J Comp Physiol A (1996) 179:169 184
R. M. Johnston 9 A. Bekoff
Patterns of muscle activity during different behaviors in chicks:
implications for neural control
Accepted: 6 January 1996
A b s t r a c t The large behavioral repertoire that spans the
embryonic and postembryonic stages of development
make chicks an ideal system for identifying patterns of
muscle activity that are common to different behaviors
and those that are behavior-specific. The main goal of
this work was to identify the similar and dissimilar
aspects of the recruitment patterns and the regulation
of muscle activity during three distinct postembryonic
behaviors: walking, swimming and airstepping. We
identified two synergies that were common to each of
these behaviors. The synergies were not disrupted by
the absence of FT1 activity in airstepping. Within each
synergy the recruitment time, recruitment order and
duration of activity were not rigid, but varied according
to the context-specific resistance that the leg encoun-
tered. Unlike the other muscles, FT2 activity was not
recruited as part of the same synergy in each behavior.
When weight-bearing contact with the substrate did
not occur, as in swimming and airstepping, as well as in
walking in chicks with deafferented legs, FT2 activity
was not recruited as part of either synergy, but was
recruited during the time between them. Although not
identical, embryonic motility and hatching motor pat-
tern both show the two synergies described for the
postembryonic behaviors. Like the latter behaviors, the
synergies tolerated the absence of activity from specific
muscles. Thus, we suggest that the CNS produces dif-
ferent behaviors using many of the same muscles by
organizing the patterned activity around two common
synergies while permitting the different muscles that
R. M. Johnston (N:~I) 1 . A. Bekoff
Department of Environmental, Population and Organismic Biology
and The Center for Neuroscience, University of Colorado,
Boulder, CO 80309-0334, USA
Present address:
1ARL Division of Neurobiology, University of Arizona,
Tucson, AZ 85721, USA
9 Springer-Verlag 1996
participate in a synergy to be modified in tandem or on
an individual basis. Furthermore, the common syner-
gies are established early during prenatal development
in chicks.
Key words Electromyogram - Kinematics 9
Development. Chicken. Locomotion
Abbreviations alF anterior iliofibularius 9
CF caudilioflexorius - CNS central nervous
system 9 EMG electromyogram 9
F T femorotibialis 9 GL gastrocnemius lateralis 9
P1 protraction 1 9 P2 protraction 2 9 plF posterior
iliofibularis 9 R retraction 9 SA sartorius -
TA tibialis anterior 9 plF posterior iliofibularis 9
ms millisecond
Introduction
Animals display a wide variety of behaviors using many
of the same muscles (e.g. walking, airstepping, scratch-
ing and paw shake in cats, Giuliani and Smith 1985;
Koshland and Smith 1989; Pratt and Loeb 1991;
embryonic motility, hatching and walking in chicks,
Bekoff 1986, Bekoff et al. 1987; walking, searching,
rocking and grooming in stick insects, B/issler and
Wegner 1983; swimming, jumping and kicking in lo-
custs, Pfliiger and Burrows 1978; flight and walking in
locusts, Ramirez and Pearson 1988; and different
modes of walking in lobsters, Ayers and Davis 1977;
Ayers and Clarac 1978). In some cases, different behav-
iors show the same general recruitment patterns for
muscle activity (i.e. synergies) and only subtle differ-
ences in the timing and duration of motor activity
distinguish one behavior from another (Gruner and
Altman 1980; Giuliani and Smith 1985; Bekoff 1988). In
contrast, in other cases extensive changes in the timing
of muscle activity, which produces different synergies,
170 R. M. Johnston, A. Bekoff: Patterns of muscle activity during different behaviors in chicks
can distinguish one behavior from another. For
e x a m p l e , in stick insects, specific m u s c l e s t h a t e x t e n d
f r o m t h e b a s a l p a r t o f the leg to the w i n g in t h e s a m e
s e g m e n t , a r e a c t i v a t e d as a g o n i s t s d u r i n g w a l k i n g , b u t
r e c r u i t e d as a n t a g o n i s t s d u r i n g flight ( B a s s l e r 1989).
In cats, specific m u s c l e s o f the h i n d l i m b a r e r e c r u i t e d
d u r i n g the s a m e s y n e r g y d u r i n g w a l k i n g , b u t in
different s y n e r g i e s d u r i n g p a w s h a k e ( S m i t h 1986).
T h u s , b y r e o r g a i n z i n g the s y n a p t i c i n p u t s c o n v e r g i n g
o n t o the m o t o r n e u r o n s the n e r v o u s c a n p r o d u c e
a v a r i e t y o f m o t o r p a t t e r n s u s i n g m a n y o f the s a m e
muscles.
V a r i o u s s o u r c e s of m o d u l a t o r y i n p u t s h a v e b e e n
s h o w n to influence specific f e a t u r e s o f t h e m o t o r p a t -
t e r n s in different b e h a v i o r s . S e l e c t e d e x a m p l e s i n c l u d e
n e u r o m o d u l a t o r y influences t h a t d i c t a t e the e x p r e s s i o n
o f v a r i o u s m o t o r p a t t e r n s in the s t o m a t o g a s t r i c s y s t e m
o f d e c a p o d c r u s t a c e a n s ( M e y r a n d et al. 1991; W e i m a n n
et al. 1991); b r a i n s t e m m e c h a n i s m s i n v o l v e d in c h o i c e
o f e l e c t r o m o t o r b e h a v i o r in fishes ( K e l l e r a n d H e i l i g e n -
b e r g 1989); s p i n a l m e c h a n i s m s r e s p o n s i b l e for s e l e c t i o n
of different t y p e s o f s c r a t c h reflexes in t u r t l e s (Stein a n d
C u r r i e 1989); a n d the i n f l u e n c e o f s e n s o r y afferents
r e s p o n s i b l e for the i n i t i a t i o n o f h a t c h i n g in c h i c k s
(Bekoff a n d K a u e r 1982; B e k o f f a n d S a b i c h i 1987).
Thus, establishing the relationships among behaviors
has facilitated our understanding of how behaviors are
organized by the CNS and by modulatory inputs.
C h i c k e n s p r o v i d e a n i d e a l s y s t e m in w h i c h to e x a m -
ine the r e l a t i o n s h i p s a m o n g b e h a v i o r s . D u r i n g the e m -
bryonic and postembryonic stages of development,
chicks produce a variety of behaviors involving the
legs, such as different t y p e s o f e m b r y o n i c m o t i l i t y ,
h a t c h i n g , w a l k i n g , b a c k w a r d w a l k i n g , s w i m m i n g , air-
stepping, jumping, foot shaking and head scratching.
P r e v i o u s w o r k e s t a b l i s h e d the r e l a t i o n s h i p s b e t w e e n
h a t c h i n g a n d w a l k i n g b e h a v i o r s ( B e k o f f et al. 1987).
H o w e v e r , less is k n o w n a b o u t the r e l a t i o n s h i p s a m o n g
different p o s t e m b r y o n i c b e h a v i o r s . T h e g o a l o f this
s t u d y w a s to i d e n t i f y t h e c o m m o n a n d d i s t i n c t f e a t u r e s
o f m o t o r a c t i v i t y d u r i n g t h r e e different p o s t e m b r y o n i c
b e h a v i o r s : w a l k i n g , s w i m m i n g a n d a i r s t e p p i n g . By se-
lecting b e h a v i o r s f r o m the s a m e d e v e l o p m e n t a l stage,
b u t w h i c h o c c u r r e d in different c o n t e x t s , we h o p e d to
r e v e a l the e x t e n t to w h i c h the r e c r u i t m e n t p a t t e r n s a n d
r e g u l a t i o n o f m u s c l e a c t i v i t y c o u l d be m o d i f i e d . W e
show that not only are common recruitment patterns
seen a m o n g these t h r e e b e h a v i o r s , b u t t h a t these re-
cruitment patterns are shared with embryonic behav-
iors as well.
Materials and methods
Animals
Experiments were performed on 1-to- 3 day old chicks (Gallus gallus)
hatched from fertile eggs obtained from a local supplier and incu-
bated at the University of Colorado, Boulder. Chicks were housed
in heated and lighted bins with food and water ad libitum. The
results presented here were collected from 10 different chicks per
behavior with 10 separate measurements per chick. This sample size
was determined to be appropriate for estimating population para-
meters and reducing the Type l error rate for a two-level nested
experimental design (Sokal and Rohlf 1995; Machlis et al. 1985).
Chicks were selected for this study based on their ability to initiate
walking in response to the sound made by lightly tapping a finger on
a table.
Electromyograms
Electomyogram (EMG) recordings were used to provide a measure
of the output of the motor circuits within the central nervous system.
Each chick was anesthetized with halothane and maintained on
a respirator throughout the preparation procedure. Bipolar hook
electrodes made from enamel-coated stainless steel wires (75 ~m
diameter) were implanted through a small incision in the overlying
skin into the major muscles of the right leg parallel to the long axis of
their fibers. The electrode wires were threaded underneath the skin
to the mid-lumbar region and attached to the long recording leads.
The leads were light-weight and flexible and allowed the chick to
move about freely. A one cm length of shielding wire attached to the
recordings leads was reinforced with solder and fashioned into the
shape of a thin, smooth tongue. This was inserted between the
rostral region of the synsacrum (Fig. 1D) and the overlying skin and
secured in place with cyanoacrylate adhesive. The anchored tongue
provided a stable base for connecting the electrodes to the recording
leads. This provided no apparent discomfort to the animals or
irritation to the surrounding tissues.
To monitor intralimb coordination, recordings were made
from 6 major muscles of the right hindlimb (Fig. 1A): gastrocnemius
lateralis (GL-ankle extensor), tibialis anterior (TA: ankle
flexor), femorotibialis (FT: knee extensor), caudilioflexorius (CF:
hip extensor-knee flexor), sartorius (SA: hip flexor-knee extensor)
and iliofibularius (IF: knee flexor-hip extensor) (muscle nomen-
clature and functions are based on Bekoff and Kauer 1984). To
monitor interlimb coordination, the left GL was implanted as
well. Following recovery from the anesthetic, chicks were housed
individually in heated and lighted bins with food and water ad
libitum. The chicks were allowed to recover for 24 h before record-
ings began.
Chicks were enticed to walk along a runway by lightly tapping on
the opposite end of the runway. As discussed previously (Johnston
and Bekoff 1992), we did not restrict the speed at which the chick
moved along the runway and refer to the entire range of this mode of
locomotion as walking. However, we did omit any walking episodes
where the chick deviated from a straight path and the beginning and
ending steps. For analysis we selected steps from the middle portion
of an episode where there were no apparent changes in walking
speed. Swimming behavior was observed when a chick was placed in
a Plexiglas tank of warm water (approximately 35C). Chicks are
buoyant and capable of propelling themselves through the water
quite well. However, to avoid potential differences in muscle activity
associated with turning behavior, we recorded swimming in place by
holding onto the recording leads near the synsacrum while taking
care not to support the chick in any way. To elicit airstepping
behavior each chick was suspended with its legs pendent by holding
the recording leads close to the synsacrum. The chicks showed no
discomfort in any of these experimental situations. EMG activity
was amplified, filtered, and stored on a Vetter eight channel recorder
for subsequent analysis. Following each recording, the chicks were
euthanised with carbon dioxide as recommended by the Panel on
Euthanasia of the American Veterinary Medicine Association
(1993). Post-mortem dissections were used to confirm the precise
location of each electrode.
R. M. Johnston, A. Bekoff: Patterns of muscle activity during different behaviors in chicks
B cP
k,,,dllta~ ~.A~-L . J.L,I L,a..~
BD
i i
Time (ms)
D S
I 'ankl
Fig. 1 A Muscles of the hindlimb examined using electromyogra-
phy (see text for further explanation and abbreviations). B An
example of an E M G record showing the variables used to quantify
the motor activity. CP, cycle period with respect to the reference
muscle; L, latency to onset of activity with respect to the reference
muscle; BD, burst duration. C Diagram representing the average
patterned activity normalized to cycle period: latency/cycle period
and duration/cycle period. The onset of each bar represents the mean
phase value for a muscle and the length of each bar represents the
mean normal duration value for a muscle. Abscissa represents nor-
malized cycle period. Two normalized cycles are shown. D Drawing
of the right hindlimb and pelvic skeleton of a post-hatching chick.
Dots on the skeleton represent ink marks placed on the skin overlying
bony landmarks of the lateral surface of the hindlimb: anterior and
posterior synsacrum (s), the proximal and distal ends of the femur
(/), distal end of the tibiotarsus (tb) and the midpoint of the tar-
sometatarsal (tm) segment. These points were digitized to generate
a stick figure representation of the leg as shown in the ('enter panel.
Changes in joint angle calculated from the stick figures were plotted
versus time. An increase in joint angle was defined as extension and
a decrease in joint angle was defined as flexion
E M G activity synchronized with movement kinematics
A Video/EMG synchronizer was used to directly correlate muscle
activity and the overt motion of the hindlimb. The synchronizing
device, when supplied with a video signal, generated a numeric
display that was updated prior to the start of each new video field
(i.e. every 16.7 ms). In addition, a variable amplitude DC voltage was
171
C
i, r CP
1
1
L
i
i
BD
o o.s l'.o ;.s
Normalized cycle period
,"\ flexion
<
\k// \\J l
extension
Time (ms)
generated which was used to synchronize the numeric display to the
concurrent E M G recording.
In each behavior, five chicks were used for synchronizing the
E M G recordings with the movement kinematics. In addition to
implanting EMG electrodes in select muscles, the hindlimb was
prepared for video recordings as described previously (Johnston and
Bekoff 1992). Basically, the skin overlying the knee was secured to
the underlying cartilage of the femur and the hip, knee and ankle
joints where marked with small, black dots (Fig. 1D). Video record-
ings were made as each animal performed each behavior. Kinematic
data were digitized once every 16.7 ms using Peak Performance
software. E M G activity was collected and stored as described above.
The numeric synchronizer display allowed us to correlate on a one-
to-one basis each video field with a DC voltage trace on the E M G
recordings. The latency to bursting activity in a given muscle was
quantified with respect to onset of extension (and flexion) move-
ments at each joint (Fig. 1D). An increase in joint angle was defined
as extension and a decrease in joint angle was defined as flexion. In
addition, we described the position of the leg during each behavior
based on retraction and protraction stages (for complete details on
defining movement stages and kinematic details refer to Johnston
and Bekoff 1992). Briefly, in each behavior a cycle contained
one retraction period and two protraction periods. Retraction
(R) was defined from the onset of hip extension to the onset of
hip flexion, which marked the beginning of the first protraction
period. Protraction 1 (P1) lasted until the onset of knee extension
which corresponded to the beginning of the second period of pro-
traction. Protraction 2 (P2) continued until the leg began the next
retraction period. In walking, retraction roughly corresponded to
the stance phase and protraction corresponded to the swing phase of
the cycle.
172 R.M. Johnston, A. Bekoff: Patterns of muscle activity during different behaviors in chicks

Analyses and variable definitions
Quantitative analysis of EMG recordings were used to describe and
compare the motor activity of walking, swimming and airstepping.
Data were analyzed using Run Technologies software and values for
cycle periods, burst durations, latencies, normalized durations and
phase values were calculated (Fig. 1B, C). A cycle was defined from
the onset of bursting activity in GL to the onset of the next activity
period in GL; cycle period was defined as the duration between
contiguous cycles. Within each cycle the burst duration of a given
muscle was defined from the onset of activity to the offset of activity.
To quantify whether the onsets in different muscles occurred syn-
chronously, the latency to bursting activity with respect to the
beginning of the cycle (GL onset) was quantified. Burst durations
and latency to burst onset were also expressed as a proportion
of their cycle period to define normalized duration and phase,
respectively.
Except where indicated, all means are based on N = 10 for each
behavior: 10 animals per behavior with 10 separate values per
animal. A critical level of ~ < 0.05 and two-tailed probabilities were
used to determine statistical significance throughout this study. We
compared sample means within and among behaviors using analysis
of variance in conjunction with Tukey's HSD post hoc test (Systat,
1992). Percentages and proportional data were transformed prior to
testing. In addition, all assumptions for the statistical tests used in
this study were met. To determine whether average burst durations
show similar degrees of variability, the ratio of their variances (i.e.
mean square) for specific pairs of muscles were statistically com-
pared based on an F distribution (Sokal and Rohlf 1995). Regression
analysis was used to describe the relationship between burst dura-
tion and cycle period. Although both of these variables are depen-
dent (i.e. they each vary), we calculated least square regressions
rather than Model II regressions (Sokal and Rohlf 1995) to facilitate
comparisons with other studies. However, analyses based on the
Model II approach did not result in different conclusions. In the
regressions, the slope, /3, described the linear relationship between
the burst duration and cycle period; the coefficient of determination,
r 2, described the proportion of the variation in these data that was
accounted for by the regression. In addition, we took advantage of
the assumption test of homogeneity of slopes in analysis of
covariance to determine whether specific slopes differed statistically
from one another.
Results
Interlimb coordination
Despite the common pattern of alternating movements
between right and left legs, these three behaviors
showed differences in interlimb coordination (Fig. 2).
In walking (Fig. 2A), activity in the right GL overlap-
ped activity in the left GL during a significant and large
portion of the cycle (25%). The onset of activity in the
left GL overlapped with the ongoing activity in the
right GL; similarly, the onset of activity in the right GL
overlapped with the ongoing activity in the left GL. In
contrast to walking, neither swimming nor airstepping
showed significant periods of overlapping activity be-
tween the right and left GL muscles. In swimming
(Fig. 2B), the extensor activity in one leg terminated as
a c t i v i t y i n t h e c o n t r a l a t e r a l leg w a s i n i t i a t e d . T h e g a p
(3%) between contralateral activity in swimming was
n o n s i g n i f i c a n t . H o w e v e r , in a i r s t e p p i n g (Fig. 2C), t h e r e
w a s a s i g n i f i c a n t g a p b e t w e e n G L a c t i v i t y in t h e r i g h t
a n d left legs ( 9 % o f t h e cycle).
Cycle periods
The frequency distributions show that walking occur-
red over a much broader range of cycle periods than

Fig. 2A-C Summary of A Walking

quantified EMG activity for
right GL and left GL in walking Right GL
A, swimming B and airstepping
C. Burst durations and latency Left GL
to burst onset have been
expressed as a proportion of I I I I I
a cycle. The onset of each bar
represents the mean phase value
for a muscle and the length of
each bar represents the mean B Swimming
normal duration value for
Right GL
a muscle. Abscissa represents
normalized cycle period. Two Left GL
cycles in each behavior are
shown. N = 10 for right GL and I I I I I
left GL in each behavior (10
animals per behavior; 10 values
per animal). Phase left GL with
respect to the right GL
(mean + s.d.: walking
C Airstepping
0.44 0.02; swimming Right GL
0.48 + 0.05; and airstepping
0.51 -I- 0.06). In all cases, Left GL
standard errors were less than
0.02 and omitted for clarity I I | I I
0 0.5 1.0 1.5 2.0
Normalized cycle period
R. M. Johnston, A. Bekoff: Patterns of muscle activity during different behaviors in chicks 173

Fig. 3A-C Frequency A Walking B Swimming C Airstepping

distributions for cycle periods in
walking A, swimming B and 220 ]/
airstepping C. Cycle period was
defined from the onset of activity
in the right GL to the next onset
of activity in right GL. 120 t
Distributions were based on
pooled data for GL activity (600
values per behavior). The mean Z 80
cycle period __+standard
deviation is shown below the
abscissa and was based on 40
a sample size of N = 10 (10
animals per behavior; 10 values
per animal)
100 300
|
500 700 100 300 500 700 ~0
I -.l-
Cycle period (ms) Cycle period (ms) Cycle period (ms)

either swimming or airstepping (Fig. 3). However,
a portion of the range (175-350 ms) was shared by these
three behaviors. The mean cycle periods for walking
(362 _+ 131 ms) and swimming (308 + 55 ms) did not
differ significantly from one another, but were signifi-
cantly greater than the mean cycle period for airstep-
ping (196 + 34 ms).
Intralimb coordination: patterns of muscle activity
In contrast to the preceding example, the majority of
the muscles showed more subtle differences in their
bursting activity among these three behaviors. On
average, normalized durations of muscle activity differ-
ed among walking, swimming and airstepping; these
A Airstepping
2 2 2 2 2 2

In these three behaviors, the muscles examined showed

either one or two periods of activity (i.e. bursts) per
cycle. The muscles that burst once per cycle were: GL,
TA, CF, SA, pIF and aIF (Fig. 1A). Previous work on
the IF muscle in chicks showed that the distinct 'a' and
'p' bursts originate from either the anterior or posterior
regions of IF, respectively, and that each region re-
ceived separate innervation (Settles et al. 1987). Thus,
we considered the anterior IF (aIF) and the posterior
IF (pIF) as separate muscles. FT was the only muscle B Walking
we examined that was active twice per cycle. With 1 2 1 2 1 2 1 2
respect to the beginning of a cycle, we designated the
first burst in FT as FT1 and the second burst as FT2.
Our attempts to isolate each of these bursts to regions
within FT have been unsuccessful so far. Although
there were no apparent morphological compartments
for FT, it is possible that the recruitment of motor units
could be functionally compartmentalized.
The most obvious difference in the motor patterns
among these behaviors was the absence of FT1 activity
in airstepping (Figs. 4, 5C). The activity of FT1 was 200 ms
similar in walking and swimming, but completely ab- Fig. 4A, B Examples of E M G recordings showing FT and GL ac-
sent during airstepping. An example of FT activity tivity during airstepping A and walking B from the same animal. The
during airstepping and walking in the same animal is numbers 1 and 2 indicate the first (FTI) and second burst (FT2) of
shown in Fig. 5. During airstepping, only FT2 activity FT. A In airstepping, only the second burst in FT (FT2) was present.
However, when the same animal was placed on the substrate and
was present (Fig. 4A). However, when the same animal initiated walking B, both the first and second bursts were present.
was allowed to walk, both FT1 and FT2 bursts were The phase of FT2 activity with respect to GL was similar for walking
present (Fig. 4B). and airstepping
174 R . M . Johnston A. Bekoff: Patterns of muscle activity during different behaviors in chicks

Fig. 5A-C Summary of A Walking

normalized EMG activity for P1 P2 R PI P2 R
walking A, swimming B and GL
airstepping C. The onset oj each pIF t I , I I
bar represents the mean phase CF
FT If_m__ ! 1 ~ 1 ~
value for a muscle and the length TA
of each bar represents the mean SA
normal duration value for aIF
a muscle. The abscissa } I I I I
I I I t I
represents normalized cycle
-0.5 0 0.5 1.0 1.5
period. Two cycles for each
behavior are shown. The
numbers 1 and 2 identify the first
(FT1) and second (FT2) bursts of
FT. Note that FTI activity is B Swimming P2 R PI P2 R Pl
absent in airstepping. N = 10 for GL I I []
each muscle within each pIF
behavior: 10 chicks per muscle CF I I
with 10 measurements per FT I all III I
muscle. Also shown are the three TA I
stages of the leg movements, SA
a/F i
retraction (R), protraction 1 (P1) I I 1 I I
and protraction 2 (P2). These I 1 I I I

three stages were quantified -0.5 0 0.5 1.0 1.5

from digitized, video taped
records of each behavior that
were synchronized with the
motor activity. In all cases,
standard errors were less than C Airstepping P2 R P1 P2 R P1
0.02 and not shown for clarity GL I ii.s_
prF I
CF
i I I
TA
SA
alFi 1I i
i i i i i

-0.5 0 0.5 1.0 t.5

Normalized cycle period

differences may be related to the extent of resistance
encountered during these movements. In walking,
muscles active during the stance phase (GL, pIF and
CF), where the leg movements encountered resistance
due to contact with the ground and weight-bearing,
showed long normalized durations (Fig. 5A; Table 1)
(note that FT1 was the exception to this generalization
as discussed below). This was in contrast to the shorter
normalized durations (and delayed onset) for muscles
active during the swing phase where the leg moved
unimpeded through the air (TA, SA, aIF and FT2)
(Fig. 5A; Tables 1, 2). We use the term asymmetry to
describe this type of difference in burst durations (i.e.
long vs. short). Thus, a cycle of walking was character-
ized by asymmetrical durations of activity between
groups of muscles which corresponded with the high
resistance (stance or retraction) and the low resistance
(swing or protraction) stages of a walking cycle.
Neither swimming nor airstepping had a stance
phase. The legs encountered roughly uniform resistance
from the water throughout swimming and from the air
throughout airstepping. In contrast to the asymmetry
described during walking, the average durations of GL,
plF, CF, TA and SA each occupied 40-50% of a cycle
(Fig. 5B; Table 1). We described swimming as having
symmetrical activity durations. Note that for swim-
ming the activity in FT and aIF were the exceptions to
this generalization as discussed below.
In contrast to both walking and swimming, the legs
encountered very little resistance from the medium
during airstepping. Several of the muscles showed nor-
malized burst durations which occupied 40-50% of the
cycle: GL, TA and SA (Fig. 5; Table 1). In contrast, the
normalized duration of pIF was much shorter (Table
1). The remaining two muscles examined in airstepping,
FT and aIF, showed an interesting parallel with the
both walking and swimming. In none of the three
behaviors did FT and aIF fall into the generalized
trend where normalized durations were correlated with
the extent of resistance. Although walking, swimming
and airstepping encounter different degrees of resist-
ance during the hindlimb movements, the normalized
durations of FT1, FT2 and aIF changed little among
these behaviors (Table I; Fig. 5).
In general, the timing of motor activity differed in
these behaviors. In contrast to either swimming or
R. M. Johnston, A. Bekoff: Patterns of muscle activity during different behaviors in chicks 175

Table 1 Mean normalized

durations for each muscle in GL pie CF FT1 FT2 TA SA aIF
several chick behaviors
Walking 0.69 0.61 0.63 0.41 0.30 0.33 0.41 0.16
Swimming 0.45 0.42 0.45 0.30 0.37 0.43 0.52 0.17
Airstepping 0.40 0.24 0.35 a 0.38 0.42 0.50 0.13
Embryonic 0.40 a 0.34 0.39 a 0.34 0.43 0.36
motility
Hatching 0.48 0.38 0.42 0.47 a 0.32 0.17 0.25
0.17
Hatching- 0.42 0.35 0.37 0.33 a 0.43 0.48 0.13
deafferented legs
Walking- 0.47 0.49 0.38 0.35 0.32 0.37 0.51 0.20
deafferented legs

aIndicates the absence of muscle activity. Normal duration is defined as burst duration/cycle duration.
N = 10 for each muscle within each behavior. Data for embryonic motility (Bradley and Bekoff 1990),
hatching, deafferented hatching and deafferented walking (Bekoffet al. 1987) were recalculated based on
a sample size of N = 10:10 chicks per muscle with 10 measurements per muscle. Standard error of the
means were all < 0.02. For these data variation within each animal was similar to variation among
animals

Table 2 Mean phase values for

each muscle in several chick GL pIF CF FT1 FT2 TA SA aIF
behaviors
Walking 0.00 0.10 0.02 0.21 0.80 0.71 0.70 0.70
Swimming 0.00 0.04 - 0.01 0.09 0.70 0.44 0.47 0.51
Airstepping 0.00 0.08 0.01 ~ 0.78 0.42 0.47 0.38
Embryonic 0.00 a 0.04 - 0.05 a 0.51 0.45 0.50
motility
Hatching 0.00 0.03 0.03 - 0.02 a 0.48 0.43 0.53
0.63
Hatching- 0.00 0.02 0.00 -- 0.02 " 0.35 0.32 0.50
deafferented legs
Walking- 0.00 0.02 -- 0.04 0.00 0.67 0.51 0.45 0.51
deafferented legs

a Indicates the absence muscle activity. Phase is defined as latency to burst onset with respect to the onset
of the cycle/cycle duration. N = 10 for each muscle within each behavior. Data for embryonic motility
(Bradley and Bekoff 1990), hatching, deafferented hatching and deafferented walking (Bekoff et al. 1987)
were recalculated based on a sample size of N = 10:10 chicks per muscle with 10 measurements per
muscle. Because SA shows bursts twice per cycle in hatching, two phase values are given. Standard error
of the means were all < 0.02. For these data variation within each animal was similar to variation
among animals

airstepping, the recruitment of TA, SA and aIF activity G L - C F - p I F - F T 1 s y n e r g y b e g a n . B a s e d o n its r e c r u i t -

w a s d e l a y e d in w a l k i n g (Fig. 5). H o w e v e r , w i t h o n e
e x c e p t i o n , t h e m u s c l e s t h a t w e r e r e c r u i t e d t o g e t h e r (i.e.
s y n e r g i s t s ) in o n e b e h a v i o r c o n t i n u e d to be r e c r u i t e d
t o g e t h e r in t h e o t h e r b e h a v i o r s . W e i d e n t i f i e d t w o
s y n e r g i e s t h a t w e r e c o m m o n to e a c h b e h a v i o r : the
GL-CF-pIF-FT1 synergy and the TA-SA-aIF synergy
(Fig. 5). W i t h i n e a c h o f t h e t w o s y n e r g i e s t h e r e c r u i t -
m e n t o r d e r o f the m u s c l e s w a s n o t rigid. F o r e x a m p l e ,
a I F w a s r e c r u i t e d b e f o r e S A in a i r s t e p p i n g , b u t after S A
in s w i m m i n g (Fig. 5). U n l i k e the o t h e r muscles, F T 2
a c t i v i t y w a s n o t r e c r u i t e d as p a r t o f t h e s a m e s y n e r g y in
t h e s e b e h a v i o r s . I n w a l k i n g , F T 2 was r e c r u i t e d as p a r t
o f t h e T A - S A - a I F s y n e r g y . H o w e v e r , in s w i m m i n g a n d
a i r s t e p p i n g , F T 2 a c t i v i t y w a s r e c r u i t e d well after t h e s e
m u s c l e s h a d a l r e a d y b e e n r e c r u i t e d (Fig. 5). I n a d d i -
tion, F T 2 w a s r e c r u i t e d well b e f o r e a c t i v i t y in the
m e n t t i m e w i t h r e s p e c t to the o t h e r m u s c l e s , we d o n o t
i n c l u d e F T 2 a c t i v i t y as p a r t o f e i t h e r s y n e r g y in s w i m -
ming and airstepping. In these two behaviors, FT2
o c c u r r e d b e t w e e n t h e t w o c o m m o n synergies.
Muscle activity synchronized with movement
kinematics
For most of the muscles examined, each behavior
showed similar relationships between muscle activity
a n d c h a n g e s in j o i n t a n g l e (Fig. 6). F o r e x a m p l e , p I F
was active during knee flexion and CF was active
d u r i n g h i p e x t e n s i o n in e a c h b e h a v i o r . A l t h o u g h t h e
muscle activity occurred during either joint flexion or
e x t e n s i o n m o v e m e n t s in e a c h b e h a v i o r , the d u r a t i o n o f
176 R . M . Johnston, A. Bekoff: Patterns of muscle activity during different behaviors in chicks
Walking Swimming
Hip
Knee
/
20J
160.
SAV
l r
--&
~a
<
e-,
40.
180-
Ankle
\
\ GL~
~a
<
0
o Time (ms) 60o 0 Time (ms)
Fig. 6 E M G recordings synchronized with movement kinematics.
The onset and duration of activity in several muscles are plotted
with the corresponding changes in angular joint displacements. The
non-continuous, solid lines represent periods of activity in individual
muscles. The dashed lines represent changes in joint angles. Exten-
sion was defined as an increase in joint angle; flexion was defined as
a decrease in joint angle. In walking, the shaded area denotes the
stance period. The data shown were from a different animal in each
behavior and were typical of all other analyzed records. Synchro-
nized results were quantified from 5 different animals per behavior
with 10 samples per muscle
activity and/or phasing could differ (e.g. FT2). Figure
6 also shows that the onset of joint movement did not
always coincide with the onset of muscle activity at that
joint. For example, in each behavior, ankle extension
preceded the onset of activity in the ankle extensor, GL
(Fig. 6). Furthermore, GL activity stopped at the
transition from ankle extension to ankle flexion in both
walking and swimming. In airstepping, GL activity
continued well into ankle flexion. Even so, on average
GL and TA bursts did not show any overlapping peri-
ods of activity in airstepping (Fig. 5C).
In addition to correlating muscle activity with
flexion and extension movements at individual joints,
we also related the motor patterns to retraction and
protraction movements of the entire leg (defined in
Materials and methods; also see Johnston and Bekoff
1992, for more details on the kinematic profiles of the
legs during walking, swimming and airstepping). In
general, during retraction (R) the leg moved posteriorly
Airstepping
CF/-
,
I
all=
/ \
T /
~o o Time (ms) 6oo
as the joints extended. Protraction 1 (P1) occurred
when the leg was drawn towards the body as the joints
flexed. Protraction 2 (P2) stage identified when the leg
moved anteriorly. Figure 5 shows the relationships
between periods of muscle activity and the retraction
and protraction stages of the leg movements (also see
Table 3). Many muscles were active during more than
one stage of the leg movements. In addition, the dura-
tion of muscle activity in a particular stage of the
movement could differ among the three behaviors. For
example, in walking GL was active during almost all of
stage R and only a small portion of stage P1; in swim-
ming, GL was active for approximately half of stage
R and half of stage P1; and in airstepping, GL was
active for more than half of stage R and roughly half of
stage P1.
For many of the muscles, the movement stage in
which muscle activity was initiated remained much the
same in each behavior (e.g. GL began in stage R and
TA began in stage P1 in each behavior) (Fig. 5). How-
ever, FT2 initiated activity during P1 in walking and
P2 during both swimming and airstepping. The stage in
which the muscle activity was terminated was more
variable than that seen for initiation of activity. For
example, CF activity ended during stage R in walking
and during stage P1 in swimming and airstepping
(Fig. 5). On average, in these three behaviors, 5 out of
8 muscles terminated activity in different movement
stages, but only 1 out of 8 of the muscles initiated
activity during a different movement stage. In each
R. M. Johnston, A. Bekoff: Patterns of muscle activity during different behaviors in chicks
Table 3 Average onset (with respect to GL) and duration of retrac-
tion and protraction movements of the hindlimb (expressed as
proportion of the cycle) during walking, swimming and airstepping.
Onset
Retraction Protraction 1 Protraction 2
Walking - 0.03 0.66 0.87
Swimming - 0.19 0.29 0.61
Airstepping - 0.15 0.32 0.50
A B C muscles aIF and SA were coactive, it is likely that SA
I
Fig. 7 A - C Proposed muscle interactions between SA and alF.
A Schematic illustration showing the anatomical positions of each
muscle9 The leg profile is shown in dark lines and the muscles are
shown in stippled lines. B and C Diagrams showing the movements
of the leg during the activity of SA and aIF. The dotted lines
represent the new position of the leg profile
behavior, the GL-CF-plF-FT1 synergy occurred dur-
ing R and the TA-SA-aIF synergy occurred during P1.
However, FT2 activity occurred during P1 in walking,
but during P2 in both swimming and airstepping
(Fig. 5).
Analyses of the synchronized data also revealed that
the effects of activity in a given muscle could be
changed by the concurrent or previous activity of an-
other muscle. Two examples demonstrating such inter-
active relationships were CF and FT, and SA and aIF.
Based on their anatomical positions, activity in FT
would be expected to extend the knee and activity in
CF would be expected to extend the hip and flex the
knee (Fig. 1A). During the time when these two muscles
were coactive, knee extension was not observed (Fig. 6).
One possible explanation for this observation was that
activity in the uniarticular FT could be playing two
roles. First, activity in FT opposed knee flexion due to
activity in CF. Second, as FT contracted, it lengthened
CF thereby promoting continued hip extension by CF
activity, a movement FT could not accomplish on its
own. Figure 7 illustrates the interaction between the
muscles SA and aIF. Activity in SA would be expected
to flex the hip and extend the knee (Figs. 1, 7A) while
knee flexion was associated with the activity in the
anterior portion of IF (aIF). During the time when the
177
Standard error of the means were all < 0.01. N = 10 (10 chicks per
behavior with 10 measurements per chick
Duration
Retraction Protraction 1 Protraction 2
0.69 0.21 0.10
0.48 0.32 0.20
0.47 0.18 0.35
flexed the hip and aIF flexed the knee (Figs. 6, 7B).
When activity in aIF stopped, sustained activity in SA
could continue to flex the hip and initiate knee exten-
sion (Fig. 7C). Therefore, presumably, the initiation of
knee extension did not require the recruitment of a new
muscle; knee extension was initiated by the changing
role of SA throughout the movement.
Variability in muscle activity
Analyses based on the arithmetic means are but one
way to describe patterned activity. Analyses of the
scatter in the data provide a useful tool to examine the
variability in the patterned activity. To account for
variability in the duration of muscle activity, we plotted
burst durations against their corresponding cycle peri-
ods for each muscle in each behavior and used regres-
sion analysis to quantify the relationships (Fig. 8). Dur-
ing walking, the duration of muscles active during the
stance phase increased as cycle periods increased (GL,
pIF, CF and FT1). The slopes describing the relation-
ships for these muscles were all greater than 0.50. In
addition, changes in cycle period accounted for 66% to
89% of the variability in the duration of muscle activity
(based on r2). In contrast, the changes in the duration of
muscles active during the swing phase of walking were
only weakly associated with changes in cycle period
(slopes less than 0.20), if at all (TA, SA, aIF and FT2)
(Fig. 8). Changes in cycle period accounted for less of
the variability in the duration of muscles active during
the swing phase in walking.
In comparison to walking, the majority of the rela-
tionships between duration and cycle period changed
during swimming or airstepping. For example, in both
of these behaviors the relationships for the antagonistic
ankle muscles, GL and TA, had slopes that were rever-
sed in comparison to walking (Fig. 8). In swimming or
airstepping, the regression slope of GL was less than
that for TA; in walking the regression slope of GL was
greater than TA. Other muscles, such as pIF and CF,
showed smaller or non-significant slopes in comparison
to walking. Although the regression slope for FT2 was
greater in swimming or airstepping, the amount of
178 R. M. Johnston, A. Bekoff: Patterns of muscle activity during different behaviors in chicks

Fig~ 8 Burst duration versus Walking Swimming Airstepping

cycle period graphs for the
muscles examined during 600 13= 0.67 400 13= 0.12 400 13= 0.17
walking, swimming and r 2 = 0.08
airstepping. Regressions are not
shown for FT1 for airstepping GL ! I'i: /
because FT1 activity is absent
during airstepping. Each figure
contains 100 points compiled
i oS
from 10 animals per muscle with 600 13= 0.81 400 13= 0.50 400 6=ns
I0 values per animal, fl indicates
the slope for each regression and
~ I r2=O:~Y r2=034
r 2 is the coefficient of pIF
determination. All slopes given
showed P < 0.05. ~o o 0
Nonsignificant slopes (ns)
(P > 0.05) are not drawn. 600 ] 13= 0.63 400 1 13= 0.23 400 13----as
Regressions of each individual
animal showed the same
CF
I ':0:0
relationships as the combined .~:'- "' "
data set
~o o 0

FT1
6001.0,1
/ r2 = 0.74 411.=068
.j
r2 = 0,58

i
~o

400 13= 0.50

60011 r2
0"3613=0"15
= // r2 = 0"33. 400] 6= 0.32

FT2 -

~o
~
'7 0
. 9 .~
" .,,~ :
~I

600 13= us 400 6 = 0.65

=, [ r2 = 0 . 3 2 . ~ , , r2 = 0.42

TA Y
9 ~ ~l ~

~0 0

600 g = 0.19 6= ns
g r 2 = 0.23 i r'=Ot=
SA .:.. ,~.....,.~ ~ .',o

= o

600 1 13= 0.05 4o0 i 13=0.18 4ool 6=ns

"~ ] r2=0"14
aIF

0 ~ 0i
100 700 150 550 0 400
Cycle period (ms) Cycle period (ms) Cycle period Ires)

variability that was accounted for by the regressions
(based on r 2) remained low. The amount of variation in
SA or aIF duration remained low in swimming, al-
though the magnitude of the slopes increased in com-
parison to walking. In contrast, airstepping showed
non-significant relationships between SA or aIF dura-
tion and cycle period. Despite these many differences,
the relationship between FT1 duration and cycle peri-
od was similar in walking and swimming (FT1 was not
active during airstepping). Although the magnitude of
the slopes differed, they both showed moderate slopes
and accounted for much of the variability in the dura-
R. M. Johnston, A. Bekoff: Patterns of muscle activity during different behaviors in chicks 179

Table 4 Summary of the

statistical comparisons of Statistical results Variance (ms z)
duration variability for specific
pairs of muscles within walking W S A W S A
(W), swimming (S) and
airstepping (A) based on GL v. TA = = = GL 2622 420 183
variance ratios CF v. SA > = = CF 4639 528 237
pIF v. FT2 > = = pIF 7270 1217 107
plF v. SA > = = SA 1048 725 347
alF v. FT2 = > > TA 1015 592 342
FT1 1832 1858 a

alF 185 256 12

FT2 616 2793 110

aIndicates that comparisons were not possible because FT1 activity was absent in airstepping.
Non-significant differences are represented by the symbol, = . Significant differences where the
variance of the first muscle was greater than the second are represented by the symbol, > . For example,
the variance in duration between GL and TA as not significantly different. The variance for CF duration
was significantly greater than that for SA in walking. Significance was determined based on a critical
level of 0.05 and two-tailed probabilities: F . o 5 / 2 1 9 , 9 ] = 4.03. N = 10 for each muscle within each behavior

tion of FTI. In walking, more than 30% of the variabil-
ity in duration was accounted for by changes in cycle
period for 62.5% (5 out of 8) of the muscles examined.
Regression analysis accounted for at least 30% of dura-
tion variability in 50% (4 out of 8) of the muscles
examined in swimming, but only 14% (1 out of 7) in
airstepping. Unlike the other two behaviors, in airstep-
ping the majority of the muscles (4 out of 7) examined
showed non-significant regression relationships be-
tween duration and cycle period.
We also examined the extent to which walking,
swimming and airstepping showed common trends in
variation by statistically comparing the duration mean
squares (i.e. variance) for specific pairs of muscles that
acted primarily at the same joint, but during opposing
stages of the movement cycle (i.e. retraction and pro-
traction). This analysis showed that the extent of vari-
ation for the antagonistic ankle muscles, GL and TA,
were similar in each behavior (Table 4). However, in
walking, most of the muscles active during leg retrac-
tion had burst durations that were more variable than
the muscles active during the leg protraction move-
ments (e.g. CF-SA) (Table 4). This was in contrast to
both swimming and airstepping where each showed no
detectable differences in burst duration variability for
the majority of the muscles (e.g. CF-SA). In fact, the
same statistical conclusions were present for swimming
and airstepping for all of the comparisons.
Discussion
Relationships between joint angle,
muscle activity and behavior
The primary purpose of this study was to identify the
c o m m o n and unique features of leg muscle activity
during three distinct postembryonic behaviors: walk-
ing, swimming and airstepping. Although the behav-
ioral context differs greatly for these behaviors, we
identified many similarities in the patterns of muscle
activity. Each behavior showed similar relationships
between muscle activity and joint motion for many of
the muscles examined in this study (Fig. 6). For
example, CF was active during hip extension in each
behavior. These trends were maintained under the dif-
ferent behavioral conditions associated with walking,
swimming and airstepping and over a wide range of
cycle periods (Fig. 3). However, as seen in Fig. 6, the
synchronized results also revealed that some muscles,
such as FT2, displayed different relationships with the
joint angle profiles during different behaviors. In air-
stepping, FT2 activity was seen only at the end of knee
extension. In both walking and swimming, activity in
FT2 occurred throughout knee extension. We propose
that the delay in onset of FT2 in airstepping can be
accounted for by examining the interactions between
two other muscles, SA and alF (Figs. 6, 7). During the
time when SA and alF were coactive, aIF flexed the
knee and SA flexed the hip. When activity in aIF
stopped, activity in SA not only continued to flex the
hip, but now initiated knee extension. In walking and
swimming, aIF activity stopped midway through the
SA burst duration (Fig. 5A, B). However, in airstep-
ping, alF stopped near the beginning of SA activity
(Fig. 5C). This suggests that much of knee extension
during airstepping resulted from the bifunctional
muscle, SA; as SA shortened, FT2 may be recruited to
continue knee extension movements. Thus, the differ-
ences in the timing of these and other muscles may
indicate that the recruitment of muscles is task depen-
dent as suggested for hindlimb behaviors in cats (Pratt
and Loeb 1991).
The relationships between GL activity and the
movement profiles in airstepping also differed from
walking and swimming. In contrast to the other two
180 R. M. Johnston, A. Bekoff:Patterns of muscle activity during differentbehaviors in chicks
behaviors, in airstepping GL activity continued past
the transition from extension to flexion and into ankle
flexion (Fig. 6). It has been suggested that an out of
phase relationship between the direction of joint
motion and muscle action forcibly stretches the muscle,
thus enhancing force production needed to satisfy the
dynamic requirements of rapid oscillatory movements
(Abraham and Loeb 1985; Smith et al. 1985). In airstep-
ping, if early ankle flexion was in part due to the effects
of intersegmental dynamics, then continued activity of
the ankle extensor, GL, could aid in slowing or oppos-
ing these forces. Experiments addressing intersegmen-
tal dynamics using kinetic analyses are needed to vali-
date these suggestions.
In walking, our results showed that knee flexion
occurred during the stance phase even though the knee
extensor, FT1, was active. The observed knee flexion
could be passive as the leg yields to the weight of the
animal during the stance phase and the concurrent
knee extensor activity could be required to stabilize the
knee joint. However, because of anatomical specializa-
tions (Young 1981; Raikow 1985), knee flexion is the
only means by which the chick can continue forward
movement to change its center of mass relative to its
foot placement during walking (Gatesy 1989). There-
fore, it would appear that in chicks knee flexion during
stance does not result only from a passive yielding of
the joint, but results from muscle activity in pIF. One
possible advantage for recruitment of the uniarticular
muscle, FT, with its biarticular antagonist, pIF, during
the stance phase may be to enhance the work that the
uniarticular muscle can do in addition to contributing
to stabilizing the knee joint during the stance phase in
walking (van Ingen Schenau 1987, 1990; van Ingen
Schenau et al. 1992). Because both pIF and FT1 are
active during knee flexion in swimming, the need to
stabilize the knee or augment muscle work may not be
restricted to behaviors where contact occurs with the
substrate, such as walking. In addition, this muscle
synergy may participate in other functional roles im-
portant to the performance of the behavior. Given the
above information, it is possible that the absence of
FT1 activity during airstepping reflects that the leg
movements are unable to generate force that would
result in forward movement of the animal. Although
this hypothesis needs to be formally tested, these data
show that patterned muscle activity and coordinated
leg movements continue uninterrupted even when one
element of a motor synergy is absent.
Another possible role played by FT was to enhance
hip extension. During the time when FT1 and CF were
coactive, FT1 activity not only opposed knee flexion
due to activity in CF, but also lengthened CF thereby
promoting continued hip extension by CF activity
(Fig. 7). This suggestion reflects that the effects of activ-
ity in a given muscle can be changed by the concurrent
or previous activity of other muscles. These examples
relating muscle activity to movement kinematics re-
mind us that behavior results from the combined effects
of many muscles whose relationships change through-
out the movement. Thus, behavior is the product of
interactive and interdependent strategies used to gener-
ate coordinated movements.
Variation in patterned activity
The resistance that the leg movements encountered
from the environment differed among these three be-
haviors. During walking, the retraction or stance stage
impeded the leg movements and delayed the onset of
the protraction or swing stage where the legs encounter
only minor resistance from the air. In swimming, the
legs received uniform resistance from the water envi-
ronment during both the retraction and protraction
stages of the movements. The context of airstepping
also provided uniform, although much less, resistance
to the leg movements. (For a discussion of leg move-
ment kinematic in these three behaviors, see Johnston
and Bekoff 1992). Although not the only source of
afferent modulatory input, the extent of resistance pres-
ent during walking, swimming and airstepping, was
correlated with the changes in the duration of muscle
activity. However, when normalized for differences in
cycle periods, FT and aIF activity showed only small
changes in duration in these behaviors (Table 1; Fig. 5).
This suggests that the effects of the various sources of
modulatory inputs, including resistance from weight
support, water or air and other influences unique to
each behavior, were functionally similar for the muscles
aIF and FT. In contrast, activity in the remaining
muscles, GL, CF, plF, TA and SA, differed among
these behaviors. In walking, where resistance related to
weight support was present, these muscles showed an
asymmetry in burst durations (Fig. 5; Table 1). On
average, the durations of muscles active during the
stance phase were longer than the durations of muscles
active during the swing phase. In swimming or air-
stepping, where the legs experience more uniform
resistance, the activity of these muscles were more sym-
metrical. Asymmetrical burst durations for stance and
swing muscles are a common feature of walking in
many animals (Cracraft 1971; Grillner 1981; Jacobson
and Hollyday 1982; Gatesy 1989). Changing from
asymmetrical to symmetrical bursting activity has been
described for walking and swimming in turtles (Len-
nard and Stein 1977; Williams 1981) and in rats
(Gruner and Altman 1980). These data support pre-
vious conclusions that the asymmetries characteristic
of walking were the result of sensory modulation from
the legs that biased the output of the premotor circuit
elements underlying the muscle activity (Bekoff et al.
1987). In addition, even though resistance-related
modulation affects the activity of aIF and SA different-
ly in these behaviors, the result of their concerted action
was maintained. We propose that the premotor ele-
R. M. Johnston, A. Bekoff:Patterns of muscleactivity during differentbehaviors in chicks
ments underlying the production of these behaviors
accommodates modulation that affects muscle activity,
such as the absence of a burst (e.g. FT1 in airstepping)
or changes in the onset and duration of activity, with-
out disrupting the integrity of the motor patterns or leg
movements. Although our analysis is far removed from
the actual pattern generating elements, the flexibility in
muscle activity is consistent with ideas of plasticity that
have been well characterized in the stomatogastric sys-
tem of decapod crustaceans (Harris-Warrick and Joh-
nson 1989; Harris-Warrick and Marder 1991; Meyrand
et al. 1991; Weimann et al. 1991; Meyrand and Simmers
1992).
We identified two motor synergies common to each
behavior. With only one exception (FT2), muscles that
were recruited together in walking were also recruited
together in swimming and airstepping. Within each
synergy, changes in the timing and duration of activity
were correlated with the presence or absence of weight-
bearing by the legs. Although FT2 activity was recruit-
ed during one of the common synergies in walking, it
did not participate in either synergy in swimming or in
airstepping. In the latter behaviors, FT2 activity occur-
red between the two common synergies. Another prom-
inent difference in motor activity among these behav-
iors was the absence of FT1 activity during airstepping.
Despite its absence, the activity of the other muscles
that were part of the synergy showed patterned activity
that was similar to activity produced in walking and
swimming.
It has been proposed that the CNS simplifies control
of a multisegmental, multimuscular limb by combining
muscles into groups based on common periods of activ-
ity (i.e. synergies). Different behaviors may show differ-
ent synergies in response to the unique afferent modu-
lation associated with the movements (Koshland and
Smith 1989; Smith et al. 1985; Pratt and Loeb 1991). In
contrast, it has been proposed that the CNS is organ-
ized to control each muscle individually (MacPherson
1991). Based on our results, these two proposals are not
mutually exclusive. Comparisons of burst duration
versus cycle period regressions among walking, swim-
ming and airstepping indicate that muscles that partici-
pate in the same synergy can be differentially affected
by afferent inputs (Fig. 8). These data support previous
work suggesting that each muscle can be influenced
independently by sources of modulation (Grillner
and Wall6n 1985; Hoy et al. 1985; Smith et al. 1985;
Hoy and Zernicke 1986; Smith 1986). In addition, al-
though there are apparent differences in afferent
modulatory inputs during these three behaviors, the
majority of the muscles continue to participate in
synergies common to each of these behaviors; changes
in synergies appear to be restricted to muscles that act
at the knee (i.e. FT2) during the protraction phase of
the leg movements. Similar trends have been seen in
studies of various cyclical leg behaviors in cats (Smith
1986).
181
Relationships with embryonic behaviors in chicks;
implications for neural control
Embryonic motility and hatching share several features
of the motor activity described for the postembryonic
behaviors of walking, swimming and airstepping.
Although not identical, the two common synergies
described for the postembryonic behaviors were also
present in these embryonic behaviors (Figs. 5, 9A, B).
The differences in duration and timing of their activity
between embryonic behaviors and walking has been
correlated with differences in afferent modulation
(Bekoff 1976; Bekoff et al. 1987; Bradley and Bekoff
1990). These similarities in synergies suggest that the
mechanisms that underlie the organization of muscle
activity in postembryonic behaviors are established
early in development during the embryonic period.
Because hatching, a behavior that is normally produc-
ed only during a specific developmental period, can be
in re-elicited in posthatching chicks it has been sugges-
ted that the neural elements that produce this stage-
specific behavior are retained into the postnatal period
(Bekoff and Kauer 1984). Thus, although muscle activ-
ity is an indirect measure of the neural networks that
are involved in producing behaviors, similarities in
motor activity during the different behaviors shown in
this study may reflect elements of the pattern generat-
ing circuits that are common to these embryonic and
postembryonic behaviors in chicks (Bekoff 1986; Bekoff
et al. 1987). These ideas are consistent with direct evid-
ence from other systems that elements of circuits are
reused during different developmental stages (Levine
and Weeks 1989; Weeks and Levine 1990) and that the
same circuit can produce different behavioral patterns
(Getting and Dekin 1985; Getting 1989; Hooper and
Moulins 1989; Cazalets et al. 1990; Dickinson et al.
1990; Harris-Warrick and Marder 1991; Weimann
et al. 1991). Based on features of motor activity other
studies have also made similar suggestions that differ-
ent behaviors share pattern generating circuitry (Ayers
and Davis 1977; Ayers and Clarac 1978; Stein et al.
1986; Mortin and Stein 1989). Of course, we do not
exclude the possibility that different circuits and or
mechanisms exist that produce similar patterns of mo-
tor activity in different behaviors and developmental
stages.
Although many of the muscles show similar patterns,
the activity of FT2 and aIF in prenatal behaviors differ
in comparison to the motor profiles in the postnatal
behaviors. FT2 activity is absent in both embryonic
motility and hatching, but present in all of the postem-
bryonic behaviors that we have examined. In addition,
unlike the posthatching behaviors where aIF duration
is brief and is recruited at different times within the
synergy, the duration of aIF is long and maintains
a similar onset phase in both embryonic motility and
hatching (Tables 1, 2; Figs. 5, 9). However, data from
chicks with deafferented legs suggests that phasic
182 R. M. Johnston, A. Bekoff: Patterns of muscle activity during different behaviors in chicks

Fig. 9A-D Summary of A Embryonic Motility

normalized EMG activity
characterizing embryonic GL
motility A, hatching B and pIF
CF
hatching and walking in chicks FT
with deafferented legs (D, E). TA
The numbers 1 and 2 identify the SA
first (FTI) and second (FT2) alF
bursts of FT. Note that FT2 [ I I I I

activity is absent in both A, -0.5 0 0.5 1.0 1.5

B and C. Note that pIF activity
for embryonic motility is not B Hatching
shown because the data were not
yet available. However, data GL
suggests that both bursts of IF
are present in embryos
(Landmesser and O'Donovan FT
TA
1984). Data for leg motility in SA m m B m
9-day embryos (Bradley and alF m l
Bekoff 1990) and deafferented
hatching and walking (Bekoffet -~J.5 o15 11o 115
al. 1987) were recalculated based
on a sample size of N = 10 for
each muscle in each behavior: l0
chicks per muscle with 10
measurements per muscle in C Deafferented Hatching
each behavior. Abscissa GL
represents normalized cycle pIF
period. Two cycles for each CF
behavior are shown. Standard FT
errors were less than 0.02 and TA
SA
not shown for clarity alF m

-o.5 o 0'.5 1'.o

D Deafferented Walking

GL
plF
CF
FT z t
TA
SA
alF m
I

-0.5 o o'.5 llO 1.5

Normalizedcycle period

sensory information from the legs during hatching con-
tributes to the prolonged a I F duration. In the absence
of such input, the duration of aIF during hatching leg
movements is similar to that seen in the posthatching
behaviors (Figs. 5, 9). Thus, the apparent differences in
aIF duration between pre- and posthatching behaviors
most likely reflects afferent m o d u l a t i o n of p r e m o t o r
elements. We do not know yet the extent to which
phasic sensory information influences a I F duration
during embryonic motility. However, it is interesting
that afferent input from the legs affects the duration of
a I F differently during different stages of development.
In the absence of phasic sensory inputs from the legs,
the duration of a I F is brief during hatching (Fig. 9C),
but prolonged during walking (Fig. 9D). This difference
in response to afferent input during different develop-
mental stages may reflect the involvement of unique
a I F p r e m o t o r elements during each stage or differences
in the n e u r o m o d u l a t o r y state of the nervous system.
Among the chick behaviors discussed so far, m a n y of
the differences in patterned activity are associated with
changes in either burst of the uniarticular knee exten-
sor, FT: FT1 and FT2. O u r results show that either
FT1 or F T 2 activity could be absent in certain behav-
iors, without disrupting the activity of the other mem-
bers of the synergies. However, in behaviors where
input associated with the demands of a stance phase
were diminished, such as in swimming, airstepping and
R. M. Johnston, A. Bekoff: Patterns of muscle activity during different behaviors in chicks
deafferented walking (Figs. 5, 9), FT2 activity did not
participate in the common synergies; instead FT2 was
recruited during the time between the two synergies in
these behaviors (Fig. 5). The narrow range for recruit-
ment phase of FT2 in all of the behaviors (Table 2) may
reflect a less mutable feature of the underlying circuits
generating leg movements in chicks. We suggest that to
produce different behaviors in chicks, the CNS organ-
izes leg motor output around common synergies; with-
in these common synergies, the muscle activity can be
modified in tandem and on an individual basis. In
addition, we suggest that the basic recruitment patterns
and behavior continue even when activity from specific
muscles is absent completely or no longer part of the
synergy.
Acknowledgements We thank WC Lemon, DL Nicholl, MR Wood
and the anonymous referees for their valuable comments on the
manuscript. The experiments reported here comply with The Prin-
ciples of Animal Care, publication No. 86 26, revised 1985 of the
National Institute of Health. This work was supported by NIH
grant NS20310 to AB.
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