Changes in locomotor activity parameters with variations in cycle time in larval lamprey
Division of Biological Sciences and Interdisciplinary Neuroscience Program, University of Missouri, Columbia, MO 65211-6190, USA
Author for correspondence (e-mail: McclellanA{at}missouri.edu)
Accepted 11 September 2002
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Summary |
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For locomotor muscle activity in whole animals, the BP values increased
significantly with decreases in T (i.e. negative slopes), while the
slopes for values versus T were not significantly different
from zero. For locomotor activity in preparations in vitro, the mean
slopes for BP values versus T, although negative, were not
significantly different from zero, and phase lags were also relatively
constant with changes in cycle time.
Increases in BP with decreases in cycle time and increases in swimming speed can be expected to generate proportionately more force per cycle, presumably to compensate for the increase in viscous resistance of moving the body more rapidly through water. By contrast, constant intersegmental phase lags will ensure that the relative timing of locomotor burst activity is constant and that an approximately single S-wave along the body is retained during different swimming speeds.
Key words: central pattern generator, coordination, phase lag, oscillator, swimming, lamprey
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Introduction |
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Undulatory locomotor behavior (i.e. swimming) in most fish and certain
aquatic amphibians is a repetitive motor act that is mediated by two basic
features (Gray, 1933a,
b
,
1936
; for reviews, see
Grillner and Kashin, 1976
;
Williams, 1986
;
Roberts et al., 1997
)
(Fig. 1). (1) At each segmental
level of the body, rightleft bending is produced by rightleft
alternation of burst activity in axial muscles; and (2) rostral-to-caudal
propagating body undulations are produced by a rostrocaudal delay of axial
muscle burst activity on the same side of the body. These features result in
an S-shaped body wave that propagates toward the tail and results in both
lateral and backward force vectors (Gray,
1933a
,
b
;
Webb, 1984
;
Bowtell and Williams, 1991
).
The lateral force vectors in the rostral and caudal body are in opposite
directions and cancel, leaving the backward components of the force that push
against the water and propel the animal forward. During swimming, there is
usually approximately one S-wave along the body during different speeds of
swimming (reviewed by Williams,
1986
). A single S-wave along the body is a highly efficient manner
in which to generate backward force during swimming, since multiple S-waves
would require additional muscle contraction forces to produce multiple regions
of sharper than normal bending of the body.
|
For swimming, the CPGs in the spinal cord are thought to consist of a chain
of left and right segmental oscillators that are coupled by reciprocal
inhibition and that produce leftright alternation (for reviews, see
Grillner et al., 1995,
2000
;
Roberts et al., 1997
).
Longitudinally in the spinal cord, the oscillators are coupled by a spinal
coordinating system that is important for generating rostrocaudal phase lags
(for a review, see McClellan,
1996
).
The lamprey, a `lower' vertebrate, utilizes the `anguilliform' mode of
swimming, in which all or most of the body is `slender' and flexible, and
lateral displacements of the body gradually increase as the undulations
propagate toward the tail (Williams,
1986; Davis et al.,
1993
; also see Grillner and
Kashin, 1976
). Swimming motor activity in the lamprey and fish can
be described by several parameters
(Grillner and Kashin, 1976
;
Wallén and Williams,
1984
; McClellan and Hagevik,
1997
) (see Fig.
1B). These include (i) cycle time (T), which is inversely
related to burst frequency (f=1/T) and swimming speed, (ii)
burst duration (BD), (iii) burst proportion (BP=BD/T), (iv) burst
delay (d) and (v) intersegmental phase lag
(
=[d/T]/N), where N is the number of
intervening body segments between the recording sites. For adult lamprey
swimming in a `swim mill', burst proportion (BP) and intersegmental phase lags
(
) are relatively constant during changes in cycle time
(Wallén and Williams,
1984
; for reviews, see
Grillner and Kashin, 1976
;
Williams, 1986
), thus:
![]() | (1) |
![]() | (2) |
Recent evidence from the isolated spinal cord of adult lamprey, in which
locomotor activity was evoked by bath-applied pharmacological agents, suggests
that intersegmental phase lags might not be constant but appear to increase
with decreasing cycle times (Tegnér
et al., 1997). However, it is not known if the parameters of
locomotor activity are controlled in a similar fashion in larval lamprey. For
example, there appear to be some minor qualitative differences in the
kinematics of swimming in adult and larval lamprey (A. D. McClellan,
unpublished observations). In addition, it has been suggested that the spinal
locomotor circuitry in larval lamprey is immature compared to adults, due to a
lack or immaturity of some types of cells
(Cohen et al., 1990
). In larval
lamprey, it is important to determine how the parameters of swimming motor
activity vary with cycle time, because this information will be necessary for
formulating and testing models of spinal CPGs.
In larval lamprey, preliminary results for brain-initiated locomotor
activity in brain/spinal cord in vitro preparations suggest that the
slopes for intersegmental phase lag versus cycle time are not
significantly different from zero (i.e. is relatively constant)
(McClellan and Hagevik, 1999
).
In the present study, a much more comprehensive analysis was made using
archival locomotor activity from several of our previous studies (see
Materials and methods for list of references) to test whether in fact burst
proportions (BP) and intersegmental phase lags (
) are constant with
changes in cycle time (T) in larval lamprey. Spontaneous or
sensory-evoked locomotor muscle activity (electromyographs, EMGs) from whole
animals as well as brain-initiated in vitro locomotor activity from
brain/spinal cord preparations were further analyzed for larval lamprey. For
each animal in the whole animal or in vitro group, the slopes of the
BP and
values versus T were determined by regression analysis,
and then statistics were used to determine if the composite slope of each
parameter versus cycle time for the group was significantly different
from zero, similar to the methods previously described
(Hagevik and McClellan, 1997
;
McClellan and Hagevik,
1999
).
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Materials and methods |
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Animal groups
EMG recordings during locomotion in whole animals
Briefly, pairs of fine copper wires (56 µm diameter) were implanted in
contact with body musculature at approximately 20% body length (BL),
40% BL and 60% BL (Fig.
2Ai; electrode configurations were either 1-2-3-4 or 1-2-3-5, see
Fig. 1B). Subsequently,
locomotor behavior and motor activity occurred either spontaneously or were
elicited by brief stimulation of the oral hood or tail. During locomotion,
muscle activity (EMGs) was recorded and stored on videotape (Neurodata DR886,
11 kHz sampling rate per channel), and episodes of locomotor activity were
selected for analysis during relatively constant velocity swimming along a
straight line (Fig. 2Aii).
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Brain-initiated locomotor activity in brain/spinal cord in vitro
preparations
In vitro brain/spinal cord preparations from lamprey were prepared
as described in detail elsewhere
(McClellan, 1994; Hagevik and
McClellan, 1994
,
1999
;
McClellan and Hagevik, 1999
).
The preparations (Fig. 2Bi) were pinned dorsal side up in a recording chamber containing lamprey Ringer's
solution (McClellan, 1990
)
maintained at 6-9°C. During recordings, the Ringer's solution contained 15
mg l-1 D-tubocurarine chloride (Sigma; St Louis, MO, USA) to block
possible muscle contractions in any remaining muscle along the notochord. It
is unlikely that curare significantly altered the in vitro rhythms,
since brain-initiated in vitro locomotor activity is virtually
identical with or without 150 mg l-1 curare in the bath, or ten
times the concentration used for the present study (N=3; P. Hinton
and A. D. McClellan, unpublished data). Suction electrodes were placed in
contact with ventral roots in the rostral (approx. 20% BL), middle
(approx. 40% BL) and caudal (approx. 60% BL) spinal cord,
which correspond approximately to segments 13, 35 and 61, respectively. In
vitro spinal locomotor activity (Fig.
2Bii) was initiated by chemical microstimulation in brain
locomotor areas, as described previously in detail
(McClellan, 1994
;
Hagevik and McClellan, 1994
;
McClellan and Hagevik,
1999
).
Measurements of the parameters of locomotor activity
Selected episodes of muscle activity during locomotor behavior were played
out on a thermal array recorder (Gould TA2000) at 50 mm s-1.
Similar procedures were used for in vitro locomotor activity, except
that this activity was integrated (=50 ms) because the signal-to-noise
ratio was not always high enough to reliably determine the onsets and offsets
of locomotor bursts (see figure 2B,C in
McClellan, 1988
). The onsets
and offsets of locomotor burst activity were digitized with interactive
software and a digitizing tablet (GTCO 1117A). Data points were imported into
a spreadsheet program (Lotus 1-2-3) for performing calculations of cycle time
(in ms), burst proportion and phase lag for each locomotor cycle (see
Fig. 1B) as well as for
obtaining graphs.
Regression analysis
For each animal, the calculated parameters of locomotor activity were
imported into a statistical analysis program (InStat), and linear regression
analysis was performed for cycle times versus each of the following
parameters: BP1, BP2, BP3, BP4, BP5, 15,
23
and
34 (Fig.
1B; for example, BP1 refers to burst proportions calculated from
activity recorded at electrode 1, while
15 refers to phase
lags calculated from burst activity recorded at electrodes 1 and 5) (see
McClellan and Hagevik, 1997
).
Linear regression analysis was used to determine the slopes and
y-intercepts of a best-fit line through the data points and whether
the points could be sufficiently described by linear analysis. For each
locomotor activity parameter (i.e. EMG or in vitro activity), the
mean slopes for all of the animals within the group were averaged to determine
the composite mean ± S.D. for that particular parameter
(Table 1).
|
Statistical analysis
First, for lamprey in the whole animal or in vitro group, the
slopes of the locomotor activity parameters versus cycle time were
used to create distribution histograms (Figs
3,
4). These histograms were then
evaluated to determine if the slopes were distributed approximately uniformly
or if there were other trends (e.g. bimodal distributions). Second, for
lamprey in the whole animal or in vitro group, the proportion of
positive and negative slopes for each locomotor activity parameter
versus cycle time was analyzed using the Sign test, as previously
described (McClellan and Hagevik,
1999), to determine if the composite slope of the parameter for
the group was significantly different from zero (i.e. P
0.05) (see
Table 1).
|
|
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Results |
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As was the case for muscle activity from whole animals, for in vitro locomotor activity, the distribution histograms of the slopes for the parameters of locomotor activity versus cycle time (range: 409-3416 ms) were approximately uniformly distributed (Fig. 4). In addition, the distributions of slopes for burst proportion versus cycle time were centered around negative values (Fig. 4A), while those for intersegmental phase lag versus cycle time were mostly centered approximately around zero (Fig. 4B).
Since the distribution histograms for the slopes of locomotor activity parameters versus cycle time were approximately uniformly distributed, use of the Sign test to evaluate this data was justified (see Materials and methods). Thus, for all lamprey in the whole animal or in vitro group, the Sign test was applied to the proportion of positive and negative slopes for each locomotor activity parameter versus cycle time to determine if the composite slope was significantly different than zero. In contrast, had the distribution histograms been multimodal, with groupings of slope values, the Sign test probably would have been inappropriate. For example, if a given distribution histogram for a parameter had been bimodal, with half of the slopes centered around a positive value and half centered around a negative value, the Sign test would indicate that the slopes are not significantly different from zero, even though this obviously is not true.
Statistical test of the slopes for the parameters of locomotor
activity
Locomotor muscle activity
In individual whole animals, analysis of locomotor muscle activity (i.e.
EMGs) indicated that there was a clear tendency for burst proportions (range
of mean values for all animals 0.12-0.44) to be larger for shorter cycle
times than for longer cycle times (see Fig.
5 and legend). For all whole animals, regression analysis (lines
in Fig. 6Ai,Bi) indicated that
most of the slopes for burst proportion versus cycle time had values
that were negative (Fig. 6Ci).
Furthermore, the mean slopes of BP versus T for each parameter (i.e.
BP1-BP5) were negative and ranged from -2.5x10-4 to
-5.0x10-4 (Table
1). Analysis of the proportion of positive and negative slopes
using the Sign test indicated that the slopes for all of the BP values
versus cycle time were significantly less than zero
(P
0.05, Table 1).
Thus, for EMGs in larval whole animals, burst proportions appear to increase
significantly with decreasing cycle times (i.e. a negative slope).
|
|
In individual whole animals, intersegmental phase lags (range of mean
values for all animals 0.0039-0.0110) for locomotor muscle activity did
not appear to vary appreciably with changes in cycle time (see
Fig. 5 and legend). For all
whole animals, regression analysis (lines in
Fig. 6Aii,Bii) indicated that
the individual slopes for phase lag versus cycle time could be
positive or negative (Fig.
6Cii). The mean slopes of
versus T for each
parameter (i.e.
23,
34 and
15) ranged from
-0.17x10-6 to -1.8x10-6
(Table 1), and analysis of the
proportion of positive and negative slopes using the Sign test indicated that
these slopes were not significantly less than zero (P>0.05,
Table 1). Thus, phase lags for
muscle activity in larval whole animals do not appear to change significantly
with variations in cycle time.
In vitro locomotor activity
For brain-initiated locomotor activity recorded from in vitro
brain/spinal cord preparations, the composite mean slopes for burst proportion
(range of mean values for all animals 0.28-0.52) versus cycle
time had negative values that ranged from -0.23x10-4 to
-1.5x10-4 (Table
1). However, application of the Sign test to the proportion of
positive and negative slopes for burst proportions versus cycle time
(i.e. BP1BP5) indicated that these slopes were not significantly
different from zero (Table
1).
For intersegmental phase lags (range of mean values for all animals
0.0013-0.0055), the composite mean slopes versus cycle time
ranged from -0.97x10-6 to -2.9x10-6
(Table 1). Applying the Sign
test to the proportion of positive and negative slopes for
versus
T indicated that these slopes were not significantly different from zero
(Table 1), similar to our
previously reported preliminary results
(McClellan and Hagevik,
1999
).
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Discussion |
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In whole animals, a negative slope for burst proportion versus
cycle time that is relatively constant (e.g. -2.0x10-4)
over a modest range of cycle times indicates that as cycle times decrease, for
example from 1000 ms to 500 ms, and swimming speed increases, burst proportion
(i.e. the relative burst duration) will increase by about 0.1 (e.g. from 0.3
to 0.4; see Fig. 6Ci). Thus,
for faster swimming speeds, locomotor bursts will occupy a larger fraction of
the cycle and generate proportionately more force per cycle. For faster
swimming speeds, this increase in force generation may be necessary to
overcome the additional viscous resistance of moving the body rapidly through
water.
In whole animals, a negative slope for burst proportion versus
cycle time could be due, in part, to sensory feedback. However, this may also
be a property of the spinal CPGs, since in in vitro preparations, the
composite mean slopes for burst proportion versus cycle time,
although not significantly different from zero, were centered around negative
values (Fig. 4A). For example,
during locomotor activity in the lamprey, spinal motoneurons receive
alternating depolarizing and hyperpolarizing synaptic potentials in a
quasi-sinusoidal fashion (Russell and
Wallén, 1983;
Wallén et al., 1985
).
As cycle times become shorter, the amplitude of this quasi-sinusoidal synaptic
drive to motoneurons would be expected to increase in order to recruit
additional neurons (Davis and Murphey,
1969
; see figure 4 in Grillner
and Kashin, 1976
). If the thresholds for action potentials are
constant, at shorter cycle times an increase in the amplitude of the
sinusoidal synaptic input to motoneurons could contribute, in part, to an
increase in burst proportion.
Why have changes in burst proportion with variations in cycle time not been
observed in previous studies in the lamprey? First, in our previous studies
with larval lamprey, variations of the parameters of locomotor activity with
changes in cycle time were not analyzed statistically. In addition, in these
previous studies (e.g. McClellan
1990), the data for all animals were pooled together, and this
tends to obscure possible changes versus cycle time because each
animal has a slightly different mean BP and mean T. Second, in
contrast to the present study that examined `free swimming' in larval lamprey,
in a previous study that involved adult lamprey swimming in a `swim-mill',
changes in BP with T were not seen
(Wallén and Williams,
1984
). These differences might be due to minor kinematic
differences of swimming in larval and adult animals. However, there may be
some differences between swimming in a swim-mill, in which water is forced to
flow past a stationary animal, and `free swimming', in which an animal must
actively generate forces against the water to mediate forward progression. For
example, running on a treadmill and running over ground, although
qualitatively similar, exhibit several kinematic
(Schache et al., 2001
;
Frishberg, 1983
) and muscle
activity differences (Murray et al.,
1985
; Wank et al.,
1998
).
In larval lamprey, during the initial phase of burrowing, when an animal
attempts to penetrate the viscous substrate (e.g. sand), mean cycle times are
significantly shorter and burst proportions are significantly larger than
during swimming (Paggett et al.,
1998). Thus, in the present study, for whole animals that swam at
the shortest mean cycle times (approximately 130-250 ms), some of the increase
in burst proportions could be in response to the resistance encountered during
rapid swimming through the water. However, even for animals that swam at
longer mean cycle times (e.g. 400-750 ms), most of the slopes for burst
proportion versus cycle time were negative (e.g.
Fig. 6Ci).
For fish swimming in a `swim mill', there is some evidence to suggest that
burst proportions can increase with decreasing cycle times. For example,
during swimming in trout (figure 4A,C in
Grillner and Kashin, 1976),
for a mean cycle time of approx. 300 ms the mean burst proportion was approx.
0.320, while for a mean cycle time of approx. 135 ms during faster swimming,
the mean burst proportion increased to approx. 0.490.
Intersegmental phase lags
For locomotor muscle activity and in vitro locomotor activity in
larval lamprey, the composite slopes for intersegmental phase lag
versus cycle time were centered around zero (Figs
3B,
4B), and none of these
composite slopes were significantly different from zero
(Table 1). Thus, it appears
that intersegmental phase lags do not change significantly with variations in
cycle time, similar to our previous results
(McClellan and Hagevik,
1999).
A constant intersegmental phase lag indicates that as cycle times decrease
and swimming speeds increase, the rostral-to-caudal delay of ipsilateral burst
activity will decrease proportionally to the duration of the cycle (see
Grillner and Kashin, 1976;
Williams, 1986
). Therefore, as
cycle times change, the relative timing of burst activity will remain
approximately constant, and a single S-wave along the body will be retained,
which is a highly efficient manner for swimming.
In adult lamprey, intersegmental phase lags of locomotor activity have been
reported to be relatively constant with changes in cycle time for both whole
animals swimming in a `swim mill' and isolated spinal cords
(Wallén and Williams,
1984). In contrast, in a more recent study with isolated spinal
cords from adult lamprey, in which locomotor activity was evoked by
bath-applied pharmacological agents, data suggest that intersegmental phase
lags might not be constant but appear to increase with decreasing cycle times
(Tegnér et al., 1997
).
There are at least two possible explanations for the opposing results found in
the present study in larval lamprey in which phase lags were relatively
constant. First, perhaps there are some minor differences in the operation of
spinal locomotor networks in larval and adult lamprey (see
Cohen et al., 1990
). Second,
for whole animal and in vitro brain/spinal cord preparations in the
present study, spinal locomotor networks were activated by descending systems
in the brain. By contrast, it is not known if application of pharmacological
agents to the isolated spinal cord activates locomotor networks with the full
complement of mechanisms that occur during descending activation from the
brain.
In theory, in the lamprey, rostrocaudal phase lags could be due to at least
three mechanisms (for a review, see
McClellan, 1996): (a) short
distance coupling between oscillators in adjacent regions of the spinal cord;
(b) long distance coupling between oscillators in more separated regions of
cord; and (c) gradients in oscillator frequency along the spinal cord. Several
lines of evidence suggest that short distance coupling is much stronger in the
descending direction than ascending coupling
(Hagevik and McClellan, 1994
;
reviewed in McClellan, 1996
)
and is the main mechanism that contributes to rostrocaudal phase lags
(McClellan and Hagevik, 1999
;
Hagevik and McClellan, 1999
;
Matsushima and Grillner, 1992
;
also see Mellon et al., 1995
;
Buchanan et al., 1995
).
Related studies in other animals
In late embryonic Xenopus laevis, swimming is produced by single
spikes per cycle in motoneurons in each segment (for a review, see
Roberts et al., 1997). During
changes in cycle time, there is a constant delay, instead of a constant phase
lag, between ipsilateral rostral and caudal spikes
(Tunstall and Roberts, 1991
).
Just a short time later, in young tadpoles, the single spikes per cycle are
replaced by bursts of action potentials, and the coordinating system then
maintains a constant intersegmental phase lag during changes in cycle time
(for a review, see Tunstall and Sillar,
1993
). It has been suggested that a head-to-tail gradient of
excitation and inhibition within the spinal locomotor networks determines the
normal anterior-to-posterior propagation of swimming motor activity
(Tunstall and Sillar, 1993
;
Tunstall and Roberts, 1994
;
also see Skinner and Mulloney,
1998
).
In crayfish, the paired swimmerets make coordinated periodic power
stroke/return stroke movements, and each pair appears to be controlled by a
separate oscillator (Ikeda and Wiersma,
1964). The rostrocaudal phase lag between the movements of each
pair of appendages is approximately 25%. Coupling between the swimmeret
oscillators is thought to be asymmetrical and dominated by ascending coupling,
and the posterior segment is thought to lead each cycle of activity
(Braun and Mulloney, 1995
;
Mulloney, 1997
; for a review,
see Skinner and Mulloney,
1998
).
In the leech, swimming is produced by alternating contractions of ventral
and dorsal musculature in each body segment. The oscillators in specific
ganglia that generate the swimming pattern are thought to be coupled
symmetrically (Friesen and Hocker,
2001) with a U-shaped excitability gradient along the ventral
nerve cord (Hocker et al.,
2000
; for a review, see Friesen
and Cang, 2001
). Furthermore, unlike the lamprey spinal locomotor
networks, in the leech both short-distance and long-distance coupling appear
to be important for coordination of swimming because the phase lags for
swimming activity in the isolated nerve cord are dependent on the number of
segments (Pearce and Friesen,
1985
). Finally, phase lags for swimming in the leech appear to be
partially dependent on sensory inputs (Cang
and Friesen, 2000
), unlike that in the lamprey
(Wallén and Williams,
1984
).
Conclusions
For swimming motor activity in larval lamprey, the slopes for burst
proportion versus cycle time were negative, and in whole animals,
these slopes were significantly less than zero. These results suggest that, as
cycle times decrease and swimming speed increases, the portion of the cycle
occupied by a burst will increase, presumably to generate additional force to
compensate for the increase in viscous resistance of moving the body rapidly
through water. By contrast, intersegmental phase lags were relatively constant
during changes in cycle time, presumably to retain the ergonomically efficient
S-shaped body wave during different speeds of swimming.
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Acknowledgments |
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