Department of Biology and Program in Movement Science, Washington University, St. Louis, Missouri 63130
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ABSTRACT |
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Earhart, Gammon M. and Paul S. G. Stein. Scratch-Swim Hybrids in the Spinal Turtle: Blending of Rostral Scratch and Forward Swim. J. Neurophysiol. 83: 156-165, 2000. Turtles with a complete transection of the spinal cord just posterior to the forelimb enlargement at the D2-D3 segmental border produced coordinated rhythmic hindlimb movements. Ipsilateral stimulation of cutaneous afferents in the midbody shell bridge evoked a rostral scratch. Electrical stimulation of the contralateral dorsolateral funiculus (DLF) at the anterior cut face of the D3 segment activated a forward swim. Simultaneous stimulation of the ipsilateral shell bridge and the contralateral DLF elicited a scratch-swim hybrid: a behavior that blended features of both rostral scratch and forward swim into each cycle of rhythmic movement. This is the first demonstration of a scratch-locomotion hybrid in a spinal vertebrate. The rostral scratch and the forward swim shared some characteristics: alternating hip flexion and extension, similar timing of knee extensor activity within the hip cycle, and a behavioral event during which force was exerted against a substrate. During each cycle, each behavior exhibited three sequential stages, preevent, event, and postevent. The rostral scratch event was a rub of the foot against the stimulated shell site. The forward swim event was a powerstroke, a hip extension movement with the foot held in a vertical position with toes and webbing spread. The two behaviors differed with respect to several features: amount of hip flexion and extension, electromyogram (EMG) amplitudes, and EMG duty cycles. Scratch-swim hybrids displayed two events, the scratch rub and the swim powerstroke, within each cycle. Hybrid hip flexion excursion, knee extensor EMGs, and hip flexor EMGs were similar to those of the scratch; hybrid hip extension excursion and hip extensor EMGs were similar to those of the swim. The hybrid also had three sequential stages during each cycle: 1) a combined scratch prerub and swim postpowerstroke, 2) a scratch rub that also served as a swim prepowerstroke, and 3) a swim powerstroke that also served as a scratch postrub. Merging of the rostral scratch with the forward swim was possible because of similarities between the sequential stages of the two forms, making them biomechanically compatible for hybrid formation. Kinematic and myographic similarities between the rostral scratch and the forward swim support the hypothesis that the two behaviors share common neural circuitry. The common features of the sequential stages of each behavior and the production of scratch-swim hybrids provide additional support for the hypothesis of a shared core of spinal cord neurons common to both rostral scratch and forward swim.
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INTRODUCTION |
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A task is a behavior in which an organism achieves a particular
goal. Each task may be accomplished in more than one manner. Each
different motor strategy used to perform a particular task is called a
form of that task (Stein et al. 1986b). Locomotion is a
task where the goal of the organism is to move its center of mass.
There are several forms of overground locomotion, e.g., forward walking
versus backward walking (Buford and Smith 1990a
,b
; Grasso et al. 1998
; Stein and Smith 1997
;
Thorstensson 1986
; Winter et al. 1989
).
For some rhythmic behaviors, the features of two forms or tasks are
combined into a single behavior such that each cycle expresses features
of both forms or tasks. This blended behavior is called a hybrid
(Carter and Smith 1986a
,b
; Mortin et al.
1985
; Robertson et al. 1985
; Stein et al.
1986a
,b
).
The turtle spinal cord can produce hindlimb motor outputs for scratch
and swim tasks. During scratch, the goal of the turtle is to rub
against a stimulated site on the shell; during swim, the goal of the
turtle is to generate force against the water and move its center of
mass. There are three forms of scratch: rostral, pocket, and caudal;
each is used to rub a specific region of the shell (Mortin et
al. 1985). There are two forms of swim: forward swim and
backpaddle (Field and Stein 1997a
,b
; Lennard and
Stein 1977
; Stein 1978
). We focus on the rostral
scratch and the forward swim in the present paper.
Both the rostral scratch and the forward swim have behavioral events
during which force is exerted against a substrate. The rostral scratch
event is the rub of the foot against the stimulated site on the midbody
shell bridge (Field and Stein 1997a; Mortin et
al. 1985
). The forward swim event is the powerstroke, a hip extension movement with the foot held vertically and the toes and
webbing spread (Davenport et al. 1984
; Field and
Stein 1997a
; Lennard and Stein 1977
;
Stein 1978
; Zug 1971
). During the forward swim powerstroke, propulsive force is exerted against the water. In the
present study, the turtle's carapace was restrained; thus there was no
center-of-mass movement when the swim powerstroke occurred. The rostral
scratch and the forward swim are kinematically similar (Field
and Stein 1997a
,b
; Stein 1983
). Their motor
patterns are also similar: both have alternating hip flexor and
extensor activity and similar timing of monoarticular knee extensor
activity within the hip cycle [electromyograms (EMGs): Stein
and Johnstone 1986
; electroneurograms (ENGs): Juranek
and Currie 1998
, 2000
). Their motor patterns
differ with respect to amplitudes of activity. Juranek and
Currie (1998
, 2000
) have also demonstrated
interruption of fictive rostral scratch with fictive forward swim, and
vice versa.
The present paper demonstrates a novel interaction between the rostral
scratch and the forward swim. We provide kinematic and
electromyographic evidence for a scratch-swim hybrid behavior with
combined features of two distinct tasks, rostral scratch and forward
swim, in each of several successive cycles of a rhythmic movement.
Blending of two forms of the same task has been demonstrated previously
for scratching in the spinal turtle (Mortin et al. 1985;
Robertson et al. 1985
; Stein et al.
1986a
). This is the first demonstration in the spinal turtle of
blending of two different tasks to form a hybrid. Our data were
presented previously in an abstract (Earhart and Stein
1999
).
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METHODS |
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Surgical preparation
Red-eared turtles (n = 10), Trachemys
scripta elegans, were studied. All surgery was performed under
hypothermic anesthesia (Melby and Altman 1974). Turtles
were placed in crushed ice for at least 1 h before the start of
surgery and kept in ice throughout the procedure. For spinalization, a
channel was drilled along the midline of the carapace over the second
(D2) and third (D3) dorsal segments of the spinal cord. The spinal cord
was completely transected between the D2 and D3 segments, a wax well
was constructed around the midline channel over the exposed spinal
cord, and the well was filled with turtle saline.
After complete transection of the spinal cord, electrodes were
implanted in selected hindlimb muscles: a biarticular knee extensor
(triceps femoris pars iliotibialis), a monoarticular knee extensor
(triceps femoris pars femorotibialis), a hip flexor (puboischiofemoralis internus pars anteroventralis), and a hip extensor
(flexor cruris pars flexor tibialis internus) (Robertson et al.
1985). We used bipolar electrodes, each a pair of 100-µm silver wires with enamel coating that were glued together with Permabond 910 (National Starch and Chemical, Englewood, NJ). For hip
flexor implantation, a rectangular opening was drilled in the ventral
plastron over the pelvic region, providing access to the hip flexor
muscle belly. For the knee extensors and hip extensor, a triangular
opening was drilled in the dorsal carapace, and muscle bellies were
accessed through small incisions of the overlying skin. Electrodes for
the knee extensors and hip extensor were threaded under the skin and
into the internal cavity exposed by the hole in the carapace. Electrode
tips were implanted directly into the muscle bellies and glued in
place. Following electrode placement in the hip flexor, the hip flexor
electrode was glued to the plastron and the hole in the plastron was
sealed with wax. Following electrode placement in the knee extensors
and hip extensor, the knee extensor and hip extensor electrodes were
secured to the sides of the hole in the carapace, which was then sealed
with wax. Skin incisions overlying the implanted knee extensors and hip
extensor were closed with glue and covered with Op-Site (Smith and
Nephew Medical Unlimited, Hull, UK). The turtle was removed from ice
and warmed to room temperature.
Stimulation and recording
Reflective markers were placed over the hip, knee, ankle, and
third toe of each turtle. A band clamp that encircled the midbody was
used to suspend each turtle in a tank of water. The water level was
adjusted so that the turtle's limbs remained below the water but the
turtle could lift its head above the water for breathing. Rostral
scratching was evoked using the smooth glass tip of a probe to
stimulate mechanically the shell bridge at the SP2 site (Fig.
1) (Mortin et al. 1985).
Force was recorded using a Grass FT-03 force transducer (Astromed, West
Warwick, RI) attached to the probe. Forward swimming was evoked by
electrical stimulation of the dorsolateral funiculus (DLF) at the
anterior cut face of the D3 segment of the spinal cord (Fig. 1)
(Lennard and Stein 1977
). The cut face was accessed in
the midline channel drilled for spinalization. Distinctions between
gray and white matter were clearly visible on the anterior cut face,
allowing for visual identification of the DLF. Electrical stimulation
was delivered via the cut ends of a bipolar electrode, consisting of a
pair of 75 micrometer silver wires with enamel coating. The stimulating electrode was placed under visual guidance, and DLF stimulation in the
ranges of 2-10 V, 30-50 Hz, and 0.4-.6 ms pulse durations was
delivered. Stimulation of some DLF sites within the ranges specified
did not evoke a forward swim. In these cases, the electrode was moved
to a new site until stimulation within the specified ranges evoked a
forward swim in the hindlimb contralateral to the side of stimulation.
Seven of the 10 turtles studied produced scratch-swim hybrids in
response to simultaneous stimulation of the ipsilateral shell bridge
and contralateral DLF. One of these seven turtles also produced
scratch-swim hybrids in response to sequential stimulation in which the
termination of ipsilateral shell stimulation was followed immediately
by the onset of contralateral DLF stimulation.
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Movement was recorded by use of a mirror placed below the tank at an angle of 45°. Hindlimb movements were videotaped at 60 Hz with a shutter speed of 1/250 s. Hindlimb scratching and swimming movements were relatively planar; thus a single camera was sufficient for measurement of joint angles. EMGs from each muscle were amplified, filtered (100-1,000 Hz band-pass), and recorded on digital audio tape (DC-5 kHz band-pass). In all turtles, the monoarticular knee extensor, the hip flexor, and the hip extensor were recorded. In five of the seven turtles that produced scratch-swim hybrids, the biarticular knee extensor was also recorded. A synchronization signal, linked to opening of the camera shutter and generated by the Peak Event Synchronization Unit (Peak Performance Technologies, Englewood, CO), was recorded on the video and the digital audio tapes so that movement data and EMGs could be synchronized for analysis.
Data analysis
Kinematic analyses were performed on a total of 210 cycles, composed of 30 cycles from each of the 7 turtles that produced scratch-swim hybrids. The 30 cycles from each turtle included 10 rostral scratch cycles in response to shell stimulation, 10 forward swim cycles in response to spinal cord stimulation, and 10 scratch-swim hybrid cycles in response to simultaneous stimulation. Episodes were selected for analysis if they contained at least five full cycles of a behavior. Video tape records of selected episodes were replayed, and the X and Y coordinates for each marker manually digitized (30 Hz) using a Peak 5.2 system (Peak Performance Technologies, Englewood, CO). Hip angle was defined as the angle between the thigh and the ventral midline of the body; knee angle was defined as the angle between the thigh and the shank (Fig. 1). Hip and knee angle values increased as the respective joints extended and decreased as the joints flexed. Toe trajectories were obtained by viewing videos frame by frame and tracing the path of the third toe on an acetate sheet placed over the video screen.
The timing of behavioral events was determined from video records. For the rostral scratch, rub was defined as the time during which the foot made contact with the stimulated shell site. For the forward swim, the powerstroke was defined as the time during which the hip was extending and the foot was held in a vertical position with toes and webbing spread.
A total of 150 episodes of EMGs (50 scratch, 50 swim, and 50 scratch-swim hybrids) was analyzed in the 7 turtles that produced scratch-swim hybrids. Each episode of scratch-swim hybrid was matched with a scratch episode and a swim episode from the same turtle. Each episode consisted of at least five cycles. EMGs were digitized at 2 kHz using Cambridge Electronic Design 1401 plus hardware and Spike2 software (Cambridge, UK). EMGs were rectified and averaged so that the mean of 20 successive rectified measurements was calculated, giving 100 data points per second.
For some episodes, only EMGs were analyzed. For other episodes, both
EMGs and kinematics were analyzed. For these episodes, software custom
written by Dr. Gavin Perry merged kinematic and EMG files, aligning the
two data sets using the synchronization signal recorded on each. Onsets
and offsets of hip flexion and knee extension movements were determined
(Field and Stein 1997a). For all episodes, EMG burst
onset and offset times for each muscle were determined. EMG amplitudes
were obtained by averaging the activity within each burst. For each
muscle, amplitudes were normalized to scratch values, such that the
amplitudes for a scratch episode were 100% and amplitudes of the
related swim and hybrid episodes expressed as a percentage of the
scratch values. Cycle period was defined as the time from the onset of
one burst of hip extensor activity to the onset of the next burst of
hip extensor activity. Duty cycle, defined as the percentage of cycle
period during which a muscle was active, was calculated as burst
duration multiplied by 100 and then divided by cycle period.
Phase analyses were used to determine the timing of knee extension
onset with respect to hip movement and the timing of monoarticular knee
extensor EMG onset with respect to hip muscle activity. Dual-referent phase analyses were used to normalize the hip flexion and hip extension
phases of each behavior. Dual-referent analyses are preferred to
single-referent techniques in situations where the duty cycle of the
referent is variable. Dual-referent methods normalize for active and
inactive periods of the referent; thus changes in referent duty cycle
will not produce shifts in phase values obtained (see Fig.
2 of Berkowitz and Stein
1994b). Events occurring during the hip flexion portion of the
cycle had phase values between 0 and 0.5, whereas those occurring
during hip extension had phase values between 0.5 and 1.0.
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Kinematic phase analyses were performed using the method described by
Field and Stein (1997a). The phase at which knee
extension onset occurred was defined as the latency between hip flexion onset and knee extension onset, divided by twice the duration of hip
flexion. All knee extension onsets analyzed occurred during hip
flexion, so calculations for events occurring during hip extension are
not presented.
Motor pattern phase analyses are described in Berkowitz and
Stein (1994b). In the present study, the hip extensor rather
than the hip flexor was chosen as a referent because the hip flexor had
very short burst durations in the forward swim and use of the hip
flexor as a referent for the swim gave inconsistent results. Using the
hip extensor as a referent, hip extensor offset was given a phase value
of 0 and hip extensor onset a phase value of 0.5. The phase of
monoarticular knee extensor onset was defined as the latency between
hip extensor offset and monoarticular knee extensor onset, divided by
twice the duration of hip extensor quiescence. All monoarticular knee
extensor onsets analyzed occurred during hip extensor quiescence, so
calculations for events occurring during hip extensor activity are not presented.
Because the phase data are cyclic, vector algebra techniques
(Batschelet 1981) were used to determine average phase
values. Each phase was converted to a two-dimensional unit vector with an angle of 2
and a length of 1. Unit vectors were averaged using
vector addition. The angle of the mean vector, divided by 2
, was the
mean phase; it had values between 0 and 1. Mean angular deviation, a
measure of phase data dispersion, was also calculated.
Statistical analyses
Kinematic and myographic parameters were compared across
conditions using nonparametric statistics. Mean minimum and maximum hip
angles, mean EMG amplitudes, mean EMG duty cycles, and mean period were
compared across behaviors using the Mann-Whitney U test
(Hays 1994). Mean phase of knee extension movement onset and monoarticular knee extensor EMG onset were compared across conditions using the Watson U2 test for circular
data (Batschelet 1981
).
Pair-wise comparisons of scratch to swim, scratch to hybrid, and swim
to hybrid were used for all statistical analyses. A Bonferroni
correction was used to account for the increase in type I error that
resulted from doing multiple tests. Because three separate pair-wise
comparisons were performed, the chosen level of 0.05 was divided by
3. All comparisons were tested at the Bonferroni-adjusted level of
0.0166. Comparisons reported to be statistically significant had values
of P
0.0166.
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RESULTS |
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Mechanical stimulation of the shell bridge at SP2 evoked rostral scratching movements in the ipsilateral hindlimb. Electrical stimulation of the contralateral DLF at the anterior cut face of the D3 segment evoked forward swimming movements in the ipsilateral hindlimb. In 7 of 10 turtles, simultaneous stimulation of the ipsilateral shell bridge and the contralateral DLF evoked a scratch-swim hybrid, a rhythmic hindlimb behavior in which features of both rostral scratch and forward swim were expressed in each individual cycle of the multicycle response in the ipsilateral hindlimb. In the other three turtles, simultaneous stimulation elicited forward swimming movements only. There were no apparent differences in the scratch or swim behaviors of these three turtles, compared with those of the seven that did produce scratch-swim hybrids. Data from the three turtles that did not produce scratch-swim hybrids were not analyzed.
Kinematics
The rostral scratch, forward swim, and scratch-swim hybrid were distinguished from one another based on toe trajectory and behavioral events (Fig. 2). During the rostral scratch and the scratch-swim hybrid, the limb reached toward and the foot rubbed against the stimulated shell site. A rub against the shell did not occur in the forward swim. The scratch rub, which constituted the only event of the rostral scratch and the first of two events of the scratch-swim hybrid, is marked by asterisks in Fig. 2, A and C. For the scratch, the toe reached its most medial position anteriorly at the stimulated site on the shell bridge, SP2. The toe also reached this medial anterior position during the hybrid, but not during the swim.
During the forward swim and the scratch-swim hybrid, the limb performed a swim powerstroke: the foot was held vertically with toes and webbing spread as the hip extended. Spreading of the toes and webbing did not occur in the rostral scratch. The swim powerstroke, which constituted the only event of the swim and the second of two events of the hybrid, is marked by thick dashed lines in Fig. 2, B and C. For the swim, the toe reached its most medial position posteriorly at a location caudal to the rear edge of the carapace. The toe also reached this medial posterior position during the hybrid, but not during the scratch.
Thus the scratch-swim hybrid displayed two events: a scratch rub and a swim powerstroke. The toe trajectory of the hybrid encompassed both the scratch and the swim toe trajectories, merging the two into a single smooth trajectory.
The rostral scratch and the forward swim were also distinguished from
one another based on minimum and maximum hip angles (Fig.
3) (see also Field and Stein
1997a). The hip flexed more in the rostral scratch than in the
forward swim and extended more in the forward swim than in the rostral
scratch. Thus the minimum hip angle was smaller in the scratch than in
the swim; the maximum hip angle was larger in the swim than in the
scratch. The scratch-swim hybrid had a minimum hip angle similar to
that of the scratch and a maximum hip angle similar to that of the
swim.
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Hip angle versus knee angle plots provided an additional means of distinguishing the rostral scratch from the forward swim. The hip angle versus knee angle plot for the scratch was roughly triangular in shape (Fig. 4A), for the swim was ovoid (Fig. 4B), and for the hybrid combined elements of the two such that the base of the triangle was merged with the upper portions of the oval (Fig. 4C).
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For the rostral scratch, the hip angle versus knee angle plot (Fig.
4A) was characterized by a horizontal base, illustrating that the knee extended while the hip remained flexed (Mortin et al. 1985). At the peak of this knee extension, the foot rubbed against the stimulated site on the shell (asterisk, Fig.
4A). A similar scratch rub occurred in the hybrid (asterisk,
Fig. 4C), and the hybrid hip angle versus knee angle plot
had a horizontal base similar to that of the scratch plot. The
horizontal base and occurrence of the scratch rub were not present in
the swim, which had a hip angle versus knee angle plot with a rounded
base. Scratch minimum knee angle, denoted by the left vertical dashed lines in Fig. 4, was smaller than swim minimum knee angle. Scratch maximum knee angle, denoted by the right vertical dashed lines in Fig.
4, was larger than swim maximum knee angle. The hybrid had minimum and
maximum knee angles similar to those of the scratch.
Hip angle versus knee angle plots also illustrated the differences in hip angle minima and maxima. The bottom horizontal dashed lines on each panel of Fig. 4 show the minimum hip angle for the scratch; the top horizontal dashed lines show the maximum hip angle for the swim. The hybrid plot spans the area between both of these lines, indicating that the hybrid had hip flexion excursion similar to that of the scratch and hip extension excursion similar to that of the swim.
Mean phase values for the onset of knee extension within the
dual-referent hip movement cycle are given in Table
1. The rostral scratch and the forward
swim had very similar phasing, with knee extension onset occurring near
the middle of the hip flexion phase (Field and Stein
1997a). Hybrid mean phase values were also very similar to
those of the scratch and the swim. Differences among the three
behaviors were not significant when testing within each turtle or
across all turtles (Watson U2).
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EMG
The rostral scratch and the forward swim motor patterns were
distinguished from one another by differences in amplitudes and duty
cycles (Juranek and Currie 1998, 2000
;
Stein and Johnstone 1986
). Figure
5 shows scratch, swim, and hybrid EMGs
with the same set of vertical scales (Fig. 5, A, B1, and
C, respectively). Figure 5B2 shows the swim data
in B1 at 10 times the set of vertical gains of A,
B1, and C. This higher gain representation is provided because the monoarticular knee extensor and hip flexor amplitudes are
so low in the swim that they are difficult to see when shown with the
same set of scales as the scratch and the hybrid, as in Fig.
5B1.
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EMG amplitudes differed among the behaviors (Fig. 6). Knee extensor and hip flexor amplitudes were significantly larger for the rostral scratch than for the forward swim, whereas hip extensor amplitude was significantly larger for the swim than for the scratch (Mann-Whitney U). Knee extensor and hip flexor amplitudes were not significantly different between the scratch and the hybrid. The hybrid had hip extensor amplitudes more similar to those of the swim than those of the scratch. Hybrid hip extensor amplitudes were significantly larger than those of the scratch or the swim (Mann-Whitney U). In summary, the hybrid had knee extensor and hip flexor amplitudes similar to scratch but hip extensor amplitudes similar to swim (compare Fig. 5, A, B1, and C).
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Duty cycle was another means of distinguishing among the behaviors (Fig. 7). Knee extensor and hip flexor duty cycles were significantly higher for the rostral scratch than for the forward swim, whereas hip extensor duty cycle was significantly higher for the swim than for the scratch (Mann Whitney U). The hybrid had knee extensor and hip flexor duty cycles intermediate between those of the scratch and those of the swim. Hybrid knee extensor duty cycles were significantly different from those of the scratch and the swim (Mann Whitney U). Hybrid hip flexor and hip extensor duty cycles were not significantly different from those of the swim, but were significantly different from those of the scratch (Mann Whitney U).
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Comparisons of cycle period across the three behaviors revealed no significant differences. Mean cycle period for the rostral scratch was 0.89 ± 0.31 (SD) s, for the forward swim was 0.92 ± 0.25 s, and for the hybrid was 1.00 ± 0.25 s. We observed differences in variability of cycle period, however, noting that the swim had a very regular period whereas scratch period was more volatile. The hybrid had a stable period similar to that of the swim. Cycle period standard deviation in the scratch was significantly larger than in the swim or the hybrid (Mann Whitney U). There was no difference in cycle period standard deviation between the swim and the hybrid.
The mean phase values for the onset of the monoarticular knee extensor
in the dual-referent hip extensor cycle are given in Table 1. Rostral
scratch and forward swim had very similar phasing, with monoarticular
knee extensor onset occurring near the middle of the hip flexor phase
(Juranek and Currie 1998, 2000
). Hybrid mean phase values were also very similar to those of the scratch and
the swim. Differences among the three behaviors were not significant when testing within each turtle or across all turtles (Watson U2).
Sequential stimulation
One of the turtles in this study exhibited a substantial scratch
afterdischarge (Currie and Stein 1990) in which four to
six cycles of scratch were produced following offset of the mechanical shell stimulation. In this turtle, we were able to obtain the scratch-swim hybrid through sequential delivery of mechanical shell
stimulation followed by electrical DLF stimulation. The mechanical
shell stimulus was used to evoke rostral scratch and, coincident with
the offset of this mechanical shell stimulation, electrical DLF
stimulation was initiated. This sequential presentation produced a
response that began with rostral scratch, showed several hybrid cycles
just after the offset of mechanical stimulation and onset of electrical
stimulation, and ended with forward swim (Fig.
8). Thus the onset of electrical DLF
stimulation at the offset of scratch stimulation evoked a swim that
combined with the scratch afterdischarge to produce the hybrid. The
average number of cycles of hybrid obtained with sequential stimulation (n = 4.8 ± 0.7 cycles) was similar to the average
number of cycles of afterdischarge obtained in scratch episodes
(n = 4.4 ± 0.8 cycles).
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The rostral scratch cycles were characterized by greater hip flexion and less hip extension than the forward swim cycles. The scratch also showed higher amplitude monoarticular knee extensor and hip flexor amplitudes and lower hip extensor amplitudes than the swim. The hybrid showed hallmark features of both the scratch and the swim. The hybrid had two events, a scratch rub and a swim powerstroke. The hybrid had a minimum hip angle similar to the scratch and a maximum hip angle similar to the swim. Hybrid monoarticular knee extensor and hip flexor amplitudes were similar to those of the scratch, and hybrid hip extensor amplitudes similar to those of the swim.
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DISCUSSION |
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The turtle spinal cord produced blends of the rostral scratch and the forward swim in response to simultaneous mechanical stimulation of the ipsilateral shell bridge and electrical stimulation of the contralateral DLF at the anterior cut face of the D3 segment. The scratch-swim hybrid displayed two events: a scratch rub of the foot against the stimulated shell site and a swim powerstroke during which the hip extended and the foot was held in a vertical position with toes and webbing spread. The hybrid toe trajectory combined the trajectories of the rostral scratch and the forward swim into a single smooth path. This is the first demonstration of a scratch-locomotion hybrid in a spinal vertebrate.
Rhythmic behavior may be characterized as a sequence of stages produced
by a pattern generator (Kleinfeld 1986). Each cycle of
rhythmic behavior may be represented by a linear chain, i.e., a fixed
sequence in which specific stages occur in a particular order
(Berridge et al. 1987
). The formation of a hybrid of two behaviors depends on the biomechanical compatibility of the stages of
the two behaviors. If the stages of two behaviors are very different,
hybrid formation may be impossible. However, if the stages of one
behavior are similar to those of the other behavior, the two will be
biomechanically compatible for formation of a hybrid via merging of the
stages of the two behaviors.
Rostral scratch and forward swim are both rhythmic behaviors in which
each cycle can be represented by a sequence of stages. Both rostral
scratch and forward swim consisted of three stages, preevent, event,
and postevent, performed in sequence during each cycle. For rostral
scratch, these stages were prerub, rub, and postrub (Mortin et
al. 1985). For forward swim, these stages were prepowerstroke,
powerstroke, and postpowerstroke (Lennard and Stein
1977
). The prerub stage of the rostral scratch and the
postpowerstroke stage of the forward swim were similar; both exhibited
hip flexion movements during which the foot was held in a horizontal
position. The rub stage of the rostral scratch and the prepowerstroke
stage of the forward swim were similar; both exhibited knee extension movements that occurred while the hip was flexed. The postrub stage of
the rostral scratch and the powerstroke stage of the forward swim were
similar; both exhibited hip extension movements, although the toes and
webbing were spread during swim powerstroke but not during scratch
postrub. We speculate that the similarities of stages in these two
behaviors provided biomechanical compatibility that was consistent with
the formation of the hybrid. The scratch-swim hybrid, like the
individual behaviors, had three stages: 1) a scratch prerub
and swim postpowerstroke combination, 2) a scratch rub that
also served as a swim prepowerstroke, and 3) a swim
powerstroke that also served as a scratch postrub. The similarity of
stages between the two behaviors and the merging of stages in the
hybrid support the hypothesis that the two behaviors share some
pattern-generating circuitry.
Previous work has noted that the minimum and maximum hip angles for the
rostral scratch and the forward swim are different (Field and
Stein 1997a). We have confirmed this result and expanded on it,
demonstrating correspondence of EMG amplitudes and duty cycles with hip
angle minima and maxima. Smaller minimum hip angles in the scratch and
the hybrid were associated with higher hip flexor amplitude and duty
cycle. Greater maximum hip angles in the swim and the hybrid were
associated with higher hip extensor amplitude and duty cycle. Higher
EMG amplitudes were associated with the behavioral events during which
force was exerted against a substrate. Higher knee extensor and hip
flexor amplitudes were associated with the scratch rub; higher hip
extensor amplitudes were associated with the swim powerstroke.
Thus rostral scratch and forward swim were distinguished from one
another by EMG amplitudes. They were not distinguished from one another
by phasing of knee movement or monoarticular knee extensor activity
within the hip cycle, characteristics that are often excellent
discriminators. Rostral scratch and forward swim had similar phasing of
movement (knee extension onset during hip flexion) and of motor
patterns (monoarticular knee extensor onset near the middle of the hip
flexor burst). In contrast, forward swim and backpaddle have very
different timings of knee extension onset; knee extension onset occurs
near the middle of hip flexion for the forward swim but near the middle
of hip extension in the backpaddle (Field and Stein
1997a). The three scratch forms can also be distinguished from
one another by phasing of knee activity within the hip cycle.
Monoarticular knee extensor onset occurs during the hip flexor burst in
rostral scratch, during the hip extensor burst in pocket scratch, and
near the offset of the hip extensor burst in caudal scratch
(Robertson et al. 1985
). In the cat, paw-shake and
locomotion can be distinguished from one another by phasing of
monoarticular knee extensor activity within the cycle of ankle motor
activity. Vastus lateralis activity coincides with ankle flexor
activity in paw-shake and with ankle extensor activity during
locomotion (Smith et al. 1986
).
Other examples of hybrids
Hybrids of two different tasks or of two different forms of a task
have been demonstrated previously. Carter and Smith
(1986a,b
) demonstrated hybrids of two different tasks,
paw-shake and stepping, in normal and in spinal cats. Cats produced
several cycles of paw-shake during the swing phase of each step cycle.
Paw-shake and stepping are biomechanically compatible for hybrid
formation because the paw-shake can be performed during swing, when the foot is not in contact with the ground, without disrupting the step
cycle. Hybrids of two scratch forms in response to two-site mechanical
shell stimulation or stimulation within a transition zone have been
demonstrated in the turtle. In rostral-pocket, pocket-caudal, and
rostral-caudal hybrids, the turtle rubs the shell twice during each
cycle (Mortin et al. 1985
; Robertson et al.
1985
; Stein et al. 1986a
,b
). Two scratch forms
are biomechanically compatible for hybrid formation because each form
has different timing of knee extension with the hip cycle to perform
the rub. Two scratch rubs of different forms can be performed during
each hip cycle to form a hybrid. These studies demonstrate that spinal structures can coordinate hybrids in the absence of supraspinal inputs.
The present study adds support to this conclusion.
Hybrids of two forms of a task have also been demonstrated in humans.
Horak and Nashner (1986) reported two forms of postural movements: the ankle strategy and the hip strategy. In response to
horizontal perturbations, subjects use the ankle strategy if standing
on a broad support surface and the hip strategy if standing on a
support surface shorter than their feet. When standing on a surface of
intermediate length, subjects use a blend of ankle and hip strategies,
an ankle-hip hybrid.
Another example of human behavior that illustrates hybrid formation is
scratching. A human can scratch some sites on the side of the thorax
using either the side of the elbow or the hand. These sites can also be
scratched using a hybrid strategy: the site is rubbed with the elbow
and then with the hand during each single cycle of movement. This is
possible because the two movements are biomechanically compatible.
Other human scratch movements are not biomechanically compatible for
hybrid formation. For example, a human scratches the upper back using a
form with the elbow positioned above the shoulder; a human scratches
the lower back using a form with the elbow positioned below the
shoulder (Stein et al. 1986b). The below-shoulder and
above-shoulder forms require very different upper extremity
orientations. Biomechanical constraints prevent the human from reaching
the upper back with the below-shoulder form or the lower back with the
above-shoulder form. A human can switch between the two forms,
performing the above-shoulder form in one cycle and the below-shoulder
form in the next cycle, but the two forms cannot be incorporated into a
single, smooth hybrid cycle because of their biomechanical incompatibility.
Shared circuitry
Our concepts of how pattern generators are organized have changed
(Stein et al. 1997). Pattern generators are no longer
viewed as static, unshared circuits each exclusive to a single
behavior. In Aplysia, cerebral interneuron CC5 is known to
participate in at least six distinct behaviors (Xin et al.
1996
). Evidence from the crustacean stomatogastric system shows
that two independent networks can fuse and operate as a single
functional unit (Dickinson 1995
; Dickinson et al.
1990
; Meyrand et al. 1994
). Svoboda
and Fetcho (1996)
demonstrated resetting of the swim rhythm by
activation of an escape behavior, supporting the concept of shared
circuitry for swim and escape in goldfish. Soffe (1993)
showed that both swimming and struggling in the Xenopus
embryo are driven by a common set of premotor and motor neurons.
Previous studies in the turtle support sharing between left and right
side scratch (rostral, pocket, and caudal) circuitry (Currie and
Gonsalves 1997
, 1999
; Field and Stein
1997b
; Stein et al. 1995
,
1998a
,b
). Single-unit recordings in turtle also support
the concept of sharing of elements among left and right rostral and
pocket scratch circuits (Berkowitz and Stein 1994a
,b
).
Single-unit recordings in cat provide support for sharing of elements
for stepping and scratching (Berkinblit et al. 1978
).
The demonstration in cats of paw-shake and step hybrids also supports
the concept of shared circuitry (Carter and Smith
1986a
,b
; Smith et al. 1986
). Thus there is
strong evidence from many systems for sharing of circuitry among
different behaviors.
Stein (1983) noted kinematic similarities between
rostral scratch and forward swim. Quantitative analyses of kinematics
confirmed this observation and led to the suggestion that there may be
sharing of circuitry between rostral scratch and forward swim networks (Field and Stein 1997a
). Motor pattern similarities,
such as similar timing of the monoarticular knee extensor within the
hip cycle, also support the possibility of shared circuitry
(Juranek and Currie 1998
, 2000
;
Stein and Johnstone 1986
). Additional support comes from
the demonstration of interruption and resetting of an ongoing forward
swim by a brief rostral scratch (Juranek and Currie
1998
, 2000
; Stein 1981
).
Differences in rostral scratch and forward swim EMG amplitudes served
to discriminate between the two behaviors. Motor pattern amplitude
differences between the behaviors may be produced by changes in
interneuronal recruitment from classes active during both behaviors. A
subset of neurons may be active during each behavior, and additional
neurons may be recruited during the behavioral event of each to
increase amplitudes during the time when force is exerted against a
substrate. These additional neurons may be recruited from unshared
populations or from within classes of neurons active during both
behaviors. Such recruitment has been demonstrated in
Xenopus, where additional interneurons not active in
low-frequency swimming are recruited during struggling and during
high-frequency swimming (Sillar and Roberts
1993;Soffe 1993
).
The kinematic and myographic similarities between rostral scratch and forward swim, as well as the similarities between the sequentially generated stages of the behaviors, support the hypothesis that network elements are shared between rostral scratch and forward swim circuits. The ability of the spinal cord to blend rostral scratch and forward swim into a single smooth behavior as demonstrated in the present paper provides additional support for this concept. We hypothesize that studies using single-unit recording techniques during rostral scratch and forward swim will reveal spinal interneurons that are active during both behaviors.
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ACKNOWLEDGMENTS |
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We thank A. Berkowitz for editorial assistance and G. Perry for software development.
This work was supported by National Institutes of Health Grants R01-NS-30786 and T32-HD-07434 and by a Promotion of Doctoral Studies Award from the Foundation for Physical Therapy, Inc. to G. M. Earhart.
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FOOTNOTES |
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Address for reprint requests: P.S.G. Stein, Dept. of Biology, Washington University, St. Louis, MO 63130.
The costs of publication of this article were defrayed in part by the payment of page charges. The article must therefore be hereby marked "advertisement" in accordance with 18 U.S.C. Section 1734 solely to indicate this fact.
Received 23 July 1999; accepted in final form 3 September 1999.
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REFERENCES |
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