Neuromuscular control of trout swimming in a vortex street: implications for energy economy during the Kármán gait
Department of Organismic and Evolutionary Biology, Harvard University, Cambridge, MA 02138, USA
e-mail: jliao{at}oeb.harvard.edu
Accepted 1 June 2004
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Summary |
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Key words: electromyography, Kármán gait, fish swimming, rainbow trout, Oncorhynchus mykiss, axial muscle activity, turbulence, vortices, neural control, central pattern generators
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Introduction |
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In a recent study, trout were shown to volitionally hold station in an
experimentally generated vortex street by exhibiting a novel, rhythmic
undulating motion termed the Kármán gait
(Liao et al., 2003a). During
the Kármán gait, tail-beat frequency consistently approaches the
rate at which vortices are shed from the cylinder, and the body oscillates
laterally with a magnitude similar to the spacing of the vortices. This
indicates a phase locking of the swimming kinematics to the vortex wake and
thus a potentially passive mechanism of holding station in fast, turbulent
flows. It was hypothesized that trout use a largely passive mechanism to
generate thrust when positioned in the sinusoidal flow of a vortex street
(Liao et al., 2003a
).
Despite the substantial and widespread benefits of vortex energy capture
for fish locomotion, there are still no quantitative data that address the
diversity and extent to which vortices might affect muscle activity patterns
in swimming fishes (but see Liao et al.,
2003b). Like many types of locomotion in animals, swimming is a
rhythmic motion that is under the control of central pattern generators (CPGs;
e.g. Grillner, 1985
;
Grillner and Kashin, 1976
).
Although one useful definition of a CPG is that it can occur in the absence of
feedback from the environment (Grillner,
1975
), the importance of sensory stimuli on determining the final
motor output pattern of CPGs in naturally behaving animals cannot be
overstated (reviewed in Cohen,
1992
). Isolated spinal preparations provide a powerful opportunity
to understand the fundamental neural circuitry of locomotion, but at the cost
of shifting the emphasis away from the adaptive aspect of movement that is the
hallmark of natural animal behavior (Cohen,
1992
). As an alternative, the present study attempts to approach
the control of locomotion as a behavior at the organismal level. A novel motor
pattern associated with the Kármán gait may thus provide a
unique opportunity to examine sensory-driven motor output for freely behaving
fishes swimming among environmental vortices.
Here, electromyography is used to quantify red and white axial muscle activity to test the hypothesis that rhythmic axial muscle activity pattern in Kármán gaiting fish differs from the rostro-caudal traveling wave of muscle activity typical of fishes swimming in uniform flow. The second hypothesis to be tested is that cylinder vortices rather than axial muscle activity dominate Kármán gait kinematics. Finally, the third hypothesis to be tested is that short bouts of Kármán gaiting can proceed at times without any muscle activity.
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Materials and methods |
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Electrode construction
Electrodes were constructed by threading one end of a double-stranded,
insulated, stainless steel wire (0.005 cmdiameter; California Fine Wire Co.,
Grover Beach, CA, USA) through the barrel of a hypodermic needle (26 gauge
5/8). The tips of the wire were then stripped of insulation and splayed apart
by 0.51.0 mm. The two exposed tines were then rolled into a hook using
fine, electronic micro-forceps and pulled snug against the needle tip for
insertion (Loeb and Gans,
1986).
Surgical procedures
Trout were anesthetized in a 15±1 °C, 5-liter holding tank
containing a solution of 0.0654 g l1 tricaine
methanesulfonate (MS-222; Finquel Inc., Argent Chemical Laboratories Inc.,
Redmond, WA, USA) buffered with potassium hydroxide. Fish became unresponsive
to tactile stimuli within minutes and were transferred into a tray containing
a maintenance solution of MS-222 (0.00327 g l1 at
15±1 °C). During surgery, the gills of the fish were regularly
irrigated with a solution of dilute MS-222 and oxygenated water. Four
electrodes were inserted into the superficial, axial red muscles along the
left side of the fish (Fig. 1;
R1, 0.23 L; R2, 0.40 L; R3, 0.56 L; R4, 0.73
L). Two electrodes were also inserted into the white muscle, halfway
between the skin and the vertebral column
(Fig. 1; W2, W3). In addition,
two red muscle electrodes were placed in corresponding longitudinal positions
on the right side of the fish (denoted with an asterisk, R1* and R3*). At the
end of the surgery, all eight implanted electrode wires were gathered, glued
into one cable with cyanoacrylate (Fig.
1A) and anchored to a suture loop (4-0 gauge braided silk thread;
Ethicon Inc., Somerville, NJ, USA) located on the back of the trout to prevent
electrodes from being pulled out during the experiment.
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After surgery (3045 min), fish were transferred into a container of freshwater until a righting response was observed. They were then placed into a 600-liter recirculating flow tank (15±1 °C, working section 28 cmx28 cmx80 cm) and allowed to recover for several hours before the start of an experiment.
Experimental procedures
To generate a Kármán vortex street, a 5 cm-diameter,
D-section cylinder was used as in a previous study
(Liao et al., 2003a). A
RedLake high-speed digital video camera aimed at a 45° front-surface
mirror placed below the flow tank recorded the ventral view of the trout (250
frames s1; 1/500 s shutter speed) against a lighted
background.
Electromyography (EMG) and video data were simultaneously recorded for
trout exposed to four treatment conditions: (1) holding station behind the
cylinder placed in a flow of 3.5 L s1; (2) in the
absence of the cylinder, swimming in uniform flow at 3.5 L
s1; (3) in the absence of the cylinder, swimming in a slow,
uniform flow (1.8 L s1) that approximated what
would be the average, reduced flow velocity behind the cylinder (see
Liao et al., 2003a) and (4)
swimming in a fast, uniform flow (5 L s1) to elicit
white muscle activity (to verify the viability of white muscle electrodes).
EMG data were synchronized to video images with a voltage pulse trigger that
simultaneously stopped video and EMG recording. Care was taken to analyze only
those sequences in which fish were at least 3 cm away from the sides and
bottom of the flow tank. EMG and kinematic data were collected from several
fish for all treatment conditions. Data were analyzed from at least four
tail-beat cycles for all five fish for treatments 1 and 2.
The following kinematic variables were measured; lateral amplitude of the head, the body at the R1 insertion site and the center of mass (COM) relative to the body midline, maximum head angle relative to the x-axis (Fig. 1B), body wavelength and tail-beat frequency. The COM was determined postmortem for each fish by iteratively balancing the body between right and left side pins. Body wavelength was obtained by dividing the wave speed (determined by tracking the maxima of each wave crest as it passed down the body) by the tail-beat frequency, where tail-beat frequency was calculated by averaging at least four consecutive tail-beats over a known time.
Data analysis
During data acquisition, EMG signals were amplified 10 000 times using
Grass AC P511K preamplifiers with a 60 Hz notch filter and a 100 Hz high-pass
and 3000 Hz low-pass filter, as in previous studies (Jayne and Lauder,
1993,
1995
). A Powerlab 16SP
analog-to-digital converter (ADInstruments, Colorado Springs, CO, USA)
recorded digitized EMG signals at a sampling frequency of 4000 Hz. Signals
were post-processed in Matlab (v.6.1) using a 10th order Butterworth filter
(zero phase shifting) with a high- and low-pass frequency of 94 Hz and 1040
Hz, respectively. EMG variables such as intensity, duration, onset, offset and
area were analyzed for each tail-beat with customized software. The relative
intensity of each muscle burst was calculated as the mean spike amplitude for
the rectified EMG signal normalized by the maximum mean spike amplitude
observed. Duration was recorded as a proportion of the time elapsed relative
to one cycle of the COM. Onset and offset times were measured relative to the
start of the corresponding kinematic cycle of the COM. Rectified area, the
product of relative intensity and duration, was measured and included in the
calculation of means only if there were visible signs of muscle activity.
Statistical tests
Multiple linear regression analyses using a general linear model were
performed and compared for both flow treatments to examine the idea that
muscle activity would explain body kinematics during steady swimming but not
during the Kármán gait because of the large effect of the
vortices. The general linear model tested the simultaneous effect of
independent EMG variables (muscle intensity, duration and relative onset time
as well as their interactions) on each of the dependent swimming kinematics
variables (head angle, head amplitude, R1 amplitude and center of mass
amplitude). Note that statistical comparisons were conducted only for R1
muscle activity since R1 was the only electrode active during both swimming in
uniform flow and the Kármán gait. Furthermore, R1 was not always
active during the Kármán gait, occurring 62% of the time, while
in the remaining 38% of the time no axial muscle activity was present. Thus,
only 62% of all Kármán gait trials were statistically compared
with R1 activity during swimming in uniform flow.
Inclusion of correlated variables in a general linear model, known as
multicollinearity (Berry and Feldman,
1985), exaggerates r2 values and projects a
tighter fit to the distribution of data describing the relationship between
muscle activity and body kinematics. Two steps were taken as a conservative
approach to account for multicollinearity. First, both EMG and kinematic
variables were evaluated for independence using separate simple linear
regressions before being included in the general linear model. For example,
muscle intensity and duration were both included in the general linear model
only because, when regressed against each other, their r2
value was lower than 0.50. Second, the general linear model was iteratively
stepped through using the technique of `backward elimination' (p. 431,
Zar, 1999
) to remove the EMG
variables that had insignificant effects on the kinematic variables while
still preserving the original r2 value.
To provide a consistent comparison with data from fish adopting the
Kármán gait, the same multiple linear regression model was
applied to data from fish swimming in uniform flow. Analysis of variance
(ANOVA) was used to determine if the multivariable model relating muscle
activity and body kinematics was significant at P<0.05
(Table 1). Means and standard
errors were calculated for the rectified area, intensity and duration of
muscle activity for all individuals, with values normalized within an
individual prior to pooling the data. Multiple tail-beat cycles from each
individual across individuals were also pooled to calculate the mean tail-beat
frequency, wavelength, head amplitude and head angle along with the
corresponding errors. Unpaired t-tests were performed to determine
which variable means were significantly different between live,
Kármán gaiting trout and dead, towed trout. Bonferroni
post-hoc corrections were performed at =0.05 whenever multiple
tests were used (e.g. ANOVAs and t-tests;
Rice, 1989
). All statistical
tests were performed in Systat version 9 (PC).
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Results |
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The average rectified area for each of the electromyograms from electrodes R2R4, when averaged across several tail-beat cycles for each of five fish, was significantly lower during the Kármán gait than during swimming in uniform flow (Fig. 5A; P<0.001, n=36). There was no white muscle activity for either flow treatment. By contrast, the average rectified area for R1 activity was not statistically different between the two flow conditions. When R1 activity was present during the Kármán gait (Fig. 5B,C), it was marked by a lower relative intensity (0.33±0.05 vs 0.74±0.06; P<0.001, n=30) and longer absolute duration time (0.18±0.03 s vs 0.06±0.01 s; P<0.005, n=30) than that seen for R1 activity during swimming in uniform flow. Average, rectified R1 EMG traces for all five fish showed that relative onset time of R1 muscle activity (Fig. 6A,B) occurred earlier during the Kármán gait than for swimming in uniform flow at 3.5 L s1 (0.15±0.02 vs 0.28±0.03; P<0.05, n=30). Similarly, relative offset time of EMG bursts occurred earlier for Kármán gating trout (0.50±0.02 vs 0.65±0.02; P<0.005, n=30). As expected, trout swimming in uniform flow displayed caudal red muscle activity (R4) with delayed relative onset (0.53±0.02 vs 0.27± 0.02; P<0.001, n=42) and offset (0.71±0.02 vs 0.65±0.02; P<0.05, n=42) times compared with anterior red muscle activity (R1), illustrating the presence of an antero-posterior propagating body wave (Fig. 6A,C). By contrast, this phase delay in muscle activity was not present for trout holding station in a vortex street because they did not activate their caudal red muscles (Fig. 6B,D).
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Effect of muscle and vortices on kinematics
R1 muscle activity was correlated to certain kinematic variables during
swimming in uniform flow but not during the Kármán gait.
Specifically, R1 muscle activity was correlated to lateral head amplitude when
trout swam in uniform flow (Table
1; r2=0.68, P<0.05, n=20)
but not when trout Kármán gait (r2=0.22,
P=0.65, n=14). According to the general linear model, head
amplitude for trout swimming in uniform flow was significantly influenced by
R1 muscle intensity, duration and onset time
(Fig. 7). R1 muscle activity
was also correlated to head angle during swimming in uniform flow, but only
before a sequential Bonferroni correction adjusted the level for the
multiple independent tests required for the analysis. Note that a simple
linear regression showed a correlation between head angle and head amplitude
during swimming in uniform flow (r2=0.30,
P<0.01, n=36). Head angle was not correlated to R1 muscle
activity during the Kármán gait. Additional multiple linear
regression analyses revealed that other kinematic variables during the
Kármán gait, such as lateral body amplitude at both the R1
insertion site and the COM, were also not correlated to R1 muscle
activity.
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The motions of dead trout towed behind a cylinder were analyzed to gain
insight into the contribution of passive, vortex-induced body undulation
during the Kármán gait (Table
2). When dead trout were towed at 3.5 L
s1 on low-stretch monofilament line in the region of the
wake where live fish preferred to hold station (1.5 L downstream from
the cylinder), their motions were generally similar to live,
Kármán gaiting trout. However, quantitative kinematic analysis
revealed that live trout have higher lateral head amplitudes than towed trout
(0.10±0.01 Lvs 0.07±0.01 L, respectively;
P<0.05, n=26). Live trout also exhibit lower tail-beat
frequencies (2.21±0.06 Hz vs 2.77±0.03 Hz;
P<0.001, n=26) and longer body wavelengths
(2.14±0.08 L vs 1.47±0.07 L;
P<0.001, n=26). Only head angle was not significantly
different between live and dead trout. Taking into account blocking effects
introduced by placing the cylinder into the flow tank, the expected vortex
shedding frequency for a 5 cm-diameter cylinder in a flow of 3.5 L
s1 is 2.87 Hz, and the expected wake wavelength is 1.22
L (see Liao et al.,
2003a). Thus, the tail-beat frequency for dead trout is more
closely synchronized to the expected vortex shedding frequency than for live
trout. Similarly, the passive body of a dead trout adopts a wavelength that is
closer to the wake wavelength than that adopted for live trout.
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Discussion |
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Field observations assume that fishes in current-swept environments hold
station behind objects to save energy by drafting
(Fausch, 1993;
Heggenes, 1988
;
McMahon and Gordon, 1989
;
Shuler et al., 1994
). However,
when muscle recording and flow visualization techniques are employed, it is
clear that trout holding station behind a cylinder are using the energy of the
vortices and not just seeking refuge in reduced flow
(Liao et al., 2003b
). The
present study demonstrates that Kármán gaiting trout are not
using a traveling wave of muscle activity to generate propulsive movements
while swimming in the slower flow behind the cylinder, which would result in a
muscle activity pattern similar to that shown in
Fig. 2A. The anteriorly
localized pattern of rhythmic muscle activity during the Kármán
gait therefore reflects a shift in emphasis from propulsion to stability. When
trout are unable to effectively utilize vortices in a vortex street, as when
encountering extreme wake wavelengths or low vorticity in an environment with
high levels of background turbulence, axial muscle activity is predicted to
increase as propulsive movements are introduced into the Kármán
gait.
Contributions of muscle and vortices
The paucity of EMG signals, despite whole body undulations, reveals that
Kármán gait kinematics are largely dictated by vortices rather
than generated by axial muscle activity. Put another way, an advancing region
of low pressure down the body caused by passing vortices, rather than
sequential muscle activation, causes the body to adopt a traveling waveform.
When exposed to vortices in the cylinder wake, trout move with the transverse
(Fig. 1; z-axis)
component of the flow, generating enough thrust to balance drag to hold
position relative to the cylinder (Liao et al.,
2003a,b
).
Anterior muscles are rhythmically active during the Kármán
gait (R1, Fig. 3C; although see
discussion below on passive thrust production). However, head amplitude is
predominately determined by environmental vortices and not by muscle activity,
since R1 muscle activity is correlated to head amplitude during swimming in
uniform flow but not during the Kármán gait. This is not to say
that muscle activity does not play a potentially important role in positioning
the head favorably in the wake (e.g. muscle activity may help resist head
movement caused by vortices), only that the muscles themselves are not
controlling the absolute movement of the head at all times. The lack of
correlation between Kármán gait kinematics and R1 muscle
activity may be attributed to the fact that trout may also move their body
with their paired fins (especially the pectorals), requiring further analysis
of simultaneous paired fin and R1 muscle activity to explain body kinematics
sufficiently. These results suggest that activation of anterior axial muscles
and paired fins enables fine-scale adjustments to stabilize the body to hold
station continuously in a vortex street. An ability to control body
orientation with R1 muscle activity would lend support to the tacking
hypothesis of station holding in a vortex street
(Liao et al., 2003a), where
the camber and angle of the body must alternate from side to side to
consistently generate thrust forces.
Paired fin function and the lack of axial muscle activity
Paired fins vary widely in their movements during the Kármán
gait, ranging from oscillating, bilateral motions to sustained, unilateral
abductions. Analysis of simultaneous EMG and video data shows that when paired
fins oscillate during the Kármán gait, fish often do not exhibit
any axial muscle activity (Fig.
4). As control surfaces located anterior to the COM, paired fins
can play a large role in controlling forces generated from three-dimensional
interactions between the body and vortices. For example, the increased drag
produced by abduction of one pectoral fin was commonly observed to cause the
body to yaw to the same side, thereby changing the head angle that might
otherwise be changed by strong anterior muscle activity. Thus, trout pectoral
fins function differently from that of classical labriform swimmers
(Drucker and Jensen, 1997;
Gibb et al., 1994
;
Walker and Westneat, 1997
) in
that they control body orientation rather than provide flapping propulsion.
Like other fishes, trout use their pectoral fins for both self-correcting
control (i.e. the fin is held out stationary from the body and not oscillated)
and powered movements (i.e. when the fin actively moves relative to the body)
to stabilize body position (Drucker and
Lauder, 2003
; Webb,
1998
) and resist absolute upstream movement in a vortex street
(Liao et al., 2003a
). These
observations suggest that paired fins may play a larger locomotory role in
perturbed environments than in uniform flows. In addition, median structures
such as the dorsal and anal fin can dramatically alter the lateral body
profile and thus enhance the ability for vortex capture.
Passive thrust production in an oscillating flow
Both hydrodynamic theory and experimental data demonstrate that a passive
(i.e. non-actuated) foil can generate thrust when placed in an oscillating
flow (Beal, 2003;
Bose and Lien, 1990
;
Wu and Chwang, 1975
). As a
foil heaves from side to side in an oscillating flow such as a
Kármán street, its chord maintains a favorable angle of attack
with respect to the incident flow and thus generates lift and thrust
(Bose and Lien, 1990
;
Wu and Chwang, 1975
). Thrust
establishes a moment that acts to pitch the foil such that its trajectory
across the oscillating flow proceeds at a beneficial lift-generating angle
(Wu and Chwang, 1975
). At
predictable times during the foil's phase-locked oscillation cycle, the
transverse flow velocity also generates lift forces that act in the direction
of heaving, additionally facilitating the side to side motion of the foil.
This phenomenon is impossible in uniform flow, which by definition is limited
to a horizontal flow component (Fig.
1; x-axis). Since a flexible foil is a closer
approximation to the undulating body of a fish than a rigid foil, Wu and
Chwang's (1975
) mechanism of
passive thrust generation can be conceptually applied to a
Kármán gaiting trout by treating the body as a series of linked,
rigid foils where each foil is anchored to its neighboring foils. Differential
flow velocity across both surfaces of a flexible foil can generate thrust much
like a rigid foil. The flexible foil differs in that it can be dynamically
cambered according to local flow conditions, such that the orientation of
individual sections is angled to the incident flow in a time-dependent, and
presumably favorable, manner. In theory, it is possible that a trout in which
no axial muscles are activated can passively generate thrust while in a vortex
street. This is supported by experimental data showing that live trout can
Kármán gait temporarily without any axial muscle activity
(Fig. 4).
To test the hypothesis that trout can passively produce thrust when
phase-locked in a vortex street, freshly killed trout were towed 1.5
L downstream from the cylinder. Experiments on euthanized animals
have previously yielded valuable insight on the functional role of the
musculoskeletal system's intrinsic properties during aquatic locomotion. For
example, when dead anuran larvae were externally actuated to swim, their
swimming kinematics and pattern of vortex shedding were similar to those of
live larvae, supporting the finding that the posterior portion of the tail
undulates passively in live animals
(Wassersug and Hoff, 1985).
Likewise, electrical stimulation of the precaudal muscles in dead pumpkinseed
sunfish demonstrated that a mechanical body wave, once initiated, could
propagate passively down the entire body
(McHenry et al., 1995
).
Dead trout towed downstream of the suction region of a cylinder
(Liao et al., 2003a) not only
synchronized their body kinematics to the vortex street but also frequently
moved upstream on slack line, conclusively demonstrating that thrust can be
generated passively. Note that towed rubber fish models of varying
stiffnesses, and even frozen trout, once completely thawed, did not move
upstream on slack line, indicating that proper body compliance is crucial for
passive thrust generation in a vortex street. The oscillating body motions of
dead, towed trout were generally similar to live, Kármán gaiting
trout volitionally holding station behind the cylinder. In both cases, head
angle was the same, posterior body oscillations were similar in amplitude,
tail-beat frequency approached the vortex shedding frequency of the cylinder,
and body wavelength was longer than the wake wavelength
(Fig. 8A,B). Previous work has
shown that Kármán streets with the same vortex shedding
frequency but different wavelengths elicit similar head angles in trout
(Liao et al., 2003a
) but could
not address whether head angle was a result of vortex buffeting or axial
muscle activity. The present study shows that head angles are the result of
vortex interactions and are not controlled by anterior red axial muscles.
Statistically identical head angles in dead and live trout behind a cylinder
(Table 2) support the idea that
vortices may play a large role in automatically aligning the head angle to
facilitate Kármán gaiting. This suggests that head angles in
live fish need not be the result of anterior muscle activity or paired fin
movements, given that fish are positioned an appropriate distance downstream
from the cylinder. Therefore, as the result of the inherent compliance of
their musculoskeletal system and their downstream positioning in a vortex
street, trout can generate thrust in oscillating flows using a similar
mechanism to that outlined for rigid hydrofoils
(Wu and Chwang, 1975
). These
data reveal, paradoxically, that at times no axial muscle activity is needed
for fish to hold station in turbulent flows.
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Quantitative analyses show that Kármán gait kinematics do
differ between dead and live trout. When dead trout synchronized to the vortex
wake and moved forward on slack line, their body kinematics were analyzed for
several tail-beats. Compared with live trout, dead trout behind a cylinder
have a relatively shorter body wavelength and higher tail-beat frequency,
which not surprisingly is in closer accord to the hydrodynamic characteristics
of the vortex street. Consequently, this suggests that Kármán
gaiting live trout have a greater body stiffness than dead trout towed in the
cylinder wake. However, live trout show no evidence of stiffening their body
via simultaneous, bilateral muscle activation
(Fig. 3C), as has been found
previously for steadily swimming (Long,
1998) and startled (Westneat
et al., 1998
) fishes. Greater body stiffness in live trout,
perhaps conferred by postural or tonic muscle activity
(Brainerd and Monroy, 1998
),
may augment the ability to Kármán gait continuously in a vortex
wake.
Towed trout frequently pitched and rolled about their body axis. As a result of this instability, dead trout spent proportionately less time Kármán gaiting than did live trout. That is, when towed trout stabilized enough to Kármán gait they were more frequently drawn upstream into the suction region than live trout, ultimately coming into physical contact with the cylinder. The paired fins of dead trout were not observed to be passively abducted by the unsteady flows of the vortex street. This seems to suggest that paired fins play a key role in stabilizing the body in the vortex street by generating drag rather than by producing thrust. Therefore, the ability to Kármán gait continuously relies on the selective ability to produce drag to stay in the appropriate downstream region of the vortex street and avoid the suction region rather than on active body undulation to produce thrust. The difference in kinematics between dead and live trout emphasizes that, while a fundamental component of the behavior may be passive, the ability to Kármán gait consistently requires active control.
A novel pattern of rhythmic muscle activity in swimming fish
The concept of a central pattern generator (CPG) may provide a valuable
framework to understand the novel pattern of muscle activity during the
Kármán gait. CPGs are coordinated networks of neurons that can
produce rhythmic body movements such as swimming in the absence of sensory
feedback (Brown, 1914;
Cohen et al., 1988
;
Grillner and Wallén,
1985
). Spinal preparations of lampreys and dogfish have taken
advantage of this fact and contributed enormously to our understanding of the
feedforward aspects of CPGs (Cohen and
Wallén, 1980
; Grillner,
1974
; Grillner and
Wallén, 1984
). Despite wide recognition that sensory
feedback is an integral part of CPGs during natural behaviors
(Cohen, 1992
;
Grillner and Wallén,
1984
), data on how environmental conditions can alter CPGs during
adaptive locomotion are less forthcoming (but see
Sillar and Roberts, 1992
).
Along these lines, turbulent flows characteristic of many aquatic environments
pose a unique challenge to the neuromuscular system of fishes because they
warrant an adaptive response; a fish must be able to accommodate potentially
destabilizing flows while still generating motor commands to provide
propulsion.
The ability to Kármán gait continuously (vs short
bouts in dead, towed trout) requires sensory feedback. When trout respond to
periodic vortices, such as are commonly shed behind inanimate objects in flow
and by propulsive animals (Webb,
1998; Weihs,
1973
), they display a motor pattern unlike that of any documented
for swimming fish. Kármán gaiting trout abandon the sequential
muscle contraction template of steady undulation and reveal the ability to
decouple segmental muscle activity both down and across the body. Does the
ability to selectively shut off motor output in all but the anterior-most
region of an undulating body provide evidence for the modulation of a
pre-existing CPG? Studies have demonstrated that multiple CPGs exist along the
spinal cord and can generate rhythmic activity independently of their
neighbors (Grillner and Kashin,
1976
; Grillner and
Wallén, 1984
). While the periodic nature of a vortex street
offers a tractable system by which to study how animals interact with
vortices, at the same time exposing a moving animal to a rhythmic stimulus
poses a challenge in interpreting the animal's motor response. Is the rhythmic
muscle activity of the Kármán gait due to the action of a CPG or
is it simply a local feedback response to periodically encountered
vortices?
A study based on kinematics and EMGs alone cannot conclusively answer this
question; both mechanisms are feasible. However, the following two lines of
evidence would certainly suggest that Kármán gait muscle
activity could be under the influence of a CPG. First, if indeed under the
control of a CPG, Kármán gait muscle activity should exist in
the absence of sensory feedback. This hypothesis could be tested by blocking
the sensory systems of trout to see if they could still Kármán
gait continuously. The ability to do so would suggest that a default motor
program exists and it has been entrained to an external stimulus. Evidence for
CPG synchronization to an external stimulus already exists in fishes; the
rhythmic, undulatory movements of spinal dogfish and lampreys can readily be
made to entrain on a physical or hydrodynamic stimulus
(Grillner, 1974;
Grillner and Wallén,
1984
). In the absence of two major sensory modalities, vision and
the lateral line (responsible for detecting water flow), trout have been shown
to continuously hold station behind a cylinder
(Montgomery et al., 2003
; J.
C. Liao, manuscript in preparation). These data suggest that trout may be
employing a default motor pattern and are not just reacting reflexively to the
presence of local vortices. Second, if a vortex was additionally introduced
out of phase to the shedding cycle of the cylinder and elicited a motor
response, this would imply that fish are reacting to vortices on a case by
case basis. However, if the introduced vortex does not elicit a motor response
but instead the motor output pattern continues to track the default frequency
imposed by the cylinder shedding frequency, this would suggest that there is
indeed a pattern generator at work. Alternatively, shed vortices could be
abruptly stopped to see if fish still exhibited rhythmic motor patterns of the
same frequency as the vortex shedding frequency. This could be accomplished by
generating vortices with a vertical strut (as in
Webb, 2004
) oriented along the
plane normal to the flow instead of a cylinder, with a sudden rotation of the
strut parallel to the flow causing a stop in vortex generation.
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Acknowledgments |
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