
press
). Despite widespread interest in limb development (e.g.
Sordino et al., 1995
;
Ahn et al., 2002
), the muscle
morphology and function of early developing fish fins remains to be
explored.
To investigate the use of pectoral fins in larval zebrafish locomotion, we
examined axial bending and fin movement during routine swimming, and compared
it with swimming following the startle response, a behavior thought to be
produced at near-peak velocity that does not involve fin movement. Both our
preliminary observations and reports in the literature
(Batty, 1981;
Borla et al., 2002
;
Müller and van Leeuwen,
2004
) found that the fins and axis were active simultaneously
during routine larval fish swimming. Previous work on tetrapod locomotion
demonstrating that alternation of the limbs and lateral bending of the axis
are coordinated tightly during locomotion
(Ashley-Ross, 1994
;
Bennett et al., 2001
) drove our
hypothesis that relative movements of limbs and axis of larval fish would be
similarly patterned. Through the comparison of slow and fast swimming we
suggest that the use of fins may be associated with the hydrodynamics
experienced by the fish at different swimming speeds. In addition, we describe
the pectoral fin musculature and discuss its functions in fin movement.
This work complements the previous work of Budick and O'Malley
(2000), and Müller and
van Leeuwen (2004
), and
focuses on the coordination of fin movements during slow swimming and the
neural implications of kinematic patterns. Based on our data in larval
zebrafish, and similar data in plaice larvae
(Batty, 1981
), we suggest that
fishes and tetrapods may use similar neural coordination of axial and
appendicular structures, and that the mechanisms for that coordination may
have been conserved from an ancestral condition.
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Materials and methods |
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Digital video recording of locomotion
For behavioral imaging, larvae were transferred to 10% Hanks solution and
placed into Petri dishes (3.5 cm indiameter). Behavioral observations were
made after acclimation to room temperature (25°C) for 15 min. Fish were
placed under a Leica MZ 6 microscope (Wetzlar, Germany) with an attached
high-speed Redlake MotionScope PCI 2000S video camera (San Diego, CA, USA).
Black and white video at 1000 frames s1 and 240x210
pixel resolution was saved directly to a PC utilizing the Redlake Imaging
MotionScope 2.21.1 software. Only spontaneous swimming events were collected
for slow swimming trials. A glass micropipette was directed at the caudal
region of the fish to elicit fast swimming responses.
Behavior analysis
Behavioral trials for slow swimming (30 total; three trials per individual
for ten fish) and post-startle swimming [15 total; three trials per individual
for five fish (a subset of the individuals used in slow swimming trials)] were
analyzed with a customized program for digitizing the axial midline using
LabView 5.0.1 software (National Instruments, Austin, Texas, USA; with virtual
instruments designed by J. R. Fetcho, Cornell University, NY, USA). In
addition, the timing and coordination of fin movements and parameters used to
calculate Reynolds number (Re=VL/µ,
where V and L are the velocity and length of the fish, and
and µ are the density and viscosity of water) were determined by
viewing trials frame-by-frame in NIH Image 1.62 (NIH, Bethesda, MD, USA). For
each trial, we quantified kinematic data during the middle of a straight
swimming bout for one tail-beat cycle and the three fin strokes that
overlapped it (two on one side of the body, one on the other).
We defined each fin cycle (locomotor cycle) using three events: the frame
just prior to start of fin abduction, the frame of maximum lateral abduction,
and the first frame post adduction. The refractory period between fin cycles
was defined by indeterminate fin activity, which results from a fin positioned
adjacent to the body. Points of maximal medial axial curvature correspond to
when the tip of the fish's tail changes direction
(Budick and O'Malley, 2000).
Only swimming after the first two tail strokes was examined, both for fast and
for slow locomotion, to avoid the asymmetric initial bends and acceleration
associated with the initiation of movement. Asymmetrical bends begin when
maximal convexity is achieved for the first time in the same direction as the
initial turn (which is at the end of the second beat), and ends when the axis
cycles back to this configuration. All statistical tests were performed with
JMP 3.1.6 (SAS Institute, Cary, NC, USA).
Morphological imaging and analysis
A subset of the -actin transgenic zebrafish were stained with
Calcein green (Molecular Probes, Eugene, OR, USA) to visualize the cleithrum
and endoskeletal components of the pectoral fin. Fish were immersed in a 0.2%
Calcein green solution following Du et al.
(2001
) for 15 min and allowed
to swim freely. Fish were then rinsed in 10% Hanks and anesthetized with MS222
and embedded in agar for confocal imaging.
-actin GFP fish and
Calcein-stained fish (Calcein green +
-actin GFP) were positioned with
their left side down in 1.2% agar on a glass coverslip floor of a small Petri
dish. The agar was covered with a 50% mixture of 10% Hanks solution and MS222
to prevent desiccation and fish movement while imaging. The pectoral girdle
musculature was imaged under a Zeiss LSM 510 laser-scanning confocal imaging
system (Thornwood, NY, USA).
Single optical sections and image stacks (40 x objective, 1028 x1028 pixel resolution, 100 slices, 0.8 µm interval for three-dimensional reconstruction) of the pectoral girdle musculature and fin membrane were saved to a PC. Three-dimensional reconstructions were produced using Zeiss LSM 510 software. Fin surface area was calculated in ImageJ 1.30 (NIH, USA) using three-dimensional lateral view projections of the fin (musculature and membrane). The number of muscle fibers constituting the pectoral musculature were counted using three-dimensional projections and Z stacks to aid in the visualization of the fin.
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Results |
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Slow swimming with the fins and axis was significantly slower,
approximately an order of magnitude lower, than fast swimming
(Fig. 2A). Fast swimming was
more effective at propelling the larval fish forward, covering more than four
times the distance traveled during slow swimming
(Fig. 2B). The average duration
of locomotor cycles was significantly shorter during fast swimming events
(Fig. 2C). Re
calculated for the slow swimming condition averaged 43±3
(Fig. 2D). During fast
swimming, in which the fins are tucked and the axis alone propels the fish,
Re numbers were significantly higher (427±31) than those of
slow swimming, corresponding to a change in velocity (P<0.0001,
Fig. 2A). Axial movement of
zebrafish swimming possesses attributes of traveling and standing waves with a
loose node present slightly posterior to the pectoral girdle (in agreement
with Müller and van Leeuwen,
2004).
|
We further investigated the fin movements and coordination of the fins and
axis in the slow swimming gait (Table
1). The duration of a complete fin abductionadduction
cycle, including the refractory period
(Drucker and Jensen, 1996a)
when a fin is positioned against the body, averaged 41.23±0.94 ms and
is not significantly different from the duration of a tail-beat cycle
(40.23±0.94 ms, P=0.4602,
Fig. 3A). The mean duration of
the refractory period was 5.27±0.62 ms. The mean durations of the
abduction and adduction phases across three fin cycles were not significantly
different (17.66±0.44 ms vs 18.30±0.54 ms,
P=0.3680; Fig. 3B).
The mean time points of maximum fin abduction during slow swimming events
(0.10, 19.80 and 40.07 ms) coincided with, and were not significantly
different (P>0.05) than, maximum axial bending (1.00, 21.17 and
40.30 ms), indicating that the fins and axis are highly coordinated
(Table 1).
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Morphology
Pectoral fins in the larval stage are composed of a flexible endoskeletal
disk (Grandel and Schulte-Merker,
1998), fin membrane with actinotrichia, and muscles that actuate
the fin membrane. The fin musculature, composed of two relatively simple
muscles, is separated along the sagittal plane by an endoskeletal disk.
Confocal microscopy sections (Fig.
4AC) through these muscles in a transgenic fish that
expresses green fluorescent protein in muscle fibers
(Higashijima et al., 1997
)
indicate the position of the abductor/adductor musculature along the fin.
Planar views of the abductor and adductor muscles
(Fig. 4A,B,E,F), illustrate
that muscle fibers run in a sheet on the fin extending upwards from its base.
The abductor muscle is located on the rostral side of the fin and pulls the
fin forward when it contracts. The adductor muscle is located on the caudal
side of the fin and pulls the fin back against the body when it contracts. The
abductor and adductor originate along the anterolateral and anteromedial
surface of the cleithrum, respectively, and insert onto the fin membrane
(Fig. 4F).
|
The fin musculature represents a functional fin blade surface area of 25590±993 µm2 (82055±2535 µm2 total fin blade area) in the lateral plane of the abductor (Table 2). The majority of the fin musculature is only one muscle fiber thick. The abductor and adductor muscles are composed of essentially the same number of muscle fibers (54.4±1.4 and 51.8±1.9, respectively; P=0.1902; Table 2). A number of fibers converge at the origination of the fin musculature, along the midline of the fin, which is about two muscle fibers thick. Muscle fibers along the midline run parallel from origination to insertion. The musculature servicing the leading edge and trailing-edge of the fin travel at opposite angles of curvature with respect to the midline fibers, with trailing-edge fibers having the largest relative curvature (Fig. 4A,B,E).
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Discussion |
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Locomotion in larval zebrafish
Axial locomotion in larval zebrafish has been well described in several
recent studies (Budick and O'Malley,
2000; Müller and van
Leeuwen, 2004
), the first at 6 and 9 dpf, the second at 25,
7 and 14 dpf. We chose to focus on 5 dpf larvae because previous work on the
neural control of swimming (e.g. Liu and
Fetcho, 1999
; Hale et al.,
2001
) and previous kinematic studies (e.g.
Budick and O'Malley, 2000
;
Borla et al., 2002
) have been
done at that age. In the present study we further examine the pectoral fins,
focusing on the steady swimming component of the slow start and compare it
with straight forward swimming following the, previously described, fast start
(Budick and O'Malley, 2000
;
Müller and van Leeuwen,
2004
).
To examine the relationship between fin and axial movement during steady
swimming, we examined only the component of slow swimming in which the fish is
swimming straight with equivalent left and right angular head movement, and
with little change in angle between tail strokes (limiting initiation and end
movement bias). We restricted trials because of our primary interest in the
coordination of steady forward locomotion. For these components of the
swimming trials, we found that pectoral fin beats matched both the frequency
and phase of tail beats. We conclude that the fins and axis are highly
coordinated by showing that the number of fin movements matched the number of
points of maximal axial curvature (Fig.
1) and that there are no significant differences between the
timing of fin maximum lateral abduction and maximum axial curvature
(Table 1). This differs
slightly from the findings of Müller and van Leeuwen
(2004) that the pectoral fins
are active during slow starts at the same frequency (typically below 30 Hz)
but not necessarily the same phase as axial movements during what they call
`slow-start swimming'. The pectoral fins and tail were found to be in phase in
most sequences of slow start swimming in Müller and van Leeuwen
(2004
), although during burst
swimming the pectoral fins were occasionally found to be out of phase with the
tail (U. Müller, personal communication). We attribute our findings of
tight finaxial coordination to the extent of the slow swimming events
examined (i.e. steady swimming no burst of acceleration or
deceleration).
Comparison to limbaxis coordination in other taxa
The pattern, and relative timing, of fin and axial movement observed during
slow swimming (Fig. 5A) bears a
striking resemblance to the fore limb and axial coordination of some
amphibians and reptiles, and the walking and running gait of many tetrapods
(Fig. 5C,D; Daan and Belterman,
1968; Ritter,
1992
). In most cases, the limbs are coordinated so that one cycle
of axial bending corresponds to one limb cycle. Periods of maximal axial
curvature generally coincide with maximal extension of limbs. In tetrapods,
coordination of these behaviors involves the integrated activity of central
pattern generators controlling the abductionadduction rhythms of the
limbs and lateral bending of the body
(Devolvé et al., 1997
;
Bem et al., 2003
).
|
The timing of limb activity, specifically the duration of
abductionadduction phases, varies among larval and adult fishes as well
as tetrapods. Unlike in larvae, the abductionadduction phases of
pectoral swimming of adult fishes are not equal in duration. Studies by Gibb
et al. (1994) on bluegill
sunfish, Walker and Westneat
(1997
) on a wrasse, and
Drucker and Lauder (1997
) on a
surfperch, demonstrate that fin adduction is shorter in duration than
abduction. A comparison of timing of larval fin cycles to the swing/stance
cycle in tetrapods reveals that cycle duration varies depending on locomotor
speed (Biewener, 2003
). Work on
the salamander, Dicamptodon
(Ashley-Ross, 1994
), has shown
that the stance and swing phase durations during the step cycle are nearly
equal (Fig. 5C). However,
kinematics of lizard limbs have shown that stance is longer in duration than
the swing phase during running (Reilly and
Delancey, 1997
). Differences in timing of limb movements in
vertebrates may reflect specializations based on morphological, behavioral and
function requirements.
Fricke and Hissman (1992) have shown that the coelacanth (Latimeria chalumnae) can coordinate its pectoral fins with the caudal fin in a similar fashion to tetrapods and larval fishes. Fins were coordinated with a phase difference of 180° (abduction of one fin and adduction of the other). Pectoral fins were employed in an alternating fashion during accelerated forward movement, and have the ability to synchronize after a sudden start and during the following behaviors: curve swimming, accelerated movement to gliding, and upside down swimming (Fricke and Hissman, 1992). The pattern observed in the coelacanth provides additional behavioral evidence that a finaxis motor pattern may be primitive among Osteichthyes (Sarcopterygii and Actinopterygii).
We suggest that the neural control of finaxis coordination observed
in tetrapods and larval fishes evolved prior to the split of sarcopterygian
(lobe-finned) and actinopterygian (ray-finned) fishes and, although not common
in the swimming modes of adult fishes, may have been conserved in the larvae
of some species. Work by Grillner and Wallen
(1985) suggests that the
neural circuits controlling rhythmic axial oscillation in lamprey, one of the
most basal vertebrate lineages, could be employed with limb CPGs to generate
the pattern of axial muscle activity observed in tetrapods. Our data and other
larval data (Batty, 1981
)
support this hypothesis by demonstrating that an axial traveling wave of
bending, typical of fishes, can occur with rhythmic limb movements and may
represent an intermediate condition of circuit coordination in which the axial
bending and fore limb CPGs are integrated temporally but without substantial
modification to the axial movement pattern. Furthermore, axial kinematics of
adult eels (Gillis, 1996
), in
which axial movement alone generates propulsion, demonstrate a similar pattern
to slow swimming in zebrafish, suggesting that use of pectoral fins does not
necessarily alter axial patterns.
The diversity of vertebrates provides many opportunities to examine the
diversity and evolution of coordination of limbs and axis. For example, Azizi
and Horton (2004) recently
found that the elongate salamander (Siren lacertina), which lacks
hind limbs, is able to decouple appendicular movements and tail movements
during aquatic walking, which the authors suggest may be related to
elongation. This example highlights one of several possible evolutionary
modifications of a primitive limbaxial circuit.
Fin function during slow swimming
The presence of coordinated fin activity during slow swimming does not
necessarily mean that the fins are participating in generating propulsive
force. Fin movement may contribute to respiration
(Osse and van den Boogaart,
1999) or may be used to stabilize the body during swimming. Equal
abduction and adduction phases of pectoral fin movements are highly
coordinated with axial movement. As suggested by Batty
(1981
) for pectoral and axial
movements in plaice larvae, the synchronization of these pectoral fin
movements with axial movements may serve to offset head yaw by counteracting
the recoil effect produced by the tail movement. Larval zebrafish pectoral fin
strokes are timed precisely to do this, improving efficiency by reducing drag
induced by axial swimming movements. The functions of the fins in respiration,
stability and propulsion remain to be tested. Clarifying the roles of fin and
axial coordinated movement patterns may provide important insight into the
evolution and diversification of vertebrate locomotion.
The difference in Re number between slow and fast swimming
suggests that hydrodynamic forces may be related to fin use during steady
swimming. For larval fishes, the pattern of finaxis locomotor
coordination (Batty, 1981;
Müller and van Leeuwen,
2004
; this paper) seems to be associated with swimming in low
Re conditions. There was a tenfold difference in Re values
between slow swimming with pectoral fins and fast swimming with axial movement
alone (43±3 and 427±31, respectively). Re values and
movement pattern reported here are similar to those described by Batty
(1981
), and Müller and van
Leeuwen (2004
), in larval
plaice and zebrafish, respectively. Zebrafish maintain pectoral fin and axial
coordination in a significantly decreased Re environment (Re
ranging from 311), which was achieved by increasing the viscosity of
water using polyvinyl pyrrolidone (Sigma-Aldrich, Saint Louis, MO, USA; D.H.T.
and M.E.H., unpublished). This finding suggests that coordinated alternating
fin movements with the axis can occur through a wide range of low Re
numbers.
Fin muscle structure and implications for function
The 5 day time period of the zebrafish studied here represents the first
phase of pectoral fin development (Grandel
and Schulte-Merker, 1998). Despite their early development, larval
zebrafish pectoral fins are fully functional and perform normal locomotor
behaviors. Based on kinematic and morphological data
(Grandel and Schulte-Merker,
1998
; Thorsen et al.,
2004
; this paper), we believe that larval zebrafish musculature
moves along with the fin membrane and is a functional component of the fin
blade. We predict the abductor/adductor muscles are able to bend with the fin
through its full range of motion. The only stationary structure of the
pectoral girdle appears to be the cleithrum, which anchors both abductor and
adductor muscles.
Muscle fibers are relatively evenly distributed along the fin membrane,
although the muscle fibers inserting at the midline of the fin are longer than
those of the leading or trailing-edge fibers. A distributed network of muscle
fibers along the abductor and adductor muscles suggests an even force
distribution along the fin. Neural innervation patterns
(Thorsen et al., 2004) suggest
independent control of the leading, middle and trailing-edge components of the
fin musculature. We predict then, that in the larval condition, the pectoral
musculature has variable control of the fin due to innervation patterns and
muscle curvature enabling asymmetries in fin movement. High-resolution,
high-speed video technology could be used to test these predictions.
Conclusion
The patterns of movement described here suggest a similarity in the neural
control of limbs and the body axis. We suggest that the same basic
limbaxis motor control circuit has been conserved evolutionarily and is
present in fishes and salamanders; however, in fishes it is only used during
early development when animals experience low Re conditions, whereas
tetrapods have retained and modified it for function in adults. We believe
that a number of factors, including Re, stability, fin musculature
and a primitive neural circuit, contribute to produce the behavior of the
zebrafish during slow swimming. Many questions remain regarding the function
of fins throughout development, how fins are controlled through
sensorymotor mechanisms, neural circuitry for generating fin
abductionadduction rhythms and fine control of motion. The simplicity
of the pectoral fin musculature composed of one muscle at one limb joint makes
the larval zebrafish an excellent model to address many of these
questions.
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Acknowledgments |
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References |
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